Retrospective Theses and Dissertations
1971
A survey of tapetal types and tapetal characteristics
in the Leguminosae
Paul Adelbert Buss Jr.
Iowa State University
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Buss, Paul Adelbert Jr., "A survey of tapetal types and tapetal characteristics in the Leguminosae " (1971). Retrospective Theses and
Dissertations. Paper 4386.
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BUSS, Jr., Paiil Adalbert, 1936A SURVEY OF TAPETAL TYPES AND TAPETAL
CHARACTERISTICS IN THE LEGUMINOSAE.
Iowa State University, Ph.D., 1971
Botany
University Microfilms, A XEROX Company, Ann Arbor, Michigan
THIS DISSERTATION HAS BEEN MICROFILMED EXACTLY AS RECEIVED
A survey of tapetal types and tapetal
characteristics in the Leguminosae
by
Paul Adalbert Buss, Jr
A Dissertation Submitted to the
Graduate Faculty in Partial Fulfillment of
The Requirements for the Degree of
DOCTOR OF PHILOSOPHY
Major Subject;
Plant Morphology
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Signature was redacted for privacy.
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Signature was redacted for privacy.
D^^ rZrad^^e College
Iowa State University
Of Science and Technology
Ames, Iowa
1971
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ii
TABLE OF CONTENTS
Page
INTRODUCTION
1
LITERATURE REVIEW
5
Tapetal Classification
5
Tapetal Nuclear Number in the Leguminosae
9
Mimosoideae
Caesalpinioideae
Papilionoideae
10
11
12
Somatic Polyploidy
14
Crystals in Tapetal Cells
22
MATERIALS AND METHODS
24
Plant Materials
24
Microtechniques
25
Paraffin Preparation
Anther Squashes
25
26
Photographic Techniques
27
Developmental Studies
27
OBSERVATIONS
28
Tapetal Types in the Leguminosae
28
Tapetal Nuclear Number and Nuclear Behavior
29
Mimosoideae
Caesalpinioideae
Papilionoideae
Tapetal Crystals
30
33
40
49
DISCUSSION
55
SUMMARY
62
iii
TABLE OF CONTENTS (continued)
Page
LITERATURE CITED
64
SUPPLEMENTARY BIBLIOGRAPHY
78
ACKNOWLEDGEMENTS
85
APPENDIX A:
86
SUMMARY OF TAPETAL CHARACTERISTICS
Chart 1.
Mimosoideae
86
Chart 2.
Caesalpinioideae
89
Chart 3.
Papilionoideae
92
APPENDIX B: FIGURES
101
APPENDIX C;
147
SOURCES FOR SPECIES STUDIED
1
INTRODUCTION
The tapeturn is the cell layer immediately surrounding the sporogenous
tissue and spores in many sporangia.
Because of this location and the
morphological changes which occur during its development, it has received
considerable attention, particularly in relation to its presumed nutri­
tional role in spore and pollen development (Mascre, 1919, 1921; Py, 1932;
Cooper, 1952; Takats, 1959, 1962; Knox, 1962; Heslop-Harrison, 1963, 1964;
Moss and Heslop-Harrison, 1967; Vasil, 1967; Echlin and Godwin, 1968;
Heslop-Harrison and Dickinson, 1969; and others).
According to Davis
(1966), however, the tapeturn has not received the attention it deserves
as far as its potential systematic importance is concerned.
Partial infor­
mation is available for only 231 of the 411 angiosperm families recog­
nized by Hutchinson (1959).
One aspect which may be of taxonomic significance in certain taxa is
the number of nuclei per tapetal cell.
In most angiosperm families, ta-
petal cells become binucleate or multinucleate.
In 26 families, however,
species are reported in which the tapetal cells remain uninucleate
(Wunderlich, 1954; Davis, 1966). This condition may result from lack of
nuclear division (Bonnet, 1912; Cooper, 1933; Carniel, 1952, 1954), from
endomitosis or other related phenomena (Carniel, 1952, 1954, 1963; Turala,
1958, 1963; and others), or secondarily from nuclear fusion in tapetal
cells that were binucleate or multinucleate at an earlier stage (Bonnet,
1912; Mascr/ and Thomas, 1930; Cooper, 1933; Smith, 1933; Steil, 1935,
1950; Roever, 1935; Brown, 1949; Francini, 1951; Carniel, 1952, 1954,
1963; Wunderlich, 1954; Nair and Kahate, 1961).
2
Of the 26 families of angiosperms with uninucleate tapetal repre­
sentatives, 15 are reported to be always uninucleate, whereas the remaining
11 families contain some uninucleate taxa as well as some which are binucleate or multinucleate.
Of the latter 11 families, three deserve
special mention; Boraginaceae, Orchidaceae and Leguminosae.
Svensson (1925), Strey (1931) and Millsaps (1940) reported that the
tapetal cells of Cynoglossum of the tribe Cynoglosseae (Boraginaceae) were
uninucleate,
Millsaps further suggested that this nuclear condition might
be a tribal character, since in the other tribes there were two or more
nuclei per tapetal cell.
Unfortunately, this conclusion was based on
the study of only about five species.
In the Orchidaceae, according to Swamy (1949), "The tape turn is of the
secretory type and its cells are uninucleate in all monandrous orchids.
A binucleate type is observed only in Paphiopedilum (Diandrae),"
Francini
(1931) and Carniel (1952) also observed only multinucleate tapetal cells
in this genus.
Again, there are too few observations for a convincing
generalization to be made.
In the Leguminosae, however, a significant tapetal pattern, based on
considerably more published observations, seemed to be indicated. After
examining 43 species from 24 families of angiosperms, Cooper (1933) pro­
posed three tapetal groups;
3) plurinucleate cells.
legumes he examined.
1) uninucleate cells; 2) binucleate cells;
In group 1, Cooper listed the five species of
All were in the subfamily Papilionoideae.
Previously,
Maheshwari (1931) examined the mimosoid Albizia lebbek, which was
3
uninucleate at all stages. In the caesalpinloid Cassia didymobotrya,
however, Sethi (1930) reported tapetal cells with two to four nuclei.
Newman (1933, 1934) later reported a uninucleate tapeturn in Acacia
baileyana, an additional mimosoid.
Referring to these previous studies, particularly Cooper's classi­
fication of 1933, Newman (1934) commented, "It is interesting to find that
species of the Papilionaceae and Mimoseae are associated in group 1, while
a Caesalpineous species is in group 3, otherwise than might be expected
in view of the floral forms of these subfamilies."
A few other authors have commented specifically on the occurrence of
a constant tapetal nuclear number in the legume subfamilies. Dnyansagar
(1949, 1955) and Maheshwari (1950) both reported that the species of the
subfamily Mimosoideae which had been examined were uninucleate throughout
floral development.
According to Pantulu (1942), who summarized some of
the available information on papilionoid legumes, "Uninucleate tapetal
cells, therefore, appear to be a common feature of the Papilionaceae."
The first author, however, to actually suggest that the tapetal
nuclear number could be of systematic value was Tlxier (1965), who had
studied chromosome numbers and tapetal nuclear behavior in some legumes
from Vietnam and Laos.
He stated that, "According to the cytotaxonomic
plan, the number of nuclei in the tapetal cells and their change in nuclear
type and chromosome number may furnish a supplementary cytotaxonomic
character."
In addition to the above references, there are several others which
mention the tapetal nuclear number in legumes, usually very briefly and
4
superficially.
ly lacking.
In most studies, however, tapetal information is complete­
Of the approximately 600 genera and 13,500 species, less
than ten percent (51) of the genera and one percent (88) of the species
had been examined up to 1965.
Although a small sample, it did indicate
that the tapetal nuclear number might be of phylogenetic significance,
particularly at the subfamily level.
This study was undertaken with the primary objective of extending
observations on the tapetum in the three subfamilies.
The hypothesis
to be tested was that a multinucleate or binucleate tapetum is character­
istic of the Caesalpinioideae and a uninucleate tapetum of the Mimosoideae
and Papilionoideae.
5
LITERATURE REVIEW
Tapetal Classification
Goebel (1901) first established tapetal types based on tapetal be­
havior during pollen formation.
Although not the first to observe dif­
ferences in tapetal behavior, Goebel was the first to recognize the need
for classifying the different conditions which he and others had observed.
He defined two major tapetal types, plasmodial and secretion (secretory),
between which he admitted that there are a number of transitions.
According to him, in the plasmodial type (sometimes called the amoeboid
type—Pickett, 1916; Schnarf, 1923, 19 29; Davis, 1966; and many others) the
cell walls are disrupted and the protoplasm oozes out among the sporocytes
and developing spores to be utilized by the spores or pollen grains.
This type of tapetum, considered by Goebel to be typical of ferns,
Equisetum and the seed plants, had been observed in other plants by
earlier workers (Strasburger, 1882; Campbell, 1897, 1900; Caldwell, 1899;
Duggar, 1900).
In contrast, Goebel described cells of the secretory tapetum (glandular
type of some authors--Maheshwari, 1950; Hindmarsh, 1964; Davis, 1966;
others), as remaining in place and continuing to "excrete" soluble sub­
stances into the (anther) fluid until final dissolution at the time of
pollen maturity,
Goebel felt that this type of tapetum was restricted to
Selaginella, Lycopodium and Isoetes.
6
Hannig (1911) reviewed the previous literature on the plasmodial
tapetum.
Although he accepted the classification of Goebel, he intro­
duced the term "periplasmodium" to describe the actual protoplasmic mass.
It was not his intention to designate a new capetal type.
After Hannig's
review, however, many investigators adopted the term periplasmodium as
a new type instead of merely applying it to the protoplasmic mass.
Thus,
plasmodial tapetum and periplasmodial tapetum have become two different
types when they should be synonymous.
Tischler (1915) described a periplasmodium in the Commelinaceae
and also found it to be common in the Araceae and other families of the
monocotyledonous order Helobiales.
On the basis of these findings he
suggested that this type of tapetum was of systematic value in the mono­
cotyledons.
While he recognized that there were minor differences in
the appearance of the periplasmodium in different plants, he did not classi­
fy these subtypes.
Clausen (1927), mainly on the basis of the work of Tischler and
previous authors, who had examined a number of monocots, divided the plas­
modial tapetum, which he referred to as a periplasmodium, into four sub­
types, which differed from each other only in time of formation or number
of nuclei,
Juel (1915) examined a number of dicotyledons and concluded that the
secretory tapetum was not only more common in this group, but also in the
angiosperms in general.
Most recently, in a comprehensive review on angiosperm embryology
that also included information on tapetal types, Davis (1966) recognized
7
only the two original tapetal types of Goebel (1901), while admitting
that there might be intergrading subtypes.
She supported the conclusion
of Juel (1915) that the secretory tapeturn was more common. Of the 231
families for which she had information, 181 (mostly dicotyledons) re­
portedly had only the secretory type, 29 families had only a plasmodial
tapetum, and 21 fa'^tlies had both types represented.
A slightly different approach to tapetal classification was taken by
Cooper (1933).
Based on his own observations, which included mostly
dicotyledons, he proposed three groups of tapetal cells;
2) binucleate; 3) plurinucleate.
1) uninucleate;
He did not indicate whether the tapeta
were of the secretory or plasmodial type, but his observations were made
on cells from all stages of anther development, suggesting that they re­
mained intact during their entire development (i.e.,
cellular).
His
classification, based on nuclear number, deviates from those of previous
authors, but has merits that are discussed later.
Also based on tapetal nuclear characters is the classification of
Garrigues (1951).
He believed that it was necessary to compare the ploidy
level of tapetal cells rather than merely nuclear number.
He argued that
most tapetal cells were octoploid and could be divided into three groups;
1) cells with one 8n nucleus; 2) cells with two
nuclei; 3) a tapetum
composed of cells, some with an 8n nucleus, others with two 4n nuclei or
with four-2n nuclei. This classification has not received much recogni­
tion and is frequently untenable because one species may show all three
types, or various intermediates, depending on degree of endomitosis or
nuclear fusion (Carniel, 1952, 1963; D'Amato, 1952b).
8
In two extensive investigations on the anther tapeturn of angiosperms, Carniel (1952, 1963) proposed a phyletic scheme of the origin
of the various tapetal types and subtypes (Figure 1).
basic types, true periplasmodial and cellular.
He recognized two
The true periplasmodial
was equivalent to the plasmodial tapeturn of Goebel (1901).
A sharp dis­
tinction was made, however, between a true and a false periplasmodium.
The latter condition he did not consider a tapetal type, but rather a
tapetal stage resulting from the premature degeneration of a cellular
tapeturn.
Carniel considered his concept of a cellular tapeturn as equivalent
to Goebel's secretory tapeturn and divided it into two subtypes, uninucleate
and multinucleate.
Cooper (1933).
These subtypes are comparable to groups 1 and 3 of
Carniel further subdivided the multinucleate category
into two classes based on nuclear behavior.
In one class, the tapetal
cells remain in a permanent anaphase-like figure following raeiosis in
the pollen mother cells (PMCs).
In the other class, the tapetal nuclei
remain in a prophase or raetaphase-like
stage, referred to as "arrested
prophase".
Wunderlich (1954), who accepted Carniel's scheme, reported further on
the nuclear condition of tapetal cells.
She also presented a list of
those species in which the tapetal cells reportedly became secondarily
uninucleate by fusion or incomplete mitosis (see also Bonnet, 1912;
Cooper, 1933; Steil, 1935, 1950; Carniel, 1952, 1954, 1963).
9
With regard to the type of tapeturn in the Leguminosae, Davis (1966)
has said that most of the legumes have a secretory or cellular tapetum.
In the Caesalpinioideae, however, Venkatesh (1956b) reported and figured
a plasmodial tapetum in three species of Cassia.
Lens esculenta (Shukla,
1954) and Adenanthera pavonica (Dnyansagar, 1954b) were reported to have
intermediate tapetal conditions.
In Lens, the walls of the tapetal cells
dissolved, but the cellular contents did not wander among the microspores.
They formed instead a peripheral Plasmodium (periplasmodium). In Adenan­
thera, the cells retained their walls, but were separated one from another
and wandered among the microspores, which they continued to nourish.
Several investigators have mentioned, usually without figures or dis­
cussion, either a plasmodial or periplasmodial tapetum in other legumes
(Corti, 19461 Larson and Lewis, 1963; Chubirko, 1967). Most of these
latter reports are subject to some doubt, since the same species which
they describe as plasmodial or periplasmodial have been reported to be of
the secretory (cellular) type by other researchers.
In these cases, fur­
ther observations are necessary to clarify the matter, since as Carniel
(1952, 1963) suggested, a false periplasmodium can be formed by degenera­
tion of the cellular tapetum at any stage of development.
Tapetal Nuclear Number in the Leguminosae
As mentioned previously, tapetal classification based on nuclear
number (Cooper, 1933) has merit, at least in a few plant groups.
In the
Leguminosae, according to Wunderlich (1954), Davis (1966) and Dnyansagar
10
(1949, 1955), the tapeturn is uninucleate except for the subfamily Caesalpinioideae, which may be binucleate, multinucleate, or rarely uni­
nucleate.
Of the studies reported in the literature, most have been super­
ficial and unsupported by photographs, although some have shown drawings.
Only the more important papers concerned with the tapetum of legumes are
cited below.
A more complete list of species and investigators is given
in Appendix A, Charts 1, 2, and 3.
Mimosoideae
Of the approximately 45 genera and 2,100 species recognized, in
only 21 species of 13 genera is there any information on the tapetum.
The first report on number of nuclei per tapetal cell was by Maheshwari (1931), who found a consistently uninucleate tapetum throughout
anther development in Albizia lebbek.
Newman (1933, 1934), who reported
the same condition in Acacia baileyana, was the first to comment on differ­
ences in tapetal nuclear number in the family (see quote on p. 3).
One investigator has contributed most of the observations on the
tapetum in this subfamily (Dnyansagar, 1949, 1951a,b, 1952, 1954a,b, 1955,
1957, 1958). In describing the embryology of 12 species in 11 genera
(Appendix A, Chart 1), he reported the tapetum to be uninucleate in all
cases. Similar reports have been given by Singh and Shivapuri (1935),
Narasimhachar (1948, 1951) and Mulay and Dhami (1955).
Tixier (1965) examined nine species of mimosoid legumes, but he noted
tapetal nuclear behavior in only four taxa;
Leucaena glauca, Enterolobium
11
cyclocarputn. Mimosa invisa and Pithecolobium dulce.
All were reported
to be uninucleate.
This large subfamily, with approximately 125 genera and 2,100
species, has received the least attention with regard to the tapeturn.
In­
formation is available for only five genera and 22 species, of which 17
are in Cassia.
Sethi (1930), who examined Cassia didymobotrya, was the first in­
vestigator to report more than one nucleus per tapetal cell in a legume.
This species, as well as C, purpurea (Chose and Alagh, 1933) and C. tora
(Datta, 1934), contained two to four (occasionally six to seven) nuclei
per tapetal cell.
For almost twenty years there were no further reports, until Carniel
(1952) described tapetal cells in Cassia austrails and C. laevigata.
These
were mainly binucleate, but some tapetal cells were uninucleate (with a
distinctly larger nucleus), while others contained three or four nuclei.
Most of the species in this subfamily for which information is avail­
able were studied by Venkatesh (1956a, b, 1957), who reported on Cassia,
subgenera Fistula, Lasiorhegma and Senna.
Of the 13 species he examined
(Appendix A, Chart 2), all but those of the subgenus Lasiorhegma (C. absus,
C. kleinii, and C. mimosoides) were binucleate or trinucleate.
These
three species, considered highly specialized on the basis of other charac­
teristics (Bentham, 1871; Irwin, 1964), were uninucleate and possessed
a plasmodial (amoeboid) tapeturn.
12
Another exception to binucleate tapetal cells was reported by Tixier
^ (1965), who found only uninucleate cells in Poin ciana regia (Delonix
regia).
He showed drawings in which tapetal nuclei resembled prophase-
like images, but he did not mention the type of tapetum present.
The first photograph (and the only one known to me in this subfamily)
to show tapetal cells and tapetal nuclei was by Francini (1951), who
examined Ceratonia siliqua.
He reported binucleate tapetal cells, except
for a few rare uninucleate cells, which he said were the result of nuclear
fusion.
In Caesalpinia crista (Mukherjee and Thakur, 1959) and C. pulcherrima
(Tixier, 1965), the tapetal cells are reportedly binucleate. In the
latter species, Tixier also reported the appearance of raetaphase-like
images at the stage when the microsporocytes had completed meiosis. This
condition persisted until final dissolution of the tapetal cells,
Nair and Kahate (1961) examined Parkinsonia aculeata, which they
reported possessed a secretory tapetum with two to five nuclei per cell.
In a fine structure study on pollen wall development in this same species,
Larson and Lewis (1963) mentioned, but did not illustrate, a periplasmodial tapetum.
Neither did they mention the nuclear number of the
tapetal cells.
Papilionoideae
Although considerable research has been conducted in this largest
and most important subfamily (about 400 genera and 9,200 species), few
investigators have dealt with the tapetum.
There are published records
for only 45 species from 33 genera (Appendix A, Chart 3),
13
The first report on tapetal nuclear number in a papilionoid legume,
and also the first in any member of the Leguminosae, was by Castetter
(1925), who reported uninucleate tapetal cells in both annual and bi­
ennial varieties of Melilotus albus.
Shortly after, Latter (1926) and
Weinstein (1926) independently reported the same condition in Lathyrus
odoratus and Phaseolus vulgaris, respectively.
Of the 43 species of angiosperms examined by Cooper (1933), five
were papilionoid legumes (four species of Medicago and two varieties of
Melilotus albus).
The tapeturn was uninucleate in all during their de­
velopment.
There have been two somewhat dubious reports of binucleate tapetal
cells in this subfamily.
Cooper (1938) showed a drawing representing the
tapeturn of Pisum sativum with a cell in nuclear division; however, only
one division figure is present. Furthermore, it is uncertain whether this
division would give rise to a binucleate tapetal cell or merely a second
uninucleate tapetal cell.
lijima (1962) supposedly showed a binucleate
tapetal cell in Vicia faba, but the photograph is of such poor quality
that no conclusion can be drawn from it.
Carniel (1952) examined these
same two species, as well as a number of other papilionoid legumes (Carniel,
1954, 1963), and reported only uninucleate tapetal cells.
In a study of microsporogenesis in Glycine max cv. Biloxi, Nielsen
(1942) showed what seems to be the first photograph of tapetal cells in
a legume.
Even at the tetrad stage, the tapetal cells had only a single
nucleus per cell.
14
Pantulu (1942) reported uninucleate tapetal cells in Desmodium
gangeticum, Cyamopsis psoralioides and Tephrosia purpurea. He claimed
that this condition was "always" found in the Papilionoideae.
In a
more recent study, which included information on the tapetum in two
species of Desmodium, Buss, Galen and Lersten (1969) described, with the
aid of photographs, the development of a uninucleate cellular or secretory
tapetum.
Somatic Polyploidy
Somatic polyploidy is the multiple replication of chromosomal
material within a normally diploid cell.
Usually this is accomplished
by an increase in the number of nuclei, some or all of which may later
fuse, natural chromosome doubling or by an increase in the volume of
chromatin material within an intact nucleus of a nondividing cell.
At
least in higher plants, cells and tissues with quite varied degrees of
differentiation and function are polyploid (D'Amato, 1952a,b; Chiarugi,
1954; Tschermak-Woess, 1956).
The anther tapetum, according to Ranquini (1928) and Brown and Bertke
(1969), is virtually always polyploid.
Strasburger (1882) observed oc­
casional fusion of nuclei in the usually binucleate tapetal cells of
several members of the Liliaceae.
Since that time, there have been many
additional reports of fusion; also other processes which lead to poly­
ploidy in this tissue have been described (D'Amato, 1952b).
These
processes can be divided into three classes; 1) normal mitosis without
cytokinesis; 2) abortive mitosis and fusion of nuclei; 3) endoduplication
or supernumerary chromonemal reproduction.
15
Of these three classes, mitosis without cytokinesis, i.e., forma­
tion of binucleate or multinucleate cells, appears to be most common in
the tapetum of angiosperms (Wunderlich, 1954; Davis, 1966).
Various in­
vestigators have attempted to account for continued mitoses in the tapetum.
Davis (1961) suggested that they might be the result of a "sympathetic"
reaction to the onset of meiosis. Garrigues (1951) postulated the oc­
currence of an "excito-mitotique" substance emitted by the mother cells
during the course of reduction division.
So far, however, such a sub­
stance from the mother cells has not been found.
According to D'Amato (1952b, 1965), fusion of nuclei, lagging chromo­
somes and non-mitotic division of nuclei are frequent in ephemeral tissues
such as endosperm and tapetum.
In the late nineteenth century, amitosis
or interphase fission was described as occurring in the tapetum.
Strasburger (1882), however, after reexamining his material, concluded
that the figures he had earlier interpreted as amitotic were merely
closely appressed nuclei of regularly binucleate tapetal cells.
Even­
tually some of the nuclei fused to form one, or occasionally more than
one, large nucleus. Tischler (1906) reported nuclear disturbances such
as fragmentation and lobing of tapetal nuclei in various Ribes hybrids.
He also concluded that amitosis did not occur in the tapetum.
Still
later, other investigators found additional evidence of nuclear fusion
and incomplete division in the tapetal cells of a number of plants
(Winkler, 1906; Bonnet, 1912; Mascre and Thomas, 1930; Cooper, 1933;
Smith, 1933; Roever, 1935; Steil, 1935, 1950; Davis, 1961). A special
16
type of incomplete division, chromosome "stickiness", was described by
D'Amato (1947) and Battaglia (1949).
This often led to anaphase bridges
and eventually to restitution nuclei which were irregularly shaped and
polyploid.
The third class, endoduplication or supernumerary chromonemal
reproduction (Lorz, 1947), i.e., intranuclear growth through chromonemal
or chromosomal multiplication without visible nuclear division, is sub­
divided into three subclasses; a) polyteny; b) polysomaty; c) endomitosis,
including arrested mitosis.
In each of these processes, the chromosomal
material is somehow increased during interphase or early prophase without
any nuclear division.
Polyteny, although not yet reported in the tapeturn, has been dis­
covered in the ephemeral embryo suspensor cells in Phaseolus coccineus
and P. vulgaris (Nagl, 1962a, b, 1967, 1969). In this type of polyploidy
the chromatin strands of each chromosome are repeatedly duplicated, but
instead of separating they remain together, forming "giant" chromosomes
like those found in the well known salivary gland cells of certain members
of the insect order Diptera.
be as high as 4096.
The ploidy level in the suspensor cells may
As our knowledge increases, polyteny will probably
be found to occur in the tapeturn also.
The details of polysomaty are not understood, but it is believed
that during interphase or early prophase the chromatids of each chromosome
replicate twice for each mitotic cycle (Lorz, 1947; D'Amato, 1952b;
Brown and Bertke, 1969). This produces the so called "diplochromosomes"
17
or "quadruple chromosomes", four or eight chromatids joined side by side
(Witkus and Berger, 1947; Avanzi, 1950).
According to D'Amato (1965) and
Brown and Bertke (1969), this type of endopolyploidy regularly occurs in
tapetal cells of Spinacia, Cannabis and Allium.
Favarger (1944) also
reported paired chromosomes in tapetal cells of six members of the
Caryophyllaceae.
Brown and Stack (1968) reported that in Haplopappus
gracilis (2n=4) tapetal cells have 2n=8 and 2n=16 metaphase chromosomes
as they undergo the last two regular nuclear divisions.
The third subtype, endomitosis, appears from the literature to be
more common in the tapeturn than the preceding two subtypes.
This process
was first reported in water striders, the insect genus Gerris.
Geitler
(1939) described a series of stages, endoprophase to endotelophase, within
an intact nuclear membrane.
There were no strong metaphase contractions
and no anaphase spindles were formed to separate the chromosomes.
Eventu­
ally at telophase the chromosomes, which were still relatively long,
separated simply by "falling apart" and the nucleus, now with twice as
many chromosomes, was reconstituted and reverted to interphase.
With
each endomitotic division the chromosome number was doubled, but no
nuclear or cell division occurred.
Although Geitler is given credit for describing endomitosis, D'Amato
(1952b) pointed out that Winge (1917) had described much earlier a similar
series of mitotic stages in the tapetal nuclei of Humulus japonicus and
Atriplex littoralis.
Shortly after Geitler's discovery, two reports on endomitosis in
plants appeared (Witkus, 1945—Spinacia oleracea; Brown, 1949—Solanum
18
lycoperslcum).
According to these authors, the first division in the
tapetal nucleus was usually a normal mitosis. This nuclear division,
however, was not followed by cytokinesis; therefore, the cells became
binucleate.
Following this mitotic division, one or more endomitotic
divisions, described as of the Gerris type, occurred.
These gave rise
to binucleate tapetal cells with 8n or 16n nuclei.
Other investigators later reported endomitosis in tapetal cells of
various plant families (Avanzi, 1950; Berger, Witkus and Joseph, 1951;
Mechelke, 1952; Scarascia, 1952; Carniel, 1952, 1954, 1963; Steffen and
Landmann, 1958; Turala, 1958, 1963; Turala and Urbaéska-Worytkiewicz,
1964; others).
Some of these reports have been challenged, Carniel (1952), Geitler
(1953) and Tschermak-Woess (1956) denied that Witkus (1945), Brown (1949),
Avanzi (1950), Berger et al. (1951) and Scarascia (1952) had described
true endomitosis, since a regular mitotic division usually preceded the
so called endomitotic divisions.
Also, the chromosomes were more highly
contracted than "typical" endomitotic chromosomes, and occasionally there
were rudimentary, but defective, spindles. Furthermore, in Solanum
lycopersicum (Brown, 1949), the nuclear membrane and nucleolus both dis­
appeared during endomitosis,
Carniel, Geitler,and Tschermak-Woess inter­
preted the process instead as inhibited or arrested mitosis.
Carniel
(1952) claimed that the chromatin material was inhibited at prophase of
mitosis, and applied the term "prophasich gehemmte Mitose" (arrested
prophase).
19
Mechelke (1952) studied the tapeturn in Antirrhinum majus and several
mutant forms and described different degrees of inhibited mitosis.
Prior
to meiosis in the pollen mother cells, some of the tapetal nuclei under­
went a normal mitosis with unusually contracted chromosomes, which re­
sulted in binucleate cells.
During mitosis, these tapetal nuclei showed
various stages of arrested mitosis, from prophase to telophase, within
the intact nuclear membrane.
This suggested endomitosis, but rudimentary
non-functional spindles were present.
He occasionally observed chromo­
somes and nuclei which, because of their large size, were considered
highly polyploid.
These he attributed to a "Polymermitose" in which the
chromosomal material was replicated many times without any visible divi­
sion.
Carniel (1963) considers the "Polymermitose" to be equivalent with
his metaphase arrested mitosis, and not a case of polyteny.
In some plant tissues, including the tapetum, normal dividing chromo­
somes are invisible.
Often these nuclei contain heterochromatic bodies
which resemble diakinesis or metaphase chromosomes.
These heterochromatic
bodies, first described in roots, are usually referred to as "prochromo­
somes" (Overton, 1905) or "chromocenters" (Baccarini, 1908; Gregoire,
1931; Eichhorn, 1930, 1935),
Often there are as many as there are
chromosomes; however, they may be fewer than the somatic number (Turala,
1958, 1963),
Occasionally as a result of fusion of nuclei or internal
increase in the number of chromosomes, the number of chromocenters will
be greater than the somatic number.
Because of this number correlation,
some investigators have suggested that each chromosome is represented by
a heterochromatic region (Overton, 1905; Levan and Hauschka, 1953),
20
These two terms have been applied to the nuclear material of nondividing tapetal cells.
Most authors use the term chromocenter (Carniel,
1952, 1963; Turala, 1958, 1963; Turala and Urbanska-Worytkiewicz, 1964;
others); however, according to Brown and Bertke (1969), the term pro­
chromosome should apply when the number of chromocenters is the same as
the number of somatic chromosomes.
In Plantago
ovata (Stack and Brown,
1969) the prochromosomes, like the regular chromosomes, increased in
number, but always in exact multiples of the base number.
An increase in size or number of prochromosomes or chromocenters is
usually taken as evidence for endopolyploidy, particularly that due to
endomitosis (Turala, 1958; Carniel, 1952).
There are still differences of opinion as to the precise meaning of
the term endomitosis and what intranuclear phenomena are.
Even Geitler
(1953) admitted that endomitosis might be regarded as an arrested mitosis.
With respect to the processes leading to polyploidy in the tapetal
cells of the Leguminosae, mitosis without cytokinesis and endopolyploidy,
attributed to endomitosis, arrested prophase and polysoraaty, all have
been reported. So far, polyploidy by means of continued mitosis is known
only in the subfamily Caesalpinioideae,
Here, binucleate and multi­
nucleate tapetal cells have been reported in almost all of the genera and
species examined (Sethi, 1930; Chose and Alagh, 1933; Datta, 1934;
Francini, 1951; Carniel, 1952; Venkatesh, 1956a, 1957; Mukherjee and
Thakur, 1959; Nair and Kahate, 1961; Tixier, 1965),
Except for two
dubious reports (Cooper, 1938; lijima, 1962), the Mimosoideae and
21
Papilionoideae are always uninucleate (Pantulu, 1942; Dnyansager, 1949;
Maheshwari, 1950).
In these two subfamilies polyploidy, when present,
appears to be due to endomitosis, arrested prophase or polysomaty.
The only known reports of these types of endopolyploidy in legumes
are those by Carniel (1952, 1954, 1963) and Tixier (1965). Carniel
(1952) described arrested prophase in the binucleate tapetal cells of
Cassia australis and C, laevigata.
In both, the chromosomes were repre­
sented by large distinct chromocenters.
metaphase chromosomes.
These resembled late prophase or
Carniel also reported significant differences in
the size of tapetal cells and chromocenters.
From cytological measure­
ments he was able to determine that some of the nuclei were 4n, others 8n
and a few 16n.
Carniel (1952) reported endomitosis as occurring in the tapetal
cells of two representatives of the uninucleate Papilionoideae (Lupinus
polyphyllus and L. regalis).
Later (Carniel, 1954, 1963), he extended
observations on endomitosis to Lupinus angustifolius and Lathyrus vernus.
In all four species the nuclear volume was increased several times while
the number of chromocenters, most of which were prominent, remained con­
stant. In Lupinus angustifolius, the nuclear material was not in discrete
chromocenters.
It more nearly resembled an early prophase nucleus with
thin chromatin strands.
Buss et al. (1969) showed similar tapetal cells
in two species of Desmodium,
In Vicia faba (Carniel, 1952) the tapetal
nuclei contained distinct chromosomes which were like diplochromosomes
or quadruple chromosomes resulting from polysomaty.
22
The only other report of endomitotic activity in the tapeturn of
legumes is by Tixier (1965), who reported "...a tendency toward
endomitosis or polysomaty..in Enterolobium cyclocarpum, Pithecolobj-um
dulce, Mimosa invisa and Leucaena glauca (Mimosoideae). He did not
elaborate, but did comment that this condition was not observed in other
legumes.
He briefly described the formation of lobed nuclei, claimed to
be octoploid, in the binucleate tapetal cells of Caesalpinia pulcherrima.
He also showed drawings of tapetal nuclei of Delonix regia and £,
pulcherrima with distinct chromocenters.
Crystals in Tapetal Cells
Crystals in tapetal cells have only rarely been reported in the
literature, mostly in the Commelinaceae.
Mascre (1925), Maheshwari and
Singh (1934), Carniel (1952) and Yasui (1952) reported calcium oxalate
raphide crystals in the periplasmodial tapetum of Tradescantia virginiana.
Commelina benghalensis, Spironema fragrans and Tradescantia sp., re­
spectively.
In two studies on microsporogenesis in Tradescantia paludosa.
Walker (1957) and Walker and Dietrich (1961) showed, without any mention
or discussion, photographs (Figures 8-10, 12, 18, 24) of meiotic stages,
in which large needle-like structures could be seen.
These are probably
raphide crystals from the periplasmodial tapetal cells. The only other
reports of tapetal crystals are by Stejskal-Streit (1940), who described
small calcium oxalate crystals in the form of tetragonal pyramids, oc­
curring two to four per cell, in Salvia verticillata (Labiatae); and by
23
Buss et al. (1969), who described and showed photographs of small discoid
to rhomboid prismatic crystals in two species of Desmodium (Leguminosae).
Although not truly tapetal crystals, Heslop-Harrison (1963) reported
the accumulation of crystalline particles, visible in the light micro­
scope, within plastids in Cannabis tapetal cells.
These were thought
to be storage proteins, since they were partially mobilized as the tapeturn
degenerated. In addition to the above reports of crystals, there are a
few descriptions of non-crystalline tapetal inclusions (Latter, 1926;
Wunderlich, 1954).
24
MATERIALS AND METHODS
Plant Materials
The Leguminosae is the third largest family of flowering plants,
with approximately 600 genera and 13,500 specie^ divided into the sub­
families Mimosoideae, Caesalpinioideae and Papilionoideae.
In this study
the classification of Taubert (1894) was followed, except that in the
Caesalpinioideae, the tribes Kramerieae and Tounateae have been removed,
and in the Papilionoideae, the Swartzieae (Bentham and Hooker, 1865) and
Taubert*s subtribe Psoraliinae of the tribe Galegeae, now recognized as
a distinct tribe, the Psoraleae, have been added.
In order to supplement the rather small number of species locally
available, and to represent as many tribes and genera as possible, seeds
of many species from various sources (Appendix C) were obtained.
These
were planted in plastic pots in a greenhouse of the Department of Botany
and Plant Pathology at Iowa State University.
No attempt was made to con­
trol the prevailing light and temperature conditions. Preserved flower
buds generously supplied by various collectors (Appendix C) were also used.
Tapetal type, number of nuclei and other characteristics were observed
from materials which were prepared in the following manner.
^Hutchinson (1964), in the introduction to the order Leguminales,
gives the number of genera as about 570. However, the number of genera
listed for each subfamily in the text adds up to 690 and the number of
species approaches 18,000. These figures (Isely, 1969; personal com­
munication) are ..."probably moderately excessive." At the other extreme,
Taubert (1894) gives a conservative number of about 450 genera and about
9,000 species. The figures given here are therefore a compromise.
25
Microtechniques
Paraffin preparation
As the plants began to flower, inflorescences or individual flower
buds were fixed in the field or brought to the laboratory.
They were
placed in either CRAF III (Sass, 1958) or 10% acrolein (Feder and O'Brien,
1968), then aspirated until they sank.^
Following fixation for 24 hours,
the buds in CRAF III were dehydrated at room temperature using a tertiarybutyl alcohol (TBA) dehydration series (Sass, 1958), gradually infiltrated
with 61°C Tissuemat (three changes) and embedded in fresh Tissuemat,
Although CRAF III was usually a satisfactory fixative, the best re­
sults were obtained using the 10% acrolein solution (24 hours at 4°C)
with a modified Feder and O'Brien (1968) dehydration schedule. Dehydra­
tion was carried through n-butyl alcohol, after which the material was
transferred to 100% TBA at room temperature and then processed as given
above.
Sections were cut at 7 - 10 pm on a Spencer.AO "828" rotary micro­
tome using a steel knife.
The ribbons were floated on 1% formalin solution
over a thin layer of Haupt's adhesive (Johansen, 1940) on a glass slide.
The slide was then placed on a slide warmer until the ribbons were fully
expanded.
The excess formalin was then removed and the slides allowed to
dry overnight prior to staining.
2
Flower buds collected by Richard W. Pohl, Gerrit Davidse and Richard
Maxwell were preserved in Newcomer's fixative (Newcomer, 1953), Those fur­
nished by Duane Isely, Donald F. Galen, Nels R, Lersten, Don Windier and
Roberta Waddle were preserved in FAA (Appendix C), These materials were fur­
ther processed in the same manner as described for the CRAF fixed material.
26
Of the several stain combinations used, including Heidenhain's
iron-hematoxylin (Johansen, 1940), Johansen's safranin (Johansen, 1940)
and self-mordanted safranin (Gray and Pickle, 1956), Gray and Pickle's
safranin followed by fast green counters tain was best.
Slides affixed with paraffin sections were mounted permanently in
piccolyte,
A small lead weight was placed on the coverglass and the slide
was left on a slide drying plate for approximately 10 days or until dry.
Anther squashes
The preparation of stained paraffin sections is time consuming, and
considerable detail of tapetal cells is lost.
To determine tapeta1 nuclear
number and nuclear behavior in a large number of species, squashes were
made of whole anthers.
Individual anthers were removed from buds which had
been fixed in 10% acrolein and dehydrated in two changes ©f methyl cellosolve, They were placed in a drop of 45% propio-carmine stain on a slide,
A coverglass was added and the anther carefully "squashed" by gentle tap­
ping using the
tip of a dissecting needle.
To intensify the stain, the
slide was passed through the flame of an alcohol lamp (taking care not to
boil the stain) and then further "squashed" between two paper towels,
making certain that the pressure was applied uniformly on the coverglass.
Slides which contained suitable material were photographed immediately,
or made permanent by the freezing technique described by Bowen (1956), For
comparative reasons buds at or near the tetrad stage were selected.
27
Photographie Techniques
Photomicrographs were made on Kodak Panatomic-X 35mm film using a
Leitz Ortholux microscope fitted with an Orthomat camera.
Contrast was
enhanced by using a green (Wratten 58) photographic filter.
For the
photographic identification of crystals, both analyzer and polarizer
discs were used.
Developmental Studies
To follow tapetal cell ontogeny, representative species from each
subfamily were selected for developmental studies. Those selected were;
Desmanthus depressus (Mimosoideae), Cercis canadensis and Ghamaecrista
fasciculata (Caesalpinioideae), Desmodium glutinosum, D. illinoense and
Psoralea tenax (Papilionoideae).
Desmanthus depressus was selected because it lacked compound pollen
grains or pollinia and because, unlike most other mimosoids examined, it
had tapetal cells that remained in arrested prophase. Cercis canadensis,
a locally abundant perennial tree, showed a typical tapeturn (mostly
binucleate with only occasional multinucleate cells) and Ghamaecrista
fasciculata, a common herbaceous annual, showed an advanced character, a
uninucleate plasmodial tapeturn,
Psoralea tenax, a herbaceous perennial,
and the two species of Desmodium, both herbaceous perennials, were
selected to show the extremes of tapetal nuclear activity in this sub­
family and for the development of crystals in the tapetal cells.
28
OBSERVATIONS
3
Observations on tapetal type (cellular
or plasmodial), number oi
nuclei per cell, nuclear behavior and distribution, and morphology of
crystals in the tapetum were made on 167 species in 89 genera distributed
among the three subfamilies. For comparison, all observations were made
on tapetal cells at the late tetrad or microspore stage.
Earlier
(pretetrad) and later (pollen grain) stages, in some instances, are also
included. These observations, with similar information from the litera­
ture where available, are summarized in Appendix A, Charts 1, 2, and 3.
Tapetal Types in the Leguminosae
All species examined in the Mimosoideae and Papilionoideae, and all
but six species in the Caesalpinioideae, possessed a cellular (secretory
or glandular tapetum which remained intact until the microspore stage,
or sometimes even until after pollen formation.
After that time the
tapetum rapidly degenerated. In the remaining six caesalpinioid species
(four of Cassia and two of Chamaecrista^) the tapetal cells appeared to
lose their walls sometime
during the sporogenous or early sporocyte
stage and separated from each other to form a Plasmodium (periplasmodium)
or amoeboid mass, which oozed among the developing microspores (Figures
52-60).
^Based on Carniel (1952), I consider the cellular tapetum to be syn­
onymous with the secretory tapetum. This term also indicates the major
difference between this type of tapetum and the plasmodial tapetum,
^Chamaecrista is sometimes considered merely a section within Cassia.
I consider it as a separate genus, based on a treatment by Isely (1958).
29
Tapetal Nuclear Number and Nuclear Behavior
With regard to number of nuclei in tapetal cells, the species of
Mimosoideae and Papilionoideae examined were all uninucleate, while the
Caesalpinioideae, with some exceptions discussed below, were always binucleate or multinucleate.
Concerning the nuclear behavior, I observed
that some tapetal cells had nuclei which were sometimes two or more times
larger than the rest.
Also, in some species, particularly those with uni­
nucleate tapetal cells, the nuclear material was represented by chromocenters instead of chromosomes. In other species, the nuclei lacked
chromocenters.
Such cytological phenomena, according to some investi­
gators (Carniel, 1952; Turala, 1958, 1963), are often associated with
endopolyploidy.
Because these were incidental to the main study and be­
cause I did not conduct spectrophotometrie or other volumetric measure­
ments on the nuclei, the interpretations given here are based strictly
on visual observations.
Because there is disagreement among cytologists on what nuclear
phenomena properly constitute the endomitotic processes, I have chosen to
recognize three levels of activity based upon the appearance of the tapetal
nuclei:
interphase, early prophase and late prophase.
Interphase nuclei—the nucleus, which may be either lightly or
darkly stained, does not show any sign of
organized chromocenters or chromonemal strands
(Figures 95, 96, 114, 122).
Early prophase nuclei--the nucleus shows evident chromonemal
strands interconnecting prophase-like chromatin,
which is usually associated with the nuclear
membrane (Figures 34, 35, 46, 77, 124, 153).
30
Late prophase nuclei—the nucleus exhibits distinct chromocenters
which resemble diakinesis or raetaphase
chromosomes. Nucleoli may or may not be visi­
ble (Figures 5, 6, 8, 9, 31, 105, 144-151,
186, others).
Mimosoideae
This subfamily, with about 45 genera and 2,100 species, is dis­
tributed mainly in the tropics and subtropics of the southern hemisphere.
This limited my investigation to seven genera and 16 species.
These
represented, however, four of the six tribes recognized by Taubert (1894).
The tapeturn is always uniseriate and no differences between the inner and
outer tapeturn, like those described by Periasamy and Swamy (1966), were
observed.
In all taxa examined (Appendix A, Chart 1), there was
only a
single nucleus per tapetal cell. This agreed with all published reports.
To determine if a uninucleate tapeturn was constant throughout de­
velopment or merely the result of nuclear fusion, I traced the critical
stages in Desmanthus depressus, an herbaceous annual. I was unable to
determine the ontogenetic origin of the wall layers, but by the microsporocyte stage there are three wall layers external to the tapetum,
which has been enlarging (Figure 2).
Two rows of six to 12 pollen mother
cells (PMCs) are produced in each locule (Figures 2, 3). In sectioned
locules, the tapetal nuclei often stain so densely that much of the detail
is obscured.
In smear preparations at the sporocyte stage (Figures 4, 5),
however, tapetal cells with a single nucleus and prominent chromocenters
are obvious.
The chromocenters remain until after the tetrads and in­
dividual microspores are released from their surrounding callose sheaths
31
(Figures 6, 8, 9). This peculiar nuclear behavior, interpreted as late
prophase, is similar to the "arrested prophase" described by Carniel
(1952) for Cassia australls and C, laevigata or the chromocenters of the
endomitotic nuclei of Lupinus po'lyphyllus, L. regalis and Lathyrus vernus
(Carniel, 1952, 1954),
Microspore nuclei did not display similar chromo­
somal behavior.
Following meiosis II the microspores separated, became vacuolate
and underwent mitosis to form two-celled pollen grains (Figure 10).
The
tapetum, although near collapse, remained until after pollen was fully
engorged with food reserves (Figure 11). Finally it disappeared completely.
The development of pollen and tapetum in Desmanthus depressus, with the
exception of chromocenters in the nuclei, was similar to that described
in the uninucleate papilionoid genus Desmodium (Buss et al., 1969).
The tapetum in Desmanthus is, therefore, a good example of a cellular
type of tapetum.
Although a uninucleate tapetum was constant in this
subfamily,
other differences in the tapetum and in microspore formation were noted.
One point of interest was the occurrence in Prosopis juliflora of occasional
tapetal septa which bisected the locule (Figure 12),
Similar tapetal
septa in other Leguminosae have previously been described only in one
other mimosoid, Dichrostachys cinerea (Dnyansagar, 1954a), and in three
papilionoid species, Lathyrus odoratus (Latter, 1926), Desmodium glutinosum
and D, illinoenae (Buss et al., 1969).
With regard to nuclear behavior in tapetal cells, Desmanthus depressus,
D. illinoensis and Schrankia uncinata were the only species which had
32
tapetal nuclei at late prophase.
Except for Calliandra confusa and Mimosa
sp., the remaining taxa had tapetal nuclei which remained at an early
prophase stage (Figures 12, 14-17).
Other than the late prophase nuclei,
no evidence for endopolyploidy was observed.
Another difference observed was the occurrence of separate pollen
grains in Desmanthus depressus (Figure 11), D. illinoensis and Prosopis
juliflora (Figure 13).
All of the remaining species examined had com­
pound pollen grains or pollinia made up of varying numbers of microspores
(four, eight or 16).
Schrankia uncinata. Mimosa pigra, M. pudica and M.
had pollinia with only four microspores (tetrads).
In M. pudica, in addi­
tion to only four microspores, the tapetal cells were substantially larger
than individual microspores or entire pollinia and contained large prom­
inent vacuoles (Figure 14).
Acacia, Albizia and Calliandra pollinia con­
tained either eight or 16 microspores, depending on the number of PMCs
included in the locule or the number grouped together prior to meiosis.
In Albizia julibrissin the PMCs are in tetrads (Figure 15); following
meiosis a polyad of 16 microspores was produced.
in Figure 16.
Ten of these are shown
Similar polyads were observed in three species of Calliandra,
while a fourth species, C. eriophylla, produced only eight microspores
(octad). In Albizia and Calliandra, the tapetal cells usually were smaller
than the adjacent microspores. In the three species of Acacia, all with
polyads, the tapetal cells varied in size, but in general were about the
same size as the microspores.
Two tapetal cells and two of the 16 micro­
spores (these were separated by squashing) are shown in Acacia sp.
33
(Figure 17), The most striking characteristic of this plant was the oc­
currence of crystals in the tapetal cells, the only mimosoid known to
possess them, either from personal observation or from the literature,
Caesalpinioideae
This subfamily, with about 125 genera and 2,100 species, also occurs
mainly in the tropics and subtropics.
Representatives of a few genera
(Cercis, Ghamaecrista, Gleditsia and Gymnocladus), however, occur in Iowa,
A total of 12 genera and 25 species were examined (Appendix A, Chart 2),
As noted previously (p, 28), both cellular and plasmodial tapeta
occur in this subfamily.
most frequent.
The cellular tapetum, however, is by far the
Only six highly advanced herbaceous species had a plasmodial
tapetum; these are discussed on pp. 38-39,
Based on the,most frequent .
number of nuclei per tapetal cell, three levels of the cellular tapetum
were recognized;
binucleate, multinucleate and uninucleate.
The tapetal cells in most members of this subfamily are binucleate,
but occasional multinucleate or uninucleate cells occur along with them.
To determine when the tapetal cells became binucleate and whether they
continued to divide during the meiotic cycle, I traced tapetal development
in redbud, Cercis canadensis. Although I examined many anthers, I was
not able to determine the exact time of division.
However, shortly after
tapetal cells and sporocytes could be distinguished, many tapetal cells
were already binucleate (Figure 18),
At this time there were three or
four wall layers external to the tapetum (Figures 21, 23),
The anthers of Cercis are many times larger than those of Desmanthus
34
and contain numerous rows of PMCs (Figures 18, 21-23).
In a smear
preparation at diakinesis (Figure 19), a tapetal cell is seen with two
relatively large nuclei, each containing several darkly stained prominent
nucleoli, not chromocenters, which persist throughout tapetal cell dif­
ferentiation.
As the PMCs undergo meiosis, some tapetal cells also at­
tempt further mitotic division (Figure 20).
No further divisions in the
tapetal cells occurred after meiosis II. Cytokinesis in these cells is
inhibited so that the tapetal cells contain two or occasionally more nuclei.
Sections of anthers at different stages of meiosis II (Figures 21-23)
do not reveal any changes in the tapetum.
At the tetrad stage (Figure 23)
the endothecium is filled with dark staining material, possibly tannin.
In a smear preparation at about this same stage (Figure 24), the tapetal
cells are densely granular and appear to be uninucleate. This condition
is brought about by the peculiar crowding of the nuclei, which show only
light staining threads of chromonemata and large nucleoli, some of which
may be the product of earlier nucleolar fusions.
Each tapetal cell, how­
ever, contains two or more nuclei (Figure 25, arrows) which also may later
fuse.
Even at the late microspore stage (Figure 26), the tapetal cells
with four to nine nucleoli are intact.
These nuclei appear to be in a
very early prophase stage, which is maintained until the tapetum finally
disappears.
Similar tapetal cells, that is, bi- to multinucleate with early
prophase nuclei, were observed in Bauhinia variegata, Gleditsia triacanthos,
Gymnocladus dioica and Parkinsonia aculeata.
Larson and Lewis (1963)
35
reported a periplasmodial tapeturn in Parkinsonia aculeata.
Contrary to
this report, I observed throughout anther development, a cellular bito multinucleate tapetum.
In Gleditsia triacanthos many, if not all, of the tapetal cells were
binucleate by early sporocyte stage (Figure 27),
Occasional cells had
more than two nuclei (Figure 27, arrows). Throughout the remainder of
meiosis and until after microspore release (Figures 28-30), the tapetal
cells showed distinct nuclei.
At the microspore stage (Figure 30) there
are two nuclei per cell, but the number of nucleoli has been reduced and
only minimal evidence of chromonemata exists. This stage corresponds then
to early prophase.
In Cassia bonariensis (Figure 31) the tapetal cells are mostly bi­
nucleate and each nucleus contains many small chromocenters (late pro­
phase),
Occasionally a tapetal cell has only one nucleus, but with a
volume of nuclear material comparable to those with two nuclei (Figure
31, lower right).
This may be due to fusion of two nuclei, although no
actual fusions were observed,or to inhibited division of this nucleus.
The upper cell resembles the so called endotelophase of Brown (1949),
Somewhat similar nuclei were observed in Cassia artemisioides (Fig­
ures 32-34) and C,
11225 (Figure 35), except that the nuclear material
was not organized into distinct chromocenters.
Rather, it was loosely
arranged, like the chromatin of an early prophase nucleus.
An enlargement
of a single tapetal cell of C, artemisioides (Figure 34) reveals two
nuclei which are slightly irregular and which may eventually "bud off"
36
to become three or more nuclei. The nuclei of C. s£. 11225 (Figure 35)
are even more extremely lobed; although each cell is basically "binucleate" the nuclei are in contact with each other.
It is not known
whether these nuclei are fusing or whether they are separating.
This
nuclear configuration resembles the fusion nucleus figured by Mechelke
(1952, Figure 39) in Antirrhinum.
The tapetal cells of Caesalpinia pulcherrima were unusual in their
early development.
Instead of dividing prior to meiosis, the tapetal
cells remained uninucleate until approximately the beginning of meiosis
or even until later (Figures 36, 37),
They rapidly completed one or more
nuclear divisions to become binucleate or multinucleate (Figures 38-39).
By the microspore stage, the tapetal nuclei appeared completely normal,
i.e., in prophase with small chromocenters (Figure 40). Two other
species, C. gilliesii and C. eriostachys, were similar in tapetal charac­
teristics.
Some species examined had tapetal cells which were mainly multi­
nucleate.
The most interesting of these was Hoffmanseggia jamesii, a
common weedy herbaceous species of the deserts of the southwestern United
States.
Although I was not able to determine when the first division oc­
curred in the tapetal cells, many of them were already binucleate or even
multinucleate by the PMC stage (Figure 41, arrows).
This figure also
shows a tapetal nucleus which has only recently undergone karyokinesis.
In an enlargement of tapetal cells similar to those of Figure 41, the
nuclei appear to be "budding" or "pinching" off (Figure 42). Between
37
the sporocyte stage and microspore stage, additional divisions or
"nuclear buds" may occur, resulting in a large number of nuclei in some
tapetal cells (Figures 43, 45), while adjacent tapetal cells have only
two or three nuclei (Figure 44). The tapetal cells still are intact
even at the late microspore or early pollen grain stage. The maximum
number of nuclei observed in this species was eight, but seven was more
common (Figures 43, 45).
In Brownea sp., a tropical species, from two to eight .nuclei were
also observed.
Figure 46 shows a tapetal cell with five small nuclei
and an adjacent tapetal cell with only one large nucleus.
These two
species so far represent the maximum number of nuclei known in the sub­
family.
Although most frequently the tapetal cells in the cellular Caesalpinioideae are bi- to multinucleate, occasional uninucleate tapetal cells
occur.
Thus far, however, there has been only one report in which the
tapetum was cellular throughout development and entirely uninucleate.
Tixier (1965), who examined Delonix regia, noted this seemingly rare
condition.
He did not elaborate, except to mention that this differed
from Caesalpinia pulcherrima, which was constantly binucleate, I re­
examined Delonix regia to determine if the tapetum was uninucleate and
if so, whether it might be associated with a plasmodial tapetum,
A portion of a longitudinal section of a locule of Delonix regia
at the microsporocyte stage (Figure 47) shows a cellular tapetum with
rather long, rectangular uninucleate tapetal cells at right angles to the
locule.
At the end of each locule and along the outer walls, particularly
38
at the center, two or occasionally three rows of tapetal cells, which
vary in size, are present (Figure 48). In smear preparations at the
tetrad stage (Figures 49, 50) mainly uninucleate tapetal cells are present.
The capacity of tapetal cells to undergo further division has not been
entirely lost, because occasional cells show t\:o nuclei (Figure 49,
small arrows).
In a cross section .(Figure 51), differences in tapetum
thickness and cell size are shown.
ginning to disperse.
This figure also shows callose be­
No nuclear divisions occurred after this stage.
The only report of a plasmodial uninucleate^ tapetum in the
Caesalpinioideae (Venkatesh, 1956b) was in three species of Cassia, sub­
genus Laslorhegma (£, absus, £, kleinii and £. mimosoides), Prior to
meiosis the tapetum was cellular and uninucleate, but as the pollen mother
cells underwent meiosis, the tapetum became plasmodial and surrounded
the tetrads.
The Plasmodium persisted until the pollen grains had rounded
off, then was completely absorbed.
I observed a similar plasmodial tapetum in the following species;
Cassia leptadenia, C, mimosoides, C. s£, 1353, C. sp, 11222, Chamaecrista
fasciculata and £. stenocarpa.
Of these six species, Chamaecrista
fasciculata (Figures 52-57) and Cassia mimosoides (Figures 58-60) re­
ceived the most attention.
The time of plasmodial formation in £, fasciculata differed from that
reported by Venkatesh (1956b).
When the tapetum first became distinguish-
Plasmodium by definition infers a coenocytic or multinucleate con­
dition. As applied here, the tapetum was uninucleate prior to structural
modification. Since divisions were not observed, it is assumed that the
cellular fragments remain uninucleate.
39
able it was cellular and uninucleate.
Later, as the tapetal cells en­
larged, the walls seemingly became modified so that by the sporocyte
stage the tape turn lost its shape and formed a Plasmodium which surrounded
the sporocytes (Figure 52). At this stage the Plasmodium was very vacu­
olate. In sectioned material, individual cells were not distinguishable,
so the tapetum appeared coenocytic.
However, in a smear preparation just
prior to diakinesis, cells with only one nucleus were seen (Figure 53).
As meiosis continued, the tapetum became even more fragile and the nuclei
became scattered throughout the tapetal mass (Figure 54).
In a cross
section of a locule at the tetrad stage, the Plasmodium can be seen both
externally and internally to the microspore tetrads (Figure 55). Even
after this stage, the Plasmodium occasionally showed cellular fragments
(cells), some of which contained nuclei (Figure 56).
Following the re­
lease of the microspores, the Plasmodium was still present, but showed
signs of degeneration.
The nuclei were prominent and exhibited chromo-
centers similar to those shown in Desmanthus depressus (Figures 6, 8, 9).
No divisions in the tapetal nuclei of either species of Chamaecrista were
observed.
The plasmodial tapetum in Cassia mimosoides was more fragile than the
tapetum in Chamaecrista fasciculata.
was more of a "soup" (Figure 58).
By the tetrad stage, the Plasmodium
Portions of the Plasmodium occasionally
showed distinct but scattered nuclei, some of which contained smàll
chromocenters (Figure 59).
Finally, at the pollen grain stage, there
were only remnants, mainly nuclei of the Plasmodium (Figure 60).
40
Except for a single very inconclusive electron micrograph of a re­
portedly periplasmodial tapetum in Parkinsonia aculeata (Larson and Lewis
1963), Figures 52-60 are the first photographs of a Plasmodium in a
legume.
From the squash technique it appears that until the tetrad stage
the Plasmodium is more or less cellular and not jusL a free protoplasmic
mass,
Papilionoideae
This subfamily, with about 400 genera and 9,200 species, is world
wide in distribution.
Moreover, many genera and species occur in the tem­
perate regions of the United States, thus they are readily available.
Seventy genera and 126 species were examined (Appendix A, Chart 3). They
represented 10 of the 12 generally recognized tribes.
Only the Dalbergieae
and Swartzieae were unavailable.
The tapetum in all species was of the cellular type, uniseriate and
constantly uninucleate.
cells were observed.
No differences between the inner and outer tapetal
The major variable characteristics were tapetal cell
size, nuclear behavior and the presence or absence of crystals.
These
differences, however, were not restricted to any particular taxon.
To avoid too frequent repetition of information, only selected mem­
bers of each tribe, beginning with the Hedysareae, are described here.
More complete tapetal information on these and the remaining species, in­
cluding citation of all photographic figures, is listed in Appendix A,
Chart 3.
41
Hedysareae
Desmodium glutinosum and D, illinoense were selected
as representative of cellular tapetal development for the entire sub­
family. The development of the tapeturn and pollen as previously re­
ported by Buss et al. (1969) is here repeated with only minor modifica­
tions.
Although I examined many anthers, I was unable to determine the
ontogenetic origin of the cell layers surrounding the sporogenous tissue.
When sporogenous cells became defined, there were three external cell
layers present (Figure 61), After the tapetum began to enlarge, two or
occasionally three, parietal layers were present between the tapetum and
the epidermis (Figure 62).
As in some mimosoids and most caesalpinioids
described previously, the tapetal cells were often irregular in shape and
of many sizes (Figures 63, 64, 77).
Only 12-24 PMCs, occurring in two
rows of 6-12 cells, are produced in each of the anther locules (Figures
61-64, 187, 188).
Occasional locules were bisected by a transverse tapetal septum
(Figures 64, 65), similar to the septum described in Prosopis juliflora
(Figure 12) and several other legumes,
Callose is secreted by each PMC beginning prior to meiotic prophase.
However, it is not secreted uniformly, so that many, perhaps all, PMCs
remain in physical contact during meiosis I.
During early prophase I
(Figure 65) the PMCs all appear to be connected, except where the locule
is bisected by a transverse septum (Figure 65). By metaphase I more
callose appears to have been secreted, although all PMCs are still
42
associated through broad connections (Figure 66). By anaphase I (Figure
67, right locule) contacts between PMCs are less noticeable.
After
meiosis I contact is restricted to pairs or trios of PMCs (Figure 68), and
following meiosis II (Figure 69) each young tetrad is completely isolated
by its callose sheath.
Cytokinesis within tetrads is by furrowing (Figures 70-72).
Occasion­
al delicate cytoplasmic strands still join the separating microspores
(Figure 71), suggesting that the microspores are actually "pulled apart".
After cytokinesis each microspore and each tetrad is surrounded by
callose (Figures 72, 73), identified from anther squashes and paraffin
sections according to the callose-aniline blue-fluorescence method (Jensen,
1962),
Usually callose of the tetrad and of the individual microspores
fluoresces, but under partial fluorescence (Figure 82) the walls of the
adjacent tapetal cells also appear bright.
However, under complete
fluorescence only the callose surrounding the tetrads and microspores ap­
pears bright (Figure 83),
Microspores are released into the locule by dissolution and dispersal
(Figure 74) and final loss of the callose (Figure 75), After callose
dissolution, tapetal cells were still intact, but separated readily from
each other (Figure 76),
A squash preparation at this stage showed that
the tapetal cells were still quite variable in size and shape; they ap­
peared to have no cell wall (Figure 77), The loss of the wall, however,
has not been confirmed.
At the vacuolate pollen grain (2-celled) stage the tapeturn, while
still present, appeared to be near collapse (Figure 78),
A paraffin
43
section from another anther at a comparable stage shows intact tapetal
cells and three adjacent wall layers (Figure 81).
Even after the pollen
became engorged with food reserves (Figure 79) some tapetal cells remained.
Finally, as the endothscium developed its characteristic thickenings,
the tapeturn disappeared (Figure 80). Like Desmanthus, the tapetum in
Desmodium is another good example of a cellular (secretory or glandular)
type of tapetum.
Besides these two species of Desmodium, I observed tapetal charac­
teristics in another 12 genera and 24 species, some of which are repre­
sented in Figures 84-92. This included the common peanut, Arachis hypogaea,
which has been studied by many cytologists, all of whom have failed to
mention the tapetum. The tapetal cells in Arachis (Figure 89) and Adesmia
muricata (Figure 90) appear to be filled with food reserves which eventual­
ly disappear as the pollen grains are filled.
These two species, together
with Adesmia tenella, Alysicarpus longifolius (Figure 91) and Alysicarpus
vaginalis (Figure 92), possessed distinct chromocenters in their nuclei.
The remaining species were about equally divided between those having
interphase nuclei and those having early prophase nuclei. In general,
the tapetal cells in this tribe are as large as, or larger than, the
microspores. They remain intact until after the pollen grains become
filled with food reserves (Figure 92).
Galegeae
Previously, only eight genera and 10 species of this
very large tribe had been examined.
I examined 10 genera and 20 species,
Tapetal cells of some of these species are shown in Figures 93-105.
Stored
44
food was readily apparent in the tapetal cells of Astragalus cicer
(Figures 99-101), Galega officinalis (Figure 97), Indigofera pilosa
(Figure 104), Sesbania arabica (Figure 95) and Tephrosia incana (Figure
94). With regard to nuclear behavior, most of the species remained at
early prophase (Figures 99, 102).
Only two of the species, Biserrula
pelecinus (Figures 105, 193) and Indigofera pilosa (Figure 104) possessed
'chromocenters.
Occasional tapetal cells contained very large nuclei, sug­
gesting polyploidy as a result of intranuclear doubling (Figure 99).
Sophoreae and Podalyrieae
these two tribes.
There are no previous reports from
In the Sophoreae I examined Sophora japonica (Figures
106-108) and Cladrastis lutea (Figures 109-111). The tapetal cells were
very similar in all respects. In the Podalyrieae I examined Baptisia
leucantha, B. leucophaea leucophaea (Figures 112-114) and Thermopsis
montana.
Except for minor differences in nuclear behavior, the tapetal
cells of these two tribes were alike.
In the Sophoreae the nuclear
material is associated with the nuclear membrane and is not organized into
chromocenters (early prophase nuclei).
In the Podalyrieae, although the
nucleus is granular, there are no chromocenters and no chromonemata. The
nuclei in this tribe correspond to interphase nuclei (Figure 114). In
both tribes the tapetal cells were many times larger than the microspores
(Figures 108, 110, 111, 114).
Genisteae
examined.
Only five genera and eight species had previously been
Corti (1946) reported a plasraodial tape turn in Genista monosperma.
45
All of my observations in this tribe, eight species and six genera, in­
dicate only a cellular uninucleate tapetum (Figures 115-123).
Most of
the species examined had nuclei which corresponded to interphase of ac­
tivity (Figures 117, 121, 122).
In Lupinus elegans (Figure 119) there
were chromocenters similar to those reported by Carniel (1952, 1954).
Trifolieae
Previously, only three genera and seven species,
mainly in the genus Medicago, had been studied.
I examined six genera
and 10 species, including some of the same species studied by previous
investigators.
My observations on the tapetal cells confirmed previous
reports of a cellular uninucleate tapetum in this tribe (Figures 124-132).
I examined for the first time species of Ononis, Parochetus and Trigonella.
The tapetal nuclei in most species remained at early prophase (Figures
124, 126, 131). Tapetal nuclei in Ononis pubescens (Figure 129) approach
activity similar to late prophase.
Interphase nuclei were seen only in
Trifolium incarnatum (Figure 132).
Occasional nuclei in Parochetus communis
(Figure 131, lower right) were approximately twice as large as the sur­
rounding nuclei.
A most unusual tapetal characteristic observed in this tribe was the
occurrence of a yellow carotenoid substance, Pollenkitt (Pankow, 1958),
found throughout the cytoplasm in Ononis pubescens (Figures 127, 128) and
0. speciosa. It gave a granular appearance to the cytoplasm.
Pollenkitt
was observed only in freshly fixed material and disappeared when treated
with alcohol. It also disappeared as the pollen grains became engorged
and the exine thickened, suggesting that it is in some way associated with
the pollen grains.
46
Loteae
tribe.
Only two species had been examined previously in this
Hansen (1953) mentioned a cellular tapeturn in Lotus corniculatus,
but did not give the number of nuclei.
According to Chubirko (1967), the
tapeturn in Lotus corniculatus is uninucleate, but "pseudoplasmodial". The
tapetal cells reportedly become separated from the adjacent wall layers
and form a periplasmodium around the developing microspores,
I found, on
the contrary, that Lotus corniculatus had a typical cellular uninucleate
tapeturn which did not break down to form a Plasmodium (Figures 139, 140).
Besides L. corniculatus, I examined L, requieni, Anthyllis tetraphylla
(Figures 133, 134), Coronilla varia (Figures 135-138) and Securigera
securidaca (Figures 141, 196), The tapetal cells were comparatively
larger than the microspores with nuclei mainly at early prophase (Figures
136-138).
Psoraleae
There are no known reports in this tribe dealing with
the tapetum. I examined five genera and 15 species (Figures 142-159).
I traced, by means of anther squashes, tapetal nuclear development in
Psoralea tenax.
At the time when the PMCs are at zygotene of meiosis
(Figure 142), each tapetal nucleus shows heterochromatin appressed to the
nuclear membrane. This gradually condenses during the early stages of
meiosis (Figure 143) so that by the tetrad stage (Figure 144) there are
distinct chromocenters. These remain until the final dissolution of the
tapetal cells (Figures 145, 146).
Many other species in this tribe also
exhibited chromocenters (Figures 147-149, 150, 151).
Exceptions were Dalea
argyraea (Figures 154, 155), D, lagopus, Eysenhardtia polystachya,
Petalostemon candidum, P. purpureum (Figures 156, 157), Psoralea adscendens
47
and P. argophylla (Figures 152, 153). In the latter species, the nuclear
material with interconnecting chromonemata is organized like a prophase
nucleus. Tapetal nuclei in Amorpha canescens (Figures 158, 159). A
fruticosa and Dalea alopecuroides apparently remain at interphase.
Vicieae
Previous reports mentioning the tapeturn in members of
this tribe are available only from five genera and eight species.
Two
investigators, Cooper (1938) and lijima (1962), reported the occurrence
of binucleate tapetal cells in Pisum sativum and Vicia faba. respectively.
In my material, Cicer arietinum (Figure 165), Lathyrus nissolia (Figures
163, 164), L. odoratus. Lens culinaris, Vicia americana (Figure 162),
V. faba and V. monantha (Figures 160, 161), I did not find any evidence
for binucleate tapetal cells.
However, when tapetal cells were ruptured,
free nuclei were found next to other nuclei.
resemble a binucleate cell (Figure 164).
Such a situation may then
According to Shukla (1954),
the tapeturn in Lens esculenta is periplasmodial, and although the cells
lost their walls they did not wander among the microspores. In Lens
culinaris, as well as the other species cited, the tapeturn was cellular
and always intact.
I did not observe any abnormal tapetal cells.
The
nuclei in this tribe are usually large and densely staining, and, with
the exception of Cicer arietinum (Figure 165), the tapetal nuclei remain
at interphase.
Phaseoleae
Previous investigators had examined only seven genera
and seven species. I examined 18 genera and 30 species (Figures 166-186).
The size of the tapetal cells varied, but in general they were about the
48
same size as the microspores or pollen grains.
With regard to nuclear
behavior in this tribe, Centrosema pubescens (Figures 185, 186), C,
virginiana, Glycine max (Figure 184), Rhynchosia sp, (Figure 183), R.
tomentosa and Vigna unguiculata all possessed nuclei with prominent
chromocenters.
Abrus precatorius (Figure 171), Amphicarpa bracteata,
Apios americana (Figure 176), Cajanus cajan (Figures 169, 170), Clitoria
ternatea (Figure 166), Vigna cylindrica, V. racemosa and V, sesquipedalis
(Figure 173) had nuclei which remained at interphase.
The remainder of
the species examined exhibited early prophase nuclei (Figures 168, 174,
175, 177-182, 191). In Erythrina sp. there were marked differences in
size between several of the tapetal nuclei (Figures 177, 178).
Even
the nucleolus was approximately twice the regular size (Figure 178). In
Glycine max some tapetal cells contained enlarged nuclei with approxi­
mately twice as many chromocenters.
As stated previously, no volumetric
analyses were made on these nuclei, but visual observation suggests that
these enlarged nuclei are polyploid.
Dalbergieae and Swartzieae
No representatives of these tribes
have previously been studied and none were available for this investigation.
As a general point of observation, although I examined a large number
of tapetal cells, many under the oil immersion objective, I did not ob­
serve any Ubisch bodies or sporopollenin granules.
These structures, how­
ever, have been observed in other families (Davis, 1966) at the light
microscope level.
They either are too minute to be seen with the light
49
microscope or else they do not occur in this family.^
Tapetal Crystals
Except for occasional large distinctive prismatic crystals observed
in the anther connective of a few species, calcium oxalate crystals were
restricted to the tapetum.
Here they were observed in 84 out of 167
species and 52 out of 89 genera (Appendix A, Charts 1, 2, and 3).
The development of tapetal crystals was not followed in all species.
However, based on observations from representatives of each subfamily, I
was able to determine that the stages in crystal formation are essentially
the same in all three and are nearly identical to those described in
Desmodium (Buss et al., 1969). Therefore, the crystal development as
given for Desmodium is repeated here with only minor modifications.
Sections of young anthers of D. glutinosum and D. illinoense, before
meiosis and tapetal cell enlargement, were examined under polarized light.
At this stage (Figure 187) no crystals were seen.
As the tapetal cells
enlarged, small oval crystals appeared (Figure 188, arrows). The crystals
reached maximum size (about 9 jum in these two species) during prophase I
(Figure 189), thereafter remaining prominent until tapetal dissolution
(Figure 190).
The mature crystals were flat and prismatic with oval to
rhomboid or variously shaped faces (Figures 77, 189, 190). In sections
only certain tapetal cells seemed to have crystals (Figures 189, 190),
6
Observations from several electron micrographs of tapetal cells of
Desmodium glutinosum also reveal no Ubisch bodies.
50
but in squash preparations most tapetal cells, unless ruptured, contained
one or occasionally more crystals (Figure 77),
These crystals disappeared
when treated with concentrated nitric acid or concentrated hydrochloric
acid, but were unaffected by acetic acid.
Crystals are usually found in cytoplasmic vacuoles, but in my ma­
terial, due to the harsh treatment associated with fixation and the
preparation of tapetal squashes and sections, it was not always possible
to determine if the crystals were located in vacuoles or whether they were
found free in the cytoplasm.
Not all genera had the same size, shape or number of crystals per
tapetal cell.
In addition to the flat rhomboid or variously sided pris­
matic crystals (Figures 189-191), some were lens-shaped (Figures 138, 193),
others were large tetragonal prismatic crystals (Figure 194).
Occasion­
ally, tiny prismatic crystals were clustered together in two's or three's
(Figure 192) or scattered throughout the tapetal cell like crystal sand
(Figure 196).
One species, in addition to rhomboid crystals, had styloid
•prismatic crystals (Figures 49, 50, 195).
The distribution of tapetal crystals in the Leguminosae is sporadic
and is not confined to any taxon.
Only one of the 16 mimosoid legumes
examined. Acacia sp., had crystals.
They were small prismatic crystals
and occurred one or two per cell (Figure 17, tip of arrows).
It is not
known whether the lack of crystals is characteristic of this subfamily
or, as is more likely, the infrequent occurrence is due strictly to the
limited sample.
51
In the Caesalpinioideae, tapetal crystals occurred more frequently.
Of the 25 species examined, 13 contained crystals.
They included
Gleditsia triacanthos (Figures 27, 28, 30, arrows), Cassia artemisioides,
C. leptadenia, C. mimosoides (Figure 58), C.
11225 (Figure 35), C.
sp. 11244, Chamaecrista fasciculata (Figures 53, 54, 56, 57), £. stenocarpa,
Caesalpinia eriostachys, C. gilliesii, C. pulcherrima (Figure 39),
Cercidium microphyllum and Delonix regia (Figure 49-51), In Gleditsia
both lens-shaped and flattened rhomboid prismatic crystals occurred
(Figures 27, 28, 30). In others, Caesalpinia pulcherrima (Figure 39,
arrow), Chamaecrista fasciculata (Figure 54, 57, arrows) and Cassia
mimosoides (Figure 58, arrows), there were also tetragonal crystals.
Delonix regia, in addition to rhomboid crystals, had styloid prismatic
crystals (Figures 49, 50, 195). This is the first report of styloid
crystals in this subfamily (Metcalfe and Chalk, 1950).
In the Papilionoideae I observed crystals in 70 species from 45
genera (Appendix A, Chart 3). All ten of the tribes examined are repre­
sented.
In the Hedysareae, in addition to Desmodium glutinosum and D.
illinoense (Figures 77, 81, 188-190), crystals also were found in four
other species of this genus.
Each tapetal cell in Aeschynomene indiea had
one or more small clusters of prismatic crystals (Figure 152).
Similar
crystals occurred in Arachis hypogaea, Onobrychis crista-galli and
Stylosanthes sp.
In the Galegeae, crystals were found in eight of 10 genera and 13
of 20 species. These included Astragalus cicer (Figures100, 194),
52
A. crassicarpus, A. inflexus, Biserrula pelecinus (Figures 106, 193),
Galega officinalis, Indigofera echinata,
subulata, Olneya tesota
(Figure 103), Robinia pseudo-acacia, Sesbania arabica (Figure 95),
£. sesban,
sp. and Wisteria sinensis.
The most striking crystal shape
in this tribe was the tetragonal prismatic crystal.
This type was ob­
served in three species each of Astragalus and Sesbania and in Olneya
tesota.
The other members of this tribe had lens-shaped, irregular
prismatic or flattened rhomboid-shaped crystals.
All species examined in the tribes Sophoreae and Podalyrieae had
tapetal crystals.
In the Sophoreae solitary lens-shaped or irregular
prismatic crystals were observed in Sophora japonica (Figure 108, arrow)
and Cladrastis lutea (Figures 110, 111, arrow).
In the Podalyrieae,
Baptisia leucantha, B. leucophaea leucophaea (Figures 112, 113
arrows)
and Thermopsis montana had one to several scattered small prismatic
crystals per tapetal cell.
Only two of eight species in the Genisteae had tapetal crystals.
They were Crotalaria saltiana (Figure 116) and Lotononis bainesii (Fig­
ures 121, 123).
This sample is too small to make any conclusions con­
cerning the over all occurrence of crystals in the tribe.
In the Trifolieae, six of ten species possessed crystals.
Although
a small sample, it appears that crystals are of common occurrence in this
tribe.
They were found in Medicago sativa (Figure 124) and Melilotus
alba, two species that have been studied cytologically many times, without
any reports of tapetal crystals.
Besides these two species, crystals
53
were also found in Ononis mitissima, 0. pubescens (Figures 127, 128,
arrows), 0. speciosa and Parochetus communis (Figures 130, 131, arrows).
Most of these species had lens-shaped or small prismatic crystals.
Of the five species examined in the Loteae, only Coronilla varia
and Securigera securidaca had crystals.
In Coronilla the crystals are
lens-shaped and occur one per cell (Figures 135, 136, 138). In Securigera
there are many small prismatic crystals scattered throughout the cell
(Figures 141, 196).
Crystals were present in all five genera and 11 of the 15 species in
the Psoraleae.
They were found in Amorpha canescens (Figures 158, 159),
A. fruticosa, Dalea alopecuroides, D. argyraea (Figures 154, 155), D.
lagopus, Eysenhardtia polystachys, Petalostemon candidum, P. purpureum
(Figures 156, 157), Psoralea argophylla, P. dentata, P. tenax (Figure
146) and P. ££. The crystals were mainly rhomboid, although some lensshaped crystals were also observed.
rhomboid crystal.
Figure 146 shows a side view of a
Crystals occurred in most cells, but without polariza­
tion they did not always show up in photographs.
All four genera and seven species in the Vicieae had crystals.
These included Cicer arietinum, Lathyrus nissolia (Figures 163, 164),
L. odoratus. Lens culinaris. Vicia americana (Figure 162, arrows), V.
faba, and V. monantha (Figure 160 161).
tetragonal prismatic crystals occur.
Both small prismatic and
A tetragonal crystal, seen in
longitudinal view, is shown in Figure 162 (upper left).
The number of genera and species examined in the Phaseoleae was
i
1
54
greater than for the other tribes.
Of the 18 genera and 30 species
examined, 11 genera and 14 species had crystals.
following;
They included the
Amphicarpa bracteata, Cajanus cajan (Figures 169, 170,
arrows), Canavalia gladiata (Figure 175, arrows), Centrosema pubescens,
Dolichos biflorus, D. lablab (Figure 179, 180, 191), Glycine max, Mucuna
pruriens, Phaseolus coccineus (Figure 182, arrow), Pueraria thunbergiana
(Figure 167, arrow), Rhynchosia tomentosa, R, usambarensis (Figure 181,
arrow), R. S£, and Strophostyles umbellata (Figure 168, arrow). Lensshaped (Figures 170, 175, 181), small prisms (Figures 167, 182) and
rhomboid-shaped crystals (Figures 168, 169, 179, 180) were observed in
this tribe.
My observations on crystal shape in this family agree with those of
Pobequin (1943), who reported lens-shaped and prismatic crystals of the
trihydrate form in the vegetative tissues of this family, and Frey (1929),
who described the various shapes which the trihydrate form of calcium
oxalate can assume,
the tapetal cells.
Raphide and druse crystals were never observed in
55
DISCUSSION
The tapeturn in most angiosperm families has not been very extensively
investigated for taxonomic characteristics.
In this study of the three
subfamilies of the Leguminosae, the tapetum was surveyed specifically to
determine if certain tapetal characteristics could be of systematic value.
One of these characteristics, perhaps the most unusual, was the occur­
rence of calcium oxalate crystals. Comparatively little is known concern­
ing the factors which regulate the rate and mode of crystallization,
although they are usually considered to be by-products of metabolic activ­
ity, Furthermore, crystals ordinarily occur in long-lived tissues of
some roots, sterna and leaves. Their presence in tapetal cells, which
although active metabolically are only ephemeral, is puzzling and not
understood.
Although crystals seem to be rare in tapetal cells of most angiosperms, they are rather frequent in legumes, especially in the Caesalpinioideae and Papilionoideae.
Their infrequent occurrence in the Mimosoideae
may indicate that crystals are also rare in this subfamily.
However,
before valid conclusions can be made, a larger and more diverse sample
will be necessary.
Of the two basic crystal types, lens-like and prismatic, the latter
with its several shapes and sizes (tetragonal, flat rhomboid or with
various numbers of sides, small prismatic, styloid) was the most abundant.
One or more shapes were observed in each of the three subfamilies.
The occurrence of two or more crystal shapes within a single tapetal
cell or within a species suggests that crystal shape is not rigidly
56
determined. This is also supported by evidence that a specific crystal
shape is. usually not restricted to any one taxon.
One possible exception
is the occurrence of styloid prismatic crystals in the tapetal cells of
Delonix regia. This represents the only known report of such crystals
from any tissue in any member of the subfamily Caesalpinioideae, although
they are occasionally found in vegetative tissues of the other two sub­
families.
It also represents the only occurrence of styloid crystals in
this study.
Although not carried out in this study, shapes of crystals from the
tapetal cells need to be compared with those found in the rest of the
plant to determine if they are similar.
From this information distinct
lines of crystal evolution, similar to those reported for Allium (Chartschenko, 1933), may be possible.
In the Leguminosae, septate microsporangia, when present, have gener­
ally been restricted to mimosoid species with pollinia (Rosanoff, 1865;
Engler, 1876; Dnyansagar, 1954a). In this subfamily the septa, which
appear to be genetically fixed and linked with pollinia, may be of taxonomic value.
My observations on species known to possess pollinia were
mainly from squashes, therefore, I was not able to determine whether or
not septa were present.
Because of their similarity to the tapeturn, septa have been regarded
as nutritive (Periasamy and Swamy, 1959; others). Lersten (1971), who
has reviewed the literature on septate microsporangia in vascular plants,
challenges this nutritional view.
He suggests that septa are usually
derived from a sterilization of sporogenous tissue and are simply a
means of reducing the number of sporogenous cells, Lersten predicts
57
that future investigations will reveal septa to be common, particularly
in herbaceous animal-pollinated taxa.
It may be that they will be common
in highly specialized, small anthered papilionoid legumes.
At first it was thought that the patterns observed in tapetal nuclei,
i.e., interphase, early prophase and late prophase, might be character­
istic of certain taxa, and therefore of systematic value. Delay (1940),
who studied interphase nuclei in roots from approximately 40 species of
legumes, proposed a phylogenetic scheme to the tribal level based on the
type of nucleus.
Although she did not use the same terms employed in this
investigation, the behavior was about the same.
The Mimosoideae, Caesal-
pinioideae and the papilionoid tribes Genisteae and Phaseoleae were
reported to have non-reticulate nuclei with distinct chromocenters (late
prophase).
The other tribes had different degrees of reticulate or netted
nuclei with or without small chromocenters (interphase or early prophase).
Based on a much larger sample, my findings on behavior of tapetal
nuclei do not support Delay's conclusion that the type of nucleus is dis­
crete enough to distinguish between the tribes.
I found, on the contrary,
that the three types of nuclear behavior were more or less randomly dis­
tributed throughout the three subfamilies and were represented in most
tribes.
Nuclear behavior, therefore, does not appear to be of systematic
value.
Several additional points regarding nuclear behavior in tapetal cells
might be mentioned.
Brown and Bertke (1969) have suggested that all
tapetal cells increase their chromosomal material one way or another.
Some investigators have attributed part or all of this increase to endopolyploidy by endomltosis.
However, there is inconsistency in description
58
and considerable disagreement as to what constitutes endomitosis.
There­
fore, this entire area of nuclear behavior needs to be reviewed; and as
D'Amato (1954) pointed out, until the processes are better understood
cytologists need to remain openminded so that dogmatic statements do not
hinder the furthering of knowledge on endopolyploidy.
Before conclusions on intranuclear duplication, particularly in the
uninucleate tapetal cells of legumes, can be made, accurate spectrophoto­
metrie measurements will be necessary.
As determined in this investigation, the characteristics of most taxonomic significance are type of tapeturn and number of nuclei per cell.
In
the Leguminosae, the tapetum is cellular or exceptionally plasmodial.
Most reports of a plasmodial tapetum have been of tapetal cells which,
during meiosis or at the microspore stage, separated from the parietal
layer, underwent wall changes, and formed a peripheral periplasmodium.
Carniel (1952, 1963) regards this type of tapetum as either a false periplasmodial or an amoeboid tapetum, and cautions that it may result from
premature degeneration of a normally cellular tapetum.
A true periplas-
modial tapetum is produced prior to, or at the beginning of, meiosis and
is not just an occasional event.
My observations, some on species prev­
iously reported to be plasmodial, support Carniel and further indicate
that a plasmodial condition may result from various techniques employed
in fixation and preparation of the anther tissue.
Furthermore, different
environmental stresses may affect the condition of the anthers and
therefore the tapetum.
The only examples of a plasmodial tapetum which seem to be valid and
consistent are those by Venkatesh (1956b) and those described in this
59
investigation.
Thus far, this type is limited to herbaceous members of
the genera Cassia and Chamaecrista (Caesalpinioideae). Some investigators
(Irwin and Turner, 1960; others) consider these two as a single genus.
Cassia.
If so considered, those species with a plasmodial tapetum are in
the subgenus Lasiorhegma and mainly in section Chamaecrista.
However,
regardless of whether these are considered as one genus or two (footnote
4, p. 28), the occurrence of a plasmodial tapetum, which is always uni­
nucleate, seems to be a supplementary taxonomic characteristic in a sec­
tion of this subfamily.
Because the plasmodial (amoeboid) tapetum is characteristic of a few
lower vascular plants and of some "lower" monocotyledons and dicotyledons,
Eames (1961) considered it to be primitive.
However, evidence from
families such as the Magnoliaceae (Maneval, 1914; Reed, 1947), Winteraceae
(Sampson, 1963), Rosaceae (Cooper, 1933; others) and others (Wunderlich,
1954; Davis, 1966) considered by other characteristics to be among the
more primitive angiosperms, indicates that the cellular tapetum is more
common and primitive.
The widespread occurrence of the cellular tapetum
in the Leguminosae and the restricted occurrence of the plasmodial type
support this conclusion.
In addition to a cellular tapetum, the primitive families cited above
have binucleate to multinucleate tapetal cells.
In the Leguminosae, con­
sidered by most phylogenists, including Taubert (1894), Engler (1915),
Melchior (1964), Hutchinson (1964, 1969) and Leppik (1966), to be derived
from the Rosaceae, the tapetum is either constantly uninucleate or else
binucleate to multinucleate.
Based on available information, the binucleate
and multinucleate conditions occur only in the Caesalpinioideae.
The other
60
two subfamilies and several caesalpinioid exceptions, namely those species
with a plasmodial tapeturn and Delonix regia, are uninucleate.
Therefore,
with respect to nuclear number, the Caesalpinioideae is unique and seems
to be the most primitive of the three subfamilies.
This conclusion agrees with and seems to support evidence from floral
morphology.
The presumed primitive members of the Caesalpinioideae have
flowers most like those in the Rosaceae, particularly the subfamily Chrysobalanoideae which is unicarpellate and has both actinomorphic and zygomorphic flowers.
Although not as conclusive in indicating phylogeny,
chromosome numbers and seed morphology also support the view that the
caesalpinioids are the most primitive.
Based on these same criteria, there is general agreement that the
Caesalpinioideae and Papilionoideae are closely related, and that the
latter subfamily is derived.
Morphological connections between these two
subfamilies may be inferred from the way the tribe Swartzieae has been
treated,
Bentham and Hooker (1865) placed this tribe in the Papilionoideae,
while Taubert (1894) considered it to be allied with the Caesalpinioideae.
Turner and Fearing (1959), who studied chromosome numbers in these
two subfamilies, have suggested the Swartzieae as a possible connecting
link between them.
They reported a base number of x=8 in Swartzia and in
several of the older caesalpinioid tribes.
According to these authors,
this base number represents the original base number for the entire family.
The other base numbers x=7, 9, 10, 11, probably have arisen by aneuploid
loss or gain.
Senn (1938), in his chromosomal review of this family, concluded that
the Papilionoideae was derived from a primitive form or primitive forms of
61
8-chromosome legumes.
Corner (1951) and Isely (1955), in their investigations on seeds of
the Leguminosae, observed that there appeared to be only two basic seed
types: a mimosoid-caesalpinioid type and a papilionoid type.
Corner (1951)
and Kopooshian and Isely (1966) each studied species of Swartzia.
Accord­
ing to these authors the seeds were intermediate between the Caesalpinioideae and the Papilionoideae, and each had a different combination of
characters.
Because the Swartzieae seems to be intermediate in many characters
and primitive in others, an investigation of this tribe Would be desireable since it might reveal intermediates in nuclear number and help to
bridge the gap between the Caesalpinioideae and the Papilionoideae.
Tapetal characteristics have clearly been shown to be significant
in delimiting the Caesalpinioideae.
While the Papilionoideae and Mimo-
soideae both have a uninucleate tapetum, it is not possible to use this
at present to shed much light on the relationships between these two
otherwise morphologically distinct taxa.
62
SUMMARY
1. The tapeturn in 167 species from 89 genera representing the three
subfamilies was studied for tapetal type, number of nuclei, nuclear be­
havior and occurrence of calcium oxalate crystals.
2.
Except for six caesalpinioid species (four of Cassia and two of
Chamaecrlsta), the tapetum in the Leguminosae is cellular throughout devel­
opment.
In these species the tapetum is plasmodial.
3. The number of nuclei per tapetal cell will distinguish the Mimosoideae and Papilionoideae from the Caesalpinioideae.
Tapetal cells in
the latter subfamily, except for Delonix regia and those species with a
plasmodial tapetum, are binucleate or multinucleate. The other two sub­
families are always uninucleate.
4. The cellular tapetal type and the binucleate or multinucleate
tapetal condition are considered primitive to the cellular uninucleate
and the plasmodial types.
5.
Tapetal cells differ in size and shape; however, there are no
significant differences between the tapetal cells on the epidermal side
of the microsporangium and those on the connective side.
6.
Nuclei in the tapetal cells of many legumes contain chromocenters
resembling diakinesis or metaphase chromosomes.
In other species the
nuclei lack chromocenters, but resemble early prophase or interphase
nuclei. This nuclear behavior occurs in all three subfamilies and does
not appear to have systematic value.
This behavior may be associated
with endopolyploidy.
7.
Calcium oxalate lens-like or variously shaped prismatic crystals
63
occur in tapetal cells.
They are more frequent in the Papilionoideae
(70 of 126 species) and the Caesalpinioideae (13 of 25 species).
Only
one species out of 16 of the Mimosoideae, Acacia s£., had tapetal crystals.
The presently known distribution and shape of crystals in this family does
not permit their use in delimiting taxa.
8.
Styloid crystals, which have not been reported previously from
any cell type in the Caesalpinioideae, were found in Delonix regia.
9.
Occasional tapetal septa bisecting anther locules were observed
in the non-pollinial species, Prosopis juliflora, Desmodium glutinosum
and D, illinoense.
10. Ubisch bodies were not observed.
11. The tapeturn as a source of taxonomic characteristics is worthy
of continued investigation.
64
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très variedades de Cicer arietinuro L. y de sus hibridos. Agrociencia
1; 110-118. Original not available; cited in Biological Abstracts
51; 58473. 1970.
Larson, D. A, and C. W. Lewis, Jr. 1961. Fine structure of Parkinsonia
aculeata pollen. I. The pollen wall. American Journal of Botany 48;
934-943.
List, A. 1963. Some features of embryo and endosperm development in
Gleditsia triacanthos. American Journal of Botany 50; 622.
Martin, J. N. 1913. The physiology of pollen in Trifolium pratense.
Botanical Gazette 56; 112-126.
Martin, J. N. 1914. Comparative morphology of some Leguminosae.
Botanical Gazette 58; 154 -167.
Moggi, G. 1950. Embryologia ed embriogenesi in Cytisus laburnum.
Nuovo Giornale Botanico Italiano , Nuova Serie, 57; 186-209.
Mukherjee, S. K.
pulcherrima.
1952. Abnormal microsporocytes in Caesalpinia
Current Science 21; 290.
82
Oganesyan, R. A. 1966. Some data on the microsporogenesis and microgametogenesis in Pisum sativum (Translated title). Biologicheskii
Zhurnal Armenii 19; 59-63. Original not available; cited in
Biological Abstracts 48; 113598. 1967.
Pantulu, J. V. 1945, Studies in the Caesalpiniaceae. I. A contribu­
tion to the embryology of the genus Cassia. Journal of the Indian
Botanical Society 24; 10-24,
Pantulu, J, V. 1951, Studies in the Caesalplîdaceae, II, Development
of the endosperm and embryo in Cassia occidentalis. Journal of the
Indian Botanical Society 30; 95-99,
Paul, A. K. 1937. Development of ovule and embryo sac of Tamarindus
indica. Journal of the Indian Botanical Society 16; 151-157.
Paul, A. K. and R, M, Datta, 1950, The chromosome number and the de­
velopment of the embryo sac in Crotalaria intermedia. Science and
Culture 15; 280-281.
Pellegrini, 0. 1954, Ricerche embriologiche sulla famiglia delle
Caesalpiniaceae. Delpinoa 7; 138-160. Original not available; cited
in G, L. Davis, 1966. Systematic embryology of the angiosperms.
Pp. 68, John Wiley and Sons, New York, New York,
Poljakova, R. F, 1958. Development of the male gametophyte in Trifolium
pratense. I. Changes in the vegetative nucleus and formation of the
generative cell. Vestnik Leningradskogo Universitéta, Seriya Biologii,
3; 63-76.
Rao, V. S. and K, Sirdeshmukh, 1956, The floral anatomy of Delonix
regia. Journal of the University of Bombay 25; 35-44,
Rao, V, S,, K, Sirdeshmukh and M. G, Sardar, 1958, The floral anatomy
of Leguminosae, Journal of the University of Bombay 26; 65-138,
Rau, M, A. 1950. Development of the embryo in Trigonella foenum-graecum.
Journal of the Indian Botanical Society 29; 210-213.
Rau, M. A. 1951a. Development of the embryo in Aeschynomene indica.
New Phytologist 50; 124-126,
Rau, M, A. 1951b.
Papilionaceae.
Development of the embryo in certain members of the
Phytomorphology 1; 80-86,
Rau, M, A, 1954, The development of the embryo of Cyamopsis, Desmodium,
and Lespedeza, with a discussion on the position of the Papilionaceae
in the system of embryogenic classification, Phytomorphology 4; 418430,
83
Reed, E. L, 1924, Anatomy, embryology and ecology of Arachis hypogaea.
Botanical Gazette 78: 289-310.
Romm, J. H, 1952. The development and structure of the vegetative and
reproductive organs of Kudzu, Pueraria thunbergiana (Sieb. and Zucc,)
Benth. Iowa State Journal of Science 27: 407-419.
Rosanoff, S. 1865. Zur Kenntniss des Baues und der Entwickelungsgeschichte
des Pollens der Mimoseae. JahrbUcher fUr Wissenschaftliche Botanik 4:
441-450.
Roscoe, M. V. 1927. Cytological studies in the genus Wisteria.
Botanical Gazette 84: 171-186.
Samal, K. K. 1936. The development of the embryo sac and embryo in
Crotalaria juncea. Journal of the Indian Botanical Society 15: 19-31.
Saxton, W. T. 1907. On the development of the ovule and embryo sac in
Cassia tomentosa. Transactions South African Philosophical Society
18: 1-5.
Schmidt, W. 1902. Untersuchungen tiber die Blatt und Samenstruktur
bei den Loteen. Beihefte Botanisches Centralblatt 12: 425-482.
Schnarf, K. 1937. Studien ilber den Bau der PollenkBrner der Angiospermen. Planta 27: 450-465.
Sen, N. K. and R. Krishnan. 1961. Binucleate pollen mother cells in
Clitoria ternata. Current Science 30: 306-307.
Soueges,* R. 1927. Embryogénie des Légumineuses. Développement du
proembryon chez le Trifolium minus. Comptes Rendus de la Academie
des Sciences, Paris, Serie D,184: 1018-1019.
Strasburger, E. 1880. Einige Bemerkungen liber vielkernige Zellen und
ûber die Embryogenie von Lupinus. Botanische Zeitschrift Jahrbucher
38: 843-854; 857-868.
Trankovskii, D. A. 1964. The pollen grain development in two Lathyrus
hybrids. Biulleten Moskovskogo Obshchestva Ispytatelei Prirody
Biologie 69: 91-97.
Veillet-Bartoszewska, M. 1956a. Recherches embryologiques sur le
Dolichos lablab. Bulletin de la Société Botanique de France 103:
235-240.
Numerous other papers with nearly identical titles, but dealing with
different species have been published by Soueges (see Davis, 1966). None
of these contained any information on the tapeturn.
84
Veillet-Bartoszewska, M. 1956b. Recherches embryogéniques sur le
Glycyrrhiza foetida. Bulletin de la Société Botanique de France
103; 439-443.
Venkatesh, S. G, 1951. The inflorescence and flowers of Dichrostachys
cinerea. Proceedings of the Indian Academy of Science, Section B,
34; 183-187.
Young, J. 0, 1940. Cytological investigations in Desmodium and Lespedeza. Botanical Gazette 101; 839-850.
Young, W. J. 1905. The embryology of Melilotus albus.
the Indiana Academy of Science 15; 133-141.
Proceedings of
85
ACKNOWLEDGEMENTS
I wish to express my appreciation to Dr. Nels R, Lersten for his
assistance in the selection of the problem and for his advice, patience
and encouragement during the investigation and preparation of this manu­
script, The technical advice and discussions with Dr. Harry T. Homer, Jr.
and Dr. Duane Isely have been helpful and are appreciated.
Special thanks are extended to Dr, Willis H, Skrdla and Dr. Raymond
Lo Clark of the
Regional Plant Introduction Station, Ames, Iowa, for
their cooperation in obtaining seed of many species used in this study. I
would also like to thank Dr, Richard W, Pohl and Mr, Gerrit Davidse for
special collections of cytological material,
I am grateful to the Department of Botany and Plant Pathology for the
facilities made available and for financial assistance during this study,
I also acknowledge financial support from a National Science Foundation
summer fellowship,
I thank
John T, Jones and family for their role in the completion
of this manuscript.
Last but not least, I publicly thank my wife, Janet, and family for
their patience, encouragement and sacrifices to make the completion of
this work possible.
86
APPENDIX A:
SUMMARY OF TAPETAL CHARACTERISTICS
The ordering of subfamilies and tribes in the following charts is
not intended to reflect any particular phylogenetic scheme, but rather
is merely a convenient way of arranging the material. Following each
subfamily and tribe are the approximate number of genera and species.
The number of genera and species of each subfamily and each tribe that
have been reported by others is listed next.
my observations.
Chart 1.
Mimosoideae
Below these figures are
loielp
f
I
e
ivnm
IS
g.
w w o»
ooo
Iff
1
1
S-
|:|g
e
M
s1
3
i
I
H
X
r
" "m I»I "
•M ^S
II
r
00
f-x f—
«
8%
g
+++
f.
S ^»w u»
OOO
S
u.Ȥ g g g
* # *
y y o 777
#4
£5gfir
!
IM>
+ + + + + +
++
++++++
++
Cellular tapetun
Plaamodlal tapeturn
+++
++
++++++
++
Uninucleate
Blnucleate
Multinucleate
laterphaae nuclei
+
+
++
+
++
+
+
Early prophase nuclei
Late prophase nuclei
Cryatals
Figure
88
Ttxoa
Rtfmenc*
L#uc««na
L. gl«uc«
Mtoe»»
M. iMBâU
RT Invita
M. pudlca
N. teaalana
HT niblcaulla
SeliTaiikla
S. uncfaata
4. Admaatbarlaaa
I
HI i
I Ss
1 1 a1
i
Dayanaagar, 1949
TlKlar, 1965
+
+
+
+
Doyaoaagar, 1951a
Tlxlar, 1965
Bust
Haratlnhachar,1951
Butt
Butt
Mulay and Dhaml,
1955
Butt
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
Butt
+
+
t
+
+
+
+
+
14
+
16 Ci 100 ap.
4 C: S ap.
1 Ci
1 ap.
Adwanthara
A. pavwSTca
Doyansagar, 1954b
1958
Dlchreataehva
P. citwtâa
Dnyanaagar, 1954a
Haptunla
*. ol«rac#a
Proaopla
P. Wlflora
T:tplclewa
5. Plptadaaiaaa 5 Oi
0 Gt
0 Oi
4* +
+• +
+
Singh and Shivaputii +
19S5
Dnyanaagar, 1952
+
K trifluatra
6. Parklaaa
I1
!
Biiaa
Duyaoaagar, 1957
+
+
Dnyanaagar, 1954a
+
+
+
•
+
12,13
50 sp.
0 fp.
0 ap.
2 Gi 40 ap.
1 ap.
0 Gi 0 ap.
1 OI
Parkla
P. blglanduloaa
*Datcribad aa intanaadlat* batwaan callular and plaamedial (aaoabotd), but mora Ilka tha plaaaodial
tap#turn.
89
Chart 2.
Caesalpinioideae
Ipipio
* * *
S&
ff 1
#
M» #
iO
£0
oT
IL
minin
• • • |n|rMotolnirï|otn|o|n|ntolS
• • • • « • • • • « • « 1^
g
1 5
1g 1
|lS 1
isNile #
'p
K)W O
AOO
II
o o iS
non nnn
•"*
S
•"Ou*
ooS
•5 5 -S
M Om
CAO
M O%
SSS
ggg
yyy
STîî
yy
£?®SÎÎÎÎ?ïy^ # rr
»
&&&&%
S«o
SSS
g
C oaa
ooo
on n
ooSS KB8
"8 <3 <3 •S -S 5
rt
vO
O
o
r- k» w r- ^^
^
^
S<
51
+++
I
k
I
+
++
+++++++++
Cellular tapeturn
++
+
+
+
Plaamodial tapetu*
++
+
+
+
Uninucleate
+++
+
++
+++++++++
+
+
Blnucleate
+
++++++
+
+
Multinucleate
+
+
+
+
+
+
+
++
Interphase nuclei
Early prophase nuclei
Late prophase nuclei
+
Crystals
Figure
H» io
I
ipipip in
Sli
1
1
ooo
e
ooo
o
6 p.
sr
7s
s
1
e
I Iff»
II
•X4WO
AAA
•rIS iplol.ololo ipio in:
lal i«»s|p»si8
#
r
^^
cjSBI
o o u*
•S «s *0
«0*^8
•Sv*S
III
II
Iff
I
s^g I,
«
ning^
si
5H
Cl
• +
+
+
+
++
++ + +
+
++
+
+
+
+
+
++ + +
+
+
+
+
+
+
+ +
+ + + +
++
+
++
+
+
++
++
+
+
Cellular tapecum
Plaaaodial tapeturn
Uninucleate
++++
+
Blnucleate
++
+
Multinucleate
Interphaae nuclei
++
++
++
+
S:
1>
+
+
Early prophase nuclei
+
++
++
w
2
r*
5
&at« propha«« nucl#!
++
Cryatala
Figure
92
Chart 3. Papilionoideae
93
I
Reference
Taxon
Papilionoldeae
400 G: 9100 ap
45 ap.
33 G:
70 C: 126 ap.
50 G:
0 G:
2 G:
14. Sopboreae
II
g
II 111
I
B. S
1I
i
S
3
350 sp.
0 sp.
2 sp,
CleJraatl»
Ç. lute»
Buaa
+
+
+
+ 109-111
Sophor»
S. ieponlc»
Buas
+
+
+
+ 106-108
Baptiaia
B. leucantha
1*
leucophaea
Buss
Buss
+
+
+
+
ThetBopal»
T. aontana
Buaa
+
+
Buss
Buas
Banerjl and Samal,
1936
Buaa
Tlxiet, 1965
+
+
?
+
+
+
+
+
+
+
Cytiaua
put
. purpureu»
. ac
acoparlua
Camlel, 1952
Buaa
+
+
+
Caniata
C. noneapema
Cortl, 1946
15. PodalyriCM 30 Ci
0 G:
2 Ci
16. Geniateae
50 Ci
5 C:
6 C:
Crotalarla
C. incaôa
Ç. Intetaadla
Ç, iuncea
Ç. aaltlan»
C. verrucoia
§
Laburnum
L. Mggroidea
Lotoaonl»
L. balnesll
450 «p.
0 ap.
3 sp.
+
+
+
+ 112-114
+
+
975 •P
8 •P
8 sp.
+
+
+
+
117
+
+ 115,116
+
J
Camlel, 1952
Buaa
+
+
+
+
+
120
Buaa
+
+
+
+ 121-123
94
Taxoa
R«f«tanc«
Luplnus
anguatlfoltu»
L. «l«g«ns
+
Carnlal, 1963
Buaa
Catnlal, 1932,1963
Carnlal, 1932,1963
+
+
+
+
+
+
+
+
Buaa
+
+
Cooper, 1933
Cooper, 1933
Cooper, 1933
Raavea, 1930
Cooper, 1933
Cblldera, 1932
Buaa
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
Caatetter, 1935
Cooper, 1933
Buaa
Cooper, 1933
+
+
+
+
+
+
+
+
+ 123,126
Tixler, 1965
+
+
Ô. «pacloaa
Buaa
Buaa
Buaa
+
+
+
+
+
+
Parochatua
P. caawml*
Bua*
L, poly^lXu»
Ulex
£. «urop—u»
+
+
+
118 119
+
17. TrlfollM* 6 Gi 430 ap.
3 GI
6 GI
1 «p.
10 ip.
M»dlcaflO
M. giutinoi*
M. —tlT«
Malllotu»
M. «Ibû#
M. »lbw cv, Radflald
Yallow
M, «uavaolani
Onoola
0. ultlaalna
Ô. pa^tegiu
Trlfollaa
T. incarnatu»
T. ptatiwaa "
Tritonalla
T. waSTca
T. fotniMHgrMcua
18. Lotaaa
8 GI 130 ap.
2 Gi
4 GI
2 ap.
3 ap.
124
+
+
+
+
+
+
+
+
+
Buaa
Hindnarah, 1964
Buaa
+
+
+
+
+
+
Buaa
Buaa
+
+
+
+
130,131
132
+
+
ipipiog i».
!î
isilisli ISl
SSHillI
»r
riir
p ri? r
++
+
++
+
+0.
+ + + +_
vO
Ln
Cellular tapeturn
Plaaoodlal tapetua
++
+
Uninucleate
Blnucleata
Multinucleate
Interphaae nuclei
++
Early prophase nuclei
Late propbase nuclei
Cxystala
Figure
96
i M
3 g
Reference
3 i I
J
II
11111 f K M
GllrlclJU
G. maeul'atJ
G, «aplaa
Tixler, 1963
Chandravadana,1965
+
+
+
+
lodlgofera
I. «chinata
J[. piloga
I, psaudotlnctoria
I. iubulata
Buss
Buss
Buss
Buss
+
+
+
+
+
+
+
+
miUtla
M. ovallfolia
Pal, 1961
+
+
Buss
+
+
Carniel, 1952
Buss
+
+
+
+
Buss
Buss
Buss
+
+
+
+
+
+
+
+
Buss
+
+
+
+
+
+
+
+
+
Pantulu, 1942
Buss
Buss
Bugg
+
+
Bug g
Sugg
+
+
+
+
Bug#
Buga
Bug g
Bufg
+
+
+
+
+
+
+
+
T«xon
3 .
_
+
+
IM
+
+
+
+
OInava
0. tesoU
Roblnla
R. pgeudo-acacia
R. pgaudo-acacla
+
+
+
+
+
+
+
+
103
S«*b#nia
S.
arabica
I*
S, «««ban
93
Taphrosta
T.
T.
T.
T,
Incana
purpurea
aubt^lora
vlrglnlanâ
Wigterla
W. «Inensii
20. Psoraleae
91,94
+
+
+
+
10 C: 350 sp.
0 Ci
5 Ci
teorpha
A. canaiceng
A, frutlCQga'
0 ip.
15 gp.
+
+
198,139
Dalea
D. alepecuroldag
D. argyraea
£. ISriâ
D. lagopui
Eyianhardtla
»• polyitachva
Bu««
+
+
154,155