Bot. J . Linn. SOC., 70: 183-212. With 9 plates
April 1975
The structure and development of the
haustorium in parasitic Scrophulariaceae*
LYTTON J . MUSSELMAN, F.L.S.
Department of Biology, Old !lominion University,
Norfolk, Virginia, U.S.A.
AND
WILLIAM C. DICKISON
Department of !lotany, University of North Carolina,
Chapel Hill, U.S,A .
Accepted for publication November I974
The structure and development of roots and haustoria in 37 species of parasitic Scrophulariaceae was studied using light microscopy.
The mature haustorium consists of two regions: the swollen “body” and the parent root,
which resembles non-haustorial roots in structure. The body arises from the parent root and is
composed of an epidermis, cortex, central region of xylem (the vascular core), a region of
parenchyma (the central parenchymatous core), and the portion of the haustorium contained in
the host tissue (the endophyte). The xylem of the vascular core is composed predominately of
vessel elements. The central parenchymatous core is composed of parenchyma and collenchyma. Vessels extend from the vascular core through the central parenchymatous core t o
the endophyte. The endophyte is composed of parenchyma cells and vessel elements. No
phloem is present in the body of the haustorium.
Early stages in the development of the haustorium are exogenous. Initial periclinal divisions
in the epidermis or outer cortex are followed by hypertrophy of cortical parenchyma. These
events are followed by development of the vascular core from the pericycle, attachment of
haustorium to the host by a specialized layer of cementing cells or root hairs, and penetration
of the host by dissolution of host cells.
CONTENTS
Introduction
. . . . . .
Materials and methods
. . .
Root anatomy and development
Primary root
. . . .
Lateral roots
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184
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189
190
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* This study represents a portion of a thesis submitted to the Graduate School, The University of
North Carolina a t Chapel Hill by t h e first author in partial fulfillment of the requirements for the degtee
of Doctor of Philosophy. The assistance of Drs C. Ritchie Bell and M a x H. Hommersand is gratefully
acknowledged. Appreciation is also extended to those botanists who supplied material used in this study.
14
183
184
L. J. MUSSELMAN AND W. C. DICKISON
Secondary structure . , . . . . . . . . . . . . . . . . 1 9 0
Periderm
. . . . . . . . . . . . . . . . . . . . . 191
Root dimorphism
. . . . . . . . . . . . . . . . . ,191
The mature haustorium . . . . . . . . . . . . . . . . . . . 191
General morphology . . . . . . . . . . . . . . . . . . 192
Anatomy of the mature haustorium
. . . . . . . . . . . . ,193
The vascular core
. . . . . . . . . . . . . . . . . ,193
The axial strands . . . . . . . . . . . . . . . . . . , 1 9 5
The central parenchymatous core
. . . . . . . . . . . . . ,196
The vascular cambium
. . . . . . . . . . . . . . . . . 196
Cortex . . . . . . . . . . . . . . . . . . . . . . 196
Periderm
. . . . . . . . . . . . . . . . . . . . .197
Endophyte
. . . . . . . . . . . . . . , . . . . ,197
Self-parasitic haustoria
. . . . . . . . . . . . . . . . . 198
Development of the haustorium
. . . . . . . . . . . . . . . ,199
Haustorial nucleus
. . . . . . . . . . . . . . . . . .199
Attachment t o the host root
. . . . . . . . . . . . . . -200
Development of the vascular core
. . . . . . . . . . . . . .201
Penetration of host tissue
. . . . . . . . . . . . . . . .201
Xylem continuity between host and parasite . . . . . . . . . . , 2 0 2
The primary haustorium
. . . . . . . . . . . . . . . . 202
Discussion
. . . . . . . . . . . . . . . . , , . . . .202
The mature structure of the haustorium
. . . . . . . . . . . ,202
Development
. . . . . . . . . . . . . . . . . . . . 204
Comparison of haustorial structure in Scrophulariceae, Santalaceae and Oro. . . 204
banchaceae . . . . . . . . . . . . . . . . .
The morphological interpretation of the haustoriurn . . . . . . . . . 205
The evolutionary origin of the haustorium
. . - . . . . . . . . 206
References . . . . . . . . . . . . . . . . . . . . . . . 207
INTRODUCTION
The connective structure between host and parasite is termed a
“haustorium”, a term apparently first used by De Candolle in 1813 to describe
the parasitic organ of Cuscuta (Kuijt, 1969). Although “haustorium” is widely
used to describe various plant structures in such diverse groups as fungi and
non-parasitic angiosperms, it is well ingrained in the literature on parasitic
flowering plants, especially the Scrophulariaceae, and will be retained throughout the study.
Kuijt (1969) indicated that a thorough understanding of haustorial structure
and development might be the initial step to an understanding of the
evolutionary origin and function of parasitism in flowering plants. Very little
intensive or extensive work has been done on structure and development of the
haustorium, especially in the Scrophulariaceae (Kuijt, 1969). The objectives of
this work, accordingly, were to provide a detailed description of the
development and mature structure of the haustorium of plants belonging to
selected genera in this family. Although emphasis has been placed on species
native t o the southeastern United States, plants from different regions of the
world have been examined. Observations on members of the parasitic
Santalaceae and Orobanchaceae have also been included for comparative
purposes.
The literature on the parasitic Scrophulariaceae has been well summarized by
Kuijt (1969). Less exhaustive reviews have been presented by Christmann
(1960), Schmucker (1959) and Ozenda (1965). The intentions of this
discussion are to examine important contributions relating to the anatomy of
scrophulariaceous haustoria which were not included or emphasized in earlier
reviews, and to survey the literature which has appeared since 1969.
HAUSTORI UM IN PARASITIC SCROPHULARIACEAE
185
The first anatomical investigation of the parasitic members of the Scrophulariaceae was apparently that of Bowman (1833) on the genus Lathraea. Bowman
prepared free-hand sections and noted the peculiar wall-characteristics of xylem
elements in the haustorium. The first comparative anatomical study of
haustoria was Chatin’s Anatomie comparte des vkgttaux-Plantes parasites,
which was first published in 1856 and again in 1892 (Chatin, 1892). Except for
plants of a few European genera, Chatin’s investigations were based on dried
specimens, which necessarily limited the scope of his studies. Solms-Laubach
(1 867) published the first illustrations of developing haustoria. Sablon ( 1 887a,
1887b) concluded from morphological studies on six genera of the Scrophulariaceae that the haustorium is a greatly modified root. Van Tieghem (in Sablon,
1887b) further suggested that penetration of host tissue by a haustorium is
similar to penetration of cortical tissue by a developing lateral root.
Koch ( 1 887) presented detailed anatomical descriptions of the haustoria of
Melampyrum and was of the opinion that saprophytic angiosperms arose from
parasitic angiosperms by the reduction and modification of the haustorium into
a saprophytic organ. Melampyrum was considered to represent an intermediary
stage between a saprophyte and a parasite. Similar ideas were also presented by
Koch as a result of subsequent studies on Rhinanthus (1889) and Euphrasia
(1891). Elfriede Julg ( 1 916) noted the superficial resemblance of haustoria to
the bacterial nodules of legumes; but, despite the observation of a few bacilli
and spores in the haustoria of Melampyrum and Rhinanthus, she concluded
that no mwphological similarity existed between haustoria and nodules.
Fraysse (1906) studied the anatomy and physiology of Odontites and
Euphrasia and concluded that the development of the haustorium is similar to
that of a lateral root, i.e. it arises by periclinal divisions in the pericycle or
endodermis.
Perhaps the most prolific and best known of all investigators of parasitic
angiosperms was E. Heinricher (1893, 1895, 1898a, b, 1901a, b, 1908, 1917),
who published many papers on the Scrophulariaceae (for a complete
bibliography see Kuijt, 1969). Heinricher was primarily interested in the
ecology and physiology of parasitic angiosperms, although some anatomical
observations are included in his papers.
Except for the work of Maybrook (1917) on the genus Pedicularis, and short
papers by Kusano (1908) on Siphonostegia, Cannon (1909) on Orthocarpus,
Boodle (191 3) on Buttonia, Holm (1929) on Agalinis (Gerardia Benth. non L.)
and Buchnera, and Young (1932) on Harveya, most anatomical studies during
the first part of the twentieth century were tangential to taxonomic or
ecological studies. Boeshore ( 1 920) examined the root systems of parasitic
Scrophulariaceae but added little to our knowledge of the structure of the
haustorium. Pennell (1 928) briefly considered haustoria in his systematic
studies on North American Scrophulariaceae.
Between 1930 and 1950 few papers on parasitic Scrophulariaceae appeared,
but since 1960 there has been a resurgence of interest in these plants.
Taxonomic investigations on Pedicularis, Castilleja, Cordylanthus, Euphrasia,
and Aureolaria, Agalinis and Tornanthera have also dealt with various aspects of
haustorial anatomy (Sprague, 1962; Heckard, 1962; Thurman, 1966; Yeo,
1961; Mathen 1964). Of these, only Thurman (1966) provided a detailed
description of haustorial structure and development. Autecological studies in
Castilleja, Melampyrum and Aureolaria also included references to the parasitic
186
L. J. MUSSELMAN A N D W. C. DICKISON
organ (Malcolm, 1966; Cantlon et ul., 1963; Musselman, 1969). Piehl (1962a,
b, 1963, 1965) included descriptions of the general morphology of the
haustorium of Dusistomu, Melumpyrum and Pediculuris. Williams (1960)
described the anatomy of the mature haustorium of Sopubiu rucemosu.
Although Fineran’s studies (1962, 1963a, b, c, 1965a, b) were on the genus
Exocurpus (Santalaceae), his careful and detailed discussions on haustorial
structure and development in this root parasite are of value in interpreting the
haustoria of the Scrophulariaceae.
Recently, Chuang & Heckard (197 1) have examined haustorial structure and
development in Cordylunthus. Kuijt & Dobbins (1971) were first to demonstrate the presence of sieve tube elements in a haustorium of the Scrophulariaceae, while the presence of transfer cells and collenchyma were first recorded
by Dobbins & Kuijt (1973a, b).
A review of the literature on the genus Strigu deserves special attention, since
it is the only genus in the family Scrophulariaceae which is a serious parasite of
agricultural crops. Of particular importance is Striga usiuticu (= S. luteu), which
causes considerable damage to Zeu and other gramineous crops in the Carolinas
of the eastern United States and vast areas of South Africa. Damage to crops in
the United States has been limited by a vigorous control and quarantine
program (Eplee, 1973). The literature on Strigu is voluminous (Anon., 1957).
Despite this, no detailed anatomical study on the development and mature
structure of the haustorium has appeared since the observations of Stephens
(1912). She was the first to describe the “primary haustorium” formed by the
direct transformation of the root apex into a haustorium, which she considered
t o be an organ sui generis. Additional work on the anatomy of Strigu includes
that of Saunders (1933) and Uttaman (1950), who dealt with seedling
structure, and Rogers & Nelson (1962), who used radioactive tracers to
determine the presence of phloem in the roots of plants grown in tissue culture.
Okonkwo (1966) studied the development of haustoria in tissue culture.
Ozenda & Capdepon (1972) considered the structure of Strigu gesneroides and
its similarity to holoparasitic members of the Scrophulariaceae and Orobanchaceae.
MATERIALS A N D METHODS
Specimens examined in this study and their collection data are listed in
Table 1. An effort was made to include species from each section of each
genus, although this was not possible for the two large genera Custilleju and
Pediculuris. In order to sample patterns of variation within each species,
materials were examined whenever possible from several populations in
different localities. A limited number of clearings were made from herbarium
specimens, which are identified by an asterisk. Duplicate slides are deposited in
the slide collection of the Jodrell Laboratory at the Royal Botanic Gardens,
Kew.
Material was fixed in either FAA (formalin-acetic acid-ethyl alcohol) or Craf
(chromic acid fixative) according to the suggestions of Jensen (1962). Craf
fixative generally gave better fixation for root tips and very young haustoria.
Dehydration and infiltration were carried out by the tertiary-butyl alcohol
method (Jensen, 1962). Paraplast embedding medium with a melting point of
HAUSTORIUM IN PARASITIC SCROPHULARIACEAE
187
Table 1. Specics studied of parasitic Scrophulariaceae, non-parasitic
Scrophulariaceae, Santalaceae and Orobanchaceae. Method of citation follows
suggestions of Stern & Chambers (1960)
Species and authority
Collccror and number
.
.. .
.-
~
~
Geographical origin
-~
Herbarium voucher
-.
Parasitic Scrophulariaceae
Agatinisaphylla (Nutt.) Raf.
A . maritima Raf.
A . purpurea (L.) Penn.
A . setacea (Gmel.) Raf.
A . tenuifolia (Vahl) Raf.
A . tenuifolia (Vahl) Raf.
A . linifoolia (Nutt.) Britton
A . linifolia (Nutt.) Britton
A . aspera (Dougl.) Britton
Alectra kirkii Hemsley
A . vogelii Benth.
Aureolaria laevigata Raf.
A. pedimlaria (L.) Raf.
[including A . pectinara
(Nutt.) Pennelll
A. pedicularia ( L . ) Raf.
A . pedicularia (L.) Raf.
A . pedicularia (L.) Raf.
A. pedicularia (L.) Raf.
A . pedicularia (L.) Raf.
A. pedicularia (L.) Raf.
A . pedicularia (L.)Raf.
A. flava ( L . ) Farw.
A . flava (L.) Farw.
A. flava (L.) Farw.
A. flava ( L . ) Farw.
A . virginica (L.)Penn.
A . virginica (L.) Penn.
A . grandiflora (Benth.) Penn.
A . grandiflora (Benth.) Penn.
A . grandiflora (Benth.) Penn.
Buchnera floridana Gand.
Casiilleja coccinea (L.)
Sprengel
C. sessiliflora Pursh
Cordylan thus bolanderi
(A. Gray) Penn.
C. hansenii (Ferris) Macbr.
Dasistoma macrop h ylla
(Nutt.) Raf.
Euphrasia canadensis Towns.
Musselman 4418
Musselman 4639
Musselman 4642
Musselman 3836
Musselman 4641
Musselman 1393
Musselman 1290
Musselman 4403
Musselman 3074
Greenway 10484
Okonkwo s.n.
Musselman 1 3 5 0
Musselman 849
Horry Co., S. C.
Dare Co., N. C.
Orange Co., N. C.
Chatham Co., N. C.
Orange Co., N. C.
Rock Co., Wis.
Calhoun Co., Fla.
Horry Co., S. C.
Rock Co.. Wis.
Tanganyika, Africa
Laboratory culture
Montgomery Co., Va.
Monroe Co., W. Va.
NCU
NCU
NCU
NCU
NCU
ULJ
NCU
NCU
NCU
KEW
None
NCU
NCU
Musselman 1278
Musselman 1 3 36
Musselman 4401
Musselman 1195
Musselman 91 7
Musselman 4320
Musselman 940
Musselman 4635
Musselman 950
Musselman 120 3
Musselman 4571
Musselman 4321
Musselman 4591
Musselman 928
Musselman 1167
Musselman 92 3
Musselman 4126a
Musselman 4574
Walton Co., Fla.
Decatur, Ga.
Escambia Co., Ala.
Green Co., Wis.
Winnebago Co., Ill.
Montgomery Co., Va.
Howell Co., rMiss.
Calloway Co.. Ky.
Texas Co., Mo.
Pontotoc Co., Miss.
Santa Rosa Co., Fla.
Montgomery Co.. Va.
Orange Co., N. C.
Crawford Co., Mo.
Waukesha Co., Wis.
Winnebago Co., Ill.
Leon Co., Fla.
Alamance Co., N. C.
NCU
NCU
NCU
NCU
NCU
NCU
NCU
NCU
UWM
NCU
NCU
NCU
NCU
NCU
MIL
NCU
NCU
NCU
Musselman 461 2
Heckard 2 1 1 0
Rock Co., Wis.
Modera Co., Calif.
NCU
Heckard 2 1 3 0
Musselman 4634
Shasta Co., Calif.
Dickson Co., Tenn.
Cochran 250
NC U
uc
uc
NCU
E. cuneata Forster
E. zeylandica Wettst.
Fineran s.n.
Fineran s.n.
Macranthera flammea
(Bartram) Penn.
M. flammea (Bartram) Penn.
Melampyrum lineare Desr.
M. lineare Desr.
M. lineare Desr.
Orthocarpus p urpurascens
Benth.
Pedicularis canadensis L.
P. lanceolata Michx.
Schwalbea americana L.
Musselman 1242
Gasp6 Peninsula,
Canada
Ruhines, New Zealand
Arthur Pass, New
Zealand
Washington Parish, La.
Musselman
Musselman
Musselman
Musselman
Atsatt s-n.
Jackson Co., Fla.
A w r y Co., N. C.
Tazewell Co., Va.
Monroe Co., W. Va.
Laboratory culture
NCU
NCU
NCU
NCU
None
Watauga Co., N. C.
Rock Co., Wis.
Horry Co., S. C.
NCU
NCU
NCU
4393
4592
431 3a
4364
Musselman 4567
Musselman 4625
Musselman 4577
NCU
None
None
1 88
L. J . MUSSELMAN AND W. C. DICKISON
Table 1-con t.
Species and authority
Seymeria cassioides
(J. F. Gmelin) Blake
S. cassioides (J. F. Gmelin)
Blake
S. cassioides (1. F. Gmelin)
Blake
S. pectinata Pursh
S. pectinata Pursh
'Siphonostegia chinensis
Benth.
Striga asiatica (L.) Kuntze
Collector and number
Geographical origin
Herbarium voucher
Musselman 3849
Pender Co., N. C.
NCU
Musselman 4638
Horry Co., S. C.
NCU
Musselman 13 16
Decatur Co.. Ga.
NCU
Musselman s.n.
Musselman 4399
Chiao 2915
Brunswick Co., N. C.
Jackson Co., N. C.
Nanking, China
None
NCU
KEW
Massey & Musselman
Scotland Co., N. C.
NCU
USDA Witchweed Lab.
Africa
None
KEW-
Laboratory culture
Cook Co., 111.
None
NCU
3 304
S. asiatica (L.) Kuntze
S. gesneroides (Willd.) Yatke
Musselman 4646a
Milne-Redhead & Taylor
9524
S. hermonthica (Del.) Benth.
Tomanthera auriculata
(Michx.) Raf.
Okonkwo s.n.
Musselman, Moore,
Schulenberg & Lee
3933
Nonparasitic Scrophulariaceae
'Antirrhinum orontiurn L.
*Bacopa monnieri (L.) Penn.
*Chaenorrhinum minus (L.)
Lange
'Scrophularia marilandica L.
'Synthris reniformis (Douglas)
Benth.
*Torenia asiatica L.
* Verbascum thapsus L.
Veronica peregrina L.
Hekking s.n.
Ahles 28024
Lange, Magrath &
Robinson 6748
Cooperrider 10636
Steward 7484
Gelderland, Netherlands
Pender Co., N. C.
Anderson Co., Kan.
NCU
NCU
NCU
Columbiana Co., Ohio
Yamhill Co., Ore.
NCU
NCU
McMillan s.n.
Downs 2914
Musselman 4574
Calcutta, India
Morgan Co., W. Va.
Orange Co., N. C.
NCU
NCU
NCU
Orobanchaceae
Conopholis americana
(L.) Wall.
Orobanche uniflora L.
0. aegyptiaca L.
Cistanche tubulosa (Schenk)
Wight
Musselman 4583
McDowell Co., N. C.
NCU
Leonard 5422
Halwagy, 1230
Halwagy, 1237
Durham Co., N. C.
Al-Ada'mi, Kuwait
Ras Al Jlay'ah, Kuwait
NCU
NCU
NCU
Buckleya distichophylla
(Nutt.) Torr.
Comandra umbellata (L.)
Nutt.
Pyrularin pubera Michx.
Nestronia umbellula Raf.
Musselman 4588
Haywood Co. N. C.
NCU
Musselman 4590
Forsyth Co., N. C.
NCU
Musselman 4585
Musselman 4428
Henderson Co., N. C.
Wake Co., N. C.
NCU
NCU
Santalaceae
*Slides prepared from dried herbarium material.
6 1' C gave better results than lower-melting-point (56" C) paraffins. Sections
were cut on an American Optical 820 or a Leitz 1212 rotary microtome at
10-14pm and affixed to glass slides with Haupt's adhesive (Jensen, 1962).
Coating sections with parloidin (Jensen, 1962) greatly reduced the loss of
woody sections during hydration and staining. Stained sections were mounted
in Canada balsam.
HAUSTORIUM IN PARASITIC SCROPHULARIACEAE
189
In general, a safranin-fast green stain combination (Jensen, 1962) gave
excellent results with mature tissues. Haidenhein's hematoxylin with aqueous
safranin as a counterstain (Jensen, 1962) was helpful for studying earlier stages
of root and haustorium development. Schiff's reagent (Jensen, 1962) was
employed to differentiate cell walls and also t o determine the chemical nature
of the granules in phloeotracheids. A tannic acid-lacmoid stain (Cheadle et al.,
1953) was helpful in identifying sieve-tube elements.
Clearings were prepared by diaphanization of material in 5% NaOH at 60" C
until clear. Particularly critical staining of xylem was obtained using pararosanaline hydrochloride (Boke, 1970). Cleared material was stained for one
hour, dehydrated in two changes each of 95% and absolute ethanol for ten
minutes, cleared overnight in methyl salicylate, and mounted in Canada balsam.
All material from herbarium specimens was prepared in this manner.
ROOTANATOMYANDDEVELOPMENT
Fineran (1962) stated ". . . as the haustorium is borne by the root, the form,
growth habits, and structure of the root are features which should be taken
into consideration when assessing the mode of life of a root parasite." This has
seldom been done and anatomical data for roots of parasitic Scrophulariaceae
are sparse (Boeshore, 1920; Metcalfe & Chalk, 1950). Therefore, roots were
examined in this study with regard to their development and mature structure.
Primary root
Primary roots of Agalinis aphylla, Aureolaria flava, A. grandiflora, A . pedicularia, A. virginica, Castilleja coccinea, Orthocarpus purpurascens, Schwalbea
americana, Striga asiatica and Tomanthera auriculata were examined with
respect to apical organization, root hair morphology and development.
Germination of Striga asiatica is hypogeal (Plate 1B) whereas germination of all
other genera is epigeal, as illustrated by Agalinis aphylla (Plate 1A). With the
exception of Striga, all seedlings possess root hairs along the radicle. In
Agalinis, Aureolaria and Castilleja coccinea, root hairs develop at the
radicle-hypocotyl junction to form a collar which encircles the axis (Malcolm,
1966). In plants of other genera root hairs develop acropetally along the
elongating radicle (Plate 1C). Root hairs on lateral roots appear identical in
origin and structure with those on the radicle.
Forked, branched or spirally twisted root hairs are present on seedlings
grown in Petri dishes without sterile conditions (Plate 1D-F). When seeds are
surface-sterilized with 1% commercial laundry bleach solution and germinated
under sterile conditions root hairs are spiralled but not forked or branched. The
morphology of these spiralled root hairs is similar to that reported by Szabo e t
al. (1973) for seedlings of autotrophic plants grown in sterile culture and
treated with arctiine, a phenolic compound thought to interfere with nucleic
acid functioning.
Root apices possess a dermatocalyptrogen pattern of organization (Esau,
19651, that is, the epidermis and rootcap have a common origin. This pattern
of apical organization corresponds with that reported for non-parasitic
members of the family Scrophulariaceae (Esau, 1965). The root of Striga
190
L. J . MUSSELMAN A N D W. C. DICKISON
asiatica is distinctive in lacking a root cap and is further characterized by lack
of differentiation of initials and a particularly prominent region of elongation.
A mucilaginous layer (Esau, 1965) is present in the root apex of Macranthera
flamm ea.
Lateral roots
Lateral roots arise in a manner characteristic of dicotyledons as a whole
(Esau, 1965) in that periclinal divisions in the pericycle are followed by
anticlinal divisions in the endodermis. Lateral roots arise opposite primary
xylem poles and are produced at regular intervals except in the vicinity of
developing haustoria. Production of lateral roots appears to be strongly
seasonal, occurring in the spring in perennial plants of Aureolaria spp.,
Dasistoma macrophylla, Macran thera flammea and Schwalbea americana.
The anatomy of the primary root is characteristically dicotyledonous. The
epidermis is two-layered. The width of the cortex varies between plants of
different genera and even between different individuals of the same species, but
usually consists of four to ten parenchyma cells that are often filled with
amyloplasts. Casparian strips are present on the radial and tangential walls of
the single-layered endodermis. The primary xylem is triarch or tetrarch and
alternates with regions of phloem. The semi-aquatic species, Agalinis linifolia
and A . maritima, have a well-developed aerenchyma composing the cortex.
Secondary structure
Plants of all species are characterized by the early initiation of secondary
growth from a distinctly storied cambium that becomes active at a distance of
7-10 mm from the root apex. The cambium produces secondary xylem and
phloem in the usual manner (Esau, 1965). The secondary xylem of roots is
composed of vessel elements with alternate lateral wall pitting and terminal,
simple perforation plates. Imperforate tracheary elements are libriform fibres
with greatly reduced pits. In general, the secondary xylem of roots appears to
be similar to descriptions of the wood in the stem (Metcalfe & Chalk, 1950).
N o basis was found for the report by Maybrook (1917) that the root of
Pedicularis contains only tracheids in the xylem. Contractile roots are present
in the rosette plants of Aureolaria pedicularia.
Although phloem is difficult to study because of its apparent short-lived
nature and small cell-size, sieve-tube elements and associated sieve plates,
companion cells and parenchyma are present. Sieve plates are simple, transverse
and terminal and, while not abundant, are present in every species examined
except those of Striga. Rogers & Nelson (1962) have demonstrated the
probable presence of sieve-tube elements in Striga asiatica based on radioactive
tracers, but their data d o not clearly establish the presence of sieve plates. The
reduction or complete absence of phloem in the roots of parasitic Scrophulariaceae has received considerable attention (see Kuijt, 1969).
Secondary phloem is composed of large amounts of parenchyma, which
makes up an estimated 75%of the volume of roots of species of Aureolaria and
Agalinis, whereas in other species secondary phloem is less abundant. No
sclerenchyma was observed in roots of the following species: Agalinis purpurea,
HAUSTORIUM IN PARASITIC SCROPHULARIACEAE
191
A . tenuifolia, Buchnera floridana, Euphrasia canadensis, Alectra vogelii,
Ortho carpus purpurascens, Pedicularis canadensis, P. lanceo la ta, Sey meria
cassioides, S. pectinata, Striga asiatica, S. hermonthica and Tomanthera
auriculata. Sclerenchyma in the form of elongate brachysclereids is present in
all other species examined. In Schwalbea americana the cortical parenchyma
and the parenchyma of the secondary phloem is sclerified.
Periderm
Roots of all species examined develop periderm. This tissue originates in the
outer layers of the secondary phloem. In older roots the outer cells of the
periderm become suberized, filled with tannins and other substances.
Root dimorphism
Root dimorphism, the evolutionary reduction of lateral roots to short roots
terminating in haustoria, has been suggested as a possible indication of
specialization towards holoparasitism ; such trends have been established for the
Santalalean families by Kuijt (1969). Similar trends are also present in the
Scrophulariaceae. The root systems of putatively primitive genera such as
Aureolaria, Dasistoma and Macranthera are spreading, fibrous and rather
massive, whereas in presumably advanced genera such as AZectra, Melampyrum
and Castilleja the roots are smaller and more delicate. Such root dimorphism is
especially evident at the seedling stages in Aureolaria. In the Scrophulariaceae,
all roots are potentially haustorial, that is, capable of producing haustoria, and
a differentiation into haustorial and non-haustorial roots, as in the Lennoaceae
(Kuijt, 1969), does not exist. In Striga most roots are adventitious and arise
from the stem.
Kuijt (1969) has suggested that an investigation of the anatomy of the roots
of non-parasitic Scrophulariaceae may provide data on possible trends towards
parasitism. Therefore, eight genera (Table 1 ) of non-parasitic Scrophulariaceae
were examined with regard to root structure and development. The root
anatomy of these plants is similar to that of parasitic species; however, root
hairs were not available for study.
Atsatt (1973) has discussed the possible role of micro-organisms in the
evolutionary origin of haustoria and suggested that the origin of haustoria, and
therefore the parasitic habit, arose as a compensation for loss of energy to
invading microbes. The microbes stimulated production of haustoria in a
manner similar to the production of nodules by bacteria. Fungi were
commonly observed invading roots of most genera and what appeared to be
bacterial infections were frequently noted in young roots, but in neither case
was the morphology of the root altered to produce anything resembling a
haustorium.
THE MATURE HAUSTORIUM
We regard a haustorium to be mature when a continuous xylem conduit is
present from the parasite to the host. Xylem continuity provides a distinct and
easily observable point in haustorial development and, unlike previous
192
L. J. MUSSELMAN A N D W. C. DICKISON
definitions (see Fineran, 1963a; Kuijt, 1969), is independent of size considerations. The general morphology and anatomy of the mature haustorium of
37 species in 17 genera of Scrophulariaceae is described in this section.
General morphology
In order to describe adequately the structure of the haustorium, it is
necessary to first define orientation of the mature haustorium relative to the
position of haustorial roots (roots which bear haustoria) and host roots.
Throughout this study, the ventral surface of the haustorium is considered to
be nearest the host root, the dorsal surface nearest the parent root. Following
Fineran (1963), two general regions of the haustorial root may be distinguished: (1) the “body” and (2) the parent (mother) root. The parent root is the
segment of the haustorial root that gives rise to the body of the haustorium.
The body is a swollen globose mass much larger than the parent root.
At maturity, haustoria are bell-shaped to globose structures (Plate 2A-H,
J-L), although this shape may be altered by growth pressures when haustoria
are sandwiched between host roots or other obstacles. As seen in Plate 6G, a
neck may connect the body and the parent root. The size of the haustoria on
any given haustorial root varies considerably depending on the age of the
haustorial root, the species being parasitized, and the degree of haustorial
penetration of the host tissue. Haustoria may be smaller than 0.1 mm in
diameter and still be mature. The largest haustorium observed in this study was
11.0 mm in diameter, which was produced by Aureolaria jlava. The size of
haustoria of annual plants is, of course, restricted by the limiting growing
period of the parasite; haustoria of perennial plants are generally larger than
those of annual species. Haustoria of species belonging to the tribe Buchnereae
are usually larger than those of the tribe Euphrasieae.
The location of haustoria on the root system of the parasite is correlated
with the proximity of host roots. Aside from the presence of the haustoria
themselves, a characteristic feature of some haustorial roots is their coiled
nature around host roots. Such entwining roots may extend along the host root
for several decimetres. Coiling is not present in roots that develop only a few
haustoria. Coiling may be the result of a thigmotropic response, which may
serve to place haustoria in position of access to uninfected xylem.
Haustoria are characteristically located laterally on the host root (Plate 2),
but may also rarely terminate host roots. In these cases it is difficult to
determine if the haustoria were originally (i) lateral and became terminal by
continued growth and the resultant necrosis of the host root or (ii) terminal on
the host. The fact that haustoria invariably make connection with the xylem
tissue would seem to mitigate against attachment to a root apex where
tracheary elements are not present. Haustoria of Alectra vogelii are most
abundant near the bacterial nodules on Vigna unguiculata. In Aureolaria
pedicularia and a few other species (Agalinis aphylla, Seymeria pectinata),
attachment to the host is in the vicinity of coralloid mycorrhizal roots.
Haustoria of Schwalbea americana are always attached to roots that produce
lateral roots (Plate 2G). Because these short lateral roots arise in diverse genera
(Hypericum, Ilex, Gaylusaccia), it seems possible that they may originate in
response to the attachment of a haustorium. The most frequently observed
HAUSTORIUM IN PARASITIC SCROPHULARIACEAE
193
morphological response of the host to parasitism is a decrease in the size of the
root distal to the haustorium. Host roots of any age are subject to invasion by
haustoria.
Anatomy of the mature haustorium
The regions, tissues and cells of the body of the mature haustorium are
described in this section. The anatomy of the parent haustorial root is the same
as that presented for roots generally and will not be repeated here. In this
study, major emphasis was placed upon the unifying features in haustorial
architecture rather than on detailed descriptions of haustoria from plants in
individual genera. Before describing haustorial structure, however, it is
necessary to define terminology used with reference to planes of sectioning.
Because much of the body is radially symmetrical, planes of sectioning are
defined in relation to the axial strands which are, without exception,
perpendicular to the long axis of the parent root. A transverse section of a
haustorium is one cut at right angles to the long axis of the axial strands. A
longitudinal section of a haustorium, therefore, is parallel with the long axis of
the axial strands and can be either perpendicular to, or parallel with the long
axis of the parent roots.
As noted by Kuijt (1969), the organization of the parasitic organ resembles
that of other angiosperm organs because epidermal, cortical and vascular
systems are present in the arrangement typical of dicotyledonous axes. The
epidermis and cortex composing the body of the mature haustorium are similar
to the cortex and epidermis of the parent root. The central portion of the body
(axial system-Fineran, 1963a) contains vascular tissue. Progressing from the
parent root through the haustorium towards the host the successive regions
traversed are: (1) the vascular core, (2) the central parenchymatous core
including the vessels (axial strands) that traverse it, and (3) the portion of the
haustorium contained within the host (the endophyte). A vascular cambium
develops between the central parenchymatous core and the cortex in older
haustoria.
The vascular core
The vascular core is the most conspicuous part of the haustorium and
historically has received the most study. In 1833 Bowman described the
vascular core of Lathraea and noted, “From its under surface, or point of
attachment, it sends down a tap or funnel-shaped process, generally straight but
sometimes curved, which penetrates through the cortical layers of the root to
various depths into the alburnum, but never into solid woody fibre. The tap
does not send out any lateral auxiliary branches; but a single filament or duct
passes through it, thickening in its progress upwards; and on its entering the
body of the bulb dividing into several branches, each traversing its substance in
a tortuous manner, and frequently intersecting the others, but finally
approaching and unitedly forming a confused mass under the point in contact
with the fibre. These vessels consist of a close series of minute semi-opaque oval
bodies, and have a moniliform or beaded structure” (Bowman, 1833: 405406).
The “confused mass” referred to above is the vascular core (Fineran, 1963b),
194
L. J. MUSSELMAN AND W. C. DICKISON
a compact mass of xylem in the approximate centre of the haustorium. This
region has also been variously termed the vessel mass (Thurman, 1966), the
plate of vessel elements (Chuang & Heckard, 1971), the compact tracheids
(Williams, 1960), the tracheid head (Ziegler, 1955), the tracheid plate
(Maybrook, 1917) and the plate xylem (Dobbins & Kuijt, 1973a).
Vascular cores are continuous with the xylem of the parent root by means of
transition zones (Simpson & Fineran, 1970), which have different structures in
the various genera. In these regions of the vascular cores scattered parenchyma
cells may be present. Tyloses are often abundant in the vessel elements, and
some vessel elements have unlignified cell walls. The transition zone is
particularly well-developed in occasional haustoria of Dasistoma macrophylla.
Clearings of vascular cores reveal that the structure of this part of the
haustorium is much more variable than previously reported. Three types of
haustoria may be distinguished on the basis of the morphology of the vascular
core: (i) the Siphonostegia type, (ii) the Striga type and (iii) the Aureolaria
type.
The Siphonostegiu type of haustorium is found only in Siphonostegia
(Kusano, 1908), Schwalbea americana (Plate 4F, G) and, in a modified form,
Cordylanthus. It is of particular interest because of its close resemblance to
haustoria of the Santalaceae. Schwalbea and Siphonostegia are the only genera
with an elongate neck and a welldeveloped transition zone (Plate4G). The
interrupted zone (Simpson & Fineran, 1970) is the region between the end of
the transitional zone and the vascular core and consists of abundant
parenchyma interspersed with scattered tracheary elements. At the junction of
the vascular core and interrupted zone is the sclerotic zone, a layer of
brachysclereids three cells in diameter. In most species, tyloses are common in
vessel elements located in the vicinity of the sclerotic zone. Tylose development within vessel members of a haustorium has been previously reported only
in Exocarpus (Santalaceae) by Benson (1910). Simpson & Fineran (1970) refer
to a dark-staining material occluding cells in this area but do not specifically
mention tyloses. The vascular core comprises a larger volume of the body of
the haustorium in Schwalbea (Plate 4F) and Siphonostegia than in other types
of haustoria and, as a result, encloses the parenchyma core. In the haustorium of
Cordylanthus hansenii the vascular core is multi-layered (unlike Schwalbea and
Siphonostegia) and encloses a region of parenchyma, but no interrupted or
transitional zones are present.
Alectra and Striga both have Striga types of haustoria with poorly developed
vascular cores consisting of only a few tracheary elements, some of which
contain tyloses, parallel to the long axis of the parent root (Plate 5A-C). The
similarity of these haustoria to haustoria of some members of the Orobanchaceae (Plate 5E)will be discussed later.
Five cell types compose the vascular core. These are vessel elements, vascular
tracheids, libriform fibres, parenchyma and phloeotracheids. Vascular
tracheids, libriform fibres and parenchyma (Plate 6G) resemble similar cell
types found in other parts of the plant. An estimated 95% of all cells of the
vascular core are vessel elements. These resemble the first-formed vessel
elements of lateral roots (Esau, 1965) and reflect the general shape of the
xylem elements whose development is not preceded by a “blocking out”
(Cutter, 1969), i.e. they retain the general shape of the parenchyma cells from
HAUSTORIUM IN PARASITIC SCROPHULARIACEAE
195
which they develop without undergoing elongation. The average length of 1000
vessel elements from the roots of Aureolaria uirginica (200 elements from the
roots of the secondary xylem of five different plants from one population) was
188.73 pm. The average length of 1000 vessel elements from the secondary
xylem of the vascular cores of the same plants was 43.88 pm. Bordered pits
with reduced pit diameters are present on the lateral walls of vessel elements of
the vascular core. Superficially, the mass of vessel elements in the Aureolaria
type of vascular core appear unorganized but clearings reveal that each vessel
element is a component of a much contorted vessel.
Certainly the most distinctive cell type of the vascular core is the
phloeotracheid, an imperforate element containing granules which give a
positive reaction to fast green (Plate 6D) and periodic-acid Schiff’s reagent
(Plate 6C). Although phloeotracheids are generally imperforate, Plate 6E
illustrates a perforate element. Phloeotracheids are known to occur only in
haustoria of the Santalaceae and Scrophulariaceae. Heinricher (1895) was the
first to describe these unusual haustorial cells, in Lathraea, and to record their
granular contents. The term phloeotracheid was introduced by Benson (1910)
and refers to the presumed dual function of these cells as water- and
food-conducting elements. Although phloeotracheids have been the subject of
recent study (Simpson & Fineran, 1970; Dobbins & Kuijt, 1973b; Fineran,
iped.), the extent of their occurrence in the Scrophulariaceae has not been
investigated. There was, furthermore, some doubt whether phloeotracheids
even occur in the Scrophulariaceae (Kuijt, 1969). Our observations reveal
phloeotracheids to be a consistent haustorial feature of all genera of the
parasitic Scrophulariaceae. Phloeotracheids are most abundant in the ventral
region of the vascular core (Plate 6B), although they are occasionally associated
with axial strands. Chuang & Heckard (1971) have stated that phloeotracheids
are not present in the haustorium of Cordylunthus; our observations, however,
document their presence in both the vascular core and endophyte (Plate 6F) of
this genus.
One of the most puzzling, yet frequently observed features of haustorial
anatomy is the lack of phloem in the body of the haustorium. Castilleja is the
only genus in which sieve elements have been reported (Kuijt & Dobbins, 1971),
although further study did not substantiate initial observations (Dobbins &
Kuijt, 1973a).
The axial strands
Axial strands (Stephens, 1912), also known as connecting strands (Thurman,
1966; Chuang & Heckard, 1971) and vessel strands (Dobbins & Kuijt, 1973a),
are vessels extending from the vascular core t o the host. The vessel elements
comprising these strands differ from elements of the vascular core in being
longer than broad (Plate 8D) and in possessing terminal perforation plates
(Plate 3A). Axial strands extend from the vascular core to the xylem of the
host and in different genera exhibit considerable variation in abundance (the
total number of strands per haustorium), shape (bowed or straight) and width
(number of vessel elements per strand). Buchnera (Plate 3F), Euphrasiu
(Plate 4C),Melurnpyrurn (Plate 4D) and Pediculuris (Plate 4B),possess a single,
centrally located axial strand, one vessel-element in width. Other genera possess
196
L. J. MUSSELMAN AND W. C. DICKISON
a single strand early in development but subsequently form additional strands.
A prominent bowing of the axial strands, conforming to the shape of the
cambium, occurs in those haustoria of the Aureolaria type that undergo
secondary growth (Plate 3A, C-E). In Macranthera flammea, however, the axial
strands remain straight (Plate 3B). In the Striga type of haustorium the axial
strands assume a slightly twisted appearance in longitudinal view and are all
located in the centre of the haustorium (Plate 5A, B).
The central parenchymatous core
The central parenchymatous core (Fineran, 1963b), also known as the core
parenchyma (Ziegler, 1955; Dobbins & Kuijt, 1973a), parenchymatous mass
(Chuang & Heckard, 1971), meristematic mass (Fraysse, 1906) and nucleus
(Stephens, 1912), is here defined as that portion of the mature haustorium
bounded laterally by the cortex (or cambium in older haustoria), dorsally by
the vascular core (except in the Siphonostegia type of haustorium), and
ventrally by the host. The parenchyma in the centre of the core often retains
the dense cytoplasm of the haustorial nucleus (see Development). The presence
of angular collenchyma in the central parenchymatous core was first described
by Dobbins & Kuijt (1973a) in haustoria of Castilleja and Pedicularis.
Collenchyma is also present in the central parenchymatous cores of Dasistoma,
Striga, Aureolaria and Agalinis. The amount of collenchyma varies considerably
among haustoria of the same species, perhaps reflecting differences in the
amount of stress present in different situations. Variations in the quantity of
collenchyma produced under different stresses has been experimentally
demonstrated in other plants (Cutter, 1969).
The vascular cambium
In some genera (Euphrasia, Malampyrum, Pedicularis), little if any cambial
activity is evident. The haustorial cambium arises in the periphery of the
central parenchymatous core and becomes contiguous with the cambium of the
parent root (Plate 6A). Growth rates of the cambium in the parent root and the
cambium of the body of the haustorium are not uniform. In fact, the cambium
of the body of the haustorium may be much more or much less active than the
cambium of the parent root. This difference in cambial activity becomes
strikingly evident as a result of the production of very large haustoria on very
small roots (Plate 2A, B). The host may influence cambial activity although no
data exists to support this contention. The haustorial cambium, like the
cambium of the root, is distinctly storied and produces an estimated 80%of its
derivatives t o the inside. In these respects, cambial development and function
in the parasitic Scrophulariaceae appear similar to the cambium in Exocarpus
(Fineran, 1963d). Scattered throughout the vascular core of Cordylanthus
hansenii are small patches of limited anomalous secondary growth.
Cortex
The cortex in the body of the mature haustorium is contiguous with the
cortex of the parent root and is composed of 5-10 layers of parenchyma cells.
HAUSTORIUM IN PARASITIC SCROPHULARIACEAE
197
Although elongate brachysclereids are present in the root cortex of many
species, only Dasistoma macrophylla possesses sclereids in the cortical region of
the haustorium (Plate 4A). In some haustoria the cortex may fold over the host
root and superficially resemble the mantle of the Santalaceae. The mantle of
the Santalaceae differs, however, by the absence of a collapsed zone and by the
production of intrusive cells from folds. Cortical folds are best developed in
haustoria attached to monocotyledonous roots, perhaps indicating that such
folds are associated with a lack of cambial activity in the host root. Folds are
also present in haustoria attached to small dicotyledonous roots and may be
the result of a disproportionate growth rate between host and parasite.
Perid erm
A periderm develops in all haustoria that undergo secondary growth. Unlike
the periderm of the root, the haustorial periderm originates in the inner layers
of the cortex although it eventually becomes continuous with the periderm of
the root.
Endophyte
The endophyte (Kuijt, 1969) or sucker (Kusano, 1908; Fineran, 1963d) is
the region of the haustorium that penetrates and undergoes subsequent
development within the host. It is unfortunate that Atsatt (1973) used the
term endophyte to describe a possible micro-organism in the haustorium of the
parasitic Scrophulariaceae. The endophyte is certainly an anatomically and
physiologically very important part of the parasitic organ, since it produces the
intimate association of host and parasite and, in a sense, embodies the very
essence of parasitism. Because of its ontogenetic plasticity in form and
variation, no generalizations regarding the shape of the endophyte can be made.
However, three growth stages can be distinguished: (i) intrusive (see Development), (ii) branched and (iii) mature. After the intrusive cells enter the host
root, periclinal divisions take place in the outer layers of the intrusive organ
that increase the diameter of the endophyte. The resulting cells have a storied
appearance. At this stage the endophyte may branch near its point of entry of
the host. In older haustoria no intrusive cells are evident and the host-parasite
interface consists only of parenchyma cells and vessel elements. At this late
stage of development in a large haustorium, the endophyte is as wide in
diameter as the body of the haustorium.
Except for tracheary elements, all cells of the endophyte are thin-walled and
have dense cytoplasm that becomes vacuolate with age. The parenchyma cells
of the endophyte are often branched. Intercellular spaces are lacking.
Haustorial xylem elements do not form contacts with host phloem, and xylem
contacts with host parenchyma ceIls are rare.
The tracheary elements of the endophyte are all vessel elements and deserve
special attention, since it has long been assumed that the parasitic members of
the Scrophulariaceae, except the few genera which lack chlorophyll, are water
parasites, that is, are dependent on their hosts for water. An understanding of
the elements involved in water transport is clearly necessary for an understanding of this type of parasitism. The vessel elements of the endophyte are
198
L. J . MUSSELMAN AND W. C. DICKISON
continuous with the axial strands, although isolated elements not forming a
part of any axial strand are occasionally found near host cells in Pedicularis.
These elements were first described by Sablon (1887a) and are illustrated in
Plate 8D. Terminal elements, or the vessel elements that terminate axial strands
and enter host cells, differentiate from intrusive cells and develop thick,
lignified walls (Plate 7D). The most distinctive features of terminal elements are
the pronounced lobing of the cells, a feature first recorded by Sablon (1887a)
in Melampyrum, and the presence of multiple perforation plates (Plate 7D, F),
i.e. each terminal lobe has several small perforation plates. Dobbins & Kuijt
(1973b) have indicated that the terminal elements in Castilleja have primary
walls only. The accumulation of cytoplasm near the growing tip of the
developing terminal element resembles intrusive growth in wood fibres (Esau,
1965). The tylosis-like growths within these elements have been recorded for
Striga senegalensis (Okonkwo, 1966) but are present in all genera. Terminal
elements usually enter host xylem elements through lateral wall pits (Plate
7B-D). Entrance through perforation plate openings also occurs but is
apparently less common (Plate 7F). Plate 7E is interpreted as illustrating an
intrusive cell just prior to entering a pit. Apparently, new xylem-to-xylem
contacts are made as the endophyte grows intrusively through the host and
the initial contacts become non-functional. In Alectra vogelii the axial strands
attach to host vessels both dorsally and ventrally (Plate 5D).
Selfparasitic haustoria
Self-parasitic haustoria can be classified into: (i) those which attach to roots
of a nearby plant of the same species (intraspecific parasitism), and (ii) those
which attach to roots of the same plant bearing the haustoria (auto-parasitism).
Auto-parasitic species included in this study are Agalinis linifolia, Aureolaria
grandiflora, A. virginica, A . flava, A. laevigata, Dasistoma macrophylla,
Euphrasia canadensis, Macranthera flammea and Melampyrum lineare. Species
of other families in which auto-parasitism is known have been documented by
Fineran (1965a) and Kuijt (1969). The following discussion deals with the
structure of auto-parasitic haustoria.
Although present in some annual species, e.g. Malampyrum lineare,
auto-parasitic haustoria are more abundant and attain largest sizes in root
systems of perennial plants, especially Aureolaria flava, A . virginica and
Dasistoma macrophylla. In these perennial species the roots become characteristically intermeshed and form a complex anastomosing mass that provides
many contacts for the development of auto-parasitic haustoria. In general shape
and size these haustoria resemble normal, that is, not self-parasitic, haustoria
(Plate 2J-L). If auto-parasitism becomes established when roots are young, the
distal portion of one of the roots dies back to the parasitic attachment
(Fineran, 1965a). In these situations the haustoria lack the globose shape of
normal haustoria and superficially resemble simple root grafts. These connections have in fact been assumed to be root grafts (Piehl, 1967), but their
anatomical organization is similar to that of normal haustoria.
The anatomical similarities between auto-parasitic and normal haustoria have
already been pointed out. The major differences are the small size of the
central parenchymatous core, the massive axial xylem, and the very broad,
HAUSTORIUM IN PARASITIC SCROPHULARIACEAE
199
unbranched endophyte present in auto-parasitic types. The vascular core is also
reduced in size although phloeotracheids are present. Unlike normal haustoria,
auto-parasitic haustoria can apparently also arise from older roots.
The production of self-haustoria between roots of neighbouring plants of the
same species (intra-specific parasitism) is well documented for the Scrophulariaceae (Euphrasia-Yeo, 1964; Orthocarpus-Atsatt & Strong, 1970; OdontitesGovier et al., 1967; Castilleja-Heckard, 1962; Pedicularis-Maybrook, 1917)
and the possible role of these haustoria in population nutrition has been discussed
(Atsatt & Strong, 1970). Fineran (1965a), in a detailed description of the
anatomy of self-parasitic haustoria and their role in the life history of
Exocarpus bidwillii (Santalaceae), suggested that seeds borne by the parasite
may germinate in the vicinity of the parent and form haustoria on its roots. In
this way the parent plant acts as a “nurse” for the parasite seedling until it
makes connections with other suitable hosts.
DEVELOPMENT OF THE HAUSTORIUM
Information on the developmental anatomy of haustoria of the Scrophulariaceae is limited. Descriptions of the earliest stages in ontogeny of the parasitic
organ were made on Melampyrum and Pedicularis by Koch (1887). Other
developmental studies include those of Stephens (1912) and Saunders (193 3)
on Striga asiatica, Thurman (1966) on Orthocarpus and Chuang & Heckard
(197 1) on Cordylanthus.
Reasons for the paucity of developmental data on root parasites no doubt
includes collecting difficulties resulting in the breaking of roots and haustorial
connections in field excavations. In addition, haustorial production is seasonal
in many genera. As a result, only seven species of the tribe Buchnereae
(Agalinis aphylla, A. maritima, Aureolaria grandiflora, A. pedicularia,
Dasistoma macrophylla, Macranthera flammea, Seymeria pectinata) and three
species of the Euphrasieae (Melampyrum lineare, Pedicularis canadensis, Striga
asiatica) were available for detailed developmental studies.
All roots whether primary, secondary or adventitious are capable of
producing haustoria; however, haustorial formation occurs only near the area
approximately delimited by the region of maturation along the root apex.
Haustoria are also produced near the apex of rhizomes in Agalinis linifolia.
The five stages in haustorial development are: (1) hypertrophy of the
cortical parenchyma of the haustorial root (development of the haustorial
nucleus that gives rise to the central parenchymatous core and axial strands),
(2) attachment to the host root, ( 3 ) periclinal divisions in the pericycle
(development of the vascular core), (4) penetration of host tissue, and ( 5 )
xylem continuity between host and parasite.
Haustorial nucleus
The first discernible stage in haustorial initiation is the swelling of cortical
parenchyma cells. The haustorial nucleus gives rise to the central parenchymatous core, axial strands, vascular cambium and the majority of the vascular
core. This appears to be a universal feature in the development of haustoria of
the Scrophulariaceae. The swelling a t this stage is termed a haustorial initial
15
200
L. J. MUSSELMAN AND W. C. DICKISON
(Thurman, 1966). When first recognizable it is about 1 mm in length and
consists of about 300 cells. Immediately after formation of the haustorial
initial a group of approximately 100 cells in the centre of the initial develop
very dense cytoplasm and enlarged nuclei. This very dark-staining area is
termed the nucleus (Barber, 1906), a term first applied to include all
parenchyma in the centre of the haustorium (Stephens, 1912). Later workers,
however, used the term to apply to hypertrophied cells only. To avoid
confusion the term haustorial nucleus will be used in this study. Although
actual measurements were not made, the size of the nuclei in these cells is
much larger than that of the nuclei in surrounding cells of the cortical
parenchyma and may indicate endopolyploidy. Most prominent in early
developmental stages, the haustorial nucleus remains recognizable in the
mature haustorium. Formation of the haustorial nucleus is closely followed by
periclinal divisions in the multiple epidermis. The pressure of cortical swelling
may stimulate these divisions much the same as secondary xylem development
initiates periderm formation (Esau, 1965). Other workers (Chuang & Heckard,
1971; Thurman, 1966) have described the first stages of development as taking
place in the root hypodermis. In such cases, however, it is not clear in what
sense the term hypodermis is being used.
Cell divisions form a four- to six-celled layer of compressed cells immediately
under the epidermis, termed the tiered layer (Kuijt, 1969), which in
longitudinal view resembles a stack of coins viewed on edge. The size of cells in
the tiered layer varies considerably and is apparently controlled by the amount
of resistance to penetration in the host root. For example, in Agalinis linifolia
penetrating a host root with a cortex composed of aerenchyma the cells of the
tiered layer are enlarged, whereas in Aureolaria pedicularia the tiered layer
upon entering the sclerenchymatous cortex of a fern root is composed of very
compact cells.
Attachment to the host root
At this stage the haustorium assumes a globose shape and is firmly pressed to
the host root. The firm attachment of the haustorium to the host takes place
while the haustorial nucleus is still developing, by means of the outermost cells
of the tiered layer. If the developing haustorium is separated from its potential
host, development ceases. As a result of this enlargement, the cells of the tiered
layer become stretched a t right angles to the long axis of the host root. Cells of
Orthocarpus in a similar condition have been illustrated by Thurman (1966).
These elongated cells have been variously termed palisade cells (Kuijt, 1969),
columnar cells (Malcolm, 1966) and apressorial cells (Williams, 1960). Palisade
cells are elongated, thick-walled and living a t maturity (Plate 8A,B). An
unidentified material that stains dark red with safranin and gives a negative
result with periodic-acid Schiff’s reagent is present between parasite and host
(Plate 8B). Thurman (1966) also referred to a dark-staining (with safranin)
substance between host and parasite cells. Rogers & Nelson (1 962) indicated
that no cellulose is present in this region in Striga asiatica. We were unable to
detect anything resembling “globules” reported by Piehl (1963) in the
host-parasite interface of Pedicularis canadensis.
In Macranthera flammea, Pedicularis canadensis and Striga asiatica structures
HAUSTORIUM IN PARASITlC SCROPHULARIACEAE
201
resembling root hairs arise from the haustorium and contact the host. These
root hairs have also been reported for Melampyrum lineare (Piehl, 1962a),
Pedicularis canadensis (Piehl, 1963), Rhinanthus (Kuijt, 1969), Orthocarpus
(Thurman, 1966) and Cordylanthus (Chuang & Heckard, 1971). In this study,
particular attention was paid t o the haustorial root hairs of Pedicularis
canadensis. Root hairs arise from the outer layer. of the multiple epidermis,
grow toward the host root that is often up to five millimeters away, and attach
to host cells by means of what appears to be a cementing substance similar to
that produced by palisade cells. Haustorial root hairs are unlike typical root
hairs in three ways: they are much longer, are not sloughed off as are regular
root hairs, and produce papillae-like growths in the region of contact with host
cells.
Development of the vascular core
All of the above development stages refer to the exogenous aspects of
haustorial development, i.e. no stelar tissues are involved. At the time the
haustorial nucleus becomes histologically distinguished, however, periclinal
divisions begin in the pericycle accompanied by anticlinal divisions in the
endodermis. Xylem is initially produced in a plane parallel t o the long axis of
the parent root in a manner similar to xylem development in lateral roots.
Production of xylem elements leads to an opening out of the endodermis, i.e.
divisions of the endodermis d o not keep pace with xylem development. The
number of xylem elements produced in the vascular core varies among different
genera and depends on the amount of secondary growth that takes place in the
parent root.
Penetration of host tissue
At this stage in development the haustorium is closely appressed to the host
root and the vascular core begins to develop. A longitudinal section of a
developing haustorium reveals a group of five to seven cells in the centre of the
host-parasite interface that are larger than surrounding cells and have more
densely staining cytoplasm. These cells have been termed intrusive cells (Kuijt,
1969) and in longitudinal section appear elongated in a plane at right angles to
the long axis of the host (Plate 9F). The intrusive cells arise from cells of the
muItiple epidermis and are the first cells of the haustorium to invade host
tissue. As viewed in transverse section, the intrusive cells, known collectively as
the intrusive organ (Kuijt, loc. cit.), are wedge-shaped (Plate 8A). Penetration
of host tissues appears t o be rapid, as very early stages are difficult t o locate in
sectioned material. An estimated 1000 haustoria were examined in this study
and approximately 25 were in the actual process of penetration. Penetration of
host cells is accomplished by a combination of intrusive growth and enzymatic
digestion. Penetration does not involve the rupture of the ventral portion of the
haustorium. Early stages in penetration are illustrated for Agalinis aphy lla
(Plate 9A,B), Agalinis linifolia (Plate 9C, D) and Seyrneria cassioides (Plate 9E).
Particularly striking is the plasticity of the intrusive cells, a fact also noted by
Dobbins & Kuijt (197313) in Castilleja. As illustrated in Plate 9B, intrusive cells
of Agalinis aphylla have entered a host cortical cell and are breaking through a
202
L. J. MUSSELMAN A N D W. C. DICKISON
small opening in the cell wall to invade a cell below. Conspicuously elongate
vacuoles are present in these cells. Only intrusive cells enter host roots
containing large amounts of sclerenchyma, e.g. those of Aristida stricta (Plate
9B). Plate 9D shows Agalinis linifolia entering an unidentified monocotyledonous root with abundant aerenchyma. In this case not only intrusive cells
but also cells of the tiered layer are entering the host.
The intrusive organ of Pedicularis canadensis has an organization different
from that observed in other genera. Two large apical cells that are roughly
triangular in longitudinal section and have very dense cytoplasm are subtended
by smaller cells with large vacuoles and less dense cytoplasm (Plate 9F).
Xylem continuity between host and parasite
The final stage in haustorial formation is xylem continuity between host and
parasite. Unlike cells of the vascular core, formation of xylem elements
composing the axial strands is preceded by blocking out (Plate 9D). This event
quickly follows penetration. In fact, xylem differentiation does not occur
unless penetration of the host has taken place. The direction of xylem
differentiation is from the host towards the vascular core. In Pediculuris many
xylem elements are formed in host tissue; the majority of these remain isolated
and do not become part of an axial strand (Plate 8D).
The primary haustorium
A primary haustorium is one which develops by the direct transformation of
a root apex into a haustorium. In contrast, secondary haustoria arise laterally
along the root. In the Scrophulariaceae, primary haustoria have been reported
for Striga asiatica and Lathraea squamariu (see Kuijt, 1969). The unusual
organization of the root apex of Striga asiatica has already been described. As
the root apex approaches the host root, the cells and nuclei of the apex enlarge
and apparently function as the intrusive organ, commencing penetration. A
broadening of the root apex follows the entry of the root into the host.
Development beyond this point apparently proceeds as in secondary haustoria,
but further work is needed to substantiate this.
DISCUSSION
The mature structure of the haustorium
Our observations show that the anatomical organization of the mature
haustorium is considerably more variable within the family Scrophulariaceae
than previously recorded (Kuijt, 1969). In most genera this variation is
correlated with other floral and vegetative features. The least variable haustorial
character is the dermal system and cortex, both resembling similar areas in the
root. The cortex of the haustorium of Dasistoma macrophylla is filled with
brachysclereids, a previously unrecorded feature of parasitic Scrophulariaceae.
Three general patterns of vascular cores may be distinguished: (1) the
Siphonostegia type in which the vascular core is a hollow, pear-shaped structure
borne on an elongate neck, (2) the Aureolaria type in which the vascular core
HAUSTORIUM IN PARASITIC SCROPHULARIACEAE
203
forms a solid mass of xylem elements that abut on the xylem of the parent
root, and ( 3 ) the Strigu type in which the vascular core is entirely lacking or
consists of only a few vessel elements. Likewise, the axial strands of each
haustorial type are distinctive in their origin and arrangement. In the
Siphonostegia type, axial strands arise at the tip of the vascular core. In the
Aureolaria type, axial strands are formed from the periphery of the vascular
core. In the Striga type, axial strands connect directly with the xylem of the
parent root.
The following discussion is an attempt to determine possible trends of
haustoria specialization within the parasitic genera of Scrophulariaceae studied.
Such a scheme must be considered tentative until all genera are examined.
If a haustorium is a modified lateral root, then a primitive haustorium should
be more root-like in structure than a structurally advanced haustorium. The
haustoria of Schwalbea and Siphonostegia both possess long necks surrounded
by an endodermis, i.e. more stelar tissues are involved in their development.
The similarity of the haustoria of these genera to those of the Santalaceae, a
family considered to be very distantly related to the Scrophulariaceae, is
discussed below. The Siphonostegia type of haustorium is considered primitive
within the Scrophulariaceae. Floral morphology corroborates this idea since
both Schwalbea and Siphonostegia (and the related Cymbaria) have posterior
sepals and two bracteoles subtending the flowers, floral characters considered
primitive for the tribe Euphrasieae (Pennell, 1935). The structure of the
Siphonostegiu type of haustorium will be treated in detail elsewhere.
Cordylunthus has a vascular core that is anatomically similar to that of
Schwalbea. The central parenchymatous core is enclosed by the vascular core,
no neck is present, and the vascular core abuts directly on the xylem of the
parent root. The Aureolaria type of haustorium could have been derived from
the Cordylanthus type by a shortening of the vascular core to form a disc-like
mass abutting on the parent root, and by a reduction in the amount of axial
xylem to form scattered strands that traverse the parenchymatous core.
However, many genera possessing the Aureolaria type of haustorium are
considered to be primitive in floral and vegetative characters (Pennell, 193 5 ) .
Therefore, the Aureolaria type of haustorium appears to be more specialized
than the Siphonostegia type but is found in genera considered to be primitive
in the context of the family. The independent evolution of parasitism in the
Buchnereae and Euphrasieae could explain this apparent anomaly regarding
putatively specialized haustoria in otherwise primitive genera. However, the
Aureolanu type of haustorium is well developed in some genera of the
Euphrasieae, especially Castilleja, indicating either that parasitism has arisen
twice within the family, or that the Aureolaria type of haustorium has
developed independently in each tribe.
Unfortunately, no clear intermediates between the Siphonostegiu type and
Striga type can be distinguished, although certain genera do show trends in the
reduction of xylem that may indicate specialization. Haustoria of Euphrusia,
Melarnpyrum, Pedicularis and Alectra (all considered to be advanced members
of the Euphrasieae) exhibit a reduction in the amount of xylem present in the
vascular core and also in the axial strands. Pedicularis is of particular interest as
a possible intermediate between the AureoZaria and the Striga types. The
isolated vessel elements of the endophyte in Pedicularis (Plate 8C) may
2 04
L. J . MUSSELMAN AND W. C. DICKISON
represent vestigial axial strands of which the development has been arrested,
resulting in the single axial strand that is characteristic of this genus.
It is reasonable to assume the primary haustorium of Striga asiatica
represents the most advanced haustorial type in the Scrophulariaceae.
Haustorial specialization in this species is correlated with the lack of
chlorophyll during much of its life history, reduction in leaves and lateral root
production, and the specialized apical organization of the root.
Development
Development of secondary haustoria is uniform among all genera of parasitic
Scrophulariaceae examined. This uniformity would appear to weaken the
theory of an independent origin of haustoria in the Buchnereae and
Euphrasieae. Initial stages are exogenous and include the development of a
region of hypertrophied cells in the root cortex at the region of maturation of
the root apex. This mass of swollen cells with enlarged nuclei, known as the
haustorial nucleus, gives rise to the central parenchymatous core, the axial
strands, the vascular cambium and part of the vascular core. The first-formed
elements of the vascular core, however, arise from stelar tissues. Cells of the
multiple epidermis and adjacent cells of the haustorial nucleus give rise to
intrusive cells that invade the host and differentiate into the endophyte. The
primary haustorium of Striga asiatica arises by the direct transformation of the
root apex into a haustorium.
Comparison of haustorial structure in Scrophulariaceae,
Santalaceae and Orobanchaceae
Anatomical comparisons between haustoria of plants of the Santalaceae and
Scrophulariaceae are desirable for several reasons. Both families include species
that are chlorophyll-containing root parasites. Despite the fact that the
Santalaceae are mainly tropical in distribution, considerable data are available
on haustorial structure in this family. The Santalaceae is also one of a complex
of interrelated families for which evolutionary trends relative to parasitism have
been worked out (Kuijt, 1965). Haustoria of the santalaceous genera Buckleya,
Nestronia, Comandra and Pyrularia (Table 1) were examined in the present
study to obtain comparative data.
Kusano (1908) noted that “the haustorium of Siphonostegia presents a close
resemblance to the organ of the Santalaceae”, but his evidence of parallel
evolution in haustorial structure in the two families was overlooked by
subsequent workers. The resemblance in haustorial anatomy of Siphonostegia,
Schwalbea and Santalaceae is of particular interest. Distinctive features
common to Siphonostegia, Schwalbea and some Santalaceae include the shape
of the vascular core and the presence of an interrupted zone. These are
unknown in other scrophulariaceous genera. The well-developed haustorial
neck of Schwalbea and Siphonostegia is also characteristic of many
Santalaceae, e.g. Buckleya distichophylla (Plate 5F). However, a uniform
feature of the haustorium of the Santalaceae is the collapsed layer which is
located in the cortex of the body. The collapsed layer may enfold and even
HAUSTORIUM IN PARASITIC SCROPHULARIACEAE
205
invade the host root. Kuijt ( 1 9 6 9 , in a stimulating review of the nature and
action of the haustorium in Santalalean families, suggested that the collapsed
layer may serve to advance the endophyte into the host in a manner similar to
the action of contractile roots. A collapsed layer is not present in the
haustorium of any member of the Scrophulariaceae examined in this study,
although the cambial layer in Sckwalbea may be superficially similar. Although
we did not observe haustorial glands in the santalaceous genera examined, Kuijt
(1969) noted that these glands are regular features of some haustoria of the
Santalaceae. Likewise, he observed that the intrusive cells of the haustoria of
some Santalaceae rupture or dissolve the haustorial epidermis.
The Orobanchaceae are morphologically similar to the Scrophulariaceae
subfamily Rhinanthoideae in aspects of floral and vegetative morphology
(Boeshore, 1920). Some authors have even combined the Rhinanthoideae and
the Orobanchaceae into one family (see Thieret, 1967). Like the Santalalean
complex, however, the Orobanchaceae exhibit a range of morphological and
anatomical variation in the parasitic organ that is not encountered in the
Scrophulariaceae. Haustoria of Orobancke uniflora, for example, resemble
haustoria of the Scrophulariaceae in general morphology and anatomy; but the
parasitic organ of Conopkolis americana, which consists of an intimate
intermingling of host and parasite tissue, or Epifagus virginiana, which
apparently involves a fungal relationship, bears little resemblance to the swollen
globose haustorium typical of the Scrophulariaceae. Species of Orobanchaceae
examined in this study are listed in Table 1.
The morphological continuity between haustorial structure in Striga and
Orobancke is noteworthy. The haustorial structure of these two genera is
similar in size, shape and the position and shape of the numerous, centrally
located axial strands. The axial strands are intertwined in both Orobancke
(Plate 5E) and Striga. Primary haustoria are apparently characteristic of the
Orobanchaceae (Kuijt, 1969) but in the Scrophulariaceae they are known only
in Striga and Latkraea.
The morphological interpretation of the kaustorium
The question of the morphological nature of the haustorium-is it a root or
an organ sui generis-is piquantly discussed in Kuijt (1969) and is not repeated
here. Haustoria differ in origin from lateral roots since they arise independently
of protoxylem position. The first stages of haustorial development are strictly
exogenous and the cortex is not ruptured during development. The first-formed
xylem elements of the vascular core are similar to the first-formed elements of
normal lateral root development, i.e. short and scalariformly thickened (Esau,
1965). Both roots and haustoria arise within primary tissues, although the
pericycle is active at different times in the development of each. Haustoria may
arise from rhizomes. At maturity both lateral roots and haustoria have a
three-layered arrangement of epidermal, cortical and vascular tissues characteristic of the general anatomy of angiosperm axes. Roots and haustoria both
function in the absorption and conduction of water and nutrients.
Suggestions that the haustorium represents a lateral root apex in which
development is delayed (Kuijt, 1969) hold promise in interpreting the structure
and function of the parasitic organ. Cutter & Feldman (1970) suggest that
206
L. J. MUSSELMAN A N D W. C. DICKISON
endopolyploidy may have a role in suppressing cell maturity in trichoblasts.
The large size of nuclei in the haustorial nucleus and the possibility that
endopolyploidy exists in these cells has been previously mentioned. Further
work would be desirable to determine the presence of endopolyploidy and its
possible function in haustorial development. Precursors of xylem elements are
often endopolyploid (see Cutter, 1969). The parenchymatous core may act as a
reservoir of cells that differentiate into vessels as the endophyte increases its
depth and breadth of penetration and as new axial strands differentiate. The
organization of the vascular core, a highly ordered mass of vessels, funnels the
axial strands into the parent root with maximum contact with parent root
xylem. Collenchyma may serve to support the growing organ since this tissue is
thought to serve such a function in other plant organs (Cutter, 1969).
The three types of vessel element found in the parent root, vascular core and
axial strand may reflect the influence of different levels of hormonal control.
The vessel elements of the parent root are formed in the manner typical of
angiosperms. The distinctive vessel elements of the vascular core are formed
without being “blocked out”, i.e. they do not elongate before maturation. The
vessel elements of the axial strands undergo elongation but only after host
penetration. This may be an indication of the influence of host growth factors
in haustorial development.
The effect of various growth regulators on the relative abundance of xylem
and phloem in stems is well known (see Cutter, 1969). An understanding of
hormonal control in haustorial development may provide a clue to an
understanding of the absence of phloem in this organ. The possible homeogenetic effect of host tissues on the development of haustorial cells has been
noted briefly by Dobbins & Kuijt (1973a). The development of axial strands is
definitely polar, i.e. the axial strands are always centrally located in the
Aureolaria and Striga types of haustoria.
The evolutionary origin of the haustorium
Several theories have been formulated in an attempt to explain the
evolutionary origin of haustoria. These include origin via grafts, as intimated by
Piehl (1967), microbial symbiosis (Atsatt, 1973) and root dimorphism (Kuijt,
1969).
The theory of origin by means of root grafts is appealing in its simplicity. It
would suppose that auto-parasitism preceded development of haustoria, i.e.
that auto-haustoria are root grafts that have evolved into haustoria. However,
root grafting, while common among woody plants (Graham & Bormann, 1966),
is unknown in herbaceous plants. More importantly, data from the present
study indicate that auto-haustoria are anatomically similar to normal haustoria
and simply represent haustoria that have responded to an unknown stimulus
produced by their own roots. The fact that such haustoria appear to be more
closely united with their “host” should not seem surprising considering that the
physiological barriers that must be overcome are certainly less in a neighbouring root than they might be in a host of a different family or even a different
division of the plant kingdom.
The theory of haustoria origin by microbial symbiosis has been advanced by
Atsatt (1973). This theory is based on the superficial resemblance of bacterial
HAUSTORIUM IN PARASITIC SCROPHULARIACEAE
207
nodules to haustoria. In 1916, Jiilg noted this resemblance but failed t o find
any evidence of a causal organism for the production of haustoria. N o bacteria
were observed in any haustorium. Atsatt’s idea (1973) stated that haustorial
production is caused by a symbiont, as yet unidentified, which became
incorporated into the cytoplasm and genome of the parasite and was capable of
being passed from generation to generation. The selective force for the
incorporation of the symbiont was the production of attachments to nearby
host plants, which compensated for the energy absorbed by the microbe. From
a morphological and anatomical standpoint this theory presents difficulties.
Root nodules have not been reported to invade neighbouring roots. Bacterial
infection threads were observed in root tips of several species in this study,
although the response to this infection in no way resembles the development of
either a bacterial nodule or a haustorium.
Kuijt has suggested that the parasitic organ arose by modification of a lateral
root into a parasitic organ. “Through some change in the physiology of the
root, or its juxtaposition with the root of an invading or otherwise rare species
having certain stimulatory root exudates which hitherto had not been
encountered, the growth of the former root is directed t o the latter, finally
growing into its tissues” (Kuijt, 1969: 209). While it is difficult at present to
even define the selective pressures involved in the evolutionary origin of
haustoria, one possible pre-adaptation was noted by Van Tieghem (in Sablon,
1887a), who suggested that a haustorium entered a host root in the same
manner in which a developing lateral root penetrates cortical tissue. At our
present state of knowledge, however, it is not clear whether enzymatic or
mechanical crushing is involved in the penetration of the lateral root through
the cortical tissue.
The tissue of the haustorium are considered by us to represent a lateral root
in which development is delayed and differentiation of vascular tissue is highly
specialized as a result of regulation by both indigenous and host growth factors.
Our views of the morphological nature of the haustorium are well stated by
Kuijt (1969: 190), “. . . I find no difficulty in accepting the view that these
organs are evolutionarily what they seem to be functionally, namely highly
modified roots. That haustoria in many ways dash with our traditional
concepts about the roots of vascular plants should not lead us astray. The
haustorium of parasitic angiosperms represents a root in function and
evolutionary origin.”
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KEY TO LABELLING OF PLATES
C cortex
CA cambium
COL collenchyma
EN endodermis
ENP endophyte
HR host root
HN haustorial nucleus
IC intrusive cells
I2 interrupted zone
PE pericycle
PHT phloeotracheid
PL palisade layer
PP perforation plate
PR parent root
PRX parent root xylem
RH root hair
SCL sclerenchyma
TY tylosis
V vessel
VC vascular core
EXPLANATION OF PLATES
PLATE 1
Seedlings
A. Agalinis aphylla, epigeal germination (Musselman 4418) ( ~ 2 5 0 ) .
B. Striga asiatica, longitudinal section of young seedling. Arrow indicates seed coat ( ~ 1 5 0 ) .
C. Orrhocarpus purpurascens Note acropetal sequence of root hair differentiation (Atscrft s.n.)
(~150).
D. Agalinis aphylla, seedling with spiralled root hairs (Musselman 4418) ( ~ 3 0 0 ) .
E. Schwalbea americana, seedling with branched root hair (Musselman 4577) ( ~ 3 0 0 ) .
F. Agalinis aphylla, seedling with spiralled root hair and fungal hyphae (7) (Musselman 4418)
(x457).
PLATE 2
General haustorial morphology
(A-L to same scale)
A. Seymeria cassioides on Pinus faeda. Note abundance of haustoria (arrows) on host root.
B. Dasisroma macrophylla, host roots detached (Musselman 4642).
C. Agalinis purpurea on Digiraria sanguinea (Musselman 4642).
D. Agalinis setacea on unidentified woody host. Arrows indicate haustoria. Note necrosis of
parasite root distal to point of attachment of haustoria (Musselman 3836).
E. Agalinis maritima on Disrichlis spicafa. The largest haustoria are at arrows on roots of host
(Musselman 4639).
F. Castilleja coccinea. root system and detached haustoria (arrows). Note the small size of the
haustoria which are borne on secondary roots (Musselman 4575).
G. Schwalbea americana on Ilex glabra. Arrows point to the small haustoria (Musselman 4577).
H. Alectra vogelii on Vigna unguiculafa. Haustoria (arrows) are attached near bacterial nodules,
which are very small and difficult to discern in this photograph (Okonkwo s.n.).
I. Nestronia umbellula on Pinus faeda, ventral view of a large haustorium which encircles the
host in a manner characteristic of the Santalaceae (Musselman 4428).
J. Dasisroma macrophylla. Arrow indicates auto-parasitism (Musselman 4634).
K. Dasistoma macrophylla, showing a globose haustorium in auto-parasitism between a young
and old root (arrow). Note auto-parasitism between three lower roots (Musselman 4634).
L. Dasistoma macrophylla roots. Arrow indicates auto-parasitism between roots of equal age.
Haustorium to extreme left of arrow is detached from host (Musselman 4634).
HAUSTORIUM IN PARASITIC SCROPHULARIACEAE
PLATE 3
Vascular core and axial strand morphology
A. Aureolaria pedicularia. Axial strands are bowed, the host root detached (Musselman 1278).
(Scale as in E).
B. Macranthera flammea. Axial strands are not conspicuously bowed. The vascular core is
massive. The host root is detached (Musselman 4393). (Scale as in C).
C. Seymeria pectinata on Pinus serotina (Musselman s.n.).
D. Agalinis linifolia, showing the characteristic discshaped vascular core of this tribe
(Buchnereae). Axial strands are bowed (Musselman 4403). (Scale as in E).
E. Tomanthera aun‘cuiara. The opening at t h e bottom of the figure gives the false impression
that the axial strands enter the host root (detached here) by a rupturing of haustorial tissue
(Musselman et al. 3833).
F. Buchnera floridana, young haustorium. The vascular core is just beginning to develop
(Musselman 4126a). (Scale as in C).
PLATE 4
Vascular core and axial strand morphology
A. Arrows indicate sclereids, found only in Dasisroma macrophylla, which occlude the axial
strands (Musselman 4634) (scale as in E).
B. Pedicularis lanceolata o n Carex sp.. showing the single axial strand (Musselman 4625).
C. Euphrasia canadensis with a single axial strand (Cochran 250) (scale as in B).
D. Melampyrum lineare. Note poorly developed vascular core and single axial strand in
haustorium (Musselman 431 3a) (scale as in E).
E. Castilleja coccinea. Older haustorium with bowed axial strands (Musselman 4575).
F. Schwalbea americana. Ventral portion of young haustorium, showing distinctive vascular
core (Musselman 4577) (scale as in E).
G. The same, illustrating prominent neck (at arrow) and transition zone (scale as in E).
PLATE 5
Vascular core and axial strand morphology
A. Srriga asiatica. In this species t h e vascular core is not readily discernible from t h e axial
strands (Musselman 4646a) (scale as in B).
B. As in A, but a ventral view of t h e haustorium showing attachment t o Sorghum uulgare (at
lower right). In this species t h e axial strands are compacted.
C. Alectra uogelii, showing fusion of the axial strands dorsally. Note that t h e axial strands also
branch ventrally t o attach t o the root of Vigna unguiculata (Okonkwo s.n.) (scale as in B).
D. As in C, but showing axial strands that curve under host xylem, thus attacking host xylem
from both “top” and “bottom”.
E. Orobanche unifrora, axial strands (Leonard 5422) (scale as in B).
F. Buckleya distichophylla, young haustorium. Arrow indicates parenchyma core (Musselman
4588).
PLATE 6
Cambium and phloceotracheids
A. Cordylanthus hansenii, cambium (Heckard 2 1 30) ( ~ 3 0 0 ) .
B. Dasistoma macrophylla, layer of phloeotracheids in ventral portion of vascular core
(Musselman 4634) ( ~ 3 0 0 ) .
C. Macranthera flammea, phloeotracheids of stained with fast-green. Individual granule at arrow
(Musselman 4403) ( ~ 1 0 0 0 ) .
D. Agalinis linifolia, phloeotracheid stained with periodic acid-Schiff‘s reagent. Individual
granule a t arrow (Musselman s.n.) ( ~ 1 0 0 0 ) .
E. Cordylanrhus hansenii, perforate phloeotracheid (Heckard 2130) ( ~ 1 0 0 0 ) .
F. Cordylanrhus hansenii, phloeotracheids in endophyte (Heckard 2 1 30) ( ~ 1 0 0 0 ) .
G. Cordylanthus hansenii, parenchyma cell of vascular core (Heckard 2130) ( ~ 1 0 0 0 ) .
16
211
212
L. J. MUSSELMAN AND W. C. DICKISON
PLATE 7
Intrusive cells and terminal xylem elements
A. Seymeria cassioides, intrusive cells occupying what was once a xylem ray in the root of Pinus
serotina. Host cells are on both sides of the elongate intrusive cells (Musselman 4638)(~1000).
B. Seymeria cassioides, single intrusive cell in xylem ray of Pinus serotina. Note that this cell is
invading four different tracheids of the host at one time (Musselman 4638)(~457).
C . Seymeria cassioides, intrusive cell entering a tracheid of Pinus serotina via a lateral wall pit
(Musselman 4638)(x 1000).
D. Seymeria cassioides, mature vessel element in tracheid of Pinus serotina. This element is
lobed, each lobe has several perforation plates (Musselman 4638)(~1000).
E. Seymeria cassioides, intrusive cell, undergoing lignification at lower left, in Pinus serotina
root (Musselman 4638)(~1000).
F. Aureolaria grandiflora, terminal vessel element of an axial strand in vessel element of Ufmus
rubra root. This vessel element has five perforation plates-one terminal and two on each side
(Musselman 923)(~1000).
PLATE 8
Palisade and endophyte cells
A. Agalinis linifolia, attachment to Aristida sfricta root. The palisade layer is attached t o a fibre
in the host root. Note the wedgeshaped endophyte below the host fibre (Musselman s.n.)
(xlSO).
B. As in A. Note the prominent nuclei in palisade cells (~300).
C. Pedicularis canadensis on unidentified host root (centre and extreme bottom of figure).
Many vessel elements have already differentiated (Musselman 4567)(~300).
D.As in C. Note row of eight vessel elements attached to host vessel (~457).
PLATE 9
Early stages of host entry
A. Agalinis aphylla, longitudinal section at very earliest stage in penetration of an unidentified
host (Musselman 4418)(~457).
B. Agalinis aphylla, intrusive cells which have broken through one host cell and entered the
cell beneath. Arrow at right indicates host-parasite interface (Musselman 4418)(~457).
C. Longitudinal section of young haustorium of Agalinis linifolia penetrating an unidentified
monocotyledonous root with abundant sclerenchyma (Musselman 4403)(~457).
D. Agalinis linifolia penetrating a root of an aquatic plant. Note the size of the advancing
endophyte and the differentiation of future axial strands at arrow (Musselman 4403) ( ~ 1 5 0 ) .
E. Seymeria cassioides, longitudinal view of intrusive cells penetrating the thick sclerenchymatous root of Aristida srricra. Compare with D, where the invading portion of the haustorium is
much larger (Musselman 4638)(~1000).
F, Intrusive cells of Pedicularis camdensis on unidentified dicotyledonous host. Note the
distinct organization of the endophyte (Musselman 4638)(~457).
I3ot.J.
Linn. SOL.,70 (1975)
I,. J . MIISSE1,MXN
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\V. C . DICKISON
Plate 1
Rot.?. I,inn. Soc., 70.(1975)
Plate 2
n o t . J. I , h . Soc., 70 (1975)
Plate 3
Plate 4
Bot. J . Lim. Sac., 70 (1975)
L. J. MUSSELMAN
AND
W.
c. DICKISON
Uot. J. Linn. Soc., 70 (1975)
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J. RIUSSEI,LI.AN
AND
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Bot.9. Linn. Sac., 70 (1975)
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Plate 8
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Bat. J. Linn. Soc., 70 (1975)
L. J . RllJSSELMAN
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