Annals of Botany 84, 475–499, 1999
Article No. anbo.1999.0942, available online at http :\\www.iealibrary.com on
Microsporogenesis in Monocotyledons
C A R O L A . F U R N E S S * and P A U L A J . R U D A L L
Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3AE, UK
Received : 20 January 1999
Returned for revision : 5 April 1999
Accepted : 21 June 1999
This paper critically reviews the distribution of microsporogenesis types in relation to recent concepts in monocot
systematics. Two basic types of microsporogenesis are generally recognized : successive and simultaneous, although
intermediates occur. These are characterized by differences in tetrad morphology, generally tetragonal or tetrahedral,
although other forms occur, particularly associated with successive division. Successive microsporogenesis is
predominant in monocotyledons, although the simultaneous type characterizes the ‘ lower ’ Asparagales. Simultaneous
microsporogenesis also occurs in Japonolirion and PetrosaŠia (unplaced taxa), some Araceae, Aponogeton, Thalassia
and Tofieldia (Alismatales), Dioscorea, Stenomeris and Tacca (Dioscoreales), and some Commelinanae : Arecaceae
(Arecales), and Cyperaceae, Juncaceae and Thurniaceae (Poales). Simultaneous microsporogenesis is of phylogenetic
significance within some of these groups, for example, Asparagales, Dioscoreales and Poales. An intermediate type
is recorded in Stemonaceae (Pandanales), Commelinaceae (Commelinales) and in Eriocaulaceae and Flagellariaceae
(Poales). There is little direct relationship between microsporogenesis type and pollen aperture type in monocots
(except for trichotomosulcate and pantoporate apertures), although trichotomosulcate apertures in monocot
pollen, and equatorial tricolpate and tricolporate apertures in eudicot pollen, are all related to simultaneous microsporogenesis.
# 1999 Annals of Botany Company
Key words : Microsporogenesis, monocotyledons, pollen apertures, phylogeny, tetrads, simultaneous, successive,
systematics.
INTRODUCTION
Microsporogenesis has been shown to be an important
character in monocot phylogeny through work on the order
Asparagales (Rudall et al., 1997). In this paper, microsporogenesis is reviewed in a systematic context throughout
the monocotyledons, based both on records from the
literature and from our own observations. New records are
presented, particularly for taxa that are taxonomically
isolated or otherwise hold a critical systematic position.
Microsporogenesis type is evaluated in relation to recent
monocot phylogenies, and also in relation to pollen aperture
type. Apertures in monocot pollen are either distal (located
across the distal pole in the tetrad) or derived from distal
apertures, for example, disulcate, spiraperturate and pantoporate. Inaperturate pollen is widespread and common in
monocotyledons (Furness and Rudall, 1999 a, b).
In angiosperms generally, two basic types of microsporogenesis are recognized : successive and simultaneous.
In successive microsporogenesis, a callose wall is laid down
separating the two daughter cells after the first meiotic
division, this is known as the dyad stage. Tetrads resulting
from successive division are tetragonal (or isobilateral), Tshaped, linear, rhomboidal or decussate. In simultaneous
microsporogenesis, the second meiotic division immediately
follows the first, with no wall formation until four nuclei are
present. The resulting tetrads are tetrahedral. Decussate
* For correspondence. Fax j44 (0)181 332 5278, e-mail
c.furness!rbgkew.org.uk
0305-7364\99\100475j25 $30.00\0
tetrads are also associated with simultaneous microsporogenesis, since the centres of the daughter cells (in two
pairs) are arranged in a tetrahedral orientation (Muller,
1970). Actually, intermediates exist between the two
microsporogenesis types (see reviews by Murty, 1964 ;
Bhandari, 1984 ; Blackmore and Crane, 1998). In the
‘ modified simultaneous ’ type, an ephemeral cell plate is laid
down after the first meiotic division, which then disappears
and simultaneous cytokinesis occurs, or sometimes the
second division quickly follows the first, before the cell plate
is completely formed. There are also two different modes of
cell cleavage, although again, intermediates can occur.
Generally, successive divisions occur by the formation of
centrifugal cell plates and simultaneous by centripetal
furrows, although this may not always be the case. The
patterns of organelle and plastid distribution also differ
during successive and simultaneous microsporogenesis
(Rodkiewicz, Kudlicka and Stobiecka, 1984).
MATERIALS AND METHODS
Material examined
Material was obtained from the living collections of the
Royal Botanic Gardens, Kew (HK : followed by Gardens
accession number), or collected from the wild (collectors
name and collection number given). K indicates material
from the spirit collection of the Kew Herbarium.
Species examined with both light (LM) and transmission
electron microscopy (TEM). Anigozanthos flaŠida DC. (HK :
1983-4125), Anthurium andraeanum Linden (HK : 498-63# 1999 Annals of Botany Company
476
Furness and Rudall—Microsporogenesis in Monocots
49801), Carex elata All. ‘ Bowles Golden Sedge ’ (HK : s.n.),
C. pendula Huds. (HK : s.n.), Dioscorea sylŠatica Ecklon
(HK : 1994-796), Eriophorum Šaginatum L. (HK : 307-7602977), Ficinia gracilis Schrad. (HK : 1997-6062), Globba
atrosanguinea Teijsm. & Binn. (HK : 302-84-03036), Luzula
forsteri DC. (HK : 1982-177), Narthecium ossifragum Huds.
(Furness & Rudall 1, UK), Tacca chantieri Andre! (HK :
1994-948), T. pinnatifida J. R. Forst. & G. Forst. (HK : 02186-00329), Tradescantia Širginiana L. (HK : 1983-426),
Typha laxmanni Lepech. (HK : 1995-257).
Species examined with differential interference microscopy
(DIC). Blandfordia grandiflora R.Br. (HK : 1968-1105),
Eriocaulon thwaitesii Koern. (K : E. Barnes B9, S. India),
Japonolirion osense Nakai (Hokkaido University Botanic
Garden 11826), Mayaca fluŠiatilis Aubl. (s.n., Brazil),
Narthecium ossifragum (Furness & Rudall 1, UK),
PetrosaŠia borneensis Becc. (K : Chew, Corner & Stainton
601, Mt. Kinabalu), Sciaphila albescens Benth. (K : N. Y.
Sandwith 1095, British Guiana), Tofieldia sp. cf. okubai
Makino (HK : 1979-5209), Triglochin procerum R.Br (Jacobs
S. J. 6548), Xyris trachyphylla Mart. (M. G. Sajo 16n12n97,
Brazil).
Methods
LM and TEM. Anthers dissected out of fresh buds were
placed in 2n5 % glutaraldehyde in 0n1  cacodylate buffer
(pH 7n2), de-aerated under vacuum for 1 h and fixed for
16–20 h at 4mC. They were then washed in cacodylate buffer,
postfixed in 1 % buffered osmium tetroxide for 3 h at room
temperature and washed again. Anthers were dehydrated
through an ethanol series followed by three changes of
100 % ethanol and embedded in LR White resin (London
Resin Co., Reading, UK) in gelatin capsules. Semithin
(approx. 1 µm) sections were cut using a Reichert Ultracut
and a dry glass knife, stained with toluidine blue, and
examined using a Nikon Labophot light microscope with
normal brightfield optics to determine the stage of development. Appropriate stages were mounted in DPX (SigmaAldrich Co., Gillingham, UK) and photographed using the
same microscope and a Nikon AFX-II camera attachment
(for example, Globba atrosanguinea, Fig. 5 H, I). Ultrathin
(gold) sections were then cut using a diamond knife, stained
with uranyl acetate followed by lead citrate in an LKB
Ultrostainer and examined using a JEOL JEM-1210 TEM.
DIC. For examination of microsporogenesis using differential interference microscopy (DIC), flowers of suitable
stages were fixed in FAA and transferred to 70 % alcohol,
the anthers were then removed and dissected on a microscope slide in a few drops of a modified version of Herr’s
clearing fluid (lactic acid : chloral hydrate : phenol : clove
oil : Histoclear, in proportions 2 : 2 : 2 : 2 : 1 by weight). The
slides were examined using differential interference contrast
(DIC) optics on a Leitz Dialux 20 photomicroscope. In
some taxa (for example, Juncaceae) pollen is shed as tetrads,
but in most taxa tetrads are present only in young buds,
making this character less accessible, and often several sizes
of bud have to be dissected to obtain the required tetrad
stages.
RESULTS AND DISCUSSION
Results are presented in Table 1 and discussed below in
a systematic context. The system of monocot relationships used here is based on Chase et al. (1995 b) and Chase
et al. (1999), and the orders are those recognized by the
Angiosperm Phylogeny Group (1998).
Records of microsporogenesis type for 191 taxa both
from the published literature and from our own observations
of 23 taxa are presented in Table 1. We have used literature
records from more than one source for each taxon where
possible to increase the level of reliability. More recent
records may include LM or TEM photographs (but not
always) and older records may have line drawings (but not
always). Nevertheless, when these records are arranged
according to the independent (mainly molecular) phylogeny,
a definite pattern emerges. Taxa which do not fit this pattern
or where further data are required (for example, some
Araceae and Eriocaulaceae) are discussed below. We have
found the work of some older authors such as Schnarf
(1931), for example, to be generally substantiated by more
recent data.
We have attempted to subdivide the process of microsporogenesis into types based on the patterns observed at
different stages of microspore development. Three basic
microsporogenesis types are recognized in Table 1 (see
Introduction) : (1) successive, where dyads and\or tetragonal, T-shaped, linear, rhomboidal or decussate tetrads
are described ; (2) simultaneous, where dyads are not
described and tetrads are tetrahedral or decussate ; and (3)
intermediate or irregular, where there are ephemeral cell
plates or the second division occurs quickly after the first,
before the cell plate is completely formed, and tetrads may
be described as irregular. Actually, as in many developmental processes, a continuum may exist between all three
categories, dependent upon the exact mode and timing of
meiosis (Blackmore and Crane, 1998), however, the types
recognized above do appear to have systematic significance
(see below).
‘ PrimitiŠe ’ dicotyledons
We have used the term ‘ primitive ’ dicotyledons to refer to
the phylogenetically ‘ basal ’ angiosperm groups : Ceratophyllales, Laurales, Magnoliales and Piperales, and some
unplaced familes including Amborellaceae, Austrobaileyaceae and Canellaceae (Angiosperm Phylogeny Group,
1998). These groups are all characterized by monosulcate or
monosulcate-derived pollen. Among the ‘ primitive ’ dicotyledons, which include the putative sister groups to the
monocotyledons, many taxa have simultaneous microsporogenesis, for example in Illiciaceae, Schisandraceae
and Winteraceae (Hayashi, 1960 ; Walker, 1974), which are
unplaced within the ‘ primitive ’ dicots according to the
Angiosperm Phylogeny Group (1998). Some other ‘ primitive ’ dicots have successive microsporogenesis, such as
Ceratophyllum (Ceratophyllales–Ceratophyllaceae : Takahashi, 1995), Hedycarya and Tambourissa (Laurales–
Monimiaceae : Sampson, 1982 ; Rowley and Flynn, 1990–
Furness and Rudall—Microsporogenesis in Monocots
477
T     1. Microsporogenesis and pollen aperture type in monocotyledons ; arrangement based on the orders of the Angiosperm
Phylogeny Group (1998). For Asparagales, see Rudall et al. (1997). References to Stenar (1925), Schnarf (1931), Dahlgren,
Clifford and Yeo (1985) and Grayum (1991) include literature cited therein
Taxon
Microsporogenesis type and source
  
Japonoliriaceae
Japonolirion
Simultaneous (this paper, Fig. 1 A, B)
Petrosaviaceae
PetrosaŠia
Simultaneous (this paper, Fig. 1 C)
Triuridaceae
Andruris
Successive (Ru$ bsamen-Weustenfeld, 1991)
Sciaphila
Successive (Wirz, 1910 ; Schnarf, 1931 ; Ohga and
Sinoto, 1932 ; Ru$ bsamen-Weustenfeld, 1991 ; this
paper Fig. 1D)
Seychellaria
Successive (Ru$ bsamen-Weustenfeld, 1991)
Pollen aperture type and source
Monosulcate (Takahashi and Kawano, 1989)
Monosulcate (Caddick et al., 1999 a)
Inaperturate (Ru$ bsamen-Weustenfeld, 1991)
( ?) Monosulcate (Ru$ bsamen-Weustenfeld, 1991),
monosulcate (Grayum, 1992)
Inaperturate or ( ?) monosulcate (Ru$ bsamenWeustenfeld, 1991)
Inaperturate or monosulcate (Ru$ bsamen-Weustenfeld,
1991), possibly inaperturate (Grayum, 1992)
Triuris
Successive (Ru$ bsamen-Weustenfeld, 1991)
-

Acorales :
Acoraceae
Acorus
Successive (Grayum, 1991)
Monosulcate (Grayum, 1992 ; Rudall and Furness,
1997)
Alismatales :
Alismataceae
Alisma
Successive (Stenar, 1925 ; Schnarf, 1931)
Successive (Schnarf, 1931)
Successive (Schnarf, 1931)
Successive (Schnarf, 1931)
Pantoporate (Chanda, Nilsson and Blackmore, 1988 ;
Grayum, 1992)
Pantoporate (Chanda et al., 1988)
Pantoporate (Chanda et al., 1988)
Pantoporate (Chanda et al., 1988 ; Grayum, 1992)
Simultaneous and successive (Stenar, 1925 ; Schnarf,
1931)
Monosulcate (Zavada, 1983 ; Dahlgren et al., 1985 ;
Grayum, 1992)
Successive (Grayum, 1991)
Successive (Stenar, 1925 ; Grayum, 1991 ; this paper,
Fig. 1 E–H), simultaneous (Gow, 1913)
Successive (Stenar, 1925), successive and simultaneous
(Maheshwari and Khanna, 1956)
Successive (Pacini and Juniper, 1983)
Successive (Palm, 1920, as Microcasia ; Grayum, 1991)
Successive (and simultaneous) (Banerji, 1937)
Successive (Stenar, 1925 ; Schnarf, 1931)
Successive (Stenar, 1925 ; Grayum, 1991)
Simultaneous (Gow, 1913)
Successive (Palm, 1920 ; Stenar, 1925 ; Grayum, 1991)
Successive (Grayum, 1991)
Successive (Stenar, 1925 ; Grayum, 1991)
Successive (Grayum, 1991)
Successive (Grayum, 1991)
Successive (Grayum, 1991)
Inaperturate (Grayum, 1992)
Diporate, 3–4 porate, polyporate, rarely inaperturate
(Grayum, 1992)
Inaperturate (Grayum, 1992 ; Ohashi, Murata and
Takahashi, 1983)
Inaperturate (Grayum, 1992)
Inaperturate (J. Bogner, reported in Grayum, 1992)
Inaperturate (Grayum, 1992)
Ulcerate (Erdtman, 1952 ; Grayum, 1992)
Inaperturate (Grayum, 1992)
Inaperturate (Grayum, 1992)
Monosulcate (Grayum, 1992)
Inaperturate (Grayum, 1992)
Monosulcate (Grayum, 1992)
Inaperturate (Grayum, 1992)
Inaperturate (Grayum, 1992)
Inaperturate (Grayum, 1992)
Successive (Stenar, 1925 ; Schnarf, 1931)
Monosulcate (Chanda et al., 1988 ; Grayum, 1992)
Successive (Ducker, Pettitt and Knox, 1978)
Successive (Yamashita, 1976)
Successive (Ducker et al., 1978 ; Pettitt, 1981)
Inaperturate (Ducker et al., 1978)
Inaperturate (Pettitt and Jermy, 1975)
Inaperturate (Ducker et al., 1978 ; Pettitt, 1981)
Successive (Stenar, 1925 ; Schnarf, 1931)
Successive (Schnarf, 1931)
Successive (Pettitt, 1981)
Inaperturate (Erdtman, 1952)
Inaperturate (Pettitt, 1980)
Inaperturate (Pettitt and Jermy, 1975 ; Pettitt 1980,
1981)
Inaperturate (Erdtman, 1952)
Inaperturate (Erdtman, 1952)
Inaperturate (Takahashi, 1994)
Monosulcate-operculate (Erdtman, 1952)
Inaperturate (Pettitt 1980, 1981)
Damasonium
Echinodorus
Sagittaria
Aponogetonaceae
Aponogeton
Araceae
Ambrosina
Anthurium
Arisaema
Arum
Bucephalandra
Colocasia
Lemna
Peltandra
Philodendron
Pothos
Spathyphyllum
Symplocarpus
Synandrospadix
Theriophonum
Zantedeschia
Butomaceae
Butomus
Cymodoceaceae
Amphibolis
Halodule
Thalassodendron
Hydrocharitaceae
Elodea
Enhalus
Halophila
Hydrocharis
Limnobium
Ottelia
Stratiotes
Thalassia
Successive (Schnarf, 1931)
Successive (Schnarf, 1931)
Successive (Schnarf, 1931 ; Islam, 1950)
Successive (Schnarf, 1931)
Simultaneous (Pettitt, 1981)
478
Furness and Rudall—Microsporogenesis in Monocots
T     1. (cont.)
Taxon
Microsporogenesis type and source
Pollen aperture type and source
Successive (Schnarf, 1931)
Inaperturate or faintly monosulcate (Sharma,1967)
Successive (Schnarf, 1931) ; mostly successive but
irregular (this paper, Figs. 1 I, 2A, B)
Inaperturate (Cranwell, 1953 ; Grayum, 1992)
Successive (Stenar, 1925 ; Schnarf, 1931)
Inaperturate (Erdtman, 1952 ; Grayum, 1992)
Successive (Stenar, 1925 ; Schnarf, 1931)
Successive (Palm, 1920 ; Stenar, 1925 ; Schnarf, 1930)
Pantoporate (Chanda et al., 1988)
4–5 porate (Chanda et al., 1988)
Successive (Stenar, 1925 ; Schnarf, 1931)
Inaperturate (Kuprianova, 1948 ; Pettitt and Jermy,
1975 ; Zavada, 1983)
Potamogetonaceae
Potamogeton
Successive (Stenar, 1925 ; Schnarf, 1931)
Ruppia
Successive (Stenar, 1925 ; Schnarf, 1931)
Inaperturate (Kuprianova, 1948 ; Cranwell, 1953 ; Pettitt
and Jermy, 1975 ; Grayum, 1992)
Inaperturate (Cranwell, 1953 ; Pettitt and Jermy, 1975),
tritenuate (Grayum, 1992)
Scheuchzeriaceae
Scheuchzeria
Successive (Schnarf, 1931)
Inaperturate (Kuprianova, 1948 ; Erdtman, 1952 ;
Zavada, 1983 ; Grayum, 1992)
Simultaneous (Stenar, 1925 ; Huynh, 1976 ; this paper,
Fig. 2 C)
Disulcate (Schulze, 1978b ; Huynh, 1976 ; Takahashi and
Kawano, 1989 ; Dı! az Lifante, Dı! ez and Ferna! ndez,
1990)
Successive (Schnarf, 1931)
Inaperturate (Cranwell, 1953 ; Pettitt and Jermy, 1975 ;
Grayum, 1992)
Successive (Stenar, 1925 ; Schnarf, 1931 ; Pettitt and
Jermy, 1975)
Inaperturate (Pettitt and Jermy, 1975)
Successive (Palm, 1920 ; Stenar, 1925 ; Schnarf, 1931)
Successive (Schnarf, 1931)
Ulcerate (Harling, 1958)
Ulceroidate to sulcoidate (Harling, 1958 ; Grayum,
1992)
Successive (Cheah and Stone, 1975 ; Periasamy and
Amalathas, 1991)
Ulcerate (Cheah and Stone, 1975 ; Huynh, 1980 ; Huynh
and Stone, 1981), possibly inaperturate (Grayum, 1992)
Successive or intermediate and irregular (Palm, 1920),
successive (Stenar, 1925 ; Schnarf, 1931)
Monosulcate (Van der Ham, 1991)
Velloziaceae
Barbacenia
Unknown
Vellozia
Successive (Stenar, 1925 ; Schnarf, 1931 ; Dutt, 1970 b) ;
Monosulcate (Ayensu, 1972 ; Ayensu and Skvarla,
1974), disulcate (Halbritter and Hesse, 1993)
Inaperturate ? (Small, indistinct pores) (Ayensu, 1972 ;
Ayensu and Skvarla, 1974)
Vallisneria
Juncaginaceae
Triglochin
Lilaeaceae
Lilaea
Limnocharitaceae
Hydrocleys
Limnocharis
Najadaceae
Najas
Tofieldiaceae
Tofieldia
Zannichelliaceae
Zannichellia
Zosteraceae
Zostera

Pandanales :
Cyclanthaceae
CarludoŠica
Cyclanthus
Pandanaceae
Pandanus
Stemonaceae
Stemona
Dioscoreales :
Burmanniaceae
Apteria
Burmannia
Campylosiphon
Successive (Ru$ bsamen, 1986)
Successive (Stenar, 1925 ; Schnarf, 1931 ; Arekal and
Ramaswamy, 1973 ; Ru$ bsamen, 1986)
Successive (Ru$ bsamen, 1986)
Dictyostega
Gymnosiphon
Miersiella
Successive (Ru$ bsamen, 1986)
Successive (Ru$ bsamen, 1986)
Successive (Ru$ bsamen, 1986)
Corsiaceae
Unknown
Dioscoreaceae
Dioscorea
Tamus
Simultaneous (Stenar, 1925 ; Schnarf, 1931 ; this paper,
Fig. 2 D-G)
Simultaneous (Schnarf, 1931)
Inaperturate, monosulcate (Ru$ bsamen, 1986)
1-, 2-(3-, poly-) porate, monosulcate (Chakrapani and
Raj, 1971 ; Ru$ bsamen, 1986)
(1-)2-porate (Chakrapani and Raj, 1971 ; Ru$ bsamen,
1986)
2-porate (Chakrapani and Raj, 1971 ; Ru$ bsamen, 1986)
Inaperturate (Ru$ bsamen, 1986)
2(1)-porate (Chakrapani and Raj, 1971 ; Ru$ bsamen,
1986)
Monosulcate (Erdtman, 1952), monoporate (Caddick et
al., 1999 a)
Monosulcate, 2–3 sulcate (Erdtman, 1952 ; Radulescu,
1973 ; Zavada, 1983)
Disulcate (Clarke and Jones, 1981)
Furness and Rudall—Microsporogenesis in Monocots
479
T     1. (cont.)
Taxon
Nartheciaceae
Narthecium
Microsporogenesis type and source
Pollen aperture type and source
Successive (Stenar, 1931 ; this paper, Figs 3G-I, 4
A–C)
Monosulcate (Schulze, 1978b ; Takahashi and Kawano,
1989)
Simultaneous (Caddick et al., 1999 a)
Monosulcate (Erdtman, 1952 ; Caddick et al., 1999 a)
Simultaneous (Stenar, 1925 ; Schnarf, 1931 ; this paper,
Figs 2H, I, 3 A-F), possibly successive (Palm, 1920)
Monosulcate (Cranwell, 1953 ; Grayum, 1992)
Successive (Schnarf, 1931)
Inaperturate (Cranwell, 1953), ulcerate (Ru$ bsamen,
1986)
Unknown
Successive or irregular (Rao, 1955)
4–5 pantoporate (Erdtman, 1952 ; Caddick et al., 1999 a)
Monosulcate (Caddick et al., 1999 a)
Successive (Stenar, 1925)
Monosulcate (Schulze, 1978 a)
Successive (Dutt, 1970 a)
Successive (Dahlgren and Lu, 1985)
Monosulcate (Erdtman, 1952 ; Dutt, 1970 a)
Inaperturate (Dahlgren and Lu, 1985)
Successive (Stenar, 1925)
2- polyporate (Radulescu, 1973), 2, 4 porate (Schulze,
1975 b)
Liliaceae
Fritillaria
Successive (Stenar, 1925)
Gloriosa
Lilium
Successive (Stenar, 1925)
Successive (Stenar, 1925 ; Heslop-Harrison, 1968)
Tulipa
Successive (Huynh, 1976)
Monosulcate, monosulcate-operculate (Radulescu, 1973 ;
Schulze, 1980)
Monosulcate (Radulescu, 1973)
Monosulcate (Erdtman, 1952 ; Radulescu, 1973 ;
Schulze, 1980 ; Halbritter and Hesse, 1993)
Monosulcate, monosulcate-operculate, trisulcate,
irregular, inaperturate (Romanov, 1959 ; Radulescu,
1973 ; Huynh, 1976 ; Schulze, 1980)
Stenomeridaceae
Stenomeris
Taccaceae
Tacca
Thismiaceae
Thismia
Trichopodaceae
AŠetra
Trichopus
Liliales :
Alstroemeriaceae
Bomarea
Campynemataceae
Campynema
Campynemanthe
Colchicaceae
Colchicum
Luzuriagaceae
Luzuriaga
Melanthiaceae
Veratrum
Zigadenus (as
Amaianthium)
Petermanniaceae
Petermannia
Philesiaceae
Lapageria
Smilacaceae
Smilax
Unknown
Monosulcate (Schulze, 1982 a)
Successive (Stenar, 1925)
Successive (Eunus, 1951)
Monosulcate-operculate (Radulescu, 1973 ; Halbritter
and Hesse, 1993)
Monosulcate-operculate (Halbritter and Hesse, 1993)
Successive (Conran, 1988)
Monosulcate (Erdtman, 1952)
Successive (Cave, 1966)
Inaperturate (Schulze, 1982 a, Cauneau-Pigot, 1988 ;
Furness and Rudall, 1999 a, b)
Successive (Stenar, 1925 ; Schnarf, 1931 ; Pacini and
Franchi, 1983)
Inaperturate, 1-sulcoidate, clypeate (Erdtman, 1952 ;
Schulze, 1982 b ; Pacini and Franchi, 1983 ; Furness
and Rudall, 1999 a, b)
Successive (Stenar, 1925 ; Takahashi, 1987)
Inaperturate (Takahashi, 1982, 1983, 1987)
Successive (Takahashi and Sohma, 1979)
Successive (Stenar, 1925)
Monosulcate (Takahashi and Sohma, 1979)
Monosulcate with insulae (Radulescu, 1973)
Trilliaceae
Trillium
Uvulariaceae
Disporum
Tricyrtis
Asparagales (not recorded
previously) :
Blandfordiaceae
Blandfordia

Unplaced Commelinanae :
Bromeliaceae
Aechmea
Simultaneous but irregular (this paper, Fig. 4 D–G)
Monosulcate (Schulze, 1982 c)
Successive (Schnarf, 1931)
Ananas
Bilbergia
Successive (Schnarf, 1931)
Successive (Schnarf, 1931)
Cryptanthus
Successive (Palm, 1920 ; Stenar, 1925 ; Schnarf, 1931)
Inaperturate, diffuse sulcate, sulcate with insulae, 2, 3,
4-porate, polyporate (Ehler and Schill, 1973 ;
Halbritter, 1992)
2-porate (Ehler and Schill, 1973 ; Halbritter, 1992)
Monosulcate with insulae, diffuse sulcate (Ehler and
Schill, 1973 ; Halbritter, 1992)
Monosulcate with insulae (Ehler and Schill, 1973 ;
Halbritter, 1992)
480
Furness and Rudall—Microsporogenesis in Monocots
T     1. (cont.)
Taxon
Microsporogenesis type and source
Pollen aperture type and source
Nidularium
Pitcairnea
Successive (Stenar, 1925 ; Schnarf, 1931)
Successive (Palm, 1920 ; Stenar, 1925 ; Schnarf, 1931)
Puja
Tillandsia
Successive (Schnarf, 1931)
Successive (Schnarf, 1931)
Vriesea
Successive (Stenar, 1925 ; Schnarf, 1931)
Dasypogonaceae
Dasypogon
Successive (Rudall et al., 1997)
Monosulcate (Erdtman, 1952 ; Chandra and Ghosh,
1976)
Hanguanaceae
Hanguana
Successive (Rudall, Stevenson and Linder, 1999)
Rapateaceae
Simultaneous (Tiemann, 1985)
Inaperturate (Linder and Ferguson, 1985 ; Rudall et al.,
1999 ; Furness and Rudall, 1999 a, b)
Monosulcate, trichotomosulcate (with monosulcate),
disulcate, zonisulculate (Carlquist, 1961)
Arecales :
Arecaceae
Arecoideae
Calamoideae
Simultaneous, Hydriastele and Pinanga simultaneous
and successive (Harley, 1996, 1998)
Successive (Harley, 1996, 1998)
Ceroxyloideae
Simultaneous (Harley, 1996, 1998)
Coryphoideae
Simultaneous and successive (Harley, 1996, 1998)
Nyphoideae
Phytelephantoideae
Commelinales :
Commelinaceae
Aneilema
Successive (Harley, 1996, 1998)
Unknown
Callisia
Cochliostema
Commelina
Successive (Schnarf, 1931, as Spironema)
Successive (Schnarf, 1931)
Successive (Stenar, 1925 ; Schnarf, 1931 ; Huynh, 1976,
as Commelinantia anomala)
Cyanotis
Intermediate (Rau, 1930)
Dichorisandra
Gibasis
Palisota
Tinantia
Successive (Schnarf, 1931)
Successive (Stevenson and Owens, 1978)
Successive (Palm, 1920 ; Stenar, 1925 ; Schnarf, 1931)
Succesive (Schnarf, 1931)
Tradescantia
Successive (Palm, 1920 ; Stenar, 1925 ; Schnarf, 1931 ;
Huynh, 1976 ; Nanda and Gupta, 1977 [as Rhoeo] ;
Tiwari and Gunning, 1986 a ; this paper, Figs 4 H, I,
5 A–E)
Successive (Schnarf, 1931)
Zebrina
Haemodoraceae
Anigozanthos
Xiphidium
Successive (Schnarf, 1931)
2-porate (Ehler and Schill, 1973 ; Halbritter, 1992)
Monosulcate with insulae, diffuse sulcate (Ehler and
Schill, 1973 ; Halbritter, 1992)
Monosulcate (Ehler and Schill, 1973 ; Halbritter, 1992)
Monosulcate, monosulcate with insulae, diffuse sulcate
(Ehler and Schill, 1973 ; Halbritter, 1992)
Monosulcate, monosulcate with insulae (Ehler and
Schill, 1973 ; Halbritter, 1992)
Monosulcate, disulcate, trichotomosulcate, monoporate,
triporate, incomplete zonosulcate (Harley, 1996)
Monosulcate, disulcate, monoporate, diporate,
inaperturate (Harley, 1996)
Monosulcate, trichotomosulcate, monoporate (Harley,
1996)
Monosulcate, disulcate, trichotomosulcate (Harley,
1996)
Zonosulcate (Harley, 1996)
Monosulcate (Harley, 1996)
Monosulcate, some spp. with insulae or pila (Erdtman,
1952 ; Sharma, 1967 ; Poole and Hunt, 1980)
Monosulcate (Poole and Hunt, 1980)
1–2 sulcate, some spp. with insulae, pila or spines
(Sharma, 1967 ; Poole and Hunt, 1980), triaperturate (as
Commelinantia anomala : Rowley and Dahl, 1962 ;
Huynh, 1976)
Monosulcate, some spp. with insulae or pila (Erdtman,
1952 ; Sharma, 1967 ; Poole and Hunt, 1980)
Monosulcate (Erdtman, 1952 ; Poole and Hunt, 1980)
Monosulcate (Poole and Hunt, 1980)
Monosulcate (Erdtman, 1952 ; Poole and Hunt, 1980)
Monosulcate, triaperturate (Erdtman, 1952 ; Sharma,
1967 ; Poole and Hunt, 1980)
Monosulcate (Sharma, 1967 ; Huynh, 1976 ; Poole and
Hunt, 1980)
Monosulcate (Poole and Hunt, 1967)
Successive (Stenar, 1927 ; this paper, Fig. 5 F, G)
Successive (Stenar, 1925 ; Schnarf, 1931 ; Simpson,
1989)
Diporate (or triporate) (Simpson, 1983)
Monosulcate (Simpson, 1983)
Philydraceae
Orthothylax
Successive (Hamann, 1966)
Philydrum
Successive (Hamann, 1966 ; Simpson, 1985)
Monosulcate (Hamann, 1966 ; Simpson, 1985 ; Grayum,
1992)
Monosulcate (Hamann, 1966 ; Simpson, 1985 ; Grayum,
1992)
Pontederiaceae
Eichhornia
Heteranthera
Successive (Stenar, 1925 ; Schnarf, 1931 ; Banerji and
Haldar, 1942)
Successive (Palm, 1920 ; Stenar, 1925 ; Schnarf, 1931)
Monochoria
Successive (Banerji and Haldar, 1942)
Disulcate (Simpson, 1987 ; Grayum, 1992)
Disulcate (Simpson, 1987), possibly monosulcate
(Grayum, 1992)
Disulcate (Simpson, 1987)
Furness and Rudall—Microsporogenesis in Monocots
481
T     1. (cont.)
Taxon
Microsporogenesis type and source
Pollen aperture type and source
Successive (Stenar, 1925 ; Schnarf, 1931 ; Huynh, 1976)
Disulcate (Huynh, 1976 ; Simpson, 1987 ; Grayum, 1992)
Successive (Stenar, 1925 ; Rowley and Skvarla, 1986 ;
Tiwari and Gunning, 1986 b), simultaneous
(Kracauer, 1930)
Inaperturate (Skvarla and Rowley, 1970 ; Rowley and
Skvarla, 1986)
Successive (Palm, 1920 ; Stenar, 1925 ; Schnarf, 1931)
Successive (Stone, Sellers and Kress, 1981)
Spiraperturate with a short colpus, spiraperturate with 2
pores, pantoporate (Punt, 1968)
Spiraperturate with a short colpus (Stone et al., 1981)
Successive (Palm, 1920 ; Stenar, 1925 ; Schnarf, 1931 ;
Stone, Sellers and Kress, 1979)
Inaperturate, functionally monoaperturate (Kress, Stone
and Sellers, 1978 ; Kress and Stone, 1983 ; Kress, 1986)
Marantaceae
Calathea
Successive (Schnarf, 1931)
Maranta
Successive (Stenar, 1925 ; Schnarf, 1931)
Phrynium
Thalia
Musaceae
Musa
Successive (Schnarf, 1931)
Successive (Schnarf, 1931)
Inaperturate (Erdtman, 1952 ; Furness and Rudall
1999 a, b)
Inaperturate (Erdtman, 1952 ; Saad and Ibrahim, 1965 ;
Sharma, 1967)
Inaperturate (Erdtman, 1952)
Unknown
Successive (Stenar, 1925 ; Schnarf, 1931 ; Juliano and
Alcala, 1933)
Inaperturate (Kuprianova, 1948 ; Erdtman, 1952 ;
Sharma, 1967)
Successive (Schnarf, 1931 ; Kronestedt-Robards and
Rowley, 1989)
Inaperturate (Saad and Ibrahim, 1965 ; Hesse and Waha,
1983 ; Kronestedt-Robards and Rowley, 1989)
Zingiberaceae
Alpinia
Successive (Schnarf, 1931)
Amomum
Successive (Schnarf, 1931)
Curcuma
Successive (Palm, 1920 ; Stenar, 1925 ; Schnarf, 1931)
Elettaria
Globba
Successive (Schnarf, 1931)
Successive (Schnarf, 1931 ; this paper, Fig. 5 H, I)
Zingiber
Successive (Theilade and Theilade, 1996)
Inaperturate, (monosulcate) (Sharma, 1967 ; Liang,
1988)
Inaperturate, (faintly monosulcate) (Sharma, 1967 ;
Liang, 1988)
Inaperturate, (monosulcate) (Sharma, 1967 ; Liang,
1988)
Inaperturate (Erdtman, 1952)
Inaperturate, (1–2 sulcate) (Sharma, 1967 ; Liang, 1988 ;
Furness and Rudall, 1999 a, b)
Inaperturate (Liang, 1988 ; Theilade et al., 1993 ;
Theilade and Theilade, 1996)
Pontederia
Zingiberales :
Cannaceae
Canna
Costaceae
Costus
Tapeinochilos
Heliconiaceae
Heliconia
Strelitziaceae
Strelitzia
Poales :
Abolbodaceae
Abolboda
Anarthriaceae
Anarthria
Centrolepidaceae
Brizula
Centrolepis
Cyperaceae
Bulbostylis
Carex
Successive (Tiemann, 1985)
Inaperturate (Carlquist, 1960)
Unknown
Ulcerate (Linder and Ferguson, 1985)
Successive (Hamann, 1975)
Successive (Hamann, 1975)
Ulcerate (Chanda, 1966 ; Hamann, 1975)
Ulcerate (Chanda, 1966 ; Hamann, 1975)
1-aperturate (Huang, 1972)
1–4 pores, basal pore dominant, or pores lacking or
obscure (Cranwell, 1953 ; this paper, Fig. 7 C)
1–3 sulci and 1 pore (Sharma, 1967)
Unknown
1–4 pores, basal pore dominant, or pores absent
(Cranwell, 1953)
Eriophorum
Ficinia
Fuirena
Hypolytrum
Isolepis
Kyllinga
Simultaneous (Tanaka, 1941)
Simultaneous (Juel, 1900 ; Tanaka, 1939 ; Khanna,
1963)
Simultaneous (Schnarf, 1931 ; Tanaka, 1941)
Simultaneous (Schnarf, 1931)
Simultaneous (Schnarf, 1931 ; Strandhede, 1965, 1973 ;
Dunbar, 1973), intermediate (Juel, 1900 ; Ha/ kansson,
1954)
Simultaneous (Schnarf, 1931 ; this paper, Fig. 6 B)
Simultaneous (this paper, Fig. 6 C)
Simultaneous (Schnarf, 1931)
Unknown
Simultaneous (Schnarf, 1931)
Simultaneous (Tanaka, 1941)
Mapania
Rhyncospora
Scleria
Unknown
Simultaneous (Tanaka, 1941)
Simultaneous (Tanaka, 1941)
Cyperus
Dulichium
Eleocharis
1-aperturate (Sharma, 1967)
Obscure (this paper, Fig. 6 F)
1-aperturate (Huang, 1972)
Ulcerate (Erdtman, 1952)
Unknown
1-sulcate, pantoaperturate or trichotomosulcate
(Sharma, 1967), 4-aperturate (Huang, 1972)
Ulcerate, rarely 2-poroid (Erdtman, 1952)
Basal pore (Erdtman, 1943)
1-aperturate (Huang, 1972)
482
Furness and Rudall—Microsporogenesis in Monocots
T     1. (cont.)
Taxon
Microsporogenesis type and source
Pollen aperture type and source
Simultaneous (Schnarf, 1931 ; Cranwell, 1953)
1–4 pores, basal pore dominant, or pores lacking or
obscure (Cranwell, 1953)
Unknown
Ulcerate (Chanda and Rowley, 1967)
Successive or intermediate and irregular (Palm, 1920) ;
successive or rarely with tetrahedral tetrads (Stenar,
1925 ; Schnarf, 1931 ; Arekal and Ramaswamy, 1980 ;
this paper, Fig. 9 C, D)
Mostly simultaneous, some successive tetrads
(Monteiro-Scanavacca and Mazzoni, 1978)
Successive (Ramaswamy and Nagendran, 1996)
Spiraperturate (Sharma, 1965 ; Thanikaimoni, 1965 ;
Ueno, 1980 ; Furness, 1985, 1988)
Successive or intermediate and irregular (Palm, 1920) ;
successive (Schnarf, 1931)
Ulcerate (Erdtman, 1952 ; Ferguson and Linder, 1985)
Hydatellaceae
Hydatella
Unknown
Trithuria
Unknown
Monosulcate or monoporate (Bortenschlager, 1966),
monosulcate (Hamann, 1976)
Monosulcate (Bortenschlager, 1966 ; Hamann, 1976 ;
Linder and Ferguson, 1985)
Scirpus
Ecdeiocoleaceae
Ecdeiocolea
Eriocaulaceae
Eriocaulon
Leiothrix
Syngonanthus
Flagellariaceae
Flagellaria
Joinvilleaceae
JoinŠillea
Juncaceae
Distichia
Juncus
Luzula
Oxychloe
Mayacaceae
Mayaca
Poaceae
Many genera
Agropyron
Oryza
Panicum
Paspalum
Phragmites
Triticum
Zea
Restionaceae
Elegia
Hypolaena
Leptocarpus
Restio
Sparganiaceae
Sparganium
Thurniaceae
Typhaceae
Typha
Xyridaceae
Xyris
Clypeate (Thanikaimoni, 1965)
Spiraperturate (Thanikaimoni, 1965 ; Ramaswamy and
Nagendran, 1996)
Unknown
Ulcerate (Chanda and Rowley, 1967)
Simultaneous (Schnarf, 1931)
Simultaneous (Schnarf, 1931), intermediate (Wulff,
1939)
Simultaneous (Stenar, 1925 ; Schnarf, 1931 ; Lambert,
1969, 1970, this paper, Figs 7 E–I, 8 A–D)
Simultaneous (Schnarf, 1931)
Unknown
Ulcerate (Cranwell, 1953)
Successive (this paper, Fig. 9 E)
Monosulcate (Erdtman, 1952)
Successive
Successive
Successive
Successive
Successive
Successive
Successive
(Schnarf, 1931)
(Huynh, 1972)
(Stenar, 1925)
(Stenar, 1925)
(Palm, 1920)
(Stenar, 1925)
(Stenar, 1925 ; El-Ghazaly and Jensen, 1986)
Ulcerate (Cranwell, 1953 ; this paper, Fig. 8 G)
Ulcerate (Heusser, 1971 ; Wingenroth and Heusser,
1983)
Successive (Stenar, 1925 ; Maheshwari, 1950)
Ulcerate (Huynh, 1972)
Ulcerate (Sharma, 1967 ; Page, 1978)
Ulcerate (Sharma, 1967 ; Page, 1978)
Unknown
Ulcerate (Erdtman, 1943)
Ulcerate (Sharma, 1967 ; Rajendra et al., 1978 ; ElGhazaly and Jensen, 1986)
Ulcerate (Skvarla and Larson, 1966)
Successive
Successive
Successive
Successive
Ulcerate
Ulcerate
Ulcerate
Ulcerate
(Kircher,
(Kircher,
(Kircher,
(Kircher,
1986)
1986)
1986)
1986)
(Chanda,
(Chanda,
(Chanda,
(Chanda,
1966)
1966)
1966)
1966 ; Linder and Ferguson, 1985)
Successive (Mu$ ller-Doblies, 1969)
Simultaneous (Hamann, 1961 ; Dahlgren et al., 1985)
Ulcerate (Cranwell, 1953 ; Grayum, 1992)
Ulcerate (Zavada, 1983 ; Dahlgren et al., 1985)
Successive (Stenar, 1925 ; Schnarf, 1931 ; Skvarla and
Larson, 1963 ; Asplund, 1972 ; Takahashi and Sohma,
1984 ; this paper, Figs 8 H, I, 9 A)
Ulcerate (Skvarla and Larson, 1963 ; Grayum, 1992)
Successive (Schnarf, 1931 ; Rudall and Sajo, 1999 ; this
paper Fig. 9 F)
1–3 sulcate, operculate (Erdtman, 1952)
1991), many (but not all) Annonaceae (Magnoliales :
Walker, 1971 ; Bygrave, 1999), and Aristolochia (Piperales–
Aristolochiaceae : Samuelsson, 1914). This character requires further review in this group, for example, Lauraceae
(Laurales) were described as successive but with pre-
dominantly tetrahedral tetrads (Heo, Van der Werf and
Tobe, 1998), although Stone (1987) described Sassafras as
simultaneous. The intermediate type of microsporogenesis
is recorded in Magnolia (Magnoliales–Magnoliaceae :
Hayashi, 1960).
483
Furness and Rudall—Microsporogenesis in Monocots
C
A
B
C
C
PT
PT
D
F
E
C
C
PT
G
H
I
F. 1. A, B, Japonolirion osense (DIC). A, Tetrahedral (Th) and decussate (D) tetrads. B, Tetrahedral tetrad. C, PetrosaŠia borneensis (DIC),
tetrahedral tetrad. D, Sciaphila albescens (DIC), first meiotic division. E–H, Anthurium andraeanum. E, Tetrads in an anther locule (LM). F–H,
Tetrads surrounded by thick callose (TEM). F, Tetragonal. G, Decussate. H, T-shaped. I, Triglochin procerum (DIC), tetragonal tetrad. C l
callose, PT l plasmodial tapetum. Bars : in A–D, I l 10 µm ; in E–H l 5 µm.
484
Furness and Rudall—Microsporogenesis in Monocots
Eudicots
Most eudicots have simultaneous microsporogenesis and
tricolpate or tricolpate-derived pollen, although both the
successive and simultaneous type are recorded in Nelumbo
(Nelumbonaceae : Kreunen and Osborn, 1999) and Proteaceae (Blackmore and Barnes, 1995). Nelumbonaceae,
Platanaceae and Proteaceae are now placed in a separate
order, Proteales, basal to the other eudicots, and may
represent relicts from an ancient group (Chase et al., 1993 ;
Angiosperm Phylogeny Group, 1998 ; Bremer, Bremer
and Thulin, 1998). It is possible that the developmental
mechanisms controlling microsporogenesis are more labile
in such groups. Simultaneous microsporogenesis in eudicots
is associated with three equatorial tricolpate apertures, or
apertures derived from these, such as tricolporate.
Unplaced monocot taxa
Japonolirion and PetrosaŠia, which are probably closely
related to each other, both have the simultaneous type of
microsporogenesis (Table 1, Fig. 1 A–C). Recent molecular
data have indicated a tentative relationship with Dioscoreales (Chase et al., 1999), where the simultaneous type
also occurs (see below), although inclusion of Japonolirion
and PetrosaŠia within Dioscoreales is not well supported
(for example, by a recent analysis by Caddick et al., 1999 b).
Triuridaceae are uniformly successive (Table 1, Fig. 1 D)
and of uncertain affinity, although recent rbcL sequence
data indicate they belong in Pandanales (Chase, pers.
comm.), which are also successive (see below).
Early-branching monocotyledons
Acorales. Acorus, which has successive microsporogenesis
(Table 1), was formerly included in Araceae, but is now
placed in a separate family, Acoraceae (Acorales), sister to
the rest of the monocotyledons.
Alismatales. The Angiosperm Phylogeny Group (1998)
included Araceae, the alismatid families and Tofieldiaceae
in Alismatales. Apart from Tofieldia (Tofieldiaceae), which
has simultaneous microsporogenesis (Fig. 2 C), most taxa of
this order have successive microsporogenesis (Table 1),
although there are a few records for the simultaneous type
in Araceae and alismatids (see below). The tapetum is
plasmodial throughout Alismatales, except in Tofieldia,
which has a secretory tapetum (as in Acorus), so if Tofieldia
is correctly placed here, then reversals have occurred in
these two characters. Reversals also occur in the same
two characters (although in the opposite direction) in
Hypoxidaceae (Lilianae–Asparagales : Rudall et al., 1997 ;
Furness and Rudall, 1998).
Most Araceae have successive microsporogenesis (Table
1), although there are some records of the simultaneous
type : according to Gow (1913), in Anthurium crystallinum
the appearance of the tetrads indicates that the divisions are
simultaneous, and he also described Philodendron wendlandii
as simultaneous, although did not give the tetrad type in
either case. Other records for Anthurium are successive, and
the mainly tetragonal tetrads are surrounded by thick
callose walls (Table 1, Fig. 1 E–H). Tetrads of Arisaema
wallichianum were described as isobilateral, decussate or
tetrahedral by Maheshwari and Khanna (1956), although
microsporogenesis was described as successive. Tetrahedral
and isobilateral tetrads were recorded in Colocasia antiquorum, although it may not be typical due to irregularities
in meiosis : the first meiotic division is irregular and some of
the chromosomes do not line up on the metaphase plate but
move to the poles. The daughter nuclei do not always
contain an equal number of chromosomes and the chromosomes remaining in the cytoplasm form diminutive spindles
(Banerji, 1937).
The simultaneous type has been recorded in the alismatid
taxa Aponogeton (together with successive) and Thalassia
(Table 1), although most alismatids are successive, for
example, Triglochin (Juncaginaceae : Figs 1 I, 2 A, B). Linear
tetrads occur in some Hydrocharitaceae : in Ottelia and
Thalassia they occur with tetragonal, T-shaped and intermediate tetrads, whereas in Halophila successive transverse
partitioning of an elongated microsporocyte forms a row of
reniform pollen grains dispersed together (Islam, 1950 ;
Pettitt, 1981). Elongated microsporocytes are also found in
Stenomeris (Dioscoreales : Caddick et al., 1999 a, see below).
In Ottelia and Thalassia, pollen is spherical and dispersed
singly. The tetrad configurations in Thalassia appear more
indicative of the successive type of microsporogenesis. The
callose special cell wall surrounding the tetrads is lacking in
some Cymodoceaceae (Amphibolis, Halodule and Thalassodendron) and Hydrocharitaceae (Halophila and Thalassia)
and these have inaperturate pollen lacking exine ; the walls
are composed of polysaccharides. This is associated with
hydrophilous pollination, as is filiform pollen in Amphibolis,
Halodule, Thalassodendron and Zostera (Yamashita, 1976 ;
Ducker, Pettitt and Knox, 1978 ; Pettitt, 1981). Hydrophily
has evolved independently several times within alismatids
(Les, Cleland and Waycott, 1997).
Lilianae
Lilianae (sensu Chase et al., 1995 b) comprise four
orders : Pandanales, Dioscoreales, Liliales and Asparagales,
although the monophyly of Lilianae is not supported by
molecular data (Chase et al., 1995 a).
Pandanales. All Pandanales (Cyclanthaceae, Pandanaceae, Stemonaceae and Velloziaceae) have successive
microsporogenesis (Table 1). However, in Stemona
(Stemonaceae) the second division generally rapidly follows
the first, sometimes before the first partition wall is
completely established. The orientation of the meiotic
spindles may give rise to a row of four cells (Palm, 1920), as
in Stenomeris and Tacca (Dioscoreales : see below). Unusual
microsporogenesis has also been recorded in Pandanus
odoratissimus, in which no callose is laid down. Division is
successive, and the two cells divide by centrifugal cleavage,
then the two naked protoplasts move apart from each other
before undergoing a second similar division (Periswamy and
Amalathas, 1991). Normal callose deposition was however
reported in P. parŠus (Cheah and Stone, 1975).
485
Furness and Rudall—Microsporogenesis in Monocots
C
A
B
C
ST
Th
ST
D
ST
C
D
E
F
C
C
G
H
I
F. 2. A, B, Triglochin procerum (DIC). A, Decussate tetrad. B, Irregular tetrad. C, Tofieldia sp. cf. okubai (DIC), tetrahedral tetrads. D–G,
Dioscorea sylŠatica. D, Tetrads in an anther locule (LM). E, Tetrahedral (Th) and a decussate (D) tetrad (LM). F, Tetrahedral tetrad (TEM).
G, Decussate tetrad (TEM). H, I, Tacca chantieri (LM). H, Tetrads in an anther locule. I, Tetrahedral tetrad. C l callose, ST l secretory tapetum.
Bars : in A–C l 10 µm ; in E–G, I l 5 µm ; in D and H l 20 µm.
486
Furness and Rudall—Microsporogenesis in Monocots
C
C
F
C
C
ST
ST
A
B
C
Th
N
F
N
C
D
N
C
C
D
D
E
F
TS
ST
Tg
G
H
I
F. 3. A, E, Tacca chantieri. A, Decussate tetrad (LM). E, Detail of the proximal faces of three young microspores in a tetrahedral tetrad (TEM).
B–D, F, Tacca pinnatifida. B, Decussate tetrad. C, Centripetal furrow forming at cytokinesis (TEM). D, Detail of a developing furrow (TEM).
F, Detail of the proximal faces, with nuclei, of four young microspores in a decussate tetrad (TEM). G–I, Narthecium ossifragum (LM). G, Tetrads
in an anther locule. H, Two tetragonal tetrads with the microspores in different orientations. I, A T-shaped (TS) and a tetragonal tetrad (Tg)
tetrad. C l callose, F l furrow, N l nucleus, ST l secretory tapetum. Bars l 5 µm ; except C and F which l 2 µm, D l 1 µm and G l 20 µm.
Furness and Rudall—Microsporogenesis in Monocots
Dioscoreales. In some Dioscoreales (Burmanniaceae and
Thismiaceae), microsporogenesis is successive, whereas in
others (Dioscoreaceae and Taccaceae), it is simultaneous
(Caddick et al., 1999 a ; Table 1). Dioscoreaceae and Taccaceae (Figs 2 D–I, 3 A–F) have both tetrahedral and some
decussate tetrads, and division is by centripetal furrowing in
Tacca (Fig. 3 C, D). Narthecium, which probably belongs in
this order (Chase, pers. comm.), has the successive type
(Figs 3 G–I, 4 A–C). Stenomeris has unusual elongated
microsporocytes which appear to undergo simultaneous
division, although the orientation of the meiotic spindles
may occasionally give rise to a row of four cells (Caddick et
al., 1999 a). Interestingly, some young tetrads with four cells
forming a row were described in Tacca (Palm, 1920),
although this was interpreted as possible successive division.
Microsporogenesis has not been observed in Corsiaceae or
Trichopodaceae (Caddick et al., 1999 a) ; Trichopus was
described as successive by Rao (1955), who illustrated
dyads, and tetragonal, T-shaped, decussate, and tetrahedral
tetrads.
Liliales. Liliales are uniformly successive (Table 1).
Asparagales. Asparagales consist of a paraphyletic ‘ lower ’
asparagoid grade with simultaneous microsporogenesis
and a ‘ higher ’ asparagoid clade with successive microsporogenesis (Rudall et al., 1997). Among the ‘ lower ’
asparagoids, in most Hemerocallidaceae trichotomosulcate
apertures are associated with simultaneous microsporogenesis and regular tetrahedral tetrads, for example, in
Dianella (Rudall et al., 1997). In Blandfordia (Blandfordiaceae : Table 1, Fig. 4 D–G), which was not previously
recorded for this character, microsporogenesis is simultaneous but irregular, with monosulcate apertures, as in
Aloe (Asphodelaceae : Rudall et al., 1997), confirming its
placement in the ‘ lower ’ asparagoids. A reversal to the
successive type occurs in Hypoxidaceae (see above).
Commelinanae
The monophyly of the superorder Commelinanae is well
supported by both molecular and morphological analyses,
but several commelinoid taxa are still currently unplaced
within the group, pending further analysis.
Unplaced Commelinanae. Bromeliaceae have successive
microsporogenesis, with fairly diverse apertures, including
monosulcate, 2–4 porate and inaperturate (Table 1). Recent
molecular data place them as sister to Poales (Chase et al.,
1999). Dasypogonaceae, the possible sister group to palms
(Chase et al., 1995 b), also have successive microsporogenesis
(Table 1). Hanguana (Hanguanaceae) is successive and the
inaperturate, spinulate pollen with a thick intine indicates
possible affinities with Zingiberales (Furness and Rudall,
1999 a, b ; Rudall, Stevenson and Linder, 1999 ), but
molecular data indicate Hanguana is in a clade with both
Zingiberales and Commelinales (Fay and Chase, pers.
comm.). Rapateaceae have simultaneous microsporogenesis
(Tiemann, 1985). The diverse aperture types (Table 1)
include trichotomosulcate frequently found with monosulcate apertures in two species of Schoenocephalium
(Carlquist, 1961), which indicates simultaneous micro-
487
sporogenesis and this suggests a possible relationship with
the Cyperaceae-Juncaceae-Thurniaceae clade in Poales.
Arecales. Both simultaneous and successive microsporogenesis occur in Arecaceae and the pollen apertures
are diverse, including (unusually) trichotomosulcate associated with the simultaneous type (Table 1). Arecaceae are
isolated and phylogenetically basal within the commelinoids,
thus the developmental mechanisms controlling microsporogenesis may be more labile, as in Proteales (see above).
Commelinales. The four families of Commelinales are
uniformly successive (Table 1, Figs 4 H, I, 5 A–G) and there
appears to be only one record which deviates from this type :
Cyanotis (Commelinaceae : Table 1), where an ephemeral
cell plate is laid down after the first division. This disappears
and tetragonal tetrads are formed by simultaneous furrowing. In Tradescantia, the tetrads are located inside vacuoles
in the plasmodial tapetum (Figs 4 H, I, 5 A–E), these
vacuoles disappear if the tonicity of the fixative is increased
(Owens, pers. comm.).
The distribution of amyloplasts during microsporogenesis
in Tradescantia was observed by Rodkiewicz et al. (1984).
At the beginning of cytokinesis they form a loose group
between the two nuclei, which are divided into two parts by
a broad zone of cytoplasm where the cell plate develops. In
the dyad, the amyloplasts encircle the nuclei and at the end
of the second meiotic telophase again occupy the middle
zone of each cell. In the early tetrad stage, amyloplasts are
at the proximal walls and nuclei are at the distal. Rodkiewicz
et al. (1984) compared this with the amyloplast distribution
in the eudicot Impatiens (asterids–Ericales–Balsaminaceae)
with simultaneous microsporogenesis. Here the amyloplasts
occupy the equatorial plane, forming a dense plate separating the cell into two zones ; this plate persists during the
second division of both nuclei and then reshapes to form a
four-lobed structure with the lobes lying between the nuclei.
The cell plates then appear and the amyloplasts group at the
proximal side of each tetrad and the nuclei at the distal side.
Zingiberales. Zingiberales are a relatively well-established
and coherent order, and are uniformly successive (Table 1).
The callose walls surrounding the microsporocytes, dyads
and tetrads are thin (Fig. 5 H, I) and pollen is mostly
exineless and inaperturate (see Furness and Rudall, 1999 a,
b, for a review). Division is by centripetal furrowing in
Globba (Fig. 5 H). Simultaneous division by centrifugal
extension of cell plates was recorded in Canna (Kracauer,
1930) but has not been confirmed by other workers who
have found it to be successive (Table 1).
Poales. The successive type is predominant in Poales,
although there are no records for Anarthria, Ecdeiocolea
and JoinŠillea, and Flagellaria is variable : either successive
or intermediate with irregular tetrads. However, major
exceptions are Cyperaceae (Figs 6 A–I, 7 A–D), Juncaceae
(Figs 6 E–I, 7 A–G) and the related family Thurniaceae,
which all have simultaneous microsporogenesis (Table 1).
They are also unusual in that the meiotic products remain
together to form permanent tetrahedral tetrads in Juncaceae
and Thurniaceae, while in Cyperaceae only one meiotic
nucleus survives to form pseudomonads.
Ephemeral cell plates have been reported at the dyad
stage in Eleocharis and Juncus (Juel, 1900 ; Wulff, 1939 ;
488
Furness and Rudall—Microsporogenesis in Monocots
C
C
S
C
ST
A
B
C
C
C
C
D
E
F
C
*
*
PT
G
H
PT
I
F. 4. A–C, Narthecium ossifragum (TEM). A, Tetragonal tetrad adjacent to a secretory tapetum (ST). B, Tetragonal tetrad with the microspores
in a different orientation to A. C, Detail of one microspore in a tetrad with the sulcus (S) developing at the distal face. D–G, Blandfordia grandiflora
(DIC). D, Irregular divison, possibly forming a dyad. E, Simultaneous division. F, Young tetrahedral tetrad before cytokinesis. G, Tetrahedral
tetrad. H, I, Tradescantia Širginiana. Tetragonal tetrads surrounded by the plasmodial tapetum (PT). H, (LM). I, (TEM). Arrows l spindle fibres,
C l callose, * l primary callose wall. Bars l 5 µm ; except C l 2 µm.
Furness and Rudall—Microsporogenesis in Monocots
Ha/ kansson, 1954), although they were not found by other
workers (Table 1). In Carex, the nucleus divides to give four
nuclei, which have a tetrahedral or decussate arrangement.
One nucleus becomes larger and remains in the centre of the
cell, while the three smaller ones migrate towards one end,
and a cleavage furrow or a cell plate separates them from
the functional nucleus. These smaller nuclei may also be
divided by septa and can undergo mitosis, although they
ultimately degenerate (Tanaka, 1939 ; Khanna, 1963). Their
remnants are sealed in by thick intine at the apex of the
pear-shaped pseudomonad (Fig. 7 A, B, D). The functional
nucleus divides to give a generative and a vegetative nucleus
(Fig. 6 H) and two spindle-shaped sperm cells are formed by
the generative nucleus (Fig. 6 I). These migrate to the basal
part of the pseudomonad where the pore is situated (Fig.
7 C). Microsporogenesis in other Cyperaceae which have
been examined appears to follow this pattern (Table 1, for
example, Eriophorum, Fig. 6 A, B, and Ficinia, Fig. 6 C–F),
although in Rhyncospora the nuclei apparently degenerate
in the basal part of the pseudomonad and the generative cell
is positioned towards the apex (Tanaka, 1941). Callose walls
surrounding the microsporocytes or young pseudomonads
appear to be absent in Cyperaceae (Fig. 6 A–D). In
Eleocharis, the four nuclei have a tetrahedral or tetragonal
arrangement, less commonly a linear one. They are separated
by cell plates whose degree of completeness varies between
individual tetrads. The degeneration of three of the nuclei
and formation of pseudomonads is similar to that described
in Carex (Dunbar, 1973 ; Strandhede 1965, 1973). A variety
of apertures have been described in Cyperaceae (Table 1),
including trichotomosulcate in Kyllinga (Sharma, 1967), but
further data are required.
Hypolytrum and Mapania have spheroidal, thick-walled
pollen with one distinct aperture (ulcus), although flattened
triangular grains with poroid apertures at two of the apices
are occasionally found in Mapania humilis (Erdtman, 1952).
Erdtman (1952) questioned if the Mapanioideae actually
form pseudomonads and this is currently under investigation. The pattern of exine sculpture of mapanioid genera
clearly differs from the usual granule type in other
cyperaceous grains (Koyama, 1969).
The four nuclei in Juncaceae are usually arranged
tetrahedrally and the cells are divided by centripetal furrows.
Callose walls are absent and exine is formed around the
outside of the entire tetrad (Meyer and Yaroshevskaya,
1976 ; Figs 7 E–I, 8 D–G). The resulting permanent tetrads
are of the calymmate type (Blackmore and Crane, 1988).
Intine is deposited along the furrows and at the outer edge
between adjacent microspores in Luzula (Fig. 8 A–F). Each
of the four pollen grains has a pore where the exine thins
and is underlain by a layer of electron-dense material
which is probably the oncus containing germination proteins
(Fig. 8 G).
Pollen of Hydatella inconspicua (Hydatellaceae) is also
shed as tetrads, with monosulcate or possibly monoporate
apertures, but as it is shrunken and possibly sterile the
tetrad type and microsporogenesis type are unknown
(Bortenschlager, Erdtman and Praglowski, 1966 ; Hamann,
1976). This suggests a possible relationship with Juncaceae
and Thurniaceae, or Typhaceae (see below), depending on
489
the microsporogenesis type ; the other species of Hydatella
and the related genus Trithuria are however monosulcate
monads (Table 1), which is an unusual aperture type in
Poales, which are predominantly ulcerate (although Mayaca
and Xyris are monosulcate : Table 1). Linder and Ferguson
(1985) reported a spinulate surface in Trithuria, which is
also found in Eriocaulon (for example, Furness, 1985).
The sister pair Typhaceae and Sparganiaceae are both
successive (Table 1) and pollen is shed as permanent tetrads
in some species of Typha. These are mainly tetragonal or
rhomboidal, although linear, T-shaped, decussate and
asymmetrical forms also occur, due to different spindle
orientations during the second meiotic division (Skvarla
and Larson, 1963 ; Fig. 8 H). The developing microspores
are surrounded by individual callose walls and each
microspore in a tetrad has an exine, they are joined by
fusion of the tecta to form acalymmate tetrads (Skvarla
and Larson, 1963 ; Takahashi and Sohma, 1979 ; Figs 8 I,
9 A, B).
Microsporogenesis is also mainly successive in several
families that are now regarded as either belonging to, or
closely allied to Poales (for example, Angiosperm Phylogeny
Group, 1998) : Abolbodaceae, Eriocaulaceae (but see below), Mayacaceae and Xyridaceae (Table 1, Fig. 9 C–F).
Recent molecular sequence data place Orectanthe (which is
very close to Abolboda) sister to Xyris, close to Eriocaulaceae
and embedded in Poales (Chase, pers. comm.).
Microsporogenesis in Eriocaulon is successive (Table 1,
Fig. 9 C, D), but there are rare records of tetrahedral
tetrads, or the second division very rapidly following the
first, sometimes before the cell plate is complete (intermediate type), forming irregular tetrads. Leiothrix is
simultaneous or successive according to Monteiro-Scanavacca and Mazzoni (1978), who reported mostly tetrahedral but some isobilateral tetrads. Most Eriocaulaceae
have spiraperturate pollen (Table 1), which may relate to
this variability in microsporogenesis, since this aperture
type may be associated with unusual tetrad configurations
or partitioning after meiosis (Furness, 1985). Leiothrix has
clypeate pollen apertures according to the illustration by
Thanikaimoni (1965) (a related type in which the aperture
divides the exine into regular plates : Halbritter and Hesse,
1995). Microsporogenesis is equivocal as a character for
Eriocaulaceae since they could be derived from either a
successive or a simultaneous ancestor ; however, they are
sister to Cyperaceae–Juncaceae–Thurniaceae in some analyses (for example, Chase et al., 1995 b) ; and the presence of
simultaneous microsporogenesis supports this placement.
CONCLUSIONS
Microsporogenesis is usually (but not always) consistent
within a family. Families where it is not are often phylogenetically early diverging lineages within a group, for
example, Annonaceae, Arecaceae, Nelumbonaceae and
Proteaceae. Indeed, among angiosperms, microsporogenesis
is more diverse within ‘ primitive ’ dicots and monocots than
in eudicots. This may be because the developmental
mechanisms that control microsporogenesis are more labile
in early-branching groups. In monocotyledons, reversals
490
Furness and Rudall—Microsporogenesis in Monocots
PT
C
PT
PT
A
B
PT
C
C
PT
*
*
C
PT
D
E
F
F
C
F
PT
G
IT
H
IT
I
F. 5. A–E, Tradescantia Širginiana, tetrads surrounded by a plasmodial tapetum. A, Two tetragonal tetrads with three microspores visible (LM).
B, Tetragonal tetrad with three microspores visible (TEM). C, T-shaped tetrad (LM). D, T-shaped tetrad, different orientation to C (TEM). E,
Irregular tetrad (TEM). F, G, Anigozanthos flaŠida. F, Dyads in an anther locule (LM). G, Detail of a dyad (TEM). H, I. Globba atrosanguinea
(LM). H, Formation of a dyad by centripetal furrowing. I, A dyad. C l callose, F l furrow, IT l invasive tapetum, PT l plasmodial tapetum,
* l primary callose wall. Bars l 5 µm.
491
Furness and Rudall—Microsporogenesis in Monocots
Mc
ST
ST
FN
N
A
B
C
ST
I
GN
VN
D
E
F
SC
FN
VN
V
SC
GN
G
H
H
II
F. 6. A, B, Eriophorum Šaginatum (TEM). A, Detail of a microsporocyte (Mc). B, Young pseudomonad with a functional nucleus and four nonfunctional nuclei visible (arrowheads). C–F, Ficinia gracilis. C, Young pseudomonads with their bases adjacent to the secretory tapetum and the
non-functional nuclei at the apices, separated by septa. A tetrahedral arrangement can be seen (arrows) (LM). D, Young pseudomonads in an
anther locule (LM). E, The generative nucleus and lobed vegetative nucleus (TEM). F, A mature pseudomonad (TEM). G–I, Carex elata (TEM).
G, Vacuolate pseudomonad. H, Pseudomonad with vegetative and generative nuclei. I, Two sperm (SC) cells migrating through the cytoplasm.
FN l functional nucleus, GN l generative nucleus, I l intine, N l nucleus, ST l secretory tapetum, V l vacuole, VN l vegetative nucleus.
Bars l 5 µm ; except A and I l 1 µm, and B and E l 2 µm.
492
Furness and Rudall—Microsporogenesis in Monocots
E
I
SC
I
ST
P
ST
A
B
C
E
F
E
I
D
ST
ST
N
N
G
H
I
F. 7. A, C, D, Carex elata (TEM). A, Remnants of a non-functional nucleus (arrow) close to the pseudomonad wall where the intine is
developing. C, Detail of the base of a mature pseudomonad with the pore (P) adjacent to the secretory tapetum. The sperm cells (SC) are near
the pore. D, Detail of the apex of a mature pseudomonad with remnants of the non-functional nuclei (arrows) sealed in by thick intine. B, Carex
pendula (LM). Mature pseudomonad with the base adjacent to the secretory tapetum and thick intine at the apex. E–I, Luzula forsteri. E,
Immature tetrahedral tetrad (LM). F, Mature tetrahedral tetrad (LM). G, Immature decussate tetrad (LM). H, Immature decussate tetrad (LM).
I, A furrow (arrows) developing between two nuclei of a tetrahedral tetrad (TEM). E l Exine, I l intine, N l nucleus, ST l secretory tapetum.
Bars l 5 µm ; except A l 0n5 µm, D l 1 µm and I l 2 µm.
493
Furness and Rudall—Microsporogenesis in Monocots
I
E
E
A
B
C
E
I
E
I
E
I
D
E
F
H
I
P
EL
G
F. 8. A–G, Luzula forsteri (TEM). A, A centripetal furrow (arrows) developing. B, Detail of a furrow (arrows) with intine and some exine
developing adjacent to the outer wall of a tetrad. C, Furrows (arrows) meeting at the junction of three cells of an immature tetrahedral tetrad.
D, A mature tetrahedral tetrad with three pollen grains separated by intine (with traces of exine, arrows) and exine around the outside of
the entire tetrad. E, Detail of layered intine and the exine at the junction of two pollen grains in the tetrad shown in D. F, Detail of the intine
and exine surrounding the tetrad. G, The pore (P) of one pollen grain of a tetrad underlain by an electron-dense layer (EL). H, I, Typha laxmanni.
H, Tetrads in an anther locule (LM). I, Four microspores of a permanent tetragonal tetrad (TEM). E l exine, I l intine. Bars l 1 µm ; except
D and I l 5 µm, and H l 20 µm.
494
Furness and Rudall—Microsporogenesis in Monocots
ST
*
E
*
A
B
C
ST
C
C
C
D
E
F
F. 9. A, B, Typha laxmanni (TEM). A, Three microspores of a permanent tetragonal tetrad. B, Detail of the fused exines of two microspores.
C, D, Eriocaulon thwaitesii (DIC). C, Dyad with a centrifugal cell plate forming (*), in a locule surrounded by secretory tapetum. D, Tetragonal
tetrad in a locule surrounded by secretory tapetum. E, Mayaca fluŠiatilis, tetragonal tetrad (DIC). F, Xyris trachyphylla, tetragonal tetrads.
C l callose, E l exine, ST l secretory tapetum. Bars : in A, B, F l 5 µm ; in C, D, E l 10 µm.
in Tofieldia (early-branching monocots–Alismatales) and
Hypoxidaceae (an early-branching ‘ lower ’ asparagoid),
may also reflect this tendency.
Microsporogenesis is predominantly successive in monocotyledons, apart from in Japonolirion and PetrosaŠia, a few
Alismatales, some Dioscoreales, the ‘ lower ’ Asparagales,
some Arecaceae, and some Poales. Simultaneous microsporogenesis is of systematic significance within these
groups, for example, in Dioscoreales, Asparagales, and
Poales. Comparison of this distribution with independentlyderived (mainly molecular) phylogenies indicate that it has
arisen several times independently within monocotyledons.
Comparisons of microsporogenesis type with pollen
aperture type in monocotyledons (Table 2) demonstrate
that there is no direct relationship between the two, with the
exception of trichotomosulcate apertures which are associated with simultaneous microsporogenesis (Rudall et al.,
1997), and pantoporate which are associated with successive.
Otherwise, the main monocot aperture types are found both
in taxa with successive and simultaneous microsporogenesis
(Table 2), and a change in microsporogenesis type does not
usually relate to a change in aperture type. The situation is
however probably more complex than this, since evidence
shows that aperture position is controlled by the orientation
of the microtubules of the meiotic spindle (Heslop-Harrison,
1971 ; Sheldon and Dickinson, 1983, 1986 ; Dickinson and
Sheldon, 1984). Trichotomosulcate apertures in monocot
pollen, and equatorial tricolpate and tricolporate apertures
in eudicot pollen, are all associated with simultaneous
microsporogenesis.
Detailed studies of individual apertures have revealed
some interesting observations, for example, Asphodeline,
Asphodelus and Eremurus (Asphodelaceae) have simultaneous microsporogenesis and the sulci may be either
Furness and Rudall—Microsporogenesis in Monocots
T     2. Relationship between the main pollen aperture
types in monocotyledons and microsporogenesis type
Aperture type
Microsporogenesis type
Monosulcate
Successive, for example, Acorus, Liliaceae,
Commelinaceae. Some simultaneous, for
example, some Dioscorea, Taccaceae,
Asphodelaceae and Blandfordiaceae (‘ lower ’
Asparagales : Rudall et al., 1997).
Simultaneous, for example, Tofieldia, some
Dioscorea ; successive, for example,
Pontederiaceae.
Simultaneous, for example,
Hemerocallidaceae (‘ lower ’ Asparagales :
Rudall et al., 1997), some Rapateaceae,
some Arecaceae.
Successive, for example, Cyclanthaceae,
Pandanaceae, Poaceae (Poales) ;
simultaneous, for example, Cyperaceae,
Juncaceae (Poales).
Successive, for example, Alismataceae, some
Burmannia, some Colchicum.
Successive, for example, Costaceae ;
simultaneous, for example, some Crocus
(Iridaceae : Rudall et al., 1997) ; both types
in Eriocaulaceae or intermediate.
Successive, for example, many Araceae,
Zingiberaceae ; simultaneous, for example,
some Iridaceae (Furness and Rudall,
1999 a, b).
Disulcate
Trichotomosulcate
Ulcerate
Pantoporate (or
polyporate)
Spiraperturate
(including clypeate)
Inaperturate
longitudinal (parallel to the longest axis of the grain) or
transverse (perpendicular to the longest axis of the grain)
(Schulze, 1975 a ; Huynh, 1976 ; Dı! az Lifante, 1996), compared with the longitudinal sulcus of Lilium (Liliaceae :
successive). It is unclear at present if these apertures are
oriented differently with respect to the tetrad, or merely
appear to be oriented differently in mature grains because
the individual microspores become elongated in different
directions ; further work is required.
In future, a greater understanding of the processes and
subcellular mechanisms involved in microsporogenesis, and
ultimately of the genes controlling these mechanisms, is
required to achieve a more sophisticated understanding of
the evolution of microsporogenesis in monocot lineages.
More detailed observations on microsporogenesis are
needed, using more sophisticated techniques such as indirect
immuno-fluorescence microscopy, to gain insights into the
subcellular processes, including the early stages of cell plate
formation and the distribution and time of appearance of
spindle microtubules.
A C K N O W L E D G E M E N TS
We thank Surrey County Council and English Nature for
permission to collect material of Narthecium ossifragum,
and S. Fry (SCC) for assistance in the field. We are grateful
to H. Takahashi and Hokkaido University Botanic Garden
for material of Japonolirion osense, and M. G. Sajo for Xyris
trachyphylla. Thanks are due to our colleagues especially P.
Bygrave, L. R. Caddick, M. W. Chase, A. M. Muasya, S. J.
495
Owens, D. A. Simpson and P. Wilkin for discussion of
various aspects of this work and for help with obtaining
material. We also thank two anonymous referees for their
comments.
REFERENCES
Angiosperm Phylogeny Group. 1998. An ordinal classification for the
families of flowering plants. Annals of the Missouri Botanical
Garden 85 : 531–553.
Arekal GD, Ramaswamy SN. 1973. Embryology of Burmannia pusilla
(Wall. ex Miers) THW. and its taxonomic status. BeitraW ge zur
Biologie der Pflanzen 49 : 35–46.
Arekal GD, Ramaswamy SN. 1980. Embryology of Eriocaulon
hookerianum Stapf. and the systematic position of Eriocaulaceae.
Botaniska Notiser 133 : 295–309.
Asplund I. 1972. Embryological studies in the genus Typha. SŠensk
Botanisk Tidskrift 66 : 1–17.
Ayensu ES. 1972. Studies on pollen morphology in the Velloziaceae.
Proceedings of the Biological Society of Washington 85 : 469–480.
Ayensu ES, Skvarla JJ. 1974. Fine structure of Velloziaceae pollen.
Bulletin of the Torrey Botanical Club 101 : 250–266.
Banerji I. 1937. Sterility in Colocasia antiquorum Schott. Journal of the
Indian Botanical Society 16 : 159–164.
Bhandari NN. 1984. The microsporangium. In : Johri BM, ed. The
embryology of angiosperms. Berlin : Springer-Verlag, 71–80.
Blackmore S, Barnes SH. 1995. Garside’s rule and the microspore
tetrads of GreŠillea rosmarinifolia A. Cunningham and Dryandra
polycephala Bentham (Proteaceae). ReŠiew of Palaeobotany and
Palynology 85 : 111–121.
Blackmore S, Crane PR. 1988. The systematic implications of pollen
and spore ontogeny. In : Humphries CJ, ed. Ontogeny and
systematics. New York : Colombia University Press, 85–115.
Blackmore S, Crane PR. 1998. The evolution of apertures in the spores
and pollen grains of embryophytes. In : Owens SJ, Rudall PJ, eds.
ReproductiŠe biology in systematics, conserŠation and economic
botany. Kew : Royal Botanic Gardens, Kew, 159–182.
Bortenslager S von, Erdtman G, Praglowski J. 1966. Pollenmorphologische Notizen u$ ber einige Blu$ tenpflanzen incertae sedis.
Botaniska Notiser 119 : 160–168.
Bremer K, Bremer B, Thulin M. 1998. Introduction to phylogeny and
systematics of flowering plants. Uppsala University : Department
of Systematic Botany.
Bygrave P. 1999. Molecular systematics of the Annonaceae. PhD thesis.
Royal Botanic Gardens, Kew.
Caddick LR, Furness CA, Stobbart KL, Rudall PJ. 1999 a. Microsporogenesis and pollen morphology in Dioscoreales and allied
taxa. Grana (in press).
Caddick LR, Rudall PJ, Wilkin P, Chase MW. 1999 b. Yams and their
allies : systematics of Dioscoreales. In : Wilson KL, Morrison D,
eds. Systematics and eŠolution of monocots. Collingwood : CSIRO
(in press).
Carlquist S. 1960. Anatomy of Guayana Xyridaceae : Abolboda,
Orectanthe, and Achlyphila. Memoirs of the New York Botanical
Garden 10 : 65–117.
Carlquist S. 1961. Pollen morphology of Rapateaceae. Aliso 5 : 39–66.
Cauneau-Pigot A. 1988. Biopalynological study of Lapageria rosea and
Iris unguicularis. Storage of pollen. Grana 27 : 297–312.
Cave MS. 1966. The female gametophytes of Lapageria rosea and
Philesia magellanica. Gayana. Botanica 15 : 25–31.
Chakrapani P, Raj B. 1971. Pollen morphological studies in the
Burmanniaceae. Grana 11 : 164–179.
Chanda S. 1966. On the pollen morphology of the Centrolepidaceae,
Restionaceae and Flagellariaceae, with special reference to
taxonomy. Grana Palynologica 6 : 355–415.
Chanda S, Ghosh K. 1976. Pollen morphology and its evolutionary
significance in Xanthorrhoeaceae. In : Ferguson IK, Muller J, eds.
The eŠolutionary significance of the exine. London : Academic
Press, 527–559.
496
Furness and Rudall—Microsporogenesis in Monocots
Chanda S, Ghosh K. 1979. Apertural evolution in the pollen of
monocotyledons and early dicotyledons. Proceedings of the 4th
International Palynological Conference, Lucknow 1 : 551–567.
Chanda S, Rowley J. 1967. Apertural types in pollen of the Restionaceae
and Flagellariaceae. Grana Palynologica 7 : 16–36.
Chanda S, Nilsson S, Blackmore S. 1988. Phylogenetic trends in the
Alismatales with reference to pollen grains. Grana 27 : 257–272.
Chase MW, and 41 others. 1993. Phylogenetics of seed plants : an
analysis of nucleotide sequences from the plastid gene rbcL.
Annals of the Missouri Botanical Garden 80 : 528–580.
Chase MW, Duvall MR, Hills HG, Conran JG, Cox AV, Eguiarte LE,
Hartwell J, Fay MF, Caddick LR, Cameron KM, Hoot S. 1995 a.
Molecular phylogenetics of Lilianae. In : Rudall PJ, Cribb PJ,
Cutler DF, Humphries CJ, eds. Monocotyledons : systematics and
eŠolution. Kew : Royal Botanic Gardens, 109–137.
Chase MW, Stevenson DW, Wilkin P, Rudall PJ. 1995 b. Monocot
systematics : a combined analysis. In : Rudall PJ, Cribb PJ, Cutler
DF, Humphries CJ, eds. Monocotyledons : systematics and eŠolution. Kew : Royal Botanic Gardens, 685–730.
Chase MW, Soltis DE, Soltis PS, Rudall PJ, Fay MF, Hahn WJ,
Sullivan S, Joseph J, Givnish T, Sytsma KJ, Price C. 1999. A
combined analysis of multiple datasets and a new phylogenetic
classification of the monocotyledons. In : Wilson KL, Morrison D,
eds. Systematics and eŠolution of monocots. Collingwood : CSIRO
(in press).
Cheah CH, Stone BC. 1975. Embryo sac and microsporangium
development in Pandanus (Pandanaceae). Phytomorphology 25 :
228–238.
Clarke GCS, Jones MR. 1981. The northwest european pollen flora,
23. Dioscoreaceae. ReŠiew of Palaeobotany and Palynology 33 :
45–50.
Conran JG. 1988. Embryology and possible relationships of Petermannia cirrosa (Petermanniaceae). Nordic Journal of Botany 8 :
13–17.
Cranwell LM. 1953. New Zealand pollen studies. The monocotyledons.
Bulletin of the Auckland Institute and Museum 3 : 1–91.
Dahlgren R, Lu A-m. 1985. Campynemanthe (Campynemaceae) :
Morphology, microsporogenesis, early ovule ontogeny and
relationships. Nordic Journal of Botany 5 : 321–330.
Dahlgren RMT, Clifford HT, Yeo PF. 1985. The families of the
monocotyledons. Structure, eŠolution and taxonomy. Berlin :
Springer-Verlag.
Dı! az Lifante Z. 1996. Pollen morphology of Asphodelus L. (Asphodelaceae) : taxonomic and phylogenetic inferences at the infrageneric level. Grana 35 : 24–32.
Dı! az Lifante Z, Dı! ez MJ, Ferna! ndez I. 1990. Morfologia polinica de las
subfamilias Melanthioideae y Asphodeloideae (Liliaceae) en la
peninsula Iberica y su importancia taxonomica. Lagascalia 16 :
211–225.
Dickinson HG, Sheldon JM. 1984. A radial system of microtubules
extending between the nuclear envelope and the plasma membrane
during male haplophase in flowering plants. Planta 161 : 86–90.
Ducker SC, Pettitt JM, Knox RB. 1978. Biology of Australian
seagrasses : pollen development and submarine pollination in
Amphibolis antarctica and Thalassodendron ciliatum (Cymodoceaceae). Australian Journal of Botany 26 : 265–285.
Dunbar A. 1973. Pollen development in the Eleocharis palustris group
(Cyperaceae). I. Ultrastructure and ontogeny. Botaniska Notiser
126 : 197–254.
Dutt BSM. 1970 a. Hypoxidaceae. Bulletin of the Indian National
Academy of Science 41 : 368–372.
Dutt BSM. 1970 b. Velloziaceae. Bulletin of the Indian National Academy
of Science 41 : 373–374.
Ehler N, Schill R. 1973. Die pollenmorphologie der Bromeliaceae.
Pollen et Spores 15 : 13–45.
El-Ghazaly G, Jensen WA. 1986. Studies in the development of wheat
(Triticum aestiŠum) pollen. I. Formation of the pollen wall and
Ubisch bodies. Grana 25 : 1–29.
Erdtman G. 1943. An introduction to pollen analysis. Waltham,
Massachusetts : Chronica Botanica Co.
Erdtman G. 1952. Pollen morphology and plant taxonomy. Angiosperms.
Stockholm : Almqvist & Wiksell.
Eunus AM. 1951. Contributions to the embryology of the Liliaceae. V.
Life history of Amaianthium muscaetoxicum Walt. Phytomorphology 1 : 73–79.
Furness CA. 1985. A review of spiraperturate pollen. Pollen et Spores
27 : 307–320.
Furness CA. 1988. The northwest european pollen flora, 39.
Eriocaulaceae. ReŠiew of Palaeobotany and Palynology 57 : 27–32.
Furness CA, Rudall PJ. 1998. The tapetum and systematics in
monocotyledons. Botanical ReŠiew 64 : 201–239.
Furness CA, Rudall PJ. 1999 a. Inaperturate pollen in monocotyledons.
International Journal of Plant Sciences 160 : 395–414.
Furness CA, Rudall PJ. 1999 b. Aperture absence in pollen of
monocotyledons. In : Harley MM, Morton CM, Blackmore S, eds.
Pollen and spores : morphology and biology. Royal Botanic Gardens,
Kew (in press).
Gow JE. 1913. Observations on the morphology of the aroids.
Botanical Gazette 56 : 127–142.
Grayum MH. 1991. Systematic embryology of the Araceae. Botanical
ReŠiew 57 : 167–203.
Grayum MH. 1992. Comparative external pollen ultrastructure of the
Araceae and putatatively related taxa. Monographs in Systematic
Botany of the Missouri Botanical Garden 43 : 1–167.
Ha/ kansson A. 1954. Meiosis and pollen mitosis in X-rayed and
untreated spikelets of Eleocharis palustris. Hereditas 40 : 325–345.
Halbritter H. 1992. Morphologie und systematische Bedeutung des
Pollens der Bromeliaceae. Grana 31 : 197–212.
Halbritter H, Hesse M. 1993. Sulcus morphology in some monocot
families. Grana 32 : 87–99.
Halbritter H, Hesse M. 1995. The convergent evolution of exine shields
in angiosperm pollen. Grana 34 : 108–119.
Hamann U. 1961. Merkmalsbestand und Verwandtschaftsbeziehungen
der Farinosae. Wildenowia 2 : 639–768.
Hamann U. 1966. Embryologische, morphologische-anatomische und
systematische Untersuchungen an Philydraceen. Willdenowia 4 :
1–178.
Hamann U. 1975. Neue Untersuchungen zur Embryologie und
Systematik der Centrolepidaceae. Botanische Jahrbucher 96 :
154–191.
Hamann U. 1976. Hydatellaceae–a new family of Monocotyledonae.
New Zealand Journal of Botany 14 : 193–196.
Harley MM. 1996. Palm pollen and the fossil record. PhD Thesis,
University of East London.
Harley MM. 1999. Tetrad variation : its influence on pollen form and
systematics in the Palmae. In : Kurmann MM, Hemsley AR, eds.
EŠolution of plant architecture. Kew : Royal Botanic Gardens (in
press).
Harling G. 1958. Monograph of the Cyclanthaceae. Acta Horti Bergiana
18 : 1–428.
Hayashi Y. 1960. On the microsporogenesis and pollen morphology in
the family Magnoliaceae. Science Reports of Tohoku UniŠersity.
4th series (Biology) 26 : 45–52.
Heo K, Van der Werf H, Tobe H. 1998. Embryology and relationships
of Lauraceae (Laurales). Botanical Journal of the Linnean Society
126 : 295–322.
Heslop-Harrison J. 1968. Wall development within the microspore
tetrad of Lilium longiflorum. Canadian Journal of Botany 46 :
1185–1192.
Heslop-Harrison J. 1971. Wall pattern formation in angiosperm
microsporogenesis. In : Symposium of the Society for Experimental
Biology No. XXV. Control mechanisms of growth and differentiation. Cambridge : Cambridge University Press, 277–300.
Hesse M, Waha M. 1983. The fine structure of the pollen wall in
Strelitzia reginae (Musaceae). Plant Systematics and EŠolution
141 : 285–298.
Heusser CJ. 1971. Pollen and spores of Chile. Tucson : University of
Arizona Press.
Huang T-C. 1972. Pollen flora of Taiwan. National Taiwan University :
Botany Department Press.
Huynh K-L. 1972. The original position of the generative nucleus in the
pollen tetrads of Agropyron, Itea, Limnanthes, and Onosma, and
its phylogenetic significance in the angiosperms. Grana 12 :
105–112.
Furness and Rudall—Microsporogenesis in Monocots
Huynh K-L. 1976. Arrangement of some monosulcate, disulcate,
trisulcate, dicolpate, and tricolpate pollen types in the tetrads, and
some aspects of evolution in the angiosperms. In : Ferguson IK,
Muller J, eds. The eŠolutionary significance of the exine. London :
Academic Press, 101–124.
Huynh K-L. 1980. La morphologie du pollen de Pandanus subg.
Vinsonia (Pandanaceae) et sa signification taxonomique. Pollen et
Spores 22 : 173–189.
Huynh K-L, Stone BE. 1981. On a new subsection of Pandanus section
Cauliflora (Pandanaceae) with paniculate staminate inflorescence
structure, distinctive leaf anatomy and pollen morphology.
Botanical Journal of the Linnean Society 83 : 213–220.
Islam AS. 1950. A contribution to the life history of Ottelia alismoides
Pers. Journal of the Indian Botanical Society 29 : 79–91.
Juel HO. 1900. Beitra$ ge zur Kenntniss der Tetradentheilung. Jahrbuch
fur wissenschaftliche Botanik 35 : 626–659.
Juliano JB, Alcala PE. 1933. Floral morphology of Musa errans
(Blanco) Teodoro var. Botoan Teodoro. Philippine Agriculturalist
22 : 91–126.
Kircher P. 1986. Untersuchungen zur BluW ten- und Infloreszenzmorphologie, Embryologie und Systematik der Restionaceen im
Vergleich mit Gramineen und Šerwandten Familien. Dissertationes
Botanicae, 94. Berlin : J.Cramer.
Khanna P. 1963. Male gametophyte and obturator in Cyperus rotundus
L., and C. triceps Endl. (l Kyllinga triceps Rottb.). Current
Science 32 : 133–134.
Koyama T. 1969. Delimitation and classification of the CyperaceaeMapanioideae. In : Gunkel JE, ed. Current topics in plant sciences.
New York : Academic Press, 201–228.
Kracauer P. 1930. Die Haploidgeneration von Canna indica L.
Dissertation Berlin.
Kress WJ. 1986. Exineless pollen structure and pollination systems of
tropical Heliconia (Heliconiaceae). In : Blackmore S, Ferguson IK,
eds. Pollen and spores : form and function. London : Academic
Press, 329–345.
Kress WJ, Stone DE. 1983. Morphology and phylogenetic significance
of exine-less pollen of Heliconia (Heliconiaceae). Systematic Botany
8 : 149–167.
Kress WJ, Stone DE, Sellers SC. 1978. Ultrastructure of exine-less
pollen : Heliconia (Heliconiaceae). American Journal of Botany 65 :
1064–1076.
Kreunen SS, Osborn JM. 1999. Pollen and anther development in
Nelumbo (Nelumbonaceae). American Journal of Botany (in press).
Kronestedt-Robards EC, Rowley JR. 1989. Pollen grain development
and tapetal changes in Strelitzia reginae (Strelitziaceae). American
Journal of Botany 76 : 856–870.
Kuprianova LA. 1948. Pollen morphology and phylogeny of the
monocotyledons. Trudy Botanischeskogo Instituta Akademii
Nauk SSR. Leningrad. Series 1. Flora Sistematika 7 : 163–262. (In
Russian).
Lambert A-M. 1969. Observations sur la premie' re mitose pollinique de
Luzules. Compte Rendu de l’AcadeT mie des Sciences. Paris. Series
D. 269 : 153–156.
Lambert AM. 1970. Formation et diffe! rentiation des grains de pollen
chez les Luzules (structures et ultrastructures). Bulletin AcadeT mie
et SocieT teT Lorraines des Sciences 9 : 147–149.
Les DH, Cleland MA, Waycott M. 1997. Phylogenetic studies in
Alismatidae, II : Evolution of marine angiosperms (seagrasses) and
hydrophily. Systematic Botany 22 : 443–463.
Liang Y-H. 1988. Pollen morphology of the family Zingiberaceae in
China–pollen types and their significance in the family. Acta
Phytotaxonomica Sinica 26 : 265–281. (In Chinese with English
summary).
Linder HP, Ferguson IK. 1985. On the pollen morphology and
phylogeny of the Restionales and Poales. Grana 24 : 65–76.
Locke JF. 1936. Microsporogenesis and cytokinesis in Asimia triloba.
Botanical Gazette 36 : 159–169.
Maheshwari P. 1950. An introduction to the embryology of angiosperms.
New York : McGraw-Hill.
Maheshwari SC, Khanna PP. 1956. The embryology of Arisaema
wallichianum Hook. F. and the systematic position of the Araceae.
Phytomorphology 6 : 379–388.
497
Meyer N, Yaroshevskaya AS. 1976. The phylogenetic significance of the
development of pollen grain walls in Liliaceae, Juncaceae and
Cyperaceae. In : Ferguson IK, Muller J, eds. The eŠolutionary
significance of the exine. London : Academic Press, 91–100.
Monteiro-Scanavacca WR, Mazzoni SC. 1978. Embryological studies
in Leiothrix fluitans (Mart.) Ruhl. (Eriocaulaceae). ReŠista
Brasileira de Botanica 1 : 59–64.
Muller J. 1970. Palynological evidence on early differentiation of
angiosperms. Biological ReŠiews 45 : 417–450.
Mu$ ller-Doblies U. 1969. U$ ber die Blu$ tensta$ nde und Blu$ ten sowie zur
Embryologie von Sparganium. Botanische Jahrbucher 89 : 359–450.
Murty YS. 1964. Cytokinesis and microspore tetrad. In : Nair PKK, ed.
AdŠances in palynology. Lucknow : National Botanic Gardens,
176–202.
Nanda K, Gupta SC. 1977. Development of the tapetal periplasmodium
in Rhoeo spathacea. Phytomorphology 27 : 308–314.
Ohashi H, Murata J, Takahashi M. 1983. Pollen morphology of the
Japanese Arisaema (Araceae). Science Reports of Tohoku UniŠersity. 4th series (Biology) 38 : 219–251.
Ohga I, Sinoto Y. 1932. Cytological studies on Sciaphila japonica Mak.
(Preliminary note). II. On pollen–and embryo sac–development.
Botanical Magazine of Tokyo 46 : 311–315 (In Japanese).
Pacini E, Franchi GG. 1983. Pollen grain development in Smilax aspera
L. and possible functions of the loculus. In : Mulcahy DL,
Ottaviano E, eds. Pollen biology and implications for plant breeding.
Amsterdam : Elsevier, 183–190.
Pacini E, Juniper BE. 1983. The ultrastructure of the formation and
development of the amoeboid tapetum in Arum italicum Miller.
Protoplasma 117 : 116–129.
Page JS. 1978. A scanning electron microscope survey of grass pollen.
Kew Bulletin 32 : 311–319.
Palm BJ. 1920. Preliminary notes on pollen development in tropical
monocotyledons. SŠensk Botanisk Tidskrift 14 : 261–266.
Periasamy K, Amalathas J. 1991. Absence of callose and tetrad in the
microsporogenesis of Pandanus odoratissimus with well-formed
pollen exine. Annals of Botany 67 : 29–33.
Pettitt JM. 1980. Reproduction in seagrasses : nature of the pollen and
receptive surface of the stigma in the Hydrocharitaceae. Annals of
Botany 45 : 257–271.
Pettitt JM. 1981. Reproduction in seagrasses : pollen development in
Thalassia hemprichii, Halophila stipulacea and Thalassodendron
ciliatum. Annals of Botany 48 : 609–622.
Pettitt JM, Jermy AC. 1975. Pollen in hydrophilous angiosperms.
Micron 5 : 377–405.
Poole MM, Hunt DR. 1980. Pollen morphology and the taxonomy of
the Commelinaceae : an exploratory survey. American Commelinaceae : VIII. Kew Bulletin 34 : 639–670.
Punt W. 1968. Pollen morphology of the American species of the
subfamily Costoideae (Zingiberaceae). ReŠiew of Palaeobotany
and Palynology 7 : 31–43.
Radulescu D. 1973. Recherches morpho-palynologiques sur la famille
Liliaceae. Acta Botanica Horti Bucurestiensis 1973 : 133–248.
Rajendra BR, Tomb AS, Mujeeb KA, Bates LS. 1978. Pollen morphology
of selected Triticeae and two intergeneric hybrids. Pollen et Spores
20 : 145–156.
Ramaswamy SN, Nagendran CR. 1996. Embryology of Syngonanthus
nitens var. nitens (Eriocaulaceae). South African Journal of Botany
62 : 173–177.
Rao AN. 1955. Embryology of Trichopus zeylanicus Gaertn. Journal of
the Indian Botanical Society 34 : 213–221.
Rau NS. 1930. On reduction division in pollen-mothercells of Cyanotis
cristata. Journal of the Indian Botanical Society 9 : 79–113.
Rodkiewicz B, Kudlicka K, Stobiecka H. 1984. Patterns of amyloplast
distribution during microsporogenesis in Tradescantia, Impatiens
and Larix. Acta Societas Botanicorum Poloniae 53 : 437–441.
Romanov ID. 1959. The embryo sac and pollen morphology in Tulipa.
In : Proceedings of the IX International Botanical Congress,
Montreal. Vol. II, abstracts. Montreal : University of Toronto
Press : 331–332.
Rowley JR, Dahl AO. 1962. The aperture of the pollen grain in
Commelinantia. Pollen et Spores 4 : 221–232.
Rowley JR, Flynn JJ. 1990–1991. Tambourissa (Monimiaceae).
498
Furness and Rudall—Microsporogenesis in Monocots
Microspore development in the tetrad period. Annales des Sciences
Naturelles. Botanique. Paris. 13th series 11 : 125–147.
Rowley JR, Skvarla JJ. 1986. Development of the pollen grain wall in
Canna. Nordic Journal of Botany 6 : 39–65.
Ru$ bsamen T. 1986. Morphologische, embryologische und systematische
Untersuchungen an Burmanniaceae und Corsiaceae (Mit Ausblick
auf die Orchidaceae-Apostasioideae). Dissertationes Botanicae, 92.
Berlin : J. Cramer.
Ru$ bsamen-Weustenfeld T. 1991. Morphologische, embryologische und
systematische Untersuchungen an Triuridaceae. Bibliotheca Botanica 140 : 1–113.
Rudall PJ, Furness CA. 1997. Systematics of Acorus : ovule and anther.
International Journal of Plant Sciences 158 : 640–651.
Rudall PJ, Sajo MG. 1999. Systematic position of Xyris : flower and
seed anatomy. International Journal of Plant Sciences 160 : 795–808.
Rudall PJ, Stevenson DW, Linder HP. 1999. Structure and systematics
of Hanguana, a monocotyledon of uncertain affinity. Australian
Systematic Botany 12 : 311–330.
Rudall PJ, Furness CA, Chase MW, Fay MF. 1997. Microsporogenesis
and pollen sulcus type in Asparagales (Lilianae). Canadian Journal
of Botany 75 : 408–430.
Saad SI, Ibrahim RK. 1965. Palynological and biochemical studies of
Scitaminae. Journal of Palynology 1 : 62–66.
Sampson FB. 1982. Variation in position of the nascent generative cell
in pollen of Hedycarya (Monimiaceae). Grana 21 : 9–14.
Samuelsson G. 1914. U$ ber die Pollenentwicklung von Anona und
Aristolochia und ihre systematische Bedeutung. SŠensk Botanisk
Tidskrift 8 : 181–189.
Schnarf K. 1931. Vergleichende Embryologie der Angiospermen. Berlin :
Borntra$ ger.
Schulze W. 1975 a. Beitra$ ge zur Taxonomie der Liliifloren. I. Aphodelaceae. Wissenschaftliche Zeitschrift Friedrich-Schiller UniŠersitaW t Jena, Mathematische-Naturwissenschaftliche 24 : 403–415.
Schulze W. 1975 b. Beitra$ ge zur Taxonomie der Liliifloren. II.
Colchicaceae. Wissenschaftliche Zeitschrift Friedrich-Schiller UniŠersitaW t Jena, Mathematische-Naturwissenschaftliche 24 : 417–428.
Schulze W. 1978 a. Beitra$ ge zur Taxonomie der Liliifloren. III.
Alstromeriaceae. Wissenschaftliche Zeitschrift Friedrich-Schiller
UniŠersitaW t Jena, Mathematische-Naturwissenschaftliche 27 : 79–85.
Schulze W. 1978 b. Beitra$ ge zur Taxonomie der Liliifloren. IV.
Melanthiaceae. Wissenschaftliche Zeitschrift Friedrich-Schiller
UniŠersitaW t Jena, Mathematische-Naturwissenschaftliche 27 : 87–95.
Schulze W. 1980. Beitra$ ge zur Taxonomie der Liliifloren. VI. Der
Umfang der Liliaceae. Wissenschaftliche Zeitschrift FriedrichSchiller UniŠersitaW t Jena, Mathematische-Naturwissenschaftliche
29 : 607–636.
Schulze W. 1982 a. Beitra$ ge zur Taxonomie der Liliifloren. VII.
Philesiaceae. Wissenschaftliche Zeitschrift Friedrich-Schiller UniŠersitaW t Jena, Mathematische-Naturwissenschaftliche 31 : 277–283.
Schulze W. 1982 b. Beitra$ ge zur Taxonomie der Liliifloren. VIII.
Smilacaceae. Wissenschaftliche Zeitschrift Friedrich-Schiller UniŠersitaW t Jena, Mathematische-Naturwissenschaftliche 31 : 285–289.
Schulze W. 1982c. Beitra$ ge zur Taxonomie der Liliifloren. IX.
Anthericaceae. Wissenschaftliche Zeitschrift Friedrich-Schiller UniŠersitaW t Jena, Mathematische-Naturwissenschaftliche 31 : 291–307.
Sharma M. 1965. Pollen morphological studies of Eriocaulon L. from
India. Palynological Bulletin 1 : 45–48.
Sharma M. 1967. Pollen morphology of Indian monocotyledons.
Journal of Palynology. Special Šolume. Lucknow : Palynological
Society of India, 1–98.
Sheldon JM, Dickinson HG. 1983. Determination of patterning in the
pollen wall of Lilium henryi. Journal of Cell Science 63 : 191–208.
Sheldon JM, Dickinson HG. 1986. Pollen wall formation in Lilium : The
effect of chaotrophic agents, and the organisation of the
microtubular cytoskeleton during pattern development. Planta
168 : 11–23.
Simpson MG. 1983. Pollen ultrastructure of the Haemodoraceae and its
taxonomic significance. Grana 22 : 79–103.
Simpson MG. 1985. Pollen ultrastructure of the Philydraceae. Grana
24 : 23–31.
Simpson MG. 1987. Pollen ultrastructure of the Pontederiaceae.
Evidence for exine homology with the Haemodoraceae. Grana 26 :
113–126.
Simpson MG. 1989. Pollen wall development of Xiphidium coeruleum
(Haemodoraceae) and its systematic implications. Annals of Botany
64 : 257–269.
Skvarla JJ, Larson DA. 1963. Nature of cohesion within pollen tetrads
of Typha latifolia. Science 140 : 173–175.
Skvarla JJ, Larson DA. 1966. Fine structural studies of Zea mays
pollen. I. Cell membranes and exine ontogeny. American Journal
of Botany 53 : 1112–1125.
Skvarla JJ, Rowley JR. 1970. The pollen wall of Canna and its
similarity to the germinal apertures of other pollen. American
Journal of Botany 57 : 519–529.
Stenar H. 1925. Die embryologie der Amaryllideen. PhD Thesis,
University of Uppsala.
Stenar H. 1927. Zur Entwicklungsgeschichte der Gattung Anigozanthos
Labill. Botaniska Notiser 1927 : 104–114.
Stenar H. 1931. Die Art der Pollenbildung bei Narthecium ossifragum
Huds. Botaniska Notiser 1931 : 51–54.
Stevenson DW, Owens SJ. 1978. Some aspects of the reproductive
biology of Gibasis Šenustula (Kunth) D. R. Hunt (Commelinaceae).
Botanical Journal of the Linnean Society 77 : 157–175.
Stone DE. 1987. Developmental evidence for the convergence of
Sassafras (Laurales) and Heliconia (Zingiberales) pollen. Grana
26 : 179–191.
Stone DE, Sellers SC, Kress WJ. 1979. Ontogeny of exineless pollen in
Heliconia, a banana relative. Annals of the Missouri Botanical
Garden 66 : 701–730.
Stone DE, Sellers SC, Kress WJ. 1981. Ontogenetic and evolutionary
implications of a neotenous exine in Tapeinochilos (Zingiberales :
Costaceae) pollen. American Journal of Botany 68 : 49–63.
Strandhede SO. 1965. Chromosome studies in Eleocharis, subser.
Palustres. I. Meiosis in some forms with 15 chromosomes.
Hereditas 53 : 47–62.
Strandhede SO. 1973. Pollen development in the Eleocharis palustris
group (Cyperaceae). II. Cytokinesis and microspore degeneration.
Botaniska Notiser 126 : 255–265.
Takahashi M. 1982. Pollen morphology in North American species of
Trillium. American Journal of Botany 69 : 1185–1195.
Takahashi M. 1983. Pollen morphology in Asiatic species of Trillium.
Botanical Magazine of Tokyo 96 : 377–384.
Takahashi M. 1987. Development of omniaperturate pollen in Trillium
kamtschaticum (Liliaceae). American Journal of Botany 74 :
1842–1852.
Takahashi M. 1994. Pollen development in a submerged plant, Ottelia
alismatoides (L.) Pers. (Hydrocharitaceae). Journal of Plant
Research 107 : 161–164.
Takahashi M. 1995. Development of structure-less pollen wall in
Ceratophyllum demersum. L. (Ceratophyllaceae). Journal of Plant
Research 108 : 205–208.
Takahashi M, Kawano S. 1989. Pollen morphology of the Melanthiaceae
and its systematic implications. Annals of the Missouri Botanical
Garden 76 : 863–876.
Takahashi M, Sohma K. 1979. Pollen wall formation and tapetum in
Disporum smilacinum A. Gray (Liliaceae). Science Reports of
Tohoku UniŠersity. 4th series (Biology) 37 : 273–281.
Tanaka N. 1939. Chromosome studies in Cyperaceae, V. Pollen
development of Carex grallatoria Maxim. var. heteroclita Ku$ kenth.
ex Matsum. Japanese Journal of Genetics 15 : 153–157. (In Japanese
with English summary).
Tanaka N. 1941. Chromosome studies in Cyperaceae, XII. Pollen
development in five genera with special reference to Rhyncospora.
Botanical Magazine Tokyo 55 : 55–65.
Thanikaimoni G. 1965. Contribution to the pollen morphology of
Eriocaulaceae. Pollen et Spores 8 : 181–191.
Theilade I, Mærsk-Møller M-L, Theilade J, Larsen K. 1993. Pollen
morphology and structure of Zingiber (Zingiberaceae). Grana 32 :
338–342.
Theilade I, Theilade J. 1996. Ontogeny of pollen grains in Zingiber
spectabile (Zingiberaceae). Grana 35 : 162–170.
Tiemann A. 1985. Untersuchungen zur Embryologie, Blutenmorphologie
und Systematik der Rapateaceen und der Xyridaceen-Gattung
Abolboda (Monocotyledoneae). Dissertationes Botanicae, 82.
Vaduz : J. Cramer.
Tiwari SC, Gunning BES. 1986 a. Cytoskeleton, cell surface and the
Furness and Rudall—Microsporogenesis in Monocots
development of invasive plasmodial tapetum in Tradescantia
Širginiana L. Protoplasma 133 : 89–99.
Tiwari SC, Gunning BES. 1986 b. Development of tapetum and
microspores in Canna L. : an example of an invasive but nonsyncytial tapetum. Annals of Botany 57 : 557–563.
Ueno J. 1980. On the spiraperturate pollen grains. Japanese Journal of
Palynology 25 : 33–47. (In Japanese with English summary).
Van der Ham RWJM. 1991. Pollen morphology of the Stemonaceae.
Blumea 36 : 127–159.
Walker JW. 1971. Pollen morphology, phytogeography, and phylogeny
of the Annonaceae. Contributions to the Gray Herbarium 202 :
1–132.
499
Walker JW. 1974. Aperture evolution in the pollen of primitive
angiosperms. American Journal of Botany 61 : 1112–1136.
Wingenroth M, Heusser CJ. 1983. Pollen of the High Andean flora.
ProŠince of Mendoza, Argentina. Argentina : Consejo Nacional de
Investigaciones Cientficas y Te! cnicas.
Wulff HD. 1939. Die Pollenentwicklung der Juncaceen. Jahrbuch fuW r
wissenschaftliche Botanik 87 : 533–556.
Yamashita T. 1976. U$ ber die Pollenbildung bei Halodule pinifolia und
H. uninerŠis. BeitraW ge zur Biologie der Pflanzen 52 : 217–226.
Zavada MS. 1983. Comparative morphology of monocot pollen and
evolutionary trends of apertures and wall structures. Botanical
ReŠiew 49 : 331–379.