598Biochemical Society Transactions (2010) Volume 38, part 2
Male gamete biology in flowering plants
Scott D. Russell1, Xiaoping Gou, Xiaoping Wei and Tong Yuan
Department of Botany and Microbiology, University of Oklahoma, Norman, OK 73019, U.S.A.
Flowering plant reproduction is characterized by double fertilization, in which two diminutive brother sperm
cells initiate embryo and endosperm. The role of the male gamete, although studied structurally for over
a century at various levels, is still being explored on a molecular and cellular level. The potential of the
male to influence development has been historically underestimated and the reasons for this are obvious:
limitations provided by maternal imprinting, the much greater cellular volume of female gametes and the
general paucity of paternal effects. However, as more is known about molecular expression of chromatin-
to achieve effect by intaglio expression, passing transcripts directly into translation, the role of the male is
likely to expand. Much of the expression in the male germline that appears to be distinct from patterns of
pollen vegetative cell expression may be the result of chromosomal level regulation of transcription.
Structure, timing and physiology in
flowering plant reproduction
In flowering plants, double fertilization launches two
dramatically distinct developmental programmes. One of
the two sperm cells in a successful pollen tube fuses with the
egg cell to form the canonical zygote and embryo; a second
brother sperm cell fuses with the central cell to form the male
portion of the unique and precocious nutritive endosperm.
This unique complement is part of a temporal choreography
that is conducted most conspicuously in floral parts that are
paradoxically sporophytic and asexual, but also govern the
timing of gametophytic events . Much of this timing is
simply a matter of opportunity, as indicated by the cons-
are cryptic in cleistogamous flowers and, in the absence of
a conspicuous visual signal, nevertheless produce receptive
gametes that are timed within the flower to accomplish
The diversity of structural organization of gametophytes
is well described in previous reviews [2,3], but these gamete-
producing lineages also express their diversity in the timing
of various maturational cues. Maturation may be delayed or
hastened to match male development to female development,
and the duration of the progamic phase (from pollination to
fertilization) is adapted to optimize receptivity of male and
female gametes. Communication at the gametophytic level
was first suggested based in part on experimental evidence
from female gametophyte cell behaviour during in vitro
ovule culture and a careful observation of ultrastructural evi-
dence of gametophyte behaviour . Evidence that gametes
Key words: chromatin, fertilization, flowering plant, gamete, sperm cell, ubiquitin.
Abbreviations used: ECB, enucleated cytoplasmic body; EST, expressed sequence tag; IPT,
isopentenyl transferase; siRNA, small interfering RNA; SSH, suppression subtractive hybridization;
SSP, SHORT SUSPENSOR; Sua, sperm cell unassociated with the vegetative nucleus; Svn,
vegetative-nucleus-associated sperm; TE, transposable element; VCB, vesicle-containing body;
VN, vegetative nucleus.
1To whom correspondence should be addressed (email firstname.lastname@example.org).
are involved directly in signalling is available from studies of
the gamete cell cycle in Nicotiana (tobacco), in which entry
of the male gametes into S-phase accelerates female gamete
entry into S-phase . Thus gametes become synchronized
in their position in the cell cycle before fertilization, which
may occur in G1- or G2-phase in angiosperms, but in tobacco
occurs at G2-phase, just before fusion. Maturation of sperm
cells in the pollen tube requires passage in the gynoecium
in some flowering plants or successful fusion may not ensue
. The importance of timing is evident, as heterochronic
asexual or apomictic reproduction .
Gametes themselves are the most critical functional
element of the evolutionarily highly reduced gametophytes.
The male gametes originate as part of a ‘male germ unit’
in which the male germ lineage of the generative and later
sperm cells associate with the VN (vegetative nucleus) (Fig-
ure 1). The male germ unit forms a functional assemblage
that provides for the co-transmission of male gametes at the
time of their optimal receptivity [8,9]. Flowering plant sperm
cells have a relatively diminutive cytoplasm, a prominent
nucleus and, frequently, an elongated projection that appears
to be associated physically with the VN . Rather than
leading the male gametes, however, the ‘tail’ often follows the
lead of the VN, and the male gametes are non-motile, rather
being conveyed by actin–myosin interactions that act on an
enveloping pollen tube plasma membrane .
The female gametes are flanked by sister cells known
as synergids, which aid in the attraction, receipt and
transmission of male gametes into the embryo sac. The
egg and the central cell are the female fusion target cells,
which together with the two synergids form the functional
entity known as the ‘female germ unit’ . These cells
display characteristic features such as cellular polarity,
prominent nuclei and nucleoli, an appearance of quiescence
in the female gamete before fertilization, but are otherwise
C ?The Authors Journal compilation
C ?2010 Biochemical SocietyBiochem. Soc. Trans. (2010) 38, 598–603; doi:10.1042/BST0380598
Cell–cell Communication in Plant Reproduction603
23 Mogensen, H.L. (1992) The male germ unit: concept, composition, and
significance. Int. Rev. Cytol. 140, 129–147
24 Okada, T., Endo, M., Singh, M.B. and Bhalla, P.L. (2005) Analysis of the
histone H3 gene family in Arabidopsis and identification of the
male-gamete-specific variant AtMGH3. Plant J. 44, 557–568
25 Okada, T., Singh, M.B. and Bhalla, P.L. (2006) Histone H3 variants in male
gametic cells of lily and H3 methylation in mature pollen. Plant Mol. Biol.
26 Singh, M.B., Xu, H.L., Bhalla, P.L., Zhang, Z.J., Swoboda, I. and Russell, S.D.
(2002) Developmental expression of polyubiquitin genes and
distribution of ubiquitinated proteins in generative and sperm cells. Sex.
Plant Reprod. 14, 325–329
27 Friedman, W.E. (1999) Expression of the cell cycle in sperm of
Arabidopsis: implications for understanding patterns of gametogenesis
and fertilization in plants and other eukaryotes. Development 126,
28 Engel, M.L., Chaboud, A., Dumas, C. and McCormick, S. (2003) Sperm
cells of Zea mays have a complex complement of mRNAs. Plant J. 34,
29 Slotkin, R.K., Vaughn, M., Borges, F., Tanurdzic, M., Becker, J.D., Feij´ o, J.A.
and Martienssen, R.A. (2009) Epigenetic reprogramming and small RNA
silencing of transposable elements in pollen. Cell 136, 461–472
30 Dickinson, H.G. and Grant-Downton, R. (2009) Bridging the generation
gap: flowering plant gametophytes and animal germlines reveal
unexpected similarities. Biol. Rev. Camb. Philos. Soc. 84, 589–615
31 Tian, H.Q., Zhang, Z.J. and Russell, S.D. (2001) Sperm dimorphism in
Nicotiana tabacum L. Sex. Plant Reprod. 14, 123–125
32 Mogensen, H.L. (1996) The hows and whys of cytoplasmic inheritance in
seed plants. Am. J. Bot. 83, 383–404
33 M´ arton, M. and Dresselhaus, T. (2008) A comparison of early molecular
fertilization mechanisms in animals and flowering plants. Sex. Plant
Reprod. 21, 37–52
34 Curtis, M. and Grossniklaus, U. (2008) Molecular control of autonomous
embryo and endosperm development. Sex. Plant Reprod. 21, 79–88
35 Brownfield, L., Hafidh, S., Borg, M., Sidorova, A., Mori, T. and Twell, D.
(2009) A plant germline-specific integrator of sperm specification and
cell cycle progression. PLoS Genet. 5, e1000430
36 Bayer, M., Nawy, T., Giglione, C., Galli, M., Meinnel, T. and Lukowitz, W.
(2009) Paternal control of embryonic patterning in Arabidopsis thaliana.
Science 323, 1485–1488
37 Vielle-Calzada, J.-P., Baskar, R. and Grossniklaus, U. (2000) Delayed
activation of the paternal genome during seed development. Nature
38 Scholten, S., Lorz, H. and Kranz, E. (2002) Paternal mRNA and protein
synthesis coincides with male chromatin decondensation in maize
zygotes. Plant J. 32, 221–231
39 Ning, J., Peng, X.-B., Qu, L.-H., Xin, H.-P., Yan, T.-T. and Sun, M. (2006)
Differential gene expression in egg cells and zygotes suggests that the
transcriptome is restructed before the first zygotic division in tobacco.
FEBS Lett. 580, 1747–1752
40 Russell, S.D. (1984) Ultrastructure of the sperms of Plumbago zeylanica.
2. Quantitative cytology and three-dimensional organization. Planta 162,
41 Russell, S.D. (1985) Preferential fertilization in Plumbago: ultrastructural
evidence for gamete-level recognition in an angiosperm. Proc. Natl.
Acad. Sci. U.S.A. 82, 6129–6133
42 Gou, X., Yuan, T., Wei, X. and Russell, S.D. (2009) Gene expression
in the dimorphic sperm cells of Plumbago zeylanica: transcript
profiling, diversity, and relationship to cell type. Plant J. 60,
43 Miyawaki, K., Matsumoto-Kitano, M. and Kakimoto, T. (2004) Expression
of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis:
tissue specificity and regulation by auxin, cytokinin, and nitrate. Plant J.
44 Day, R.C., Herridge, R.P., Ambrose, B.A. and Macknight, R.C. (2008)
Transcriptome analysis of proliferating Arabidopsis endosperm reveals
biological implications for the control of syncytial division, cytokinin
signaling, and gene expression regulation. Plant Physiol. 148,
45 Saito, C., Nagata, N., Sakai, A., Mori, K., Kuroiwa, H. and Kuroiwa, T.
(2002) Angiosperm species that produce sperm cell pairs or generative
cells with polarized distribution of DNA-containing organelles. Sex. Plant
Reprod. 15, 167–178
46 Faure, J.E., Rusche, M.L., Thomas, A., Keim, P., Dumas, C., Mogensen,
H.L., Rougier, M. and Chaboud, A. (2003) Double fertilization in maize:
the two male gametes from a pollen grain have the ability to fuse with
egg cells. Plant J. 33, 1051–1062
47 Nowack, M.K., Grini, P.E., Jakoby, M.J., Lafos, M., Koncz, C. and Schnittger,
A. (2006) A positive signal from the fertilization of the egg cell sets off
endosperm proliferation in angiosperm embryogenesis. Nat. Genet. 38,
48 Rotman, N., Durbarry, A., Wardle, A., Yang, W.C., Chaboud, A., Faure, J.E.,
Berger, F. and Twell, D. (2005) A novel class of MYB factors controls
sperm-cell formation in plants. Curr. Biol. 15, 244–248
49 Chen, Z., Tan, J.L. H., Ingouff, M., Sundaresan, V. and Berger, F. (2008)
Chromatin assembly factor 1 regulates the cell cycle but not cell fate
during male gametogenesis in Arabidopsis thaliana. Development 135,
50 Russell, S.D. (1985) Sperm-specificity in Plumbago zeylanica. in
Proceedings of VIII Symposium on Sexual Reproduction in Seed Plants,
Ferns and Mosses (Willemse, M.T. M. and van Went, J.L., eds),
pp. 145–146, PUDOC, Wageningen
51 Xu, H., Weterings, K., Vriezen, W., Feron, R., Xue, Y., Derksen, J. and
Mariani, C. (2002) Isolation and characterization of male-germ-cell
transcriptrs in Nicatiana tabacum. Sex. Plant Reprod. 14, 339–346
Received 12 September 2009
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C ?2010 Biochemical Society