Abstract
Pollination, or the first contact between male and female gametophytes, is one of the most important steps in plant reproduction. After pollination, the pollen grains, male gametophytes, are hydrated and then germinate pollen tubes. The pollen tube initially penetrates and grows through the intercellular spaces of the stigma and then grows through the transmitting tract to the placenta connected to an ovule. The pollen tube grows along the surface of the ovule’s funiculus, through the micropyle, and into the female gametophyte. After the pollen tube enters the female gametophyte, it ruptures and releases two sperm cells with its contents. The two sperm cells then move toward and fuse with the egg cell and central cell to produce embryo and endosperm, respectively. Multiple sperm cells typically strive to “win the race” and fertilize an egg cell during animal fertilization; however, in flowering plants, each ovule harboring an egg cell generally encounters only one of many pollen tubes conveying plant sperm cells. This chapter mainly addresses reproductive strategies of plants following pollination from the pollen tube extension and the guidance of two sperm cells to the female gametophyte for fertilization in the ovule.
Keywords
- plant fertilization
- pollen tube guidance
- MYB98
- LUREs
- fertilization recovery system
- POEM
1. Male and female gametophytes
Discussing the journey of the pollen tube first requires an introduction to the smallest fertilization units, namely, the male and female gametophytes (Figure 1). The male gametophyte (pollen) comprises two sperm cells and one vegetative cell and is found in the stamen of a flower. The two sperm cells fertilize the egg and central cells inside the female gametophyte via a guided pollen tube journey that is described later. The female gametophyte, which is embedded in an ovule within the pistil, contains seven cells of four different types: an egg cell, a central cell, two synergid cells, and three antipodal cells. The egg and central cells are polarized such that their nuclei lie in very close proximity, a feature facilitating double fertilization of these two sperm nuclei targets [1, 2, 3]. The synergid cells are extremely essential for the attraction of pollen tubes, as discussed below [4, 5, 6, 7, 8].
2. From the stigma to the funiculus
Once a pollen grain reaches the stigma at the top of a carpel, the pollen tubes elongate toward the funiculus to form a bridge-like structure to an ovule, as shown in Figure 2. This pollen tube growth through the stigma to the funiculus is controlled via multiple signals from both sporophytic and gametophytic maternal tissues in the carpels. The roles of the female tissues in pollen tube guidance have been focused upon.
Light and transmission electron microscopy studies of
3. From the funiculus to the female gametophyte
The pollen tube is subsequently guided from the funiculus to the female gametophyte. Although the molecular mechanisms underlying this step have been relatively well elucidated, as shown in Figure 3, a complete understanding requires a discussion of synergid cell biology (Figure 1). Synergid cells within the female gametophyte are essential for reproduction. After the pollen tube grows from the stigma to the funiculus, it enters the female gametophyte by growing into one of the two synergid cells, which typically undergo cell death before or upon pollen tube arrival. Soon after arrival, the pollen tube ceases to grow and subsequently ruptures to release its sperm cells into the receptive synergid’s cytoplasm, thus triggering the completion of degeneration. Finally, one sperm cell each migrates to the egg cell and central cell to complete double fertilization of the female gametophyte [3, 16, 17, 18, 19].
Synergid cells are required for pollen tube guidance. Several studies using
MYB98, which is exclusively expressed in synergid cells (Figure 4), provides the first molecular evidence of pollen tube guidance in
MYB98 is expressed during the very early stage of synergid cellularization during female gametocyte development, consistent with the
The female gametophyte pollen tube attractants LURE1 and LURE2 have also been identified in
4. Discharge of sperm cells from the pollen tube tip to fertilization
Immediately after growth cessation, the pollen tube ruptures at or near its tip, leading to release of the pollen tube’s contents, including the two sperm cells. In
5. Fertilization recovery system
In angiosperms, double fertilization within the ovule occurs with the entry of two sperm cells, which are usually delivered by a single pollen tube. In 1904, Wylie [32] observed the insertion of two pollen tubes in an
Previously, several research groups [35, 38, 39] studied why several sperm cell–defective mutants exhibited an enhanced fertility phenotype (60–70% fertility); particularly, the frequency ratio of double pollen tube reception was almost completely consistent with the frequency of enhanced fertility (Figure 6). Additionally, the GUS staining experiment revealed that by 10 HAP, ~50% ovules had accepted a mutant allele, indicating that the mutant and wild-type pollen tubes were similarly competent to enter the embryo sac and release their contents. von Besser
According to previous report by Kasahara
6. Pollen tube-dependent ovule enlargement morphology (POEM)
In angiosperms, the pollen tube releases its contents (including sperm cells) into the embryo sac upon insertion into the ovule, thus completing double fertilization. Recently, Kasahara
In animals, once semen is discharged into the uterus, the seminal plasma carries the sperm to the egg [43, 44], whereas in plants, PTC, which transports sperm cells to the ovules, has an analogous function. In mice, fertilization requires seminal vesicle secretory protein 2, which localizes only in the seminal plasma [45]. As seminal plasma is essential for fertilization in animals, Kasahara
In angiosperms, pollination is the first step toward fertilization. Once the pollen reaches the stigma, the grains elongate to form pollen tubes and move toward the synergid cells observed within the female gametophyte. Fertilization occurs when the pollen tubes pierce the female gametophyte; this action terminates pollen tube growth and induces bursting, resulting in the deposition of the two sperm cells inside the female gametophyte. The phenomenon represents a new reproductive phase between pollen tube guidance and fertilization because PTC release itself could induce POEM. Roszak and Köhler [46] demonstrated failure of seed coat synthesis in
PTC was previously found to initiate central cell/endosperm nuclei division without fertilization when it was released to an autonomous endosperm mutant,
7. Summary
This chapter discusses the journey of the pollen tube from the stigma to fertilization as well as the POEM phenomenon. Because very few factors related to pollen tube guidance from the stigma to the funiculus of the ovule have been elucidated, additional insights into this step are eagerly awaited. However, the molecular mechanisms underlying pollen tube guidance from the funiculus to the female gametophyte are well known in
Acknowledgments
I thank Liyang Xie and Xiaoyan Liu at HBMC, FAFU for technical assistance. These works were supported by the Precursory Research for Embryonic Science and Technology (13416724, Kasahara Sakigake Project), Japan Science and Technology Agency. These works were also supported by a grant-in-aid (25840106) from the Japanese Society for the promotion of Science (JSPS). These works were also supported by FAFU-UCR Joint Center and Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University.
References
- 1.
Gifford EM, Foster AS. Morphology and Evolution of Vascular Plants. New York: W.H. Freeman and Company; 1989. p. 49 - 2.
Drews GN, Koltunow AMG. The female gametophyte. The Arabidopsis Book. 2011; 9 :e0155 - 3.
Hamamura Y, Saito C, Awai C, Kurihara D, Miyawaki A, Nakagawa T, Kanaoka MM, Sasaki N, Nakano A, Berger F, Higashiyama T. Live-cell imaging reveals the dynamics of two sperm cells during double fertilization in Arabidopsis thaliana . Current Biology. 2011;21 :497-502 - 4.
Higashiyama T, Yabe S, Sasaki N, Nishimura Y, Miyagishima S, Kuroiwa H, Kuroiwa T. Pollen tube attraction by the synergid cell. Science. 2001; 293 :1480-1483 - 5.
Márton ML, Cordts S, Broadhvest J, Dresselhaus T. Micropylar pollen tube guidance by egg apparatus 1 of maize. Science. 2005; 307 :573-576 - 6.
Kasahara RD, Portereiko MF, Sandaklie-Nikolova L, Rabiger DS, Drews GN. MYB98 is required for pollen tube guidance and synergid cell differentiation in Arabidopsis. Plant Cell. 2005; 17 :2981-2992 - 7.
Okuda S, Tsutsui H, Shiina K, Sprunck S, Takeuchi H, Yui R, Kasahara RD, Hamamura Y, Mizukami A, Susaki D, Kawano N, Sakakibara T, Namiki S, Itoh K, Otsuka K, Matsuzaki M, Nozaki H, Kuroiwa T, Nakano A, Kanaoka MM, Dresselhaus T, Sasaki N, Higashiyama T. Defensin-like polypeptide LUREs are pollen tube attractants secreted from synergid cells. Nature. 2009; 458 :357-361 - 8.
Takeuchi H, Higashiyama T. A species-specific cluster of defensin-like genes encodes diffusible pollen tube attractants in Arabidopsis . PLoS Biology. 2012;10 :e1001449 - 9.
Pruitt RE, Hulskamp M, Kopczak SD, Plownse SE, Schneitz K. Molecular genetics of cell interactions in Arabidopsis . Development. 1993:77-84 - 10.
Kandasamy MK, Nasrallah JB, Nasrallah ME. Pollen pistil interactions and developmental regulation of pollen tube growth in Arabidopsis . Development. 1994;120 :3405-3418 - 11.
Hulskamp M, Schneitz K, Pruitt RE. Genetic evidence for a long-range activity that directs pollen tube guidance in Arabidopsis . Plant Cell. 1995;7 :57-64 - 12.
Lennon KA, Roy S, Hepler PK, Lord EM. The structure of the transmitting tissue of Arabidopsis thaliana (L.) and the path of pollen tube growth. Sexual Plant Reproduction. 1998;11 :49-59 - 13.
Elliott RC, Betzner AS, Huttner E, Oakes MP, Tucker WQ, Gerentes D, Perez P, Smyth DR. AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth. Plant Cell. 1996; 8 :155-168 - 14.
Hauser BA, Villanueva JM, Gasser CS. Arabidopsis TSO1 regulates directional processes in cells during floral organogenesis. Genetics. 1998;150 :411-423 - 15.
Couteau F, Belzile F, Horlow C, Grandjean O, Vezon D, Doutriaux MP. Random chromosome segregation without meiotic arrest in both male and female meiocytes of a dmc1 mutant ofArabidopsis . Plant Cell. 1999;11 :1623-1634 - 16.
Higashiyama T, Kuroiwa H, Kawano S, Kuroiwa T. Explosive discharge of pollen tube contents in Torenia fournieri. Plant Physiology. 2000; 122 :11-14 - 17.
Rotman N, Rozier F, Boavida L, Dumas C, Berger F, Faure JE. Female control of male gamete delivery during fertilization in Arabidopsis thaliana . Current Biology. 2003;13 :432-436 - 18.
Sandaklie-Nikolova L, Palanivelu R, King EJ, Copenhaver GP, Drews GN. Synergid cell death in Arabidopsis is triggered following direct interaction with the pollen tube. Plant Physiology. 2007;144 :1753-1762 - 19.
Ingouff M, Jullien PE, Berger F. The female gametophyte and the endosperm control cell proliferation and differentiation of the seed coat in Arabidopsis. Plant Cell. 2006; 18 :3491-3501 - 20.
Ray A. Three’s company: Regulatory cross-talk during seed development. Plant Cell. 1997; 9 :665-667 - 21.
Shimizu KK, Attractive OK. Repulsive interactions between female and male gametophytes in Arabidopsis pollen tube guidance. Development. 2000;127 :4511-4518 - 22.
Punwani JA, Rabiger DS, Drews GN. MYB98 positively regulates a battery of Synergid-expressed genes encoding Filiform apparatus localized proteins. Plant Cell. 2007; 19 :2557-2568 - 23.
Punwani JA, Rabiger DS, Lloyd A, Drews GN. The MYB98 subcircuit of the synergid gene regulatory network includes genes directly and indirectly regulated by MYB98. The Plant Journal. 2008; 55 :406-414 - 24.
Márton ML, Fastner A, Uebler S, Dresselhaus T. Overcoming hybridization barriers by the secretion of the maize pollen tube attractant ZmEA1 from Arabidopsis ovules. Current Biology. 2012;22 :1194-1198 - 25.
Chen YH, Li HJ, Shi DQ, Yuan L, Liu J, Sreenivasan R, Baskar R, Grossniklaus U, Yang WC. The central cell plays a critical role in pollen tube guidance in Arabidopsis . Plant Cell. 2007;19 :3563-3577 - 26.
Takeuchi H, Higashiyama T. Tip-localized receptors control pollen tube growth and LURE sensing in Arabidopsis . Nature. 2016;531 :245-248 - 27.
Wang T, Liang L, Xie Y, Jia PF, Chen W, Zhang MX, Wang YC, Li HJ, Yang WC. A receptor heteromer mediates the male perception of female attractants in plants. Nature. 2016; 531 :241-244 - 28.
Kaothien P, Ok SH, Shuai B, Wengier D, Cotter R, Kelley D, Kiriakopolos S, Muschietti J, McCormick S. Kinase partner protein interacts with the LePRK1 and LePRK2 receptor kinases and plays a role in polarized pollen tube growth. Plant Journal. 2005; 42 :492-503 - 29.
Zhang Y, McCormick S. A distinct mechanism regulating a pollen-specific guanine nucleotide exchange factor for the small GTPase Rop in Arabidopsis thaliana . Proceedings of the National Academy of Sciences of the United States of America. 2007;104 :18830-18835 - 30.
Mori T, Kuroiwa H, Higashiyama T, Kuroiwa T. Generative cell specific 1 is essential for angiosperm fertilization. Nature Cell Biology. 2006; 8 :64-71 - 31.
Mori T, Igawa T, Tamiya G, Miyagishima SY, Berger F. Gamete attachment requires GEX2 for successful fertilization in Arabidopsis . Current Biology. 2014;24 :170-175 - 32.
Wylie RB. The morphology of Elodea canadensis. Contributions from the hull botanical laboratory. LII . Botanical Gazette. 1904;37 :1-22 - 33.
Maheshwari P. An Introduction to the Embryology of Angiosperms. New York: McGraw-Hill; 1950 - 34.
Kasahara RD, Maruyama D, Hamamura Y, Sakakibara T, Twell D, Higashiyama T. Fertilization recovery after defective sperm cell release in Arabidopsis . Current Biology. 2012;22 :1084-1089 - 35.
von Besser K, Frank AC, Johnson MA, Preuss D. Arabidopsis HAP2 (GCS1) is a sperm-specific gene required for pollen tube guidance and fertilization. Development. 2006; 133 :4761-4769 - 36.
Twell D, Wing R, Yamaguchi J, McCormick S. Isolation and expression of an anther-specific gene from tomato. Molecular & General Genetics. 1989; 217 :240-245 - 37.
Kasahara RD, Maruyama D, Higashiyama T. Fertilization recovery system is dependent on the number of pollen grains for efficient reproduction in plants. Plant Signaling & Behavior. 2013; 8 :e23690 - 38.
Rotman N, Durbarry A, Wardle A, Yang WC, Chaboud A, Faure JE, Berger F, Twell D. A novel class of MYB factors controls sperm-cell formation in plants. Current Biology. 2005; 15 :244-248 - 39.
Brownfield L, Hafidh S, Durbarry A, Khatab H, Sidorova A, Doerner P, Twell D. Arabidopsis DUO POLLEN3 is a key regulator of male germline development and embryogenesis. Plant Cell. 2009;21 :1940-1956 - 40.
Zhang J, Huang Q, Zhong S, Bleckmann A, Huang J, Guo X, Lin Q, Gu H, Dong J, Dresselhaus T, Qu LJ. Sperm cells are passive cargo of the pollen tube in plant fertilization. Nature Plants. 2017; 3 :17079 - 41.
Kasahara RD, Notaguchi M, Nagahara S, Suzuki T, Susaki D, Honma Y, Maruyama D, Higashiyama T. Pollen tube contents initiate ovule enlargement and enhance seed coat development without fertilization. Science Advances. 2016; 2 :e1600554 - 42.
Kasahara RD, Notaguchi M, Honma Y. Discovery of pollen tube-dependent ovule enlargement morphology phenomenon, a new step in plant reproduction. Communicative and Integrative Biology. 2017; 10 :e1338989 - 43.
Sasanami T, Sugiura K, Tokumoto T, Yoshizaki N, Dohra H, Nishio S, Mizushima S, Hiyama G, Matsuda T. Sperm proteasome degrades egg envelope glycoprotein ZP1 during fertilization of Japanese quail (Coturnix japonica). Reproduction. 2012; 144 :423-431 - 44.
Sasanami T, Izumi S, Sakurai N, Hirata NT, Mizushima S, Matsuzaki M, Hiyama G, Yorinaga E, Yoshimura T, Ukena K, Tsutsui K. A unique mechanism of successful fertilization in a domestic bird. Scientific Reports. 2015; 9 :7700 - 45.
Kawano N, Araki N, Yoshida K, Hibino T, Ohnami N, Makino M, Kanai S, Hasuwa H, Yoshida M, Miyado K, Umezawa A. Seminal vesicle protein SVS2 is required for sperm survival in the uterus. Proceedings of the National Academy of Sciences of the United States of America. 2014; 18 :4145-4150 - 46.
Roszak P, Köhler C. Polycomb group proteins are required to couple seed coat initiation to fertilization. Proceedings of the National Academy of Sciences of the United States of America. 2011; 108 :20826-20831 - 47.
Kang IH, Steffen JG, Portereiko MF, Lloyd A, Drews GN. The AGL62 MADS domain protein regulates cellularization during endosperm development in Arabidopsis . Plant Cell. 2008;20 :635-647 - 48.
Grossniklaus U, Vielle-Calzada JP, Hoeppner MA, Gagliano WB. Maternal control of embryogenesis by MEDEA, a polycomb group gene in Arabidopsis . Science. 1998;280 :446-450 - 49.
Luo M, Bilodeau P, Koltunow A, Dennis ES, Peacock WJ, Chaudhury AM. Genes controlling fertilization-independent seed development in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America. 1999; 96 :296-301 - 50.
Bataillon E. L’embryogénèse complète provoquèe chez les Amphibiens par figure de l′œuf vierge, larves parthénogénétiques de Rana fusca. Comptes Rendus. Académie des Sciences; 1910. p. 150 - 51.
Koltunow AM, Grossniklaus U. Apomixis: A developmental perspective. Annual Review of Plant Biology. 2003; 54 :547-574 - 52.
Nogler GA. Gametophytic apomixis. In: Embryology of Angiosperms. 1984. pp. 475-518 - 53.
Focke WO. Die Pflanzen–mischlinge, ein Beitrag zur Biologie der Gewächse. Berlin: Borntraeger; 1881