Female Gametophyte Development in Flowering Plants

ANRV410-PP61-05 ARI 26 March 2010 21:40

Wei-Cai Yang,1 Dong-Qiao Shi,1 and Yan-Hong Chen2

1Key Laboratory of Molecular and Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China; email: [email protected], [email protected] 2College of Life Sciences, Nantong University, Zhongxiu Campus, Nantong 226007, China; email: [email protected]

by Universidad Veracruzana on 01/08/14. For personal use only. Annu. Rev. Plant Biol. 2010. 61:89–108 Key Words First published online as a Review in Advance on embryo sac, synergid cell, egg cell, central cell, cell fate, ovule February 24, 2010 Annu. Rev. Plant Biol. 2010.61:89-108. Downloaded from www.annualreviews.org

The Annual Review of Plant Biology is online at Abstract plant.annualreviews.org The multicellular female gametophyte, a unique feature of higher This article’s doi: plants, provides us with an excellent experimental system to address 10.1146/annurev-arplant-042809-112203 fundamental questions in biology. During the past few years, we have Copyright c 2010 by Annual Reviews. gained significant insight into the mechanisms that control embryo sac All rights reserved polarity, gametophytic cell specification, and recognition between male 1543-5008/10/0602-0089$20.00 and female gametophytic cells. An auxin gradient has been shown for the first time to function in the female gametophyte to regulate gametic cell fate, and key genes that control gametic cell fate have also been identified. This review provides an overview of these exciting discoveries with a focus on molecular and genetic data.

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Ovule development starts as a protrusion (pri- Contents mordium) on the edges of the septum of the gy- necium. As the ovule primordium elongates, a INTRODUCTION ...... 90 finger-like structure (nucellus) is formed. Then, OVULE DEVELOPMENT ...... 90 a hypodermal cell at the tip of the nucellus starts THE TRANSITION FROM to differentiate and forms an archesporial cell, SOMATIC TO GERMLINE which produces the germline. The archesporial FATE...... 91 cell enters meiotic development to differentiate SPECIFICATION OF THE a megasporocyte, which becomes distinct by its FUNCTIONAL MEGASPORE . . . 93 large size and nuclear morphology (Figure 1a). PROGRESSION OF THE The megasporocyte then undergoes meiosis GAMETOPHYTIC MITOTIC to give rise to four haploid megaspores. In CYCLE ...... 94 most flowering plants, which include the model The Initiation of Female species and rice, micropylar mega- Gametogenesis ...... 94 Arabidopsis spores undergo programmed cell death, and the Control of the Gametophytic chalazal-most megaspore becomes functional Cell Cycle ...... 94 and ultimately forms the female gametophyte, CELLULARIZATION OF THE the embryo sac (Figure 1b). Concurrently, epi- EMBRYO SAC ...... 96 dermal cells at the proximal third of the nucel- EMBRYO SAC POLARITY AND lus divide parallel to the long axis and form two GAMETOPHYTIC CELL primodia, which become the inner and outer in- SPECIFICATION...... 96 teguments, respectively (Figure 1a). These en- THE FUNCTIONAL FEMALE close the functional megaspore, which becomes GERM UNIT ...... 99 the embryo sac, forming a narrow opening at The Egg Cell ...... 99 the micropyle where the pollen tube enters af- The Synergid Cell ...... 99 ter pollination. The Central Cell ...... 101 While nonfunctional megaspores undergo CONCLUSIONS ...... 102 cell death, the functional megaspore increases in size and undergoes a nuclear division with- INTRODUCTION out cytokinesis to produce a two-nucleate embryo sac (Figure 1c). The two daughter nuclei, A female gametophyte is a multicellular now separated to the poles by the formation haploid structure that develops into an embryo of a central vacuole (Figure 1d), proceed to by Universidad Veracruzana on 01/08/14. For personal use only. and endosperm after fertilization. In the a second karyokinesis to form a four-nucleate past decade, gametophyte development in embryo sac with nuclei in a 2n+2n configu- plants has emerged as an excellent system Annu. Rev. Plant Biol. 2010.61:89-108. Downloaded from www.annualreviews.org ration (Figure 1e). As the vacuole increases in to address fundamental questions in biology, size, the third karyokinesis takes place, which such as cell specification, cell-cell interaction, results in the formation of a huge coenocytic and the developmental role of basic cellular cell with eight nuclei that adopt a 4n+4n machinery. Significant progress has been made configuration—the eight-nucleate embryo sac to define the genetic components that govern (Figure 1f ). Thereafter, two polar nuclei, one gametogenesis. This review focuses on recent from each pole, migrate to the micropylar cyto- advances in defining genetic control of female plasm of the embryo sac and finally fuse to form gametophyte development. a diploid central nucleus. As polar nuclei migrate, cell walls are formed simultaneously, di- OVULE DEVELOPMENT viding the embryo sac into seven cells with four An ovule is a female organ within the carpel of cell types: three antipodal cells at the chalazal a flower that harbors the female gametophyte. end, a diploid central cell, two synergids, and

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an egg cell at the micropylar end (Figure 1g). The archesporial cell ﬁrst becomes morpho- Antipodal cells degenerate shortly before fer- logically distinguishable from its surrounding tilization in Arabidopsis (Figure 1h) or undergo nucellar cells by its larger size and pronounced further mitosis as seen in maize. Antipodal cells nucleus, and it is called a megasporocyte when are likely dispensable for fertilization. There- fore, the central cell, the egg, and two synergid cells form a female germ unit—a functional unit ab that is able to attract a pollen tube, interact with the tube to trigger sperm release, and complete double fertilization. As mentioned above, ovule development involves both sporophytic and gametophytic processes, and is an excellent system it to study the basic developmental mechanisms that control germline formation, cell growth and division, and gametic cell fate speciﬁcation. ot 10µm 10µm

THE TRANSITION FROM cd SOMATIC TO GERMLINE FATE In angiosperms, the initial cells of the germline, called archesporial cells, are formed de novo from the hypodermal L2 cell layer of the ovule primordium. Generally, in females, a single hy- it podermal L2 cell at the tip of the nucellus dif- fc ferentiates into the germline cell that enters the meiotic pathway, which ultimately gives rise to ot 10µm 10µm gametic cells: the egg and the central cell. −−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−→ ef

Figure 1 Development of the female gametophyte in Arabidopsis. Confocal optical section showing (a) nucleus with MMC ( green) and primordia of by Universidad Veracruzana on 01/08/14. For personal use only. inner (it) and outer (ot) integuments; (b) one-nucleate embryo sac ( green) and degenerating megaspores ( yellow) close to the Annu. Rev. Plant Biol. 2010.61:89-108. Downloaded from www.annualreviews.org micropyle; (c) an early two-nucleate embryo sac ( green); (d ) a late two-nucleate embryo sac ( green), 10µm 10µm inner (it) and outer (ot) integuments, and funiculus (fc); (e) a four-nucleate embryo sac ( green); ( f )an gh early eight-nucleate embryo sac ( green), with antipodal nuclei (pink), polar nuclei (blue), egg nucleus (red ), and synergid nuclei ( yellow); ( g) a late eight-nucleate embryo sac ( green), with antipodal nuclei (pink), polar nuclei (blue), egg nucleus (red ), and synergid nuclei ( yellow); (h) a mature four-celled embryo sac ( green), with the secondary nucleus (blue), egg nucleus (red ), and synergid nuclei ( yellow). Scalebar: 10 μm. Confocal images were modiﬁed with PhotoShop to highlight the 10µm 10µm megaspore mother cell, embryo sac, and nuclei.

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its nucleus enters the prophase of meiosis. that surround germline cells but not in the de- How the transition from a somatic cell fate veloping germline cells. This supports a role to a germline fate is controlled remains un- for MSP1 in determining germline cell fate known. However, several putative components by preventing the surrounding cells from be- that control this transition have been identi- coming germline cells, similar to MAC1 in fied through genetic approaches. In Arabidopsis, maize (64). MSP1 encodes a leucine-rich re- the SPOROCYTELESS gene (SPL/NOZZLE) peat containing receptor-like kinase (LRR- has been implicated in controlling germline RLK). This implies that signaling between cell fate. In spl mutants, archesporial cells are the archesporial cell and its neighboring cells formed in both anther and ovule primodia, but is controlled by a ligand-receptor signaling they fail to develop further, which results in a cascade, and this plays a critical role in fe- complete lack of germline in male and female male germline development. These findings organs (63, 75). This indicates that SPL plays an imply that a lateral inhibition mechanism may essential role in germline formation. A recent act in controlling the number of germline study revealed that the floral homeotic regu- cells. lator AGAMOUS (AG) can activate the SPL Because MSP1 is a membrane receptor ki- gene by binding to the CArG-box in its 3 re- nase, it likely exerts its effects by binding to a gion (24). SPL expression activated by AG in- ligand. Recently, a putative ligand OsTDL1A duces the ectopic formation of microspores on was shown to bind the extracellular domain petaloid floral organs, which indicates ectopic of MSP1 by yeast two-hybrid and BiFC ex- formation of the male germline. This finding periments (78). Similar to MSP1, TDL1A is not only showed that SPL is a direct down- expressed exclusively in nucellar cells but not stream target of AG but also demonstrated that in germline cells. Furthermore, knockdown of SPL is sufficient to trigger male germline spec- OsTDL1A expression phenocopies the msp1 ification in Arabidopsis. Whether SPL is also phenotype in the nucellus. A similar mecha- sufficient for female germline specification re- nism, mediated by TPD1-EMS1/EXS1 signal- mains unknown. SPL encodes a novel nuclear ing, controls male sporocyte fate (25, 36). These protein with limited homology to MADS-box data suggest that specification of germline cell transcription factors (63, 75). Therefore, how fate and number in plants involves a similar SPL regulates its downstream genes in germline ligand-receptor signaling system in both the specification is of great interest. Recently, re- male and female. searchers suggested that SPL may be involved in In animals, germline fate is controlled by auxin homeostasis by repressing YUCCA genes a germline-specific PIWI-associated miRNA by Universidad Veracruzana on 01/08/14. For personal use only. in lateral organ development (32). It would be (piRNA) system (33). Emerging data suggest interesting to investigate whether auxin is also that miRNA also plays an important role in

Annu. Rev. Plant Biol. 2010.61:89-108. Downloaded from www.annualreviews.org involved in germline formation. germline development in plants. MEIOSIS Several genes that control the number ARRESTED AT LEPTOTENE1 (MEL1), a of cells entering germline fate have also germline-specific member of ARGONAUTE been identified. Mutation in MULTIPLE (AGO) genes family, is specifically expressed ARCHESPORIAL CELLS 1 (MAC1) results in archesporial cells and sporogenous cells in an excessive number of archesporial cells (SCs), and disappears when SCs enter meiosis in maize (64). Similarly, in rice, the multiple in anther and ovule. Ovule development in sporocyte 1 (msp1) mutants have increased num- mel1 mutants is arrested at various stages from bers of both male and female sporocytes (45). pre-meiosis to tetrad. Chromosomes remain These excess sporocytes likely result from ex- uncondensed, and aberrant chromatin modifi- cessive archesporial cells, which suggests that cation is detected in mel1 germline cells, which MSP1 is required for archesporial cell fate. suggests that MEL1 acts on chromatin struc- The MSP1 gene is expressed in nucellar cells tures, similar to those of the PIWI subfamily of

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AGOs in Drosophila. This implies that MEL1 Observed in many species, polarity within is required for female germline development, the megasporocyte is manifested by the po- most likely by regulating cell division of lar distribution of organelles, the dynamic de- pre-meiotic germline cells, modification position of callose, and the microtubule cy- of meiotic chromosomes, and progression of toskeleton. So far, the role of this polarity on meiosis; but it does not affect the initiation, megaspore development is unknown. The dis- establishment, and early mitotic division of ruption of this polarity in megasporocytes was germline cells (46). observed in switch1 (swi1)/dyad ovules in Ara- Interestingly, the MEL1 expression domain bidopsis (42, 68). SWI1 encodes a novel protein is larger than the germline cell in anther and involved in chromatid cohesion establishment ovule primordia. Therefore, archespores may and chromosome structure during meiosis (2, be produced in excess of subsequent archespo- 38). Interestingly, dyad mutation causes de- rial cells, and the fate of archesporial deriva- fective meiosis that produces two unreduced tives may be controlled by signals from SCs. megaspores (diploid) (60). However, only the Therefore, MEL1 may suppress somatic gene chalazal megaspore, but not the micropylar expression during germline development (46). megaspore, expresses functional megaspore- How does MEL1 function? MEL1 may modify specific markers. This indicates that only the chromatin structure to repress the somatic gene chalazal megaspore is functional and suggests expression program in germline cells. Although a position-dependent mechanism. It also im- the role of MEL1 orthologs in germline forma- plies that a decision on cell fate has been made tion has not been identified in other plants, this at this stage of ovule development. In maize, demonstrates for the first time that, as in ani- a similar mutation in ameiotic (am1) has been mals, the small RNA-mediated gene silencing identified in which meiosis is replaced by a mi- pathway mediated by MEL1 plays a key role in totic division, as in swi1/dyad. Analysis of am1 plant germline formation (18). allelic mutations indicates that the division of the megasporocyte is completely blocked in some alleles, or meiosis is initiated but not SPECIFICATION OF THE completed in other alleles. However, all mei- FUNCTIONAL MEGASPORE otic processes are impaired in am1. Together, The female megasporocyte undergoes meiotic these data suggest that SWI and AM1 are es- division to produce four haploid megaspores. sential for the switch between meiotic and mi- Of the four megaspores, one, two, or four may totic division cycles and likely regulate the participate in the formation of the final female transition through a novel leptotene–zygotene by Universidad Veracruzana on 01/08/14. For personal use only. gametophyte depending on the plant species. checkpoint. AM1, which shares 30% iden- In the more advanced species, only one of the tity with SWI1, is a plant-specific chromatin-

Annu. Rev. Plant Biol. 2010.61:89-108. Downloaded from www.annualreviews.org four megaspores is functional, and the remain- binding protein with as yet unknown function ing three undergo programmed cell death. The (54). choice of functional megaspore is position de- Surprisingly, the chalazal unreduced megas- pendent and also species dependent. In most pore in dyad mutants occasionally proceeds to flowering plants, including Arabidopsis and rice, form an unreduced embryo sac that can be fer- the megaspore that is closer to the maternal tis- tilized to produce triploid seeds (60), which sue becomes the functional megaspore; distal may have implications for engineering hybrid micropylar megaspores undergo programmed seed production in agriculture. This is likely cell death. Evolution seems to favor the more linked to the truncated SWI1 protein produced defined monosporic type of gametogenesis, and in dyad. The functional dissection of SWI1 and genetic mechanisms must have evolved to de- AM1 will shed light on how meiotic to mitotic fine such developmental control. transition is regulated.

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PROGRESSION OF THE during gametogenesis remains to be clarified. GAMETOPHYTIC MITOTIC In AGP18 knockdown plants, the functional CYCLE megaspore fails to enlarge and divide. AGP18 is expressed in the female germline including The functional megaspore undergoes rapid the functional megaspore, and it is weakly ex- growth, taking up the space left by the de- pressed in somatic nucellar cells. This sug- generating megaspores, and goes through three gests that a cell surface proteoglycan is re- consecutive rounds of karyokinesis to form an quired for functional megaspore development eight-nucleate syncytial embryo sac. This sac in (1). is cellularized simultaneously to form a seven- Arabidopsis celled female gametophyte, composed of four different cell types: egg, synergid, central, and Control of the Gametophytic antipodal. In the past decade, genetic studies Cell Cycle have identified several mutations and genes that Many female gametophyte ( ) mutations, control different stages of embryo sac develop- fem which were identified through a distorted ment (50). Meanwhile, comparative expression- Mendelian segregation screen, display mitotic profiling studies and cell-specific EST sequenc- arrest of the female gametophytic division cycle ing have revealed many genes that are expressed (50). This indicates that progression of the mi- in the female gametophyte (31, 70, 74, 76, totic cycle is critical for the formation of a func- 77). We discuss progress in each developmen- tional gametophyte. Several mutants defective tal stage and focus on recent important findings in the progression of the mitotic division cycle below. have been identified and molecular cloning of these genes is starting to shed light on how cell cycle progression is regulated during female ga- The Initiation of Female metogenesis in plants. Gametogenesis The anaphase-promoting complex/ Little is known about the genetic and molec- cyclosome (APC/C) is a cell cycle–regulated, ular control of the initiation of female game- multiple-subunit E3 ubiquitin-protein ligase togenesis in flowering plants, although many that controls important transitions during gametophytic mutations block embryo sac de- mitotic progression and exit by sequentially velopment at the one-nucleate stage. Mutations targeting for degradation many cell cycle in AGL23, a type I MADS-box gene, block the regulators, such as cyclins (55). The knockout first nuclear division of the functional mega- of APC/C components often impairs female by Universidad Veracruzana on 01/08/14. For personal use only. spore (12). AGL23 expression is first detected gametophyte development. Mutations in either in the functional megaspore and persists in the NOMEGA, which encodes APC6/CDC16,

Annu. Rev. Plant Biol. 2010.61:89-108. Downloaded from www.annualreviews.org embryo sac. Together these data suggest that or APC2, which interacts with APC11 and AGL23-regulated transcription is required for APC8/CDC23, cause embryo sac arrest at the early female gametogenesis. However, AGL23 two-nucleate stage (7, 29). This indicates that may not be required for the initiation or cell di- the APC/C ubiquitin-mediated proteolysis vision of the functional megaspore, or cell cycle pathway plays a role in female gametophytic progression during subsequent embryo sac de- cell cycle control. Similarly, mutations in velopment in Arabidopsis. regulatory particle triple A ATPase (RPT ) of the Using monoclonal antibodies against cell 26S proteasome arrest embryo sac develop- wall components, female reproductive lineage ment at the one- or two-nucleate stage in the has been associated with distinct changes in rpt5a-4 rpt5b-1 double mutant, which indicates the distribution and types of arabinogalactan a defect of the ﬁrst or second mitosis of the protein (AGP) epitopes (11). Whether AGPs female gametophyte (17). Similarly, the double function in cell surface signaling or recognition mutation of two RING-ﬁnger E3 ligase genes

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RHF1a and RHF2a results in the interphase wild-type pollen form abnormal embryos, arrest of the mitotic cell cycle in the female which implies that RBR is required for a com- gametophyte. RHF1a directly targets a cyclin- plete differentiation of all gametophytic cells dependent kinase inhibitor ICK4/KRP6 for (14, 26). This indicates that rbr mutant ovules proteasome-mediated degradation (34). This are able to cellularize and form functional egg suggests that the ubiquitin/26S proteasome cells, which suggests that egg cell fate requires system helps control cell cycle progression the completion of a third nuclear division, but during female gametophyte development. not an arrest in the gametophytic cell cycle. PRL encodes the DNA replication licensing Therefore, RBR connects cell cycle control to factor subunit MCM7 that is required in all cellular differentiation processes. proliferating cells, including female germline In the indeterminate gametophyte1 (ig1) mu- cells (69). Knockout of PRL function arrests tant of maize, female gametophytes have a embryo sacs primarily at the one-nucleate stage. prolonged phase of free nuclear divisions be- Recently, we identiﬁed the slow walker1 (swa1) fore cellularization, which leads to a variety of mutation that causes slow progression of the embryo sac abnormalities, including extra egg gametophytic division cycle and female sterility cells, extra synergids, and extra central cells with owing to incomplete development of the female extra polar nuclei (16, 20). The rbr1 mutants of gametophyte at anthesis (65). Delayed pollina- Arabidopsis have a similar phenotype, with addition tests showed that a small fraction of swa1 tional defects in pollen development. This sug- ovules are able to form functional female game- gests that IG1 restricts the proliferative phase tophytes; however, they missed the correct time of female gametophyte development. for fertilization because of the slow down of fe- Together, these data suggest that timely mi- male gametophyte development when naturally totic progression of the division cycle is vi- pollinated, which indicates that coordinated tal for gametogenesis. In addition to the con- development between the male and female ga- served cell cycle machinery, other regulatory metophyte is critical for fertility in Arabidopsis. mechanisms may play a role in gametophytic SWA1 encodes a nucleolar WD40-containing cell fate in plants. One such mechanism is pro- protein that is involved in the processing of tein phosphorelay. The loss of CYTOKININ pre-18S rRNA in Arabidopsis, which suggests INDEPENDENT1 (CKI1) function also re- that RNA biogenesis plays a role in the sults in the early degeneration of gametophytic progression of the gametophytic division cycle. cells and excess nuclei (56). CKI1 encodes a Mutations in the Arabidopsis retinoblastoma- histidine kinase, which suggests that His/Asp related (RBR) gene, a key negative regulator phosphorelay signaling plays a role in female by Universidad Veracruzana on 01/08/14. For personal use only. that controls G1/S transition by repressing E2F gametogenesis. At the onset of megagameto- transcription factors, result in arrested mitosis genesis, RNA interference depletes CHR11, a

Annu. Rev. Plant Biol. 2010.61:89-108. Downloaded from www.annualreviews.org and uncontrolled nuclear proliferation, which member of the ATP-dependent SWI2/SNF2 gives rise to embryo sacs with supernumerary family of chromatin-remodeling factors. This nuclei that are irregular in size and partially en- depletion arrests uncellularized embryo sac de- closed by cell-wall-like structures (14). This in- velopment at the one-, two-, four-, or eight- dicates that cellularization and karyokinesis can nucleate stages in Arabidopsis, which indicates be uncoupled, and they are regulated indepen- a role for chromatin-remodeling in karyoki- dently. Consistently, premature cellularization nesis during female gametogenesis (22). RBR has been observed in hadad (hdd) ovules after suppresses E2F-like protein activity by re- the ﬁrst or second gametophytic division (41). cruiting chromatin-remodeling factors of the Although most proliferating rbr female game- SWI2/SNF2 family. Together, CHR11 and tophytes fail to express cell-speciﬁc markers, a RBR regulate the E2F family proteins, and fraction of ovules in selfed rbr1–1/+ siliques thereby promote nuclear proliferation during or rbr1–1/+ siliques that are pollinated with female gametogenesis. Furthermore, histone

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acetyltransferase HAM1 and HAM2 act redun- hedgehog signaling complex in animals. Both dantly during ovule development because ham1 GEM1/MOR1 and TIO have a general effect ham2 double mutant embryo sacs arrest at the on cell plate formation in somatic and repro- one-nucleate stage with a huge nucleus (30), ductive cells. The incomplete cell plate in tio which indicates that gene suppression and chro- pollen is positioned correctly, which suggests matin compaction requiring hypoacetylation of that TIO is not required for the positioning or histones in the functional megaspore block the establishment of the cell plate but has a specific first karyokinesis during megagametogenesis. role in cell plate expansion (47). In addition, knockout of TUBG1 and 2 genes, which encode γ-tubulin, results in uncellularized embryo sacs CELLULARIZATION OF THE with aberrant morphology, positioning, and EMBRYO SAC number of nuclei (53). In plant cells, the lateral Cellularization of the syncytial embryo sac expansion of phragmoplast and cell plate is reg- is controlled temporally and spatially during ulated by a kinesin-MAPKKK pathway during ovule development, and it is critical for gameto- cytokinesis; mutations in two kinesin-like pro- phytic cell fate specification. Several genes have teins, AtNACK1 and AtNACK2, that bind and been implicated in controlling this process. In activate the MAPKK kinase NPK1 result in the gemini pollen2 ( gem2), the cellularization of the mispositioning of nuclei and the formation of embryo sac is impaired: resulting in embryo nonfunctional gametophytes (72). Therefore, sacs that contain five nuclei at the micropylar they all play a role in positioning phragmoplast pole and three at the chalazal pole. Moreover, and cell plate expansion, thereby controlling the no cell boundaries or only partial cellulariza- cellularization of the embryo sac. However, it tions are observed between nuclei. Most ma- is not clear how the cell plate expansion pheno- ture mutant embryo sacs contain one or two type is associated with the karyokinesis defect. extremely large nuclei, which might arise from the fusion of free nuclei at the micropylar pole EMBRYO SAC POLARITY AND (52). However, gem2 plants also display a variety of division defects in pollen development, GAMETOPHYTIC CELL which include division asymmetry and incom- SPECIFICATION plete cytokinesis. Together, these data suggest The embryo sac is a polarized structure with that GEM2 plays a critical role in coordinating antipodal cells at the chalazal end and the egg karyokinesis and cytokinesis during gametoge- apparatus at the micropylar end. Gametophytic nesis. Interestingly, the partial cellularization of cells within the embryo sac are also highly po- by Universidad Veracruzana on 01/08/14. For personal use only. gem2 ovules can develop further and form an larized. The nucleus of the egg cell is located embryo sac with a large cell that possesses vac- toward the chalazal end of the embryo sac,

Annu. Rev. Plant Biol. 2010.61:89-108. Downloaded from www.annualreviews.org uolar characteristics of an egg cell, which sug- whereas the nuclei of the synergid and cen- gests that egg cell fate can occur in a partially tral cells are located toward the micropylar end. cellularized embryo sac, and local cellulariza- Therefore, the egg cell, and the central cell and tion may reinforce a gradient of cell fate deter- synergids have opposite polarity. The opposite minants that are established in the coenocytic polarity of the central cell and egg brings their embryo sac (52). nuclei into close proximity, which may facili- In addition, gem1/mor1 and two in one (tio) tate their fusion with the sperm nuclei during mutants display similar or even more severe double fertilization. The ﬁnal polarity of the ovule phenotypes as gem2. GEM1/MOR1 en- embryo sac is a result of coordinated nuclear codes a microtubule-associated protein (73), division and positioning, expansion of the cen- and TIO encodes an essential phragmoplast- tral vacuole, and cellularization. This polarity associated protein that is homologous to the can be traced back to the four-nucleate stage, FUSED (Fu) Ser/Thr protein kinase of the when two pairs of nuclei, separated by a large

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central vacuole, migrate to opposite ends of the in the embryo sac. IG1 encodes a LATERAL syncytial embryo sac. At the chalazal pole, the ORGAN BOUNDARIES (LOB) domain pro- nuclei are positioned one above the other with tein with high similarity to ASYMMETRIC respect to the micropylar-chalazal axis. Mean- LEAVES2 (17), which controls leaf symmetry while, the nuclei generally locate side by side in Arabidopsis. During female gametogenesis, at the micropylar end. Comparatively large nu- IG1 is expressed in functional, but not nonfunc- cleoli distinguish the two polar nuclei in the tional, megaspores; it is strong in antipodal cells eight-nucleate stage. The migration and pre- and the egg; and no signal is detected in the cise positioning of the nuclei and morphologi- synergids (16). Thus IG1 is asymmetrically ex- cal differentiation of the polar nuclei suggest an pressed in the embryo sac, which supports the early distinction between the nuclei before cel- existence of embryo sac polarity. lularization. Polar expression of genes has also Recently, Sundaresan and colleagues dis- been observed. For example, the DEMETER covered an asymmetric auxin gradient in the (DME) gene, a key regulator of gene imprint- syncytial embryo sac that plays a key role in ing during endosperm development, is polarly gametic cell specification (49). Using the syn- expressed in the micropylar domain of the em- thetic DR5:GFP or DR5:GUS reporter that is bryo sac: first in the polar nuclei and synergid responsive to auxin, the auxin response can be nuclei before cellularization and then restricted traced by monitoring reporter expression. Dur- to the central cell after cellularization. FIS2,a ing megasporogenesis, GFP or GUS expression downstream gene of DME, is expressed only in is detected at the distal tip of the nucellus and the polar nuclei but not in the future synergid increases in nucellar cells that surround the de- or egg, or antipodal nuclei (9). In rbr mutant veloping embryo sac at the early one-nucleate embryo sacs, FIS2 expression is lost or occa- stage. As the ovule develops, auxin level in- sionally deregulated, which indicates the RBR- creases within the micropylar domain of the controlled FIS2 polarity is nessessary for the embryo sac at the two- to eight-nucleate stages. differentiation of the central cell in the embryo Interestingly, the auxin response distribution is sac (26). This polarity further suggests a role less polarized in the cellularized embryo sac, for positional cues in gametic cell specification. because the reporter is expressed in all gameto- Compared to embryo sac polarity, the polar- phytic cells. These data suggest a micropylar- ity within gametophytic cells is obviously estab- chalazal gradient of auxin in embryo sacs. Con- lished after cellularization of the eight-nucleate sistently, the disruption of auxin responses by embryo sac. The differentiation of egg and syn- downregulating AUXIN RESPONSE FACTOR ergid cell fate also suggests that a lateral inhi- (AFR) gene expression, or auxin synthesis by by Universidad Veracruzana on 01/08/14. For personal use only. bition mechanism may exist for gametophytic ectopic expression of the auxin biosynthetic cell specification after cellularization (19). YUCCA1 gene, impairs gametophytic cell iden-

Annu. Rev. Plant Biol. 2010.61:89-108. Downloaded from www.annualreviews.org Although the cellular and molecular basis tities at the micropylar domain. Specifically, of gametophytic cell specification in the em- synergids adopt the fate of the egg cell in ARF bryo sac is largely unknown, emerging evidence knockdown embryo sacs, and ectopic YUCCA1 supports the involvement of positional and lat- expression results in the misspecification of all eral inhibition mechanisms in determining ga- gametophytic cells. However, no abnormalities metophytic cell fate. Several studies in maize in embryo sac polarity or changes in central cell and Arabidopsis support the idea of a positional and antipodal cell fates are observed. This sug- mechanism. In the maize ig1 mutant, embryo gests that such an auxin gradient is essential for sacs undergo extra rounds of free nuclear divi- gametophytic cell specification but not for em- sions, which result in extra egg cells, extra cen- bryo sac polarity and central cell and antipo- tral cells, and extra polar nuclei (17, 23). The fi- dal cell fates. Furthermore, auxin polar trans- nal fate of the extra nuclei as either egg nuclei or porters of the PIN family are not expressed polar nuclei depends on their relative position in the embryo sac, suggesting that the auxin

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gradient is correlated with location-specific cell fate specification during female gameto- auxin biosynthesis and diffusion (49). phyte development. Furthermore, LIS nuclear A fundamental question of female gameto- localization requires the CLO/GFA1 protein. genesis is, How is gametic cell fate determined? The findings above have several profound im- As discussed above, embryo sac polarity and an plications, as pointed out by Gross-Hardt and auxin gradient play a key role in gametophytic colleagues (19). First, all gametophytic cells are cell fate. The manipulation of auxin responses competent to adopt gametic cell fate, and LIS or synthesis results in the switching of gametic is involved in a mechanism that represses ga- and nongametic cell fates (49). Toidentify genes metic cell fate in accessory cells. Second, there that control egg cell fate, Gross-Hardt and col- might be an intracellular signaling mechanism leagues (19) mutagenized an egg cell-specific that senses the number of nuclei in a given cell. marker line and then screened for expression Third, there are two levels of cell fate regula- changes of the egg cell-specific marker. They tion: one between the gametic cell and acces- identified three mutants, lachesis (lis), clotho (clo) sory cells, and the other between the egg cell and atropos (ato), that showed deregulation of and central cell. Together, these genes might be the marker (19, 40). In lis embryo sacs, the ex- involved in an as yet unknown signaling path- pression of the egg–specific marker is expanded way that operates in gametic cells and prevents to the synergids and central cell. Consistently accessory cells from adopting a gametic cell fate. lis synergids display egg cell morphology de- Interestingly, LIS, CLO/GFA1, and ATO all fects and downregulate synergid-specific gene encode components of RNA splicing machin- expression. Pollen tube attraction is compro- ery. LIS is homologous to the yeast splicing mised, and reduced as well. These results in- factor PRP4; CLO/GFA1 is a plant homolog dicate that the synergids have adopted an egg of yeast Snu114p, likely a component of the cell fate in lis embryo sacs. Interestingly, the U5 snRNP of the spliceosome, and is required ET884 synergid-specific marker is ectopically for the cell-specific expression of LIS gene (35, expressed throughout lis embryo sacs. Similarly, 40). This implies that LIS is downstream of the central cell in lis embryo sacs also adopts CLO/GFA1 in the pathway controlling ga- an egg cell fate. Polar nuclei rarely fuse and metic cell specification. In addition, LIS and cellularize separately to give rise to small un- CLO/GFA1 are colocalized to nuclear speck- inucleate cells that are morphologically indis- les; this suggests they may form a complex as tinguishable from the egg cell. Compromised well. ATO is homologus to SF3a60, a protein central cell fate is further suggested by the that is implicated in prespliceosome formation. downregulation of expression from the cen- These findings suggest that the RNA splicing by Universidad Veracruzana on 01/08/14. For personal use only. tral cell-specific MEA promoter. Surprisingly, machinery plays an important role in gametic the antipodal cells of lis embryo sacs adopt a cell specification in the female gametophyte, al-

Annu. Rev. Plant Biol. 2010.61:89-108. Downloaded from www.annualreviews.org central cell fate as evidenced by their fusion, though the underlying mechanisms remain to and the downregulation of an antipodal-specific be elucidated. marker, and the activation of a central cell- The LIS gene is expressed strongly in repro- specific marker (19). A similar phenotype is also ductive tissues and remains high in gametic cells found in the clo/gfa1 mutant (40). Unlike that but downregulated in accessory cells shortly af- of the ig1 mutant in maize, the accessory cell ter cellularization. Combined with its mutant (synergid and antipodal cell) fates have been phenotype, this has led to a lateral inhibition mis-specified because no supernumerary nuclei model in which, upon differentiation, gametic or cells are observed in lis or clo/gfa1 embryo cells generate an inhibitory signal that is trans- sacs. One idea that accounts for these pheno- mitted to adjacent cells to prevent excess ga- types is that accessory cells are gradually re- metic cell formation (19). This model can ex- cruited as gametic cells. This demonstrates a plain the maintenance of only one egg cell in central role for LIS and CLO/GFA1 in gametic the embryo sac after the initial specification of

98 Yang · Shi · Chen ANRV410-PP61-05 ARI 26 March 2010 21:40

cell fate. However, once the egg cell is differ- THE FUNCTIONAL FEMALE entiated, a lateral inhibition mechanism may be GERM UNIT necessary to maintain cell fates because accessory cells can differentiate into gametic cells The Egg Cell later if this inhibitory mechanism is not present Egg cell specification is a result of the in- (19). terplay between the auxin gradient and the EOSTRE, which encodes a BELL-like LIS-mediated mechanism as discussed above. homeodomain protein (BLH1), plays a role in Although many egg-specific transcripts have restricting synergid cell fate. In the eostre mu- been identified through single cell library and tant, the female gametophyte is arrested at mul- EST analysis, key genes that control egg cell tiple stages that range from one-nucleate to function have not been identified. GAMETE mature embryo sacs, and some mutant embryo EXPRESSED3 (GEX3) is expressed specifically sacs collapse completely. The mutant embryo in the egg cell of the female gametophyte and sacs often display mispositioned nuclei during in pollen, and encodes a plasma membrane- the syncytial stage. Interestingly, a portion of localized protein with unknown function that eostre embryo sacs displays abnormal cell spec- has homologs in other plants. Both knockdown ification, in which one of the two synergids ex- and overexpression of GEX3 impair the female hibits polarity characteristic of the egg cell and control of micropylar pollen tube guidance (3). expresses an egg cell-specific marker. This in- Although the underlying mechanism is still un- dicates that one synergid has adopted an egg known, this demonstrates a role for the egg cell cell fate, and therefore that there are two egg in the female control of pollen tube guidance, cells in a single embryo sac, whereas the initial in addition to fertilization. central cell and the egg cell fate are not affected (51). Furthermore, the extra egg cell can be fertilized after pollination, which indicates that it is fully functional. Molecular anal- The Synergid Cell ysis showed that the eostre phenotype is caused Synergid cells are key components of the fe- by the misexpression of the EOSTRE gene, male germ unit (FGU) and are located, side by which is not expressed in the ovule in wild side with the egg cell, in the micropylar por- type. BELL functions by forming a BELL- tion of the embryo sac. Typically, the synergid KNAT heterodimer whose activity is regulated cells display an opposite polarity compared to by ovate family proteins (OFPs). Consistently, the egg cell, they have no or discontinuous cell the eostre phenotype can be reversed by a muta- wall at the chalazal end, and they are sealed by a by Universidad Veracruzana on 01/08/14. For personal use only. tion in the class II knox gene KNAT3 and phe- specialized cell wall-like structure—the filiform nocopied by disruption of AtOFP5, a regulator apparatus at the micropylar opening. Often,

Annu. Rev. Plant Biol. 2010.61:89-108. Downloaded from www.annualreviews.org of BLH1-KNAT3heterodimers (51). Together, one of the two synergids undergoes cell death these data suggest a role for BLH-KNAT3 upon arrival of the pollen tube. The synergids complex and AtOFP in gametic cell specifi- likely play important roles in the attraction and cation. Other BELL-like genes may substitute recognition of the pollen tube, sperm release, the EOSTRE function to promote egg cell fate and transportation. Therefore, genes that are in female gametophytes because the loss of involved in those processes may be expressed in EOSTRE function has no effect on female ga- synergids. However, the mechanisms by which metophyte development. In addition, it would synergid cells develop their unique features are be interesting to know whether the aberrant nu- poorly understood. clear configuration observed in eostre syncytial Mutations that affect synergid development embryo sacs or the polarity change in one of and function and genes that are specifically ex- the synergid cells has any role in gametic cell pressed in the synergids have been identified specification. (70). MYB98, which encodes a R2R3-type MYB

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transcription factor, is specifically expressed in (allelic to SIRENE, SRN) is a key gene that the synergids. Mutation in the MYB98 gene controls the recognition between the synergids specifically abolishes the formation of the fil- and the pollen tube. In fer/srn ovules, the pollen iform apparatus and has no effect on other as- tube enters a synergid and overgrows within pects of ovule development (28). Thus, MYB98 the embryo sac (23, 61), which suggests that is required specifically for the formation of FER/SRN plays a role in pollen tube reception the filiform apparatus during synergid cell dif- by the synergid. FER encodes a LRR-RLK that ferentiation. Consistently, recent studies show accumulates specifically on the plasma mem- that MYB98 binds to a specific DNA sequence brane of the synergid cells (15). Therefore, (TAAC) and regulates a subset of genes that FER may be a synergid-specific membrane re- encode secreted proteins targeted to the fili- ceptor which, upon binding to a signal from the form apparatus (59). Most synergid-expressed pollen tube, triggers a signaling cascade within genes that are downregulated in myb98 en- the synergids to prepare for fertilization and code small defensin-like cycteine-rich proteins also sends a signal to stop pollen tube growth (CRPs) that are secreted into the filiform ap- (15, 37). In support of this idea, additional paratus, which suggests that they play a role mutations are also reported in Arabidopsis.In in either the formation or the function of the the lorelei (lre) mutant, pollen tubes that reach filiform apparatus (59). Many of these genes embryo sacs often do not rupture but continue are also weakly expressed in egg and/or cen- to grow in the embryo sac, reminiscent of tral cells. Interestingly, myb98 female gameto- the fer/srn phenotype. Moreover, lre embryo phytes that lack the filiform apparatus also lose sacs often attract additional pollen tubes. their ability to guide the pollen tube to the mi- LRE encodes a small plant-specific putative cropyle; therefore, MYB98 may also play a role glucosylphosphatidylinositol-anchored protein in the production of the guidance cue. Together, and is expressed in synergid cells prior to fer- these data strongly suggest that MYB98 acts tilization (76). Pollen tubes of anxur1/anxur2 as a synergid-specific transcriptional regulator double mutants rupture before arriving at to activate downstream genes that are required the synergid cells (39). Both ANXUR1 and for pollen tube guidance and filiform apparatus 2 genes encode receptor-like kinases that formation. are specifically expressed in pollen tubes. In To attract and recognize the pollen tube, addition, mutations in ABERRANT PEROX- synergids need the ability to secrete pollen at- ISOME MORPHOLOGY2/ABSTINENCE tracting signals and receive the pollen tube. Re- BY MUTUAL CONSENT (APM2/AMC), cent studies have provided strong evidence of which is required for peroxisome transport, by Universidad Veracruzana on 01/08/14. For personal use only. this. Using laser ablation, synergids, but not impair pollen tube reception (5). This suggests any other gametophytic cells, were shown to another signaling cascade, independent of the

Annu. Rev. Plant Biol. 2010.61:89-108. Downloaded from www.annualreviews.org be required for pollen tube guidance in Torenia FER/SRN-ANXUR kinase pathway that re- fournieri (21). Also in T. fournieri, CRPs named quires intact peroxisome function in both male LUREs have been identiﬁed and are secreted and female gametophytes, although the under- by synergids to attract pollen tubes in a semi– lying mechanism remains to be elucidated. in vivo assay (48). In Arabidopsis, CRPs are en- Synergid cell death associated with fertil- coded by a large gene family and expressed in ization is a common phenomenon, which has the synergids and secreted into the ﬁliform ap- been described in many plant species and in- paratus as discussed above. However, genetic variably involves the collapse of vacuoles, a dra- data that support their role as the guidance cue matic decrease in cell volume, and complete are still lacking. disintegration of the plasma membrane and Synergid cells also play an essential role most organelles. The underlying mechanisms for pollen tube reception. FERONIA (FER) have not been revealed so far. In Arabidopsis,

100 Yang · Shi · Chen ANRV410-PP61-05 ARI 26 March 2010 21:40

synergid cell death is initiated upon pollen tube forms a heterodimer with AGL80, and its nu- arrival but before pollen tube discharge, which clear localization requires AGL80 because DIA suggests that pollen tube-synergid contact trig- nuclear localization is lost in the agl80 mu- gers a signaling cascade that induces synergid tant. AGL80 is also expressed in the polar nu- cell death (62). In gfa2 mutant ovules, the po- clei and the secondary nucleus of the central lar nuclei fail to fuse and the synergid per- cell, and a mutation in the AGL80/FEM111 sists after pollination. These ovules can attract gene in Arabidopsis specifically affects central pollen tubes but are not fertilized. This indi- cell maturation. Polar nucleoli and vacuole mat- cates that synergid cell death associated with uration fail and lead to endosperm development fertilization did not occur, which suggests a arrests after fertilization. The egg, synergid, role for GFA2 in promoting synergid cell death and antipodal cells are correctly specified (57). (10). The GFA2 gene encodes a mitochondrion- Therefore, both DIA and AGL80, most likely located DnaJ domain–containing protein sim- forming a heterodimer, are required for po- ilar to yeast Mdj1p that functions as a chaper- lar nuclear fusion and central cell differentia- one in the mitochondrial matrix. Consistently, tion. Furthermore, AGL80, by interacting with GFA2 partially complements a yeast mdj1 mu- another Type I MADS-box protein AGL62, tant, which suggests a role for mitochondria also plays a critical role in endosperm develop- in synergid cell death in plants. How GFA2 ment. AGL62 is expressed in the syncytial en- acts in the mitochondria in promoting syn- dosperm and is suppressed by the FIS Polycomb ergid cell death remains unknown. Interest- complex just before endosperm cellularization. ingly, cell deaths of nonfunctional megaspores Mutation in AGL62 causes precocious cellular- and antipodal cells are not affected in gfa2 mu- ization of the endosperm (13, 27). Together, tants; this suggests that cell death pathways these Type I MADS-box transcription factors are different between synergids and antipodal are critical for central cell and endosperm de- cells. velopment in Arabidopsis. It would be interesting to know the downstream genes controlled by the DIA-AGL80 complex. Likely candidates The Central Cell would be DD46 and DME, which are not ex- Molecular mechanisms that control the spec- pressed in agl80 mutant ovules (57). However, ification and differentiation of the central cell there is no MADS-box binding site, the CArG

are poorly understood. Genetic evidence sug- box [CC(A/T)6GG] found in either gene, which gests that Type I MADS-box genes play an im- suggests that they may activate these down- portant role in central cell development. In the stream genes indirectly. Therefore, the DIA- by Universidad Veracruzana on 01/08/14. For personal use only. diana (dia, agl61) mutant, polar nuclei of the AGL80 complex may ultimately activate the central cell are not fused, and central cell mor- transcription of Polycomb group genes in the

Annu. Rev. Plant Biol. 2010.61:89-108. Downloaded from www.annualreviews.org phology is aberrant. The mutant embryo sac is central cell to repress endosperm development able to attract a pollen tube but fertilization of prior to fertilization. the central cell does not occur (4, 71). Egg- and In magatama3 (maa3) mutant ovules, the po- synergid-specific markers, but not central cell- lar nuclei fail to fuse at pollination and contain a specific markers, are expressed in dia ovules, smaller nucleolus that lacks the vacuolar-like in- which indicates that egg and synergid fates are ternal structure as compared to that of the wild- specified, and that central cell fate is impaired in type. Consequently, central cell development is the mutant. DIA is expressed exclusively in the arrested in the mutant, which ultimately results late central cell, and the DIA protein is localized in defective micropylar pollen tube guidance in in the polar nuclei and the central cell nucleus. Arabidopsis (57). The MAA3 gene encodes a ho- All these data suggest that DIA is required for molog of yeast SPLICING ENDONUCLE- central cell differentiation and function. DIA ASE1 (SEN1) helicase involved in processing

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of a variety of RNA species in yeasts. There- Genetic analysis suggests that GLC is epistatic fore, MAA3 may regulate the RNA metabolism to MEA and plays an essential role in the ma- that is responsible for nucleolar organization ternal control of embryo and endosperm de- of the central cell and micropylar pollen tube velopment, which suggests that it might play a guidance. role in central cell competence for fertilization. The fusion of the polar nuclei is an im- The molecular nature of GLC remains to be portant step in central cell development. Elec- revealed. tron microscopy revealed that the fusion of In addition to its role in fertilization, the the polar nuclei begins with contact with en- central cell also plays a role in pollen tube guid- doplasmic reticulum (ER) membranes that are ance. Pollen tube guidance is abolished in sev- continuous with the outer nuclear membranes eral mutants that disrupt central cell develop- of the polar nuclei. First, the fusion with ment. This includes maa1 and maa3 in which the ER membranes gives rise to a continu- the polar nuclei fail to fuse (66, 67), which indi- ous outer nuclear membrane that brings the cates a defect in central cell development or/and inner nuclear membranes into close contact, the maturation of the female gametophyte. In which leads to its final fusion. So far, little is contrast, in the central cell guidance (ccg) mu- known about the molecular basis of polar nu- tant, central cell development is not affected clear membrane fusion, although many muta- because it does not display any morphological tions and genes have been identified (10, 50, abnormality and expresses a central cell-specific 58). Interestingly, most of the genes whose marker (8). CCG is expressed in the central cell mutation blocks polar nuclear fusion encode of the mature embryo sac specifically and en- mitochondrial proteins. Similarly, mutation codes a nuclear protein that might play a role in GLUCOSE 6-PHOSPHATE/PHOSPHATE in regulating the expression of a subset of genes TRANSLOCATOR1 (GPT1) also blocks polar that are necessary for pollen tube guidance in nuclear fusion in the central cell (44). One pos- the central cell. sibility is that high respiratory activity is required for central cell development because the central cell has such a large cytoplasm. Alter- CONCLUSIONS natively, an intracellular feedback mechanism Molecular mechanisms that control the among the organellar and nuclear genomes may germline, gametic cell specification, and cell- coordinate central cell development. GFA2 has cell interactions in plant gametogenesis are been implicated in the membrane fusion. In beginning to be revealed. Genes that control gfa2 mutants, the polar nuclei fail to fuse; their these processes have been identified (Table 1). by Universidad Veracruzana on 01/08/14. For personal use only. outer nuclear membranes come into contact The haploid female gametophyte provides but do not fuse (10). This suggests that GFA2, us with an exciting system to investigate

Annu. Rev. Plant Biol. 2010.61:89-108. Downloaded from www.annualreviews.org either directly or indirectly, is required for developmental roles of the RNA splicing the membrane fusion of the polar nuclei in machinery; signaling pathways mediated by Arabidopsis. membrane receptor kinases like MSP1, FER, As the polar nuclei fuse, central cell spec- and ANUXR; and genetic control of cell fates. ification and functional differentiation occur. Emerging combinatory approches that employ In glauce ( glc) mutant embryo sacs, gameto- genetics, single-cell based genomics, and phytic cells develop and are specified nor- biochemistry will undoubtedly facilitate deci- mally as manifested by the correct expression phering the genetic complexity and molecular of gametophytic cell-specific markers; how- mechanisms that control female gametogenesis ever, the central cell cannot be fertilized (43). in angiosperms.

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Table 1 List of genes discussed in the text Gene name Protein function Biological function Reference SPOROCYTELESS Transcription regulator Germline cell fate 24, 63, 75 (SPL/NOZZLE) AGAMOUS (AG) MADS-box protein binds to CArG-box Activation of the SPL gene, 24 DNA sequence meristem determinacy and floral organ identity MULTIPLE ARCHESPORIAL Not available Germline cell number 64 CELLS 1(MAC1) MULTIPLE SPOROCYTE 1 Leucine rich repeat–containing receptor Numbers of male and female 45 (MSP1) protein kinase sporocytes OsTDL1A Putative ligand of MSP1 Numbers of male and female 78 sporocytes MEIOSIS ARRESTED AT A germline-specific member of Germline development; 46 LEPTOTENE1 (MEL1) ARGONAUTE genes family regulator of early meiosis SWITCH1 (SWI1)/DYAD Novel protein Chromatid cohesion 2, 38 establishment and chromosome structure in meiosis AMEIOTIC (AM1) A plant-specific chromatin-binding Regulator of leptotene to 54 protein, with 30% identity with SWI1 zygotene transition in meiosis AGL23 Type I MADS-box family transcription Early female gametogenesis 12 factor ARABINOGALACTAN A cell surface arabinogalactan proteoglycan Functional megaspore 1 PROTEIN 18 (AGP18) development ANAPHASE-PROMOTING Multiple-subunit E3 ubiquitin-protein Mitotic progression 7, 17, 29, 34 COMPLEX/CYCLOSOME ligase (APC/C) NOMEGA/APC6/CDC16 A component of the Anaphase Promoting Cell cycle control 7, 29 Complex REGULATORY PARTICLE A regulatory subunit of the 20S Cell cycle control 17 TRIPLE A ATPASE (RPT) proteosome; a member of the AAA superfamily RING-FINGER E3 LIGASE 1a Ring-finger E3 ligase that targets a Cell cycle control 34

by Universidad Veracruzana on 01/08/14. For personal use only. and 1b (RHF1a and RHF2a) cyclin-dependent kinase inhibitor ICK4/KRP6 for proteosome-mediated degradation

Annu. Rev. Plant Biol. 2010.61:89-108. Downloaded from www.annualreviews.org SLOW WALKER 1 (SWA1) A nucleolar WD40-containing protein Cell cycle progression 65 controlling pre-18S rRNA processing RETINOBLASTOMA-RELATED Negative regulator of G1/S transition Cell cycle control 14, 26 (RBR) HADAD (HDD) Not available Cellularization of the embryo sac 41 INDETERMINATE LATERAL ORGAN BOUNDARIES Cell cycle control 16, 20 GAMETOPHYTE1 (IG1) (LOB) domain protein CYTOKININ INDEPENDENT1 Histidine kinase Cytokinin signaling 56 (CKI1) CHROMATIN-REMODELING A member of the ATP-dependent Cell division control 22 FACTOR 11 (CHR11) SWI2/SNF2 family of chromatin- remodeling factors GEMINI POLLEN2 (GEM2) Not available Cell division control 52 (Continued )

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Table 1 (Continued ) Gene name Protein function Biological function Reference GEM1/MOR1 A microtubule-associated protein Cell plate formation 73 TWO IN ONE (TIO) A phragmoplast-associated protein Cell plate formation 47 AtNACK1 and AtNACK2 M-phase-specific kinesin-like protein Phragmoplast and cell plate 72 expansion DEMETER (DME) DNA glycosylase Gene imprinting during 9 endosperm development FERTILIZATION- C2H2 zinc finger–containing polycomb Suppressor of endosperm 26 INDEPENDENT SEED2 group protein development (FIS2) LACHESIS (LIS) RNA splicing factor Gametic cell specification 19 CLOTHO (CLO)/GFA1 RNA processing Gametic cell specification 35, 40 ATROPOS (ATO) A component of prespliceosome and RNA Gametic cell specification splicing machinery EOSTRE A BELL-like homeodomain protein Synergid cell fate 51 GAMETE EXPRESSED3 (GEX3) A plasma membrane protein Pollen tube guidance 3 MYB98 MYB family transcription factor Filiform apparatus formation 59 and pollen tube guidance FERONIA (FER)orSIRENE Leucine rich repeat–containing receptor Synergid-pollen tube interaction 15, 23, 37, 61 (SRN) protein kinase LORELEI (LRE) Putative Pollen tube attraction 76 glucosylphosphatidylinositol-anchored protein ANXUR1 and 2 Pollen-specific receptor-like protein kinase Pollen tube release 39 ABERRANT PEROXISOME Src homology (SH3)-domain containing Peroxisome transport and pollen 5 MORPHOLOGY2/ peroxisomal membrane protein tube reception ABSTINENCE BY MUTUAL CONSENT (APM2/AMC) GFA2 Mitochondrion-located DnaJ Synergid cell death 10 domain–containing protein DIANA (DIA, AGL61) Type I MADS-box transcription factor, Central cell differentiation and 4, 71 forming a heterodimer with AGL80 function

by Universidad Veracruzana on 01/08/14. For personal use only. AGL80/ FEM111 Type I MADS-box transcription factor, Central cell differentiation and 57 forming a heterodimer with DIA function AGL62 Type I MADS-box transcription factor Central cell and endosperm 13, 27 Annu. Rev. Plant Biol. 2010.61:89-108. Downloaded from www.annualreviews.org development MAGATAMA3 (MAA3) RNA helicase involved in RNA splicing Central cell maturation and 57 pollen tube guidance GLUCOSE Transmembrane glucose 6–phosphate Central cell development 44 6-PHOSPHATE/PHOSPHATE translocator TRANSLOCATOR1 (GPT1) GLAUCE (GLC) Not available Central cell function 43 CENTRAL CELL GUIDANCE Putative transcription regulator Pollen tube guidance 8 (CCG) MAGATAMA 1 (MAA1) Not available Central cell development and 66 pollen tube guidance

104 Yang · Shi · Chen ANRV410-PP61-05 ARI 26 March 2010 21:40

DISCLOSURE STATEMENT The authors are not aware of any afﬁliations, memberships, funding, or ﬁnancial holdings that might be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS The authors acknowledge ﬁnancial support from the National Science Foundation of China to Y. W. C. (30830063) and D. Q. S. (3060032), and also from the Chinese Academy of Sciences to W. C. Y. (KSCX2-YW-N-048).

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Annual Review of Plant Biology Contents Volume 61, 2010

A Wandering Pathway in Plant Biology: From Wildﬂowers to Phototropins to Bacterial Virulence Winslow R. Briggs pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp1 Structure and Function of Plant Photoreceptors Andreas M¨oglich, Xiaojing Yang, Rebecca A. Ayers, and Keith Moffat ppppppppppppppppppppp21 Auxin Biosynthesis and Its Role in Plant Development Yunde Zhao pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp49 Computational Morphodynamics: A Modeling Framework to Understand Plant Growth Vijay Chickarmane, Adrienne H.K. Roeder, Paul T. Tarr, Alexandre Cunha, Cory Tobin, and Elliot M. Meyerowitz ppppppppppppppppppppppppppppppppppppppppppppppppppppp65 Female Gametophyte Development in Flowering Plants Wei-Cai Yang, Dong-Qiao Shi, and Yan-Hong Chen ppppppppppppppppppppppppppppppppppppppp89 Doomed Lovers: Mechanisms of Isolation and Incompatibility in Plants Kirsten Bomblies ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp109 Chloroplast RNA Metabolism David B. Stern, Michel Goldschmidt-Clermont, and Maureen R. Hanson pppppppppppppp125

by Universidad Veracruzana on 01/08/14. For personal use only. Protein Transport into Chloroplasts Hsou-min Li and Chi-Chou Chiu pppppppppppppppppppppppppppppppppppppppppppppppppppppppppp157 Annu. Rev. Plant Biol. 2010.61:89-108. Downloaded from www.annualreviews.org The Regulation of Gene Expression Required for C4 Photosynthesis Julian M. Hibberd and Sarah Covshoff pppppppppppppppppppppppppppppppppppppppppppppppppppp181 Starch: Its Metabolism, Evolution, and Biotechnological Modification in Plants Samuel C. Zeeman, Jens Kossmann, and Alison M. Smith ppppppppppppppppppppppppppppppp209 Improving Photosynthetic Efficiency for Greater Yield Xin-Guang Zhu, Stephen P. Long, and Donald R. Ort ppppppppppppppppppppppppppppppppppp235 Hemicelluloses Henrik Vibe Scheller and Peter Ulvskov ppppppppppppppppppppppppppppppppppppppppppppppppppp263 Diversification of P450 Genes During Land Plant Evolution Masaharu Mizutani and Daisaku Ohta ppppppppppppppppppppppppppppppppppppppppppppppppppp291

v AR410-FM ARI 6 April 2010 15:25

Evolution in Action: Plants Resistant to Herbicides Stephen B. Powles and Qin Yu pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp317 Insights from the Comparison of Plant Genome Sequences Andrew H. Paterson, Michael Freeling, Haibao Tang, and Xiyin Wang pppppppppppppppp349 High-Throughput Characterization of Plant Gene Functions by Using Gain-of-Function Technology Youichi Kondou, Mieko Higuchi, and Minami Matsui pppppppppppppppppppppppppppppppppppp373 Histone Methylation in Higher Plants Chunyan Liu, Falong Lu, Xia Cui, and Xiaofeng Cao pppppppppppppppppppppppppppppppppppp395 Genetic and Molecular Basis of Rice Yield Yongzhong Xing and Qifa Zhang pppppppppppppppppppppppppppppppppppppppppppppppppppppppppp421 Genetic Engineering for Modern Agriculture: Challenges and Perspectives Ron Mittler and Eduardo Blumwald ppppppppppppppppppppppppppppppppppppppppppppppppppppppp443 Metabolomics for Functional Genomics, Systems Biology, and Biotechnology Kazuki Saito and Fumio Matsuda ppppppppppppppppppppppppppppppppppppppppppppppppppppppppp463 Quantitation in Mass-Spectrometry-Based Proteomics Waltraud X. Schulze and Bj¨orn Usadel pppppppppppppppppppppppppppppppppppppppppppppppppppp491 Metal Hyperaccumulation in Plants Ute Kr¨amer pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp517 Arsenic as a Food Chain Contaminant: Mechanisms of Plant Uptake and Metabolism and Mitigation Strategies Fang-Jie Zhao, Steve P. McGrath, and Andrew A. Meharg ppppppppppppppppppppppppppppp535

by Universidad Veracruzana on 01/08/14. For personal use only. Guard Cell Signal Transduction Network: Advances in Understanding 2+ Abscisic Acid, CO2, and Ca Signaling Tae-Houn Kim, Maik B¨ohmer, Honghong Hu, Noriyuki Nishimura, Annu. Rev. Plant Biol. 2010.61:89-108. Downloaded from www.annualreviews.org and Julian I. Schroeder ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp561 The Language of Calcium Signaling Antony N. Dodd, J¨org Kudla, and Dale Sanders pppppppppppppppppppppppppppppppppppppppppp593 Mitogen-Activated Protein Kinase Signaling in Plants Maria Cristina Suarez Rodriguez, Morten Petersen, and John Mundy ppppppppppppppppp621 Abscisic Acid: Emergence of a Core Signaling Network Sean R. Cutler, Pedro L. Rodriguez, Ruth R. Finkelstein, and Suzanne R. Abrams pppp651 Brassinosteroid Signal Transduction from Receptor Kinases to Transcription Factors Tae-Wuk Kim and Zhi-Yong Wang pppppppppppppppppppppppppppppppppppppppppppppppppppppppp681

vi Contents AR410-FM ARI 6 April 2010 15:25

Directional Gravity Sensing in Gravitropism Miyo Terao Morita pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp705

Indexes Cumulative Index of Contributing Authors, Volumes 51–61 ppppppppppppppppppppppppppp721 Cumulative Index of Chapter Titles, Volumes 51–61 pppppppppppppppppppppppppppppppppppp726

Errata

An online log of corrections to Annual Review of Plant Biology articles may be found at http://plant.annualreviews.org by Universidad Veracruzana on 01/08/14. For personal use only. Annu. Rev. Plant Biol. 2010.61:89-108. Downloaded from www.annualreviews.org

Contents vii