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Journal of Genetics and Genomics 38 (2011) 379e390

Cytological analysis and genetic control of rice anther development
Dabing Zhang a,b,*, Xue Luo a, Lu Zhu a

Institute of Plant Science, State Key Laboratory of Hybrid Rice, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China b Bio-X Research Center, Shanghai Jiao Tong University, Shanghai 200240, China Received 11 May 2011; revised 29 July 2011; accepted 1 August 2011

Abstract Microsporogenesis and male gametogenesis are essential for the alternating life cycle of flowering plants between diploid sporophyte and haploid gametophyte generations. Rice (Oryza sativa) is the world’s major staple food, and manipulation of pollen fertility is particularly important for the demands to increase rice grain yield. Towards a better understanding of the mechanisms controlling rice male reproductive development, we describe here the cytological changes of anther development through 14 stages, including cell division, differentiation and degeneration of somatic tissues consisting of four concentric cell layers surrounding and supporting reproductive cells as they form mature pollen grains through meiosis and mitosis. Furthermore, we compare the morphological difference of anthers and pollen grains in both monocot rice and eudicot Arabidopsis thaliana. Additionally, we describe the key genes identified to date critical for rice anther development and pollen formation.
Keywords: Rice (Oryza Sativa); Anther; Developmental stages; Cellular morphology; Arabidopsis thaliana

1. Introduction Rice is one of the most important agricultural crops. Hybrid rice exhibits heterosis, or hybrid vigor, which is indicated by more rapid growth and considerablely higher yields than produced by the parental lines. Rice male sterility is frequently caused by environmental effects or genetic mutations, leading to defective anther development and pollen fertility. Since the female reproductive development remains normal in some male sterile lines, these lines can be fertilized by the pollen grains of other rice cultivars, greatly contributing to the production of hybrid seeds (Wilson and Zhang, 2009; Ouyang, et al., 2009, 2010). Furthermore, because of its small genome and high efficiency of transformation, rice also has been used as a model monocot plant for comparative studies with other model plants such as Arabidopsis thaliana (IRGSP, 2005; Jung et al., 2008).

* Corresponding author. Tel: þ86 21 34205073, fax: þ86 21 34204869. E-mail address: (D. Zhang).

Rice and other agriculturally important cereals including barley (Hordeum vulgare) and maize (Zea mays) belong to the grass family (Poaceae), which is one of the largest families in flowering plants (Linder and Rudall, 2005). As knowledge of its development can be extrapolated to other monocot crops, rice is useful not only as an excellent model plant for biological studies, but also as a model crop for agronomical improvement. Evolutionary adaptations in the organization and structure of grass inflorescence (or panicle) have resulted in their distinct morphologies from those of core eudicots and nongrass monocots (Grass Phylogeny Working Group, 2001; Zanis, 2007). The rice inflorescence or panicle has a central stem that terminates after the generation of several primary and secondary branches (Fig. 1A). Spikelets are directly formed on primary and secondary branches that are attached on the main axis called the rachis (Itoh et al., 2005). Each rice spikelet contains a flower with one pistil, six stamens and two lodicules subtended by an inner bract or prophyll, called the palea, and an outer bract called the lemma (Fig. 1B) (Yuan et al., 2009b). Each stamen consists of a filament and an

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The key genes expressed in rice are listed as well as their homologous genes in Arabidopsis. we analyzed the cellular changes of the rice anther (O.plantbiology. fi ¼ filament.. the anther. Ma. Jiao et al. Several reports published on the developmental staging of rice anther contribute to our understanding of the whole male reproductive developmental process (Feng et al.. In addition. pi ¼ pistil. En ¼ endothecium. (2005) also described the rice anther development in eight stages. Rachis. 2005). Suwabe et al. Recently. L1. 2009.. (2006a).214 [RAP2 (Rice Annotation Project 2008) http:// rapdb. sativa ssp. early bicellular pollen stage. / Journal of Genetics and Genomics 38 (2011) 379e390 Fig. 2. anther development has been divided into 14 stages based on morphological features (Sanders et al. sib ¼ secondary inflorescence branch. Ma. Wei et al. and meiosis in 12 stages.. C ¼ cavity for dehiscence. spikelet organs and anther section. 2008. 2010. includes a number of critical developmental events such as meristem specification. we compare the divergent morphology of rice anther development with that of Arabidopsis. cell differentiation. Zhang et al. 2008. 2010.. stage 1).. 9522 and Zhonghua 11) using light microscopic observations of transverse sections and divided the rice anther developmental course into 14 stages (Zhang and Wilson. late microspore]. Itoh et al. The rice anther includes two thecae linked by the connective tissue. we further characterize the cellular changes during the 14 anther developmental stages by detailed analysis of semi-thin sections of O. Morphology of rice panicle. 2009). The recently reported key genes for rice anther development identified by mutant characterization are also discussed. 2009). The anther primordium contains three layers. T ¼ tapetum. Stage 1: The stamen primordium is formed after cell divisions and differentiation of floral meristem. E ¼ epeidermis. D: section of anther at stage 9 showing the anther wall layers. 2004. 2001. sl ¼ sterile lemma. Feng et al.affrc. Itoh et al.dna. 9522. 1999). C: a mature anther of rice.. A: a mature inflorescence of rice at the heading stage. . and each theca contains two locules.1 (Ouyang et al. anther with four lobes linked to the filament by connective tissues (Fig.. 2005. 2005. The number of total protein-coding genes in rice has been estimated at 52. B: a mature spikelet of rice with formation of ovule and pollen grains. 1C) (Matsui et al. middle microspore stage. Wang et al.. Successful male reproductive development within the male organ. microspores in the locule as well as vascular tissues and connective tissues. from An1 of archesporial cells (ACs) differentiation to An8 of mature pollen grain production. late bicellular pollen stage and mature pollen stage. (2001) observed anther morphology in semi-thin sections and divided the anther developmental process into eight stages: microspore mother cell formation stage. The two locules are connected by a septum and stomium (consisting of small epidermal cells). 1999. st ¼ stamens. Tang et al. V ¼ vascular bundle. 2004.msu. which are crucial for anther dehiscence (Fig.380 D. and L3 (Fig. Cytological analysis of rice anther development Table 1 summarizes the key events that occur at all 14 stages of anther development. This observation clearly indicates that variations in gene expression occur during anther development and pollen formation. 2..go. one is longer at the base and the other is shorter. inflorescence axis. 2009. meiosis and mitosis (Scott et al. le ¼ lemma... japonica cv. 2005). japonica cv. which was meant to be consistent with that of Arabidopsis (Sanders et al. Huang et al. according to methods described by Li et al. 1999. In Arabidopsis. Wilson and Zhang. early microspore stage. 1. Transcriptome analyses in rice using staged anthers and pollen grains (or dissected tapetal cells/microspores) identified approximately] or 56.. Zhang and Wilson. L2. 2010. Ma. McCormick.000 unique transcripts in the anther and male gametophyte (Hobo et al.. microspore mother cell meiosis stage. Fujita et al. pib ¼ primary inflorescence branch. 2009).. lo ¼ lodicule. sp ¼ spikelet.797 [MSU release 6. 1B). pa ¼ palea. Here. cellto-cell communication. 2007) http://rice. 2010). sativa ssp.

2011a..8 AMS (Sorensen et al.2 2. 2006) PTC1 (Li et al...1 1.7e2. 2006. API5 (Li et al. 2007) PSS1 (Zhou et al. 2004. 2006) ASY1 (Caryl et al.D. 2010) DPW (Shi et al. 2011) OsC6 (Zhang et al. Archesporial cells divide and differentiate into primary parietal cells.. OSCP1 ¼ CYSTEINE PROTEASE 1.. PHS1 ¼ POOR HOMOLOGOUS SYNAPSIS 1.. The cytoplasm of tapetal cells become condensed.. 2011c) TDR (Li et al.. 2005) 5 6 7 The primary sporogenous cells divide and form the secondary sporogenous cells... and the L2 layer forms archesporial cells in each corner. The tapetum cells almost completely degenerate into cellular debris and Ubisch bodies on the internal surface.3e0. Yuan et al. at the end of meiosis I. Aya et al. 2011b.RIP1 ¼ RICE IMMATURE POLLEN 1. 2003.1e0. 2006b) DYT1 (Zhang et al. 2006b). 2002) TPD1 (Yang et al. Armstrong et al. one meiocyte forms two nuclei separated by a cell plate (Chen et al. AMS ¼ ABORTED MICROSPORES. pollen sacs become connected and anther dehiscence occurs.. UDT1 ¼ RICE UNDEVELOPED TAPETUM1. MEL1 ¼ MEIOSIS ARRESTED AT LEPTOTENE1. PAIR1/PAIR2/PAIR ¼ PAIRING ABERRATION IN RICE MEIOSIS 1/2/3. 0.25e0. 2008) GAMYB (Kaneko et al.. The generative cell undergoes the second mitosis and generates the mature pollen grain containing three invisible nuclei. Canales et al.2 0. 2009) CYP704B1 (Dobritsa et al. 2011c) CYP703A3 (Morant et al. Free haploid microspores.. 2010) EMS1/EXS (Zhao et al.2e0. and meiocytes are associated with the tapetal layer. The flower opens.. The microspore undergoes the first mitotic division. The tapetum becomes more condensed and vacuolated... 2006a. . 2011a. DAD1 ¼ DEFECTIVE IN ANTHER DEHISCENCE1. PTC1 ¼ PERSISTENT TAPETAL CELL 1. Wang et al. 2008) MYB33/MYB65 (Millar and Gubler. 2006) OsTDL1A (Zhao et al. 2005). 2010) 0....2 RIP1 (Han et al.. 2003. API5 (Li et al. Anther length (mm) 0. 2009) 11 2.. 2003b.2 CSA (Zhang et al. 2006) CYP703A2 (Aya et al. API5 ¼ APOPTOSIS INHIBITOR5. The tapetum completely disappears. Stage 1 2 Event Floral meristem differentiates into round-shape stamen primordia containing L1. The stamen meristem form the anther primordia with four corners..4 0. 2009b) ZEP1 (Wang et al. The microspore becomes more vacuolated with a round shape. The anther continues releasing mature pollen grains. spherical in shape and forming thin exines... 2004. the tetrad containing microspores enclosed by the callose wall is formed. Development of microspore mother cells (MMCs) surrounded by four-layered anther walls. Zhang et al.. The outer secondary parietal layer forms the endothecium layer and the middle layer. The middle layer becomes a less visible band-like structure. 2007) CYP704B2 (Li et al.2 WDA1 (Jung et al. 2006) AID1(Zhu et al.. 2006a. CSA ¼ CARBON STARVED ANTHER. and the inner secondary parietal layer develops into the tapetum. Wildtype tapetal cells become condensed and form obvious characteristic orbicules/Ubisch bodies on the inner surface facing the microspores. Meiocytes start meiotic division.. 2011b. 2009. 2000. are released from the tetrads. 2002) ZYP1(Higgins et al.. Liu et al..3 0.8e1.1e1. L2 and L3 cellular layers. 2010b) 13 14 2.1 0. EMS1/EXS ¼ EXTRA SPOROGENOUS CELLS 1/EXCESS MICROSPOROCYTES. 2011). 2005) PAIR1/PAIR2/PAIR3 (Nonomura et al.25 MSP1 (Nonomura et al. Tapetal cells become more degenerated and produce abundant electron-density Ubisch bodies. Primexines are formed by microspores outside their surface. TDR ¼ TAPETUM DEGENERATION RETARDATION. 2011b.. 2002. 2011) MS1 (Vizcay-Barrena and Wilson.. Cell divisions further generate the secondary parietal layers and sporogenous cells. After meiosis II. 0.. 2010a.. 2005) 8a 8b 9 Formation of dyads. 2010b) RIP1 (Han et al.15 Expressed genes in rice 381 Homologous genes in Arabidopsis 3 4 0. Xu et al. 2010a.2 12 2. and programmed cell death is initiated as indicated by the nuclear DNA fragmentation (Li et al.. AID1 ¼ ANTHER INDEHISCENCE1.15e0. TPD1 ¼ TAPETUM DETERMINANT1. MS1 ¼ MALE STERILITY1.45 UDT1 (Jung et al. / Journal of Genetics and Genomics 38 (2011) 379e390 Table 1 Major cytological events during rice anther development..05e0. 2011c) MADS3 (Hu et al. 2006). 2003a.... generating a generative cell and a vegetative cell. DYT1 ¼ DYSFUNCTIONAL TAPETUM1. PSS1 ¼ POLLEN SEMISTERLITY 1.. 2004) MSP1 ¼ MULTIPLE SPOROCYTES1. 2011a.45e0.. Jia et al. 2010) MEL1 (Nonomura et al.4e0. 2009a.7 10 1.

bars ¼ 35 mm. Stage 5: The primary sporogenous cells divide and form the sporogenous cells. 2. Ar ¼ archesporial cell. 2005). BP ¼ bicellular pollen. / Journal of Genetics and Genomics 38 (2011) 379e390 Eventually. at the end of meiosis I a band of numerous organelles is formed at the equatorial level of the dyad (Ma. Dy ¼ dyad cell. the endothecium. ML ¼ middle layer. 1 P ¼ primary parietal layer. 2. 2. stage 3). 2.. Stage 7: Meiocytes initiate meiotic division and contact the tapetal layer. 2010. and four newly generated haploid microspores in one tetrad are enclosed by the callose wall deposited on the primexine of the microspore (Zhang et al. stage 7). PMCs) within the locule (Fig. L2. L1. MC ¼ meiotic cell. vascular tissues and circular cell clusters close to the stomium.. Stage 4: Archesporial cells undergo periclinal divisions and generate primary sporogenous cells. T ¼ tapetum. The anther primordium is quadrangular in shape. 2006b. C ¼ connective layer. 2011a). 2011a) (Fig. The middle layer becomes a less visible bandlike structure (Fig.. whereas in Arabidopsis. Stage 8b: Meiocytes undergo meiosis II. stage 4). The primary parietal cells form two secondary parietal layers. 2006a. 2. 2010). 2 P ¼ secondary parietal cell layer.. MMC ¼ microspore mother cell. Stage 8a: Meiocytes continue the process of meiosis and become slightly separated. the three cell layers in stamen primordia. In rice.. 2006a. 2010. Li et al. 2. The archesporial cells appear slightly larger than other cells. forming ellipsoidal shaped dyads. Stem cells in the L2 layer form archosporial cells via the rapid mitotic division of cells at the four corners (Fig. Tds ¼ tetrads. Stage 6: The secondary sporogenous cells generate microspore mother cells (MMCs. The inner secondary parietal layer develops into the tapetal layer. which play roles in protecting microspore development and anther dehiscence. StR ¼ stomium region. The connective cells lie between microsporangia and vascular bundles and degenerate during later anther developmental stages. 2005). Zhang et al. and L3. Stage 2: The transverse section analyses indicate that the outermost layer is the epidermis. Tapetal cells become vacuolated and shrunken with darkly stained cytoplasm.382 D. a three-layer anther wall. and initiation of programmed cell death in tapetal cells occurs with the nuclear DNA fragmentation (Li et al. Li and Zhang. The developing anther at this stage has characteristic locules. 2. one meiocyte forms two nuclei separated by the cell plate at the end of meiosis I (Chen et al. E ¼ epidermis. 2. The tapetal layer continues to degenerate (Fig. MP ¼ mature pollen. Cytological observation and diagrams of rice anther development and pollen formation at 14 stages. 2008. Sp ¼ sporogenous cell. stage 2). During the later stages. which stems from anticlinal cell division of the L1 layer. stage 6). the middle layer and the tapetum (Fig. stage 8b) (Li et al. Stage 3: Periclinal divisions of archesporial cells generate distinct primary parietal cells (Fig. 2. and connective and vascular tissues (Fig. the L1 layer cells divide to form the epidermis and the stomium. the L3 layer cells divide and form connective cells. also called pollen mother cells. The anther at this stage has four concentric somatic layers that surround the sporgenous cells (from the surface to interior): the epidermis. Msp ¼ microspore parietal cell. Fig. . with the palea and lemma close together. and the outer secondary parietal layer further generates the endothecium layer and the middle layer. stage 8a). En ¼ endothecium. V ¼ vascular bundle. stage 5).

the anther development and pollen maturation are nearly complete. 2010).. At the beginning of the stage. such as collections of T-DNA insertion mutants. resulting in a round-shaped microspore (Fig. Stage 14: The septum breaks. Zhang et al.D. Stage 10: Tapetal cells become more degenerated with hilllike structures and form more electron-dense Ubisch bodies along the tangential surface of tapetal cells. 2. The epidermis and the endothecium degenerate further. 2010). The anther cuticle is identified as a thin hydrophobic layer continuously coating the outermost surface of the anthers and provides a protective role for microspore development. Subsequently.. offers another major protective barrier for sperm cells and provides high resistance to environmental stresses (Blackmore et al. sporopollenin. However. The biochemical nature of the pollen exine remains elusive because of the technical limitation of purifying and obtaining a large quantity of materials for analysis. 2009. and waxes contain different substances such as alkanes.. is highly insoluble. leaving only the epidermis and endothecium layers (Fig.. stage 12) (Zhang et al.. Wild-type tapetal cells reabsorb their vacuoles. 3). The microspore vacuolates with an increase of volume. the major component of the pollen/ spore exine. Key genes required for anther development in rice Recent forward and reverse genetic investigations greatly facilitated our knowledge of the molecular mechanisms of male reproductive development in plants. 2010a).. Li et al.. 2009). Li and Zhang. Thicker exine with nexine and sexine layers are formed on the outer surface of the microspores (Li and Zhang. meiosis. 1998. We had previously described the molecular regulatory networks controlling anther and pollen development in Arabidopsis and rice. Stage 11: The vacuolated microspore undergoes the first mitotic division with asymmetric cell division. the tapeta of rice and other cereals display characteristic orbicules/ Ubisch bodies.. Emerging evidence indicate that lipidic pollen exine is made of sporopollenin. Huysmans et al. 2010. although there are several morphological differences in the appearance of the rice anther compared with that of wild-type Arabidopsis anther (Fig. The middle layer becomes invisible. the vacuole diminishes gradually. Morphological difference of anthers and pollen grains between rice and Arabidopsis Overall.. 2003). The cutin matrix and waxes are the major components of the anther cuticle. 2010. At this stage. stage 13). 3B and D). The Arabidopsis anther lobes seem to be highly fused with a less obvious independent pollen sac. 2. D and E).. 2. / Journal of Genetics and Genomics 38 (2011) 379e390 383 Stage 9: Free haploid microspores are released from the tetrads as the callose wall is degraded by callase secreted from the tapetal cells.. Although both rice and Arabidopsis have secretory tapeta (Huysmans et al. Li et al. 2010).. generating a much smaller generative cell and a larger vegetative cell. we briefly introduce key regulators for anther development in rice.. 3. As a monocot.. The tapetum cells almost completely degenerate into cellular debris and Ubisch bodies on the internal surface (Fig. which contain unique secretory tapeta with specialized organelles such as elaioplasts and tapetosomes (Fig. rice anthers have obvious lobe boundaries and reticulate anther cuticles (Fig. the generative cells separate from the pollen wall and move close to the vegetative nucleus. Stage 12: The generative cell in the microspore undergoes the second mitosis and divides into two sperm cells. alcohols. Orbicules have not been observed in the Brassicaceae family including Arabidopsis. the developmental events are highly similar between rice and Arabidopsis. 1998. 1998. The two adjacent pollen sacs become linked. which cannot be seen because of the accumulation of starch and lipidic materials (Feng et al.. stage 9). 2. an extremely resilient material derived from polymerization of fatty acid metabolites and phenolic acid (Piffanelli et al. After anther dehiscence. Zhang et al. Recent genetic and biochemical investigations identified several key regulators in rice male reproductive development (Zhang and Wilson. Furness and Rudall. Stage 13: Pollen grains become more spherical in shape. 4B. microspores are falcate shaped and then become enlarged. resistant to degradation and exceptionally stable (Ahlers et al. Furness and Rudall. Here. This observation may reflect the differences in anther cuticle development in monocots and dicots. 2010. 3A and C). 1998). 2011). which are thought to export tapetum-produced sporopollenin precursors across the hydrophilic cell wall to the locule (Fig. The cutin is an insoluble polymer composed of hydroxylated and epoxy C16 and C18 fatty acids. the lemma and palea interlocking structure is opened and the filament elongates. stage 10). 2001.1. 3. rice is becoming another model crop for developmental biology due to the release of the rice genome sequence and a large number of available tools for the analysis of gene function. 2011a).. and the cytoplasm becomes condensed (Fig. 2008). ketones and wax esters (Li et al. In addition. and the anther cuticle has a longitudinal striped pattern (Fig. 2007. which are assumed to export tapetum-produced sporopollenin precursors across the hydrophilic cell wall to the locule (Fig. The secretory rice tapeta produce characteristic orbicules/Ubisch bodies. 4A and C) (Wu et al. 1998. 5) (Huysmans et al. the model eudicot plant that offers excellent advantages for developmental studies. and anther dehiscence occurs. 1998). microspores are spherical with thin exines (Li and Zhang. stage 11) (Feng et al. the exine. pollen development and anther dehiscence (Wilson and Zhang. 1997. and the anther continues the release of mature pollen grains (Fig.. particularly in Arabidopsis. Early in this stage. forming the outer wall of the pollen. full-length cDNAs and a highly efficient transformation system (Jung et al. 2009). 2. 2001. Li et al. As the starch accumulates inside the microspore. with the spherical microspores full of reserve substances (Fig. Shi et al. including such genes as those determining anther cell division and differentiation. 2010a). stage 14). Zhang and Wilson. and the tapetum completely disappears. 2010). 2. and the mature pollen grain contains three nuclei. .

Molecular control of early anther development MSP1 (MULTIPLE SPOROCYTE) transcripts. This difference may be associated with the different methods of pollination between the two plants. bar ¼ 100 mm. Li and Zhang. MSP1 is responsible for limiting the number of cells entering into male and female . The outer surface of Arabidopsis pollen grains display elegant reticulate cavities with an abundant pollen coat (tryphine) deposited inside the pollen exine (Fig. 2011). rice mature pollen exine contains a larger space between the two layers (Fig. Arabidopsis pollen exine consists of two layers. Outer surface observation of Arabidopsis and rice anthers by SEM. are observed in young panicles at stage 4. Zhang et al. 5B. rice pollen have a smooth and particulate exine patterning. B: rice anther at stage 12. bar ¼ 10 mm. / Journal of Genetics and Genomics 38 (2011) 379e390 Fig. 2007). Morant et al.2. 2010). 5A.. 3. In addition. D and F) (Li et al. 5) (Li and Zhang. 2010). 2011a. Morphological analysis also reveals that rice pollen wall ontology is distinct from that of Arabidopsis (Li and Zhang. D: enlargement of (B) showing the anther cuticle. Arabidopsis belongs to insect-pollinated (entomophilous) plants. bar ¼ 100 mm.384 D. 3. which has a wider inter-layer space between the nexine (foot layer) and sexine compared with that of Arabidopsis (Fig. 2010). and the baculum forms between the two layers.. the tectum and the foot layer. C and E). C: enlargement of (A) showing the anther cuticle. 2010. Meanwhile. Compared with that of Arabidopsis. while rice is wind-pollinated (anemophilous) (Ariizumi and Toriyama. bar ¼ 10 mm. A: Arabidopsis anther at stage 12. encoding a Leu-rich repeat receptor-like protein kinase in rice.

Zhang et al. D: pollen wall section of rice by TEM... D: enlargement of (B) showing Ubisch bodies. OsTDL1A. bar ¼ 0.. 2008). 2006. Ma. M ¼ microspore. the EXCESS MALE SPOROCYTES1 (EMS1) (also called EXTRA SPOROGENOUS CELLS. Pollen wall morphology analysis of rice and Arabidopsis at stage 12. F: proposed model of rice pollen exine structure. t ¼ tapetosome. EXS ) EMS1/EXS gene encodes a LRR-RLK. C: enlargement of (A) showing the tapetosome.. The msp1 mutant produces an excessive number of both male and female sporocytes. Ba ¼ bacula. E: proposed model of Arabidopsis pollen exine structure. 2005. Ex ¼ exine. However. In ¼ intine.D. bar ¼ 1 mm. A: pollen grain of Arabidopsis by SEM. PM ¼ plasma membrane. C: pollen wall section of Arabidopsis by TEM. bar ¼ 5 mm. Se ¼ sexine. Ne ¼ nexine. In Arabidopsis. U ¼ ubisch bodies. Zhao et al. 2003. bar ¼ 1 mm. knock-down of OsTDL1A mimics the msp1 phenotype in the ovule but not in the anther (Zhao et al. PC ¼ pollen coat. 5. co-expressed with MSP1 in both anthers and the ovule. particularly precursors for male sporocytes into the tapetum is the discovery of their counterparts in A. B: tapetal cells containing Ubisch bodies in rice at stage 12.. 2006). bar ¼ 1 mm. and its anther fails to produce the tapetum layer (Nonomura et al. 4. thaliana (Nonomura et al. The general importance of the MSP1/ OsTDL1A1-dependent pathway(s) in reproductive development. A: tapetal cells containing tapetosomes in Arabidopsis at stage 12. bar ¼ 5 mm. Tapetal cells of Arabidopsis and rice. encodes a small peptide that was shown to bind to MSP1. bar ¼ 0. Mutations of EMS1/EXS or its putative ligand TPD1 (TAPETUM DETERMINANT1) cause male sterility due to defective Fig. Wang et al. . Te ¼ texine. Te ¼ tectum.5 mm. sporogenesis and triggers the differentiation of anther wall formation in rice. 2008). 2003. Ne ¼ nexine. E: outer surface of inner side of rice tapetal layer facing the microspores observed by SEM.. Cy ¼ cytoplasm.5 mm. B: pollen grain of rice by SEM. Wang et al. bar ¼ 1 mm. bar ¼ 1 mm. / Journal of Genetics and Genomics 38 (2011) 379e390 385 Fig.

ZEP1 encodes a transverse filament protein homologous to Arabidopsis ZYP1.. The Arabdopsis ortholog of UDT1 is DYSFUNCTIONAL TAPETUM1 (DYT1).. 2011).. In addition. 2006). 2003.. Conversely. 2006). PAIR2 contains a HORMA-domain and is homologous to the Arabidopsis ASY1 (Caryl et al. TDR also plays a role in pollen exine formation. PAIR2 is required for homologous synapsis during meiosis I in rice (Nonomura et al.. and the mel1 mutant aborts chromosomes during early meiotic stages. Furthermore. TDR is able to directly regulate the expression of a cysteine protease gene OsCP1 in vivo and in vitro (Li et al. Zhang et al. and pss1 mutants display lagging chromosomes and chromosomal bridges at anaphase I and anaphase II of male meiosis. 2004).. 2003a.. such as delayed degeneration of tapetal cells and abnormal meiosis process (Kaneko et al. MYB33 and MYB65 are closely related genes of GAMYB in Arabidopsis.. 2005). 2010).. the ortholog of the Arabidopsis AMS gene encoding a bHLH transcription factor (Sorensen et al.. moderately in the endothecium and the middle layer. PSS1 encodes a kinesin-1-like protein with microtubulestimulated ATPase activity. 2006). ZEP1 may act as a central element of the synaptonemal complex.. The key functional role of AMS in anther and microspore development is the regulation of the expression of a number of genes involved in various biological activities... as the tdr microspore does not have sporopollenin precursors in its primexine. 2006b.. 2007). 2011). OsRAD21-4 (Zhang et al. GAMYB is highly expressed in stamen primordia and tapetal cells. MEL1 belongs to the ARGONAUTE (AGO) gene family.... MEIOSIS ARRESTED AT LEPTOTENE1 (MEL1) (Nonomura et al. during late pollen . 2003. 13 genes involved in tapetal development and pollen wall formation were shown to be direct regulatory targets of AMS (Xu et al. encodes a protein containing putative coiled-coil motifs and has no close homologs in other organisms. but has no expression in MMCs. The functional importance of this pathway is highlighted by the demonstration that mutants of one of these downstream AMS targets. as well as regulates the expression of genes such as Defective Pollen Wall and OsC6 that are related to lipidic synthesis and transport during anther development (Zhang et al. Jia et al. 2004). Moreover. ABORTED MICROSPORE (AMS ) encodes a post-meiotic. and in the tapetum.4.. particularly those associated with metabolism and deposition of the pollen wall.. 2002. Several key genes have been identified to be essential for meiosis during rice male reproductive development. Zhang et al. Armstrong et al. Moreover. 2009b). 2010) and PSS1 (Pollen Semi-sterility1) (Zhou et al.. PAIR2 (Nonomura et al. PAIR1 encodes a novel putative coiled-coil protein that is required for homologous chromosome pairing in male and female meiocytes in rice (Nonomura et al. 2010)... Rice GAMYB (OsGAMYB) is a transcriptional factor that positively regulates gibberellin (GA)-dependent a-amylase expression. 2010). causing defective male and female fertility (Nonomura et al. and a myb33 myb65 double mutant displays defective anther development with hypertrophic tapetal cells and premeiotic abortion of pollen development (Millar and Gubler. equal chromosomal segregation in anaphase I as well as increased numbers of crossovers (Wang et al. connective tissue and vascular bundles but not in young microspores after stage 8 (Jung et al. TDR (Li et al. ZEP1 (Wang et al. such as PAIR1 (HOMOLOGOUS PAIRING ABERRATION IN RICE MEIOSIS1) (Nonomura et al. 2011). 2010). and zep1 mutants show no formation of the synaptonemal complex in early prophase I. which is also required for proper cell differentiation in the anther (Zhang et al. Zhao et al. causing reduced male fertility (Zhou et al.. Aya et al. 2000. 2006b). 2010). 2005). The tdr mutant displays delayed tapetal degeneration and nuclear DNA fragmentation. The gamyb mutants display signs of defective anther development. 2007). 2005... and abortion of microspores after the release from the tetrad... The ams mutant displays an expanded tapetal layer and aborted microspores (Sorensen et al. 2009a)..3. EMS1/EXS is initially expressed in the precursors of sporogenous cells and the tapetum and then becomes more strongly expressed in the tapetum than in the male sporocytes (Zhao et al. and DYT1 expression is decreased in ems1/exs mutants (Zhang et al... PAIR3 (Yuan et al. Feng and Dickinson. Shi et al. an ATP Binding Cassette (ABC) transporter. 2003a.. 2008. 2006). Genes involved in meiosis Meiosis plays a central role in the life cycles of all sexually reproducing organisms and is a highly conserved process in eukaryotes. 2010a. 2008. Yang et al.. 2004. PAIR3. A novel meiosis-related gene.. tapetally expressed bHLH protein (Sorensen et al. Molecular control of postmeiotic male reproductive development Tapetum Degeneration Retardation (TDR). suggesting the conserved regulatory pathway of MSP1eUDT1 in both rice and Arabidopsis. 2002).386 D.. 2009. 2003b. Whitee Brown Complex homolog protein 27 (WBC27). The expression of UDT1 is detectable in tapetal cells and microspores from late stage 6 to stage 8.. 3. 2010). TPD1 is expressed in sporogenous cells and tapetum precursors and later is more highly expressed in the male sporocytes than the tapetum (Yang et al. the expression level of UDT1 is down-regulated in msp1 mutants (Wang et al. 2006). 3. Tapetal cell development and differentiation are critical for the early male reproduction. Xu et al. plays a key role in tapetal programmed cell death (PCD) in rice. 2002. UNDEVELOPED TAPETUM1 (UDT1) encodes a basic helix-loop-helix (bHLH)econtaining protein and plays a crucial role in the differentiation of secondary parietal cells to mature tapetal cells. 2003). 2006a. This gene was demonstrated to play a key role in homologous chromosome pairing and synapsis in rice male and female meicytes (Yuan et al. Liu et al. 2006a. / Journal of Genetics and Genomics 38 (2011) 379e390 anther cell differentiation with excess male sporocytes and lack of tapetum (Canales et al. 2002). 2006)... Xu et al... however. 2003b).. 2008). 2010). which also has a putative ortholog in rice. display defective pollen development and male sterility (Xu et al.

OsMADS3 and OsMADS58. a rice cysteine protease gene.. CYP703A3 and CYP704B2. CYP703A2 (Morant et al. Wilson and Zhang. DRL1) to form hydroxylated a-pyrone compounds for sporopollenin biosynthesis (Tang et al. 2007. and ms1 mutants show altered tapetal development without normal PCD and abnormal tapetal degeneration associated with large autophagic vacuoles and mitochondrial swelling (VizcayBarrena and Wilson. 2009). The Arabidopsis flower C-class gene. causing aborted pollen development. DEX1 (DEFECTIVE in EXINE PATTERN FORMATION) (Paxson-Sowders et al.. 2009.. The cyp704B2 mutant shows defective anther epidermal cuticle and aborted pollen grains without obvious exines (Li et al. as well as in other sinks. / Journal of Genetics and Genomics 38 (2011) 379e390 387 development. Mutation of PTC1 causes uncontrolled tapetal cell proliferation and swelling. The molecular mechanism of OsMADS3 involvement in rice male reproductive development is modulation of reactive oxygen species (ROS) levels through MT-1-4b. Aya et al. the conserved and crucial role of PTC1 is indicated by its ability to complement its Arabidopsis ortholog mutant. NEF1 (NO EXINE FORMATION 1) (Ariizumi et al. Zhang et al. Ito et al. OsAPI5 is able to interact with two DEAD-box ATP-dependent RNA helicases. abnormal Ubisch bodies/orbicules and pollen wall development... It controls programmed tapetal development and degradation during rice anther development. The csa mutant displays reduced levels of carbohydrates in later anthers and is male sterile. aborted microspores. OsMADS3 is highly expressed in the tapetum and microspores during late anther development. 2011). Normal tapetal differentiation and degeneration are required for successful male reproductive development and fertility in higher plants (Ma. 2006). The osapi5 mutant displays delayed tapetal degeneration. 2001). 2005. 2002. Timely degeneration of tapetal cells is thought to contribute to the release of wall materials.. which is a putative R2R3 MYB-type transcription factor involved in regulating sugar partitioning during male reproductive development. Arabidopsis MALE STERILITY1 (MS1) encodes a putative PHD-finger (Plant Homeo Domain) protein (Wilson et al. MT-1-4b .. 2010). The rice ortholog of CYP703A2.. Grienenberger et al. Furthermore. osmads3-4. Ito et al. MS2. APOPTOSIS INHIBITOR5 (API5) is another newly identified tapetal PCD positive regulator in rice and is critical for post-meiotic anther development and proper formation of male gametophytes (Li et al. Consistent with this function. Studies in rice identified two C-class MADS box genes. As a non-photosynthetic male reproductive organ.. including carbohydrates.. displays defective anther walls.. 2006a. 2009) and CYP704B1 (Dobritsa et al. which is conserved among terrestrial plants. Recently. 2009. The rice ortholog of CYP704B1. Recently. tapetal degeneration. CYP704B2. the anther requires the supply of photosynthetic assimilates from source organs to support normal pollen development and maturation (Goetz et al. plays a key role in specifying stamen.. delayed DNA fragmentation. 2010). 2009). which can be reduced by TETRAKETIDE a-PYRONE REDUCTASE1 and 2 (TKPR1/2) (also called DIHYDROFLAVONOL 4-REDUCTASE LIKE1. the developing pollen is immersed in locular fluid containing nutrients.. providing a new understanding of tapetal PCD control in rice (Li et al. 2004).. 2005). rice Waxdeficient anther1 (WDA1) is homologous to Arabidopsis ECERIFERUM1 (CER1). Genetic investigations have identified several genes required for Arabidopsis pollen wall development.. and regulates the expression of OsCP1. 2004. 2009). which is homologous to the anti-apoptosis protein Api5 in animals.D. Yang et al. 2007). 1999. promoted by an apoptosislike process. More interestingly.. is also crucial for viable pollen formation (Li et al. 2009).. 2011c). Within the anther. 2001. causing complete male sterility (Li et al. 2011a).. which is related to anther cuticle and pollen exine development (Jung et al. we revealed a role for OsMADS3 in regulating late anther development and pollen formation. The CSA gene is mainly expressed in the vascular tissue and the tapetum of the anther. carpel identities. 2010). Ito and Shinozaki. 2010). indicating that CYP704B2 controls a conserved biosynthetic pathway for the biopolymers sporopollenin and cutin. 2006). FLP1 (FACELESSPOLLEN1) (Ariizumi et al. ms1. 1999. 2006. is preferentially expressed in tapetal cells.. AGAMOUS (AG). ovule and floral meristem identities (Yamaguchi et al. leading to complete male sterility (Hu et al.. PTC1 is briefly expressed in tapetal cells and microspores.. These observations present new insights into programmed male reproductive development in both dicots and monocots. which encodes a monosaccharide transporter (Zhang et al. Li et al... cytochrome P450 family members. 2009. 1991. lipidic molecules and other nutrients from the tapetal cells to the developing microspores.. Yang et al. We recently identified a key regulator.. and the loss of CYP703A3 function causes defective ubicsh body and pollen exine development (Aya et al. and floral meristem determinacy as well as male reproductive development (Yanofsky et al... Kim et al.. encodes a fatty acid hydroxylase. API5-INTERACTING PROTEIN1 (AIP1) and AIP2. 2011b). Dobritsa et al. and the recombinant CYP704B2 protein has the ability to catalyze the hydroxylation of palmitic acid and unsaturated C18 fatty acids in the u position of the carbon chain. CYP703A3. including sugars and lipids from the sporophytic (somatic) tissue tapetum (Pacini et al. which is the ortholog of MS1. 2010b). 2003). Schiefthaler et al.. 1990. This finding provides the first example for transcription control of carbon partitioning in plants.. we identified a key regulator gene in rice. and a new allele.. 2006). Bowman et al. API5 encodes a nuclear protein. and OsMADS3 was shown to be required for specifying stamen.. PERSISTENT TAPETAL CELL 1 (PTC1). Expression analysis suggests that PTC1 regulates the expression of genes associated with tapetal function and pollen exine formation. 2011b). such as MS1. which is directly regulated by GAMYB. were shown to be essential for pollen exine development (Li and Zhang. 2001). In rice. and the CSA protein is able to directly regulate the expression of MST8. Fatty acylCoA esters synthesized by ACYL-COA SYNTHETASE 5 (ACOS5) can be condensed with malonyl-CoA by POLYKETIDE SYNTHASE A/LAP6 and B/LAP5 (PKSA/B) to produce a-pyronepolyketides (Souza et al.. 2007). Carbon Starved Anther (CSA). ACOS5 (Acyl-CoA Synthetase 5) (Souza et al.

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