Genetic and Epigenetic Regulation of Meiotic Fate Decision and Gametophyte Specification in Rice

Chapter

Abstract

The life cycle of sexual organisms is achieved through repeated rounds of fertilization and meiosis. After premeiotic DNA replication, plant meiosis produces four haploid spores by two sequential cell divisions without DNA replication. In most model organisms, including rice, the homologous chromosome pair is separated to opposite poles during meiosis I, and sister chromatids are separated during meiosis II. In animals, meiotic products directly mature into gametes, namely, sperms and eggs. In contrast, meiosis of land plants produces spores that undergo further somatic cell division and eventually form a multicellular haploid body containing sperms or eggs. In other words, land plants have two distinct multicellular bodies, sporophytic diploid and gametophytic haploid bodies. This type of reproductive mode is called alternation of generations and is commonly found in all land plants, some algae and fungi (Graham, Am Sci 73:178–186, 1985). These facts imply that plants have evolved unique genetic systems for reproduction, in addition to systems common to non-plant species. In this chapter, we overview the genetic and epigenetic systems regulating meiosis and gametogenesis and introduce challenges to improve the efficiency of breeding methods in rice (Oryza sativa L.).

Keywords

Meiosis Reproduction Pollen Tapetum Anther Genetics Epigenetics Asymmetric cell division 

Notes

Acknowledgments

This chapter is dedicated to Prof. Nobuo Iwata (Kyushu University, Japan), who established the fundamentals of genetic maps and cytogenetic methodologies in rice. We are grateful for Dr. Pilar Prieto (CSIC, Spain) for reading the manuscript and for giving critical comments. This work was supported by the JSPS KAKENHI grants: No.25252004, No.15 K14630, No.17H05849 (to K-I.N.), and No. JP26440168 (to K.U.). We apologize to all colleagues who have contributed to the field but could not be cited due to space limitation.

References

  1. Agarwal S, Roeder GS (2000) Zip3 provides a link between recombination enzymes and synaptonemal complex proteins. Cell 102(2):245–255PubMedCrossRefGoogle Scholar
  2. Alani E, Padmore R, Kleckner N (1990) Analysis of wild-type and rad50 mutants of yeast suggests an intimate relationship between meiotic chromosome synapsis and recombination. Cell 61(3):419–436PubMedCrossRefGoogle Scholar
  3. An XJ, Deng ZY, Wang T (2011) OsSpo11-4, a rice homologue of the archaeal TopVIA protein, mediates double-strand DNA cleavage and interacts with OsTopVIB. PLoS One 6(5):e20327.  https://doi.org/10.1371/journal.pone.0020327 PubMedPubMedCentralCrossRefGoogle Scholar
  4. Asaoka-Taguchi M, Yamada M, Nakamura A, Hanyu K, Kobayashi S (1999) Maternal Pumilio acts together with Nanos in germline development in Drosophila embryos. Nat Cell Biol 1(7):431–437.  https://doi.org/10.1038/15666 PubMedCrossRefGoogle Scholar
  5. Aya K, Ueguchi-Tanaka M, Kondo M, Hamada K, Yano K, Nishimura M, Matsuoka M (2009) Gibberellin modulates anther development in rice via the transcriptional regulation of GAMYB. Plant Cell 21(5):1453–1472.  https://doi.org/10.1105/tpc.108.062935 PubMedPubMedCentralCrossRefGoogle Scholar
  6. Bergerat A, de Massy B, Gadelle D, Varoutas PC, Nicolas A, Forterre P (1997) An atypical topoisomerase II from Archaea with implications for meiotic recombination. Nature 386(6623):414–417.  https://doi.org/10.1038/386414a0 PubMedCrossRefGoogle Scholar
  7. Bishop DK (1994) RecA homologs Dmc1 and Rad51 interact to form multiple nuclear complexes prior to meiotic chromosome synapsis. Cell 79(6):1081–1092PubMedCrossRefGoogle Scholar
  8. Bishop DK, Zickler D (2004) Early decision; meiotic crossover interference prior to stable strand exchange and synapsis. Cell 117(1):9–15PubMedCrossRefGoogle Scholar
  9. Boateng KA, Yang X, Dong F, Owen HA, Makaroff CA (2008) SWI1 is required for meiotic chromosome remodeling events. Mol Plant 1(4):620–633.  https://doi.org/10.1093/mp/ssn030 PubMedCrossRefGoogle Scholar
  10. Boddy MN, Gaillard PH, McDonald WH, Shanahan P, Yates JR 3rd, Russell P (2001) Mus81-Eme1 are essential components of a Holliday junction resolvase. Cell 107(4):537–548PubMedCrossRefGoogle Scholar
  11. Börner GV, Kleckner N, Hunter N (2004) Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117(1):29–45PubMedCrossRefGoogle Scholar
  12. Börner GV, Barot A, Kleckner N (2008) Yeast Pch2 promotes domainal axis organization, timely recombination progression, and arrest of defective recombinosomes during meiosis. Proc Natl Acad Sci U S A 105(9):3327–3332.  https://doi.org/10.1073/pnas.0711864105 PubMedPubMedCentralCrossRefGoogle Scholar
  13. Borrill P, Adamski N, Uauy C (2015) Genomics as the key to unlocking the polyploid potential of wheat. New Phytol 208(4):1008–1022.  https://doi.org/10.1111/nph.13533 PubMedCrossRefGoogle Scholar
  14. Brownfield L, Hafidh S, Borg M, Sidorova A, Mori T, Twell D (2009) A plant germline-specific integrator of sperm specification and cell cycle progression. PLoS Genet 5(3):e1000430.  https://doi.org/10.1371/journal.pgen.1000430 PubMedPubMedCentralCrossRefGoogle Scholar
  15. Brzeski J, Jerzmanowski A (2003) Deficient in DNA methylation 1 (DDM1) defines a novel family of chromatin-remodeling factors. J Biol Chem 278(2):823–828.  https://doi.org/10.1074/jbc.M209260200 PubMedCrossRefGoogle Scholar
  16. Burgoyne PS, Mahadevaiah SK, Turner JM (2009) The consequences of asynapsis for mammalian meiosis. Nat Rev Genet 10(3):207–216.  https://doi.org/10.1038/nrg2505 PubMedCrossRefGoogle Scholar
  17. Byun MY, Kim WT (2014) Suppression of OsRAD51D results in defects in reproductive development in rice (Oryza sativa L.) Plant J 79(2):256–269.  https://doi.org/10.1111/tpj.12558 PubMedCrossRefGoogle Scholar
  18. Canales C, Bhatt AM, Scott R, Dickinson H (2002) EXS, a putative LRR receptor kinase, regulates male germline cell number and tapetal identity and promotes seed development in Arabidopsis. Curr Biol 12(20):1718–1727PubMedCrossRefGoogle Scholar
  19. Cao L, Alani E, Kleckner N (1990) A pathway for generation and processing of double-strand breaks during meiotic recombination in S. cerevisiae. Cell 61(6):1089–1101PubMedCrossRefGoogle Scholar
  20. Carretero-Paulet L, Galstyan A, Roig-Villanova I, Martinez-Garcia JF, Bilbao-Castro JR, Robertson DL (2010) Genome-wide classification and evolutionary analysis of the bHLH family of transcription factors in Arabidopsis, poplar, rice, moss, and algae. Plant Physiol 153(3):1398–1412.  https://doi.org/10.1104/pp.110.153593 PubMedPubMedCentralCrossRefGoogle Scholar
  21. Chang Y, Gong L, Yuan W, Li X, Chen G, Li X, Zhang Q, Wu C (2009) Replication protein A (RPA1a) is required for meiotic and somatic DNA repair but is dispensable for DNA replication and homologous recombination in rice. Plant Physiol 151(4):2162–2173.  https://doi.org/10.1104/pp.109.142877 PubMedPubMedCentralCrossRefGoogle Scholar
  22. Che L, Tang D, Wang K, Wang M, Zhu K, Yu H, Gu M, Cheng Z (2011) OsAM1 is required for leptotene-zygotene transition in rice. Cell Res 21(4):654–665.  https://doi.org/10.1038/cr.2011.7 PubMedPubMedCentralCrossRefGoogle Scholar
  23. Che L, Wang K, Tang D, Liu Q, Chen X, Li Y, Hu Q, Shen Y, Yu H, Gu M, Cheng Z (2014) OsHUS1 facilitates accurate meiotic recombination in rice. PLoS Genet 10(6):e1004405.  https://doi.org/10.1371/journal.pgen.1004405 PubMedPubMedCentralCrossRefGoogle Scholar
  24. Chelysheva L, Vezon D, Chambon A, Gendrot G, Pereira L, Lemhemdi A, Vrielynck N, Le Guin S, Novatchkova M, Grelon M (2012) The Arabidopsis HEI10 is a new ZMM protein related to Zip3. PLoS Genet 8(7):e1002799.  https://doi.org/10.1371/journal.pgen.1002799 PubMedPubMedCentralCrossRefGoogle Scholar
  25. Chikashige Y, Tsutsumi C, Yamane M, Okamasa K, Haraguchi T, Hiraoka Y (2006) Meiotic proteins bqt1 and bqt2 tether telomeres to form the bouquet arrangement of chromosomes. Cell 125(1):59–69.  https://doi.org/10.1016/j.cell.2006.01.048 PubMedCrossRefGoogle Scholar
  26. Choi K, Zhao X, Kelly KA, Venn O, Higgins JD, Yelina NE, Hardcastle TJ, Ziolkowski PA, Copenhaver GP, Franklin FC, McVean G, Henderson IR (2013) Arabidopsis meiotic crossover hot spots overlap with H2A.Z nucleosomes at gene promoters. Nat Genet 45(11):1327–1336.  https://doi.org/10.1038/ng.2766 PubMedCrossRefGoogle Scholar
  27. Crismani W, Girard C, Froger N, Pradillo M, Santos JL, Chelysheva L, Copenhaver GP, Horlow C, Mercier R (2012) FANCM limits meiotic crossovers. Science 336(6088):1588–1590.  https://doi.org/10.1126/science.1220381 PubMedCrossRefGoogle Scholar
  28. Daley JM, Palmbos PL, Wu D, Wilson TE (2005) Nonhomologous end joining in yeast. Annu Rev Genet 39:431–451.  https://doi.org/10.1146/annurev.genet.39.073003.113340 PubMedCrossRefGoogle Scholar
  29. Davis L, Smith GR (2006) The meiotic bouquet promotes homolog interactions and restricts ectopic recombination in Schizosaccharomyces pombe. Genetics 174(1):167–177.  https://doi.org/10.1534/genetics.106.059733 PubMedPubMedCentralCrossRefGoogle Scholar
  30. d'Erfurth I, Cromer L, Jolivet S, Girard C, Horlow C, Sun Y, To JP, Berchowitz LE, Copenhaver GP, Mercier R (2010) The cyclin-A CYCA1;2/TAM is required for the meiosis I to meiosis II transition and cooperates with OSD1 for the prophase to first meiotic division transition. PLoS Genet 6(6):e1000989.  https://doi.org/10.1371/journal.pgen.1000989 PubMedPubMedCentralCrossRefGoogle Scholar
  31. Dukowic-Schulze S, Sundararajan A, Ramaraj T, Kianian S, Pawlowski WP, Mudge J, Chen C (2016) Novel meiotic miRNAs and indications for a role of phasiRNAs in meiosis. Front Plant Sci 7:762.  https://doi.org/10.3389/fpls.2016.00762 PubMedPubMedCentralCrossRefGoogle Scholar
  32. Endo M, Tsuchiya T, Hamada K, Kawamura S, Yano K, Ohshima M, Higashitani A, Watanabe M, Kawagishi-Kobayashi M (2009) High temperatures cause male sterility in rice plants with transcriptional alterations during pollen development. Plant Cell Physiol 50(11):1911–1922.  https://doi.org/10.1093/pcp/pcp135 PubMedCrossRefGoogle Scholar
  33. Fei Q, Xia R, Meyers BC (2013) Phased, secondary, small interfering RNAs in posttranscriptional regulatory networks. Plant Cell 25(7):2400–2415.  https://doi.org/10.1105/tpc.113.114652 PubMedPubMedCentralCrossRefGoogle Scholar
  34. Fei Q, Yang L, Liang W, Zhang D, Meyers BC (2016) Dynamic changes of small RNAs in rice spikelet development reveal specialized reproductive phasiRNA pathways. J Exp Bot 67(21):6037–6049.  https://doi.org/10.1093/jxb/erw361 PubMedPubMedCentralCrossRefGoogle Scholar
  35. Fu Z, Yu J, Cheng X, Zong X, Xu J, Chen M, Li Z, Zhang D, Liang W (2014) The rice basic helix-loop-helix transcription factor TDR INTERACTING PROTEIN2 is a central switch in early anther development. Plant Cell 26(4):1512–1524.  https://doi.org/10.1105/tpc.114.123745 PubMedPubMedCentralCrossRefGoogle Scholar
  36. Fung JC, Rockmill B, Odell M, Roeder GS (2004) Imposition of crossover interference through the nonrandom distribution of synapsis initiation complexes. Cell 116(6):795–802PubMedCrossRefGoogle Scholar
  37. Goldberg RB, Beals TP, Sanders PM (1993) Anther development: basic principles and practical applications. Plant Cell 5(10):1217–1229.  https://doi.org/10.1105/tpc.5.10.1217 PubMedPubMedCentralCrossRefGoogle Scholar
  38. Golubovskaya I, Grebennikova ZK, Avalkina NA, Sheridan WF (1993) The role of the ameiotic1 gene in the initiation of meiosis and in subsequent meiotic events in maize. Genetics 135(4):1151–1166PubMedPubMedCentralGoogle Scholar
  39. Graham EL (1985) The origin of the life cycle of land plants. Am Sci 73:178–186Google Scholar
  40. Grimanelli D, Leblanc O, Perotti E, Grossniklaus U (2001) Developmental genetics of gametophytic apomixis. Trends Genet 17(10):597–604PubMedCrossRefGoogle Scholar
  41. Habu Y, Ando T, Ito S, Nagaki K, Kishimoto N, Taguchi-Shiobara F, Numa H, Yamaguchi K, Shigenobu S, Murata M, Meshi T, Yano M (2015) Epigenomic modification in rice controls meiotic recombination and segregation distortion. Mol Breed 35:103CrossRefGoogle Scholar
  42. Han MJ, Jung KH, Yi G, Lee DY, An G (2006) Rice immature pollen 1 (RIP1) is a regulator of late pollen development. Plant Cell Physiol 47(11):1457–1472.  https://doi.org/10.1093/pcp/pcl013 PubMedCrossRefGoogle Scholar
  43. Han MJ, Jung KH, Yi G, An G (2011) Rice Importin β1 gene affects pollen tube elongation. Mol Cell 31(6):523–530.  https://doi.org/10.1007/s10059-011-2321-7 CrossRefGoogle Scholar
  44. Hanamata S, Kurusu T, Kuchitsu K (2014) Roles of autophagy in male reproductive development in plants. Front Plant Sci 5:457.  https://doi.org/10.3389/fpls.2014.00457 PubMedPubMedCentralCrossRefGoogle Scholar
  45. Heslop-Harrison J (1966) Cytoplasmic connexions between angiosperm meiocytes. Ann Bot 30:221–230CrossRefGoogle Scholar
  46. Heyer WD (2004) Recombination: Holliday junction resolution and crossover formation. Curr Biol 14(2):R56–R58PubMedCrossRefGoogle Scholar
  47. Higgins JD, Armstrong SJ, Franklin FC, Jones GH (2004) The Arabidopsis MutS homolog AtMSH4 functions at an early step in recombination: evidence for two classes of recombination in Arabidopsis. Genes Dev 18(20):2557–2570.  https://doi.org/10.1101/gad.317504 PubMedPubMedCentralCrossRefGoogle Scholar
  48. Higo H, Tahir M, Takashima K, Miura A, Watanabe K, Tagiri A, Ugaki M, Ishikawa R, Eiguchi M, Kurata N, Sasaki T, Richards E, Takano M, Kishimoto N, Kakutani T, Habu Y (2012) DDM1 (decrease in DNA methylation) genes in rice (Oryza sativa). Mol Gen Genomics 287(10):785–792.  https://doi.org/10.1007/s00438-012-0717-5 CrossRefGoogle Scholar
  49. Hirano T (2006) At the heart of the chromosome: SMC proteins in action. Nat Rev Mol Cell Biol 7(5):311–322.  https://doi.org/10.1038/nrm1909 PubMedCrossRefGoogle Scholar
  50. Hirose T, Zhang Z, Miyao A, Hirochika H, Ohsugi R, Terao T (2010) Disruption of a gene for rice sucrose transporter, OsSUT1, impairs pollen function but pollen maturation is unaffected. J Exp Bot 61(13):3639–3646.  https://doi.org/10.1093/jxb/erq175 PubMedPubMedCentralCrossRefGoogle Scholar
  51. Holdaway-Clarke TL, Hepler PK (2003) Control of pollen tube growth: role of ion gradients and fluxes. New Phytol 159:539–563CrossRefGoogle Scholar
  52. Hollingsworth NM, Brill SJ (2004) The Mus81 solution to resolution: generating meiotic crossovers without Holliday junctions. Genes Dev 18(2):117–125.  https://doi.org/10.1101/gad.1165904 PubMedPubMedCentralCrossRefGoogle Scholar
  53. Hong L, Tang D, Zhu K, Wang K, Li M, Cheng Z (2012) Somatic and reproductive cell development in rice anther is regulated by a putative glutaredoxin. Plant Cell 24(2):577–588.  https://doi.org/10.1105/tpc.111.093740 PubMedPubMedCentralCrossRefGoogle Scholar
  54. Hotta T, Kong Z, Ho CM, Zeng CJ, Horio T, Fong S, Vuong T, Lee YR, Liu B (2012) Characterization of the Arabidopsis augmin complex uncovers its critical function in the assembly of the acentrosomal spindle and phragmoplast microtubule arrays. Plant Cell 24(4):1494–1509.  https://doi.org/10.1105/tpc.112.096610 PubMedPubMedCentralCrossRefGoogle Scholar
  55. Hu Q, Tang D, Wang H, Shen Y, Chen X, Ji J, Du G, Li Y, Cheng Z (2016) The exonuclease homolog OsRAD1 promotes accurate meiotic double-strand break repair by suppressing nonhomologous end joining. Plant Physiol 172(2):1105–1116.  https://doi.org/10.1104/pp.16.00831 PubMedPubMedCentralGoogle Scholar
  56. Huang J, Zhao X, Cheng K, Jiang Y, Ouyang Y, Xu C, Li X, Xiao J, Zhang Q (2013) OsAP65, a rice aspartic protease, is essential for male fertility and plays a role in pollen germination and pollen tube growth. J Exp Bot 64(11):3351–3360.  https://doi.org/10.1093/jxb/ert173 PubMedPubMedCentralCrossRefGoogle Scholar
  57. Huertas P, Cortes-Ledesma F, Sartori AA, Aguilera A, Jackson SP (2008) CDK targets Sae2 to control DNA-end resection and homologous recombination. Nature 455(7213):689–692.  https://doi.org/10.1038/nature07215 PubMedPubMedCentralCrossRefGoogle Scholar
  58. Hunter N, Kleckner N (2001) The single-end invasion: an asymmetric intermediate at the double-strand break to double-holliday junction transition of meiotic recombination. Cell 106(1):59–70PubMedCrossRefGoogle Scholar
  59. Iftode C, Daniely Y, Borowiec JA (1999) Replication protein A (RPA): the eukaryotic SSB. Crit Rev Biochem Mol Biol 34(3):141–180.  https://doi.org/10.1080/10409239991209255 PubMedCrossRefGoogle Scholar
  60. Ito T, Wellmer F, Yu H, Das P, Ito N, Alves-Ferreira M, Riechmann JL, Meyerowitz EM (2004) The homeotic protein AGAMOUS controls microsporogenesis by regulation of SPOROCYTELESS. Nature 430(6997):356–360PubMedCrossRefGoogle Scholar
  61. Jeddeloh JA, Stokes TL, Richards EJ (1999) Maintenance of genomic methylation requires a SWI2/SNF2-like protein. Nat Genet 22(1):94–97.  https://doi.org/10.1038/8803 PubMedCrossRefGoogle Scholar
  62. Jessen D, Olbrich A, Knufer J, Kruger A, Hoppert M, Polle A, Fulda M (2011) Combined activity of LACS1 and LACS4 is required for proper pollen coat formation in Arabidopsis. Plant J 68(4):715–726.  https://doi.org/10.1111/j.1365-313X.2011.04722.x PubMedCrossRefGoogle Scholar
  63. Ji J, Tang D, Wang K, Wang M, Che L, Li M, Cheng Z (2012) The role of OsCOM1 in homologous chromosome synapsis and recombination in rice meiosis. Plant J 72(1):18–30.  https://doi.org/10.1111/j.1365-313X.2012.05025.x PubMedCrossRefGoogle Scholar
  64. Ji C, Li H, Chen L, Xie M, Wang F, Chen Y, Liu YG (2013a) A novel rice bHLH transcription factor, DTD, acts coordinately with TDR in controlling tapetum function and pollen development. Mol Plant 6(5):1715–1718.  https://doi.org/10.1093/mp/sst046 PubMedCrossRefGoogle Scholar
  65. Ji J, Tang D, Wang M, Li Y, Zhang L, Wang K, Li M, Cheng Z (2013b) MRE11 is required for homologous synapsis and DSB processing in rice meiosis. Chromosoma 122(5):363–376.  https://doi.org/10.1007/s00412-013-0421-1 PubMedCrossRefGoogle Scholar
  66. Ji J, Tang D, Shen Y, Xue Z, Wang H, Shi W, Zhang C, Du G, Li Y, Cheng Z (2016) P31comet, a member of the synaptonemal complex, participates in meiotic DSB formation in rice. Proc Natl Acad Sci U S A 113(38):10577–10582.  https://doi.org/10.1073/pnas.1607334113 PubMedPubMedCentralCrossRefGoogle Scholar
  67. Jia G, Liu X, Owen HA, Zhao D (2008) Signaling of cell fate determination by the TPD1 small protein and EMS1 receptor kinase. Proc Natl Acad Sci U S A 105(6):2220–2225.  https://doi.org/10.1073/pnas.0708795105 PubMedPubMedCentralCrossRefGoogle Scholar
  68. Jung KH, Han MJ, Lee YS, Kim YW, Hwang I, Kim MJ, Kim YK, Nahm BH, An G (2005) Rice Undeveloped Tapetum1 is a major regulator of early tapetum development. Plant Cell 17(10):2705–2722.  https://doi.org/10.1105/tpc.105.034090 PubMedPubMedCentralCrossRefGoogle Scholar
  69. Jung KH, Han MJ, Lee DY, Lee YS, Schreiber L, Franke R, Faust A, Yephremov A, Saedler H, Kim YW, Hwang I, An G (2006) Wax-deficient anther1 is involved in cuticle and wax production in rice anther walls and is required for pollen development. Plant Cell 18(11):3015–3032.  https://doi.org/10.1105/tpc.106.042044 PubMedPubMedCentralCrossRefGoogle Scholar
  70. Kaneko M, Inukai Y, Ueguchi-Tanaka M, Itoh H, Izawa T, Kobayashi Y, Hattori T, Miyao A, Hirochika H, Ashikari M, Matsuoka M (2004) Loss-of-function mutations of the rice GAMYB gene impair alpha-amylase expression in aleurone and flower development. Plant Cell 16(1):33–44.  https://doi.org/10.1105/tpc.017327 PubMedPubMedCentralCrossRefGoogle Scholar
  71. Keeney S, Giroux CN, Kleckner N (1997) Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88(3):375–384PubMedCrossRefGoogle Scholar
  72. Kelliher T, Walbot V (2012) Hypoxia triggers meiotic fate acquisition in maize. Science 337(6092):345–348.  https://doi.org/10.1126/science.1220080 PubMedPubMedCentralCrossRefGoogle Scholar
  73. Kelliher T, Walbot V (2014) Maize germinal cell initials accommodate hypoxia and precociously express meiotic genes. Plant J 77(4):639–652.  https://doi.org/10.1111/tpj.12414 PubMedPubMedCentralCrossRefGoogle Scholar
  74. Kim MJ, Kim M, Lee MR, Park SK, Kim J (2015) LATERAL ORGAN BOUNDARIES DOMAIN (LBD)10 interacts with SIDECAR POLLEN/LBD27 to control pollen development in Arabidopsis. Plant J 81(5):794–809.  https://doi.org/10.1111/tpj.12767 PubMedCrossRefGoogle Scholar
  75. Kim M, Kim MJ, Pandey S, Kim J (2016) Expression and protein interaction analyses reveal combinatorial interactions of LBD transcription factors during Arabidopsis pollen development. Plant Cell Physiol 57(11):2291–2299.  https://doi.org/10.1093/pcp/pcw145 PubMedCrossRefGoogle Scholar
  76. Kimble J (2011) Molecular regulation of the mitosis/meiosis decision in multicellular organisms. Cold Spring Harb Perspect Biol 3(8):a002683.  https://doi.org/10.1101/cshperspect.a002683 PubMedPubMedCentralCrossRefGoogle Scholar
  77. Ko SS, Li MJ, Sun-Ben Ku M, Ho YC, Lin YJ, Chuang MH, Hsing HX, Lien YC, Yang HT, Chang HC, Chan MT (2014) The bHLH142 transcription factor coordinates with TDR1 to modulate the expression of EAT1 and regulate pollen development in rice. Plant Cell 26(6):2486–2504.  https://doi.org/10.1105/tpc.114.126292 PubMedPubMedCentralCrossRefGoogle Scholar
  78. Kobayashi S, Yamada M, Asaoka M, Kitamura T (1996) Essential role of the posterior morphogen nanos for germline development in Drosophila. Nature 380(6576):708–711.  https://doi.org/10.1038/380708a0 PubMedCrossRefGoogle Scholar
  79. Komiya R, Ohyanagi H, Niihama M, Watanabe T, Nakano M, Kurata N, Nonomura KI (2014) Rice germline-specific Argonaute MEL1 protein binds to phasiRNAs generated from more than 700 lincRNAs. Plant J 78(3):385–397.  https://doi.org/10.1111/tpj.12483 PubMedCrossRefGoogle Scholar
  80. Koo DH, Liu W, Friebe B, Gill BS (2016) Homoeologous recombination in the presence of Ph1 gene in wheat. Chromosoma.  https://doi.org/10.1007/s00412-016-0622-5
  81. Kurakawa T, Ueda N, Maekawa M, Kobayashi K, Kojima M, Nagato Y, Sakakibara H, Kyozuka J (2007) Direct control of shoot meristem activity by a cytokinin-activating enzyme. Nature 445(7128):652–655.  https://doi.org/10.1038/nature05504 PubMedCrossRefGoogle Scholar
  82. Kurusu T, Koyano T, Hanamata S, Kubo T, Noguchi Y, Yagi C, Nagata N, Yamamoto T, Ohnishi T, Okazaki Y, Kitahata N, Ando D, Ishikawa M, Wada S, Miyao A, Hirochika H, Shimada H, Makino A, Saito K, Ishida H, Kinoshita T, Kurata N, Kuchitsu K (2014) OsATG7 is required for autophagy-dependent lipid metabolism in rice postmeiotic anther development. Autophagy 10(5):878–888.  https://doi.org/10.4161/auto.28279 PubMedPubMedCentralCrossRefGoogle Scholar
  83. Lee S, Jung K, An G, Chung Y (2004) Isolation and characterization of a rice cysteine protease gene, OsCP1, using T-DNA gene-trap system. Plant Mol Biol 54(5):755–765PubMedCrossRefGoogle Scholar
  84. Li N, Zhang DS, Liu HS, Yin CS, Li XX, Liang WQ, Yuan Z, Xu B, Chu HW, Wang J, Wen TQ, Huang H, Luo D, Ma H, Zhang DB (2006) The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell 18(11):2999–3014.  https://doi.org/10.1105/tpc.106.044107 PubMedPubMedCentralCrossRefGoogle Scholar
  85. Li H, Pinot F, Sauveplane V, Werck-Reichhart D, Diehl P, Schreiber L, Franke R, Zhang P, Chen L, Gao Y, Liang W, Zhang D (2010) Cytochrome P450 family member CYP704B2 catalyzes the ω-hydroxylation of fatty acids and is required for anther cutin biosynthesis and pollen exine formation in rice. Plant Cell 22(1):173–190.  https://doi.org/10.1105/tpc.109.070326 PubMedPubMedCentralCrossRefGoogle Scholar
  86. Li H, Yuan Z, Vizcay-Barrena G, Yang C, Liang W, Zong J, Wilson ZA, Zhang D (2011a) PERSISTENT TAPETAL CELL1 encodes a PHD-finger protein that is required for tapetal cell death and pollen development in rice. Plant Physiol 156(2):615–630.  https://doi.org/10.1104/pp.111.175760 PubMedPubMedCentralCrossRefGoogle Scholar
  87. Li X, Gao X, Wei Y, Deng L, Ouyang Y, Chen G, Li X, Zhang Q, Wu C (2011b) Rice APOPTOSIS INHIBITOR5 coupled with two DEAD-box adenosine 5′-triphosphate-dependent RNA helicases regulates tapetum degeneration. Plant Cell 23(4):1416–1434.  https://doi.org/10.1105/tpc.110.082636 PubMedPubMedCentralCrossRefGoogle Scholar
  88. Li F, Chung T, Pennington JG, Federico ML, Kaeppler HF, Kaeppler SM, Otegui MS, Vierstra RD (2015) Autophagic recycling plays a central role in maize nitrogen remobilization. Plant Cell 27(5):1389–1408.  https://doi.org/10.1105/tpc.15.00158 PubMedPubMedCentralCrossRefGoogle Scholar
  89. Li Y, Li D, Guo Z, Shi Q, Xiong S, Zhang C, Zhu J, Yang Z (2016) OsACOS12, an orthologue of Arabidopsis acyl-CoA synthetase5, plays an important role in pollen exine formation and anther development in rice. BMC Plant Biol 16(1):256.  https://doi.org/10.1186/s12870-016-0943-9 PubMedPubMedCentralCrossRefGoogle Scholar
  90. Lieber MR (2010) The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu Rev Biochem 79:181–211.  https://doi.org/10.1146/annurev.biochem.052308.093131 PubMedPubMedCentralCrossRefGoogle Scholar
  91. Lin Z, Kong H, Nei M, Ma H (2006) Origins and evolution of the recA/RAD51 gene family: evidence for ancient gene duplication and endosymbiotic gene transfer. Proc Natl Acad Sci U S A 103(27):10328–10333.  https://doi.org/10.1073/pnas.0604232103 PubMedPubMedCentralCrossRefGoogle Scholar
  92. Liu H, Nonomura KI (2016) A wide reprogramming of histone H3 modifications during male meiosis I in rice is dependent on the Argonaute protein MEL1. J Cell Sci 129(19):3553–3561.  https://doi.org/10.1242/jcs.184937 PubMedCrossRefGoogle Scholar
  93. Liu L, Zheng C, Kuang B, Wei L, Yan L, Wang T (2016) Receptor-like kinase RUPO interacts with potassium transporters to regulate pollen tube growth and integrity in Rice. PLoS Genet 12(7):e1006085.  https://doi.org/10.1371/journal.pgen.1006085 PubMedPubMedCentralCrossRefGoogle Scholar
  94. Luo D, Xu H, Liu Z, Guo J, Li H, Chen L, Fang C, Zhang Q, Bai M, Yao N, Wu H, Wu H, Ji C, Zheng H, Chen Y, Ye S, Li X, Zhao X, Li R, Liu YG (2013a) A detrimental mitochondrial-nuclear interaction causes cytoplasmic male sterility in rice. Nat Genet 45(5):573–577.  https://doi.org/10.1038/ng.2570 PubMedCrossRefGoogle Scholar
  95. Luo Q, Tang D, Wang M, Luo W, Zhang L, Qin B, Shen Y, Wang K, Li Y, Cheng Z (2013b) The role of OsMSH5 in crossover formation during rice meiosis. Mol Plant 6(3):729–742.  https://doi.org/10.1093/mp/sss145 PubMedCrossRefGoogle Scholar
  96. Malmanche N, Maia A, Sunkel CE (2006) The spindle assembly checkpoint: preventing chromosome mis-segregation during mitosis and meiosis. FEBS Lett 580(12):2888–2895.  https://doi.org/10.1016/j.febslet.2006.03.081 PubMedCrossRefGoogle Scholar
  97. Martinez-Perez E, Shaw P, Moore G (2001) The Ph1 locus is needed to ensure specific somatic and meiotic centromere association. Nature 411(6834):204–207.  https://doi.org/10.1038/35075597 PubMedCrossRefGoogle Scholar
  98. Martini E, Diaz RL, Hunter N, Keeney S (2006) Crossover homeostasis in yeast meiosis. Cell 126(2):285–295.  https://doi.org/10.1016/j.cell.2006.05.044 PubMedPubMedCentralCrossRefGoogle Scholar
  99. McMichael CM, Bednarek SY (2013) Cytoskeletal and membrane dynamics during higher plant cytokinesis. New Phytol 197(4):1039–1057.  https://doi.org/10.1111/nph.12122 PubMedCrossRefGoogle Scholar
  100. McVey M, Lee SE (2008) MMEJ repair of double-strand breaks (director’s cut): deleted sequences and alternative endings. Trends Genet 24(11):529–538.  https://doi.org/10.1016/j.tig.2008.08.007 PubMedPubMedCentralCrossRefGoogle Scholar
  101. Mercier R, Vezon D, Bullier E, Motamayor JC, Sellier A, Lefevre F, Pelletier G, Horlow C (2001) SWITCH1 (SWI1): a novel protein required for the establishment of sister chromatid cohesion and for bivalent formation at meiosis. Genes Dev 15(14):1859–1871.  https://doi.org/10.1101/gad.203201 PubMedPubMedCentralCrossRefGoogle Scholar
  102. Mercier R, Jolivet S, Vezon D, Huppe E, Chelysheva L, Giovanni M, Nogue F, Doutriaux MP, Horlow C, Grelon M, Mezard C (2005) Two meiotic crossover classes cohabit in Arabidopsis: one is dependent on MER3, whereas the other one is not. Curr Biol 15(8):692–701.  https://doi.org/10.1016/j.cub.2005.02.056 PubMedCrossRefGoogle Scholar
  103. Miao C, Tang D, Zhang H, Wang M, Li Y, Tang S, Yu H, Gu M, Cheng Z (2013) Central region component1, a novel synaptonemal complex component, is essential for meiotic recombination initiation in rice. Plant Cell 25(8):2998–3009.  https://doi.org/10.1105/tpc.113.113175 PubMedPubMedCentralCrossRefGoogle Scholar
  104. Mieulet D, Jolivet S, Rivard M, Cromer L, Vernet A, Mayonove P, Pereira L, Droc G, Courtois B, Guiderdoni E, Mercier R (2016) Turning rice meiosis into mitosis. Cell Res.  https://doi.org/10.1038/cr.2016.117
  105. Miyazaki S, Sato Y, Asano T, Nagamura Y, Nonomura KI (2015) Rice MEL2, the RNA recognition motif (RRM) protein, binds in vitro to meiosis-expressed genes containing U-rich RNA consensus sequences in the 3′-UTR. Plant Mol Biol 89(3):293–307.  https://doi.org/10.1007/s11103-015-0369-z PubMedCrossRefGoogle Scholar
  106. Moon S, Kim SR, Zhao G, Yi J, Yoo Y, Jin P, Lee SW, Jung KH, Zhang D, An G (2013) Rice glycosyltransferase1 encodes a glycosyltransferase essential for pollen wall formation. Plant Physiol 161(2):663–675.  https://doi.org/10.1104/pp.112.210948 PubMedCrossRefGoogle Scholar
  107. Moore G (2014) The control of recombination in wheat by Ph1 and its use in breeding. Methods Mol Biol 1145:143–153.  https://doi.org/10.1007/978-1-4939-0446-4_12 PubMedCrossRefGoogle Scholar
  108. Nairz K, Klein F (1997) mre11S – a yeast mutation that blocks double-strand-break processing and permits nonhomologous synapsis in meiosis. Genes Dev 11(17):2272–2290PubMedPubMedCentralCrossRefGoogle Scholar
  109. Niu BX, He FR, He M, Ren D, Chen LT, Liu YG (2013a) The ATP-binding cassette transporter OsABCG15 is required for anther development and pollen fertility in rice. J Integr Plant Biol 55(8):710–720.  https://doi.org/10.1111/jipb.12053 PubMedCrossRefGoogle Scholar
  110. Niu N, Liang W, Yang X, Jin W, Wilson ZA, Hu J, Zhang D (2013b) EAT1 promotes tapetal cell death by regulating aspartic proteases during male reproductive development in rice. Nat Commun 4:1445.  https://doi.org/10.1038/ncomms2396 PubMedCrossRefGoogle Scholar
  111. Nonomura KI, Miyoshi K, Eiguchi M, Suzuki T, Miyao A, Hirochika H, Kurata N (2003) The MSP1 gene is necessary to restrict the number of cells entering into male and female sporogenesis and to initiate anther wall formation in rice. Plant Cell 15(8):1728–1739PubMedPubMedCentralCrossRefGoogle Scholar
  112. Nonomura KI, Nakano M, Fukuda T, Eiguchi M, Miyao A, Hirochika H, Kurata N (2004a) The novel gene HOMOLOGOUS PAIRING ABERRATION IN RICE MEIOSIS1 of rice encodes a putative coiled-coil protein required for homologous chromosome pairing in meiosis. Plant Cell 16(4):1008–1020.  https://doi.org/10.1105/tpc.020701 PubMedPubMedCentralCrossRefGoogle Scholar
  113. Nonomura KI, Nakano M, Murata K, Miyoshi K, Eiguchi M, Miyao A, Hirochika H, Kurata N (2004b) An insertional mutation in the rice PAIR2 gene, the ortholog of Arabidopsis ASY1, results in a defect in homologous chromosome pairing during meiosis. Mol Gen Genomics 271(2):121–129.  https://doi.org/10.1007/s00438-003-0934-z CrossRefGoogle Scholar
  114. Nonomura KI, Nakano M, Eiguchi M, Suzuki T, Kurata N (2006) PAIR2 is essential for homologous chromosome synapsis in rice meiosis I. J Cell Sci 119(Pt 2):217–225.  https://doi.org/10.1242/jcs.02736 PubMedCrossRefGoogle Scholar
  115. Nonomura KI, Morohoshi A, Nakano M, Eiguchi M, Miyao A, Hirochika H, Kurata N (2007) A germ cell specific gene of the ARGONAUTE family is essential for the progression of premeiotic mitosis and meiosis during sporogenesis in rice. Plant Cell 19(8):2583–2594.  https://doi.org/10.1105/tpc.107.053199 PubMedPubMedCentralCrossRefGoogle Scholar
  116. Nonomura KI, Eiguchi M, Nakano M, Takashima K, Komeda N, Fukuchi S, Miyazaki S, Miyao A, Hirochika H, Kurata N (2011) A novel RNA-recognition-motif protein is required for premeiotic G1/S-phase transition in rice (Oryza sativa L.) PLoS Genet 7(1):e1001265.  https://doi.org/10.1371/journal.pgen.1001265 PubMedPubMedCentralCrossRefGoogle Scholar
  117. O’Neill MA, Ishii T, Albersheim P, Darvill AG (2004) Rhamnogalacturonan II: structure and function of a borate cross-linked cell wall pectic polysaccharide. Annu Rev Plant Biol 55:109–139.  https://doi.org/10.1146/annurev.arplant.55.031903.141750 PubMedCrossRefGoogle Scholar
  118. Oh SA, Johnson A, Smertenko A, Rahman D, Park SK, Hussey PJ, Twell D (2005) A divergent cellular role for the FUSED kinase family in the plant-specific cytokinetic phragmoplast. Curr Biol 15(23):2107–2111.  https://doi.org/10.1016/j.cub.2005.10.044 PubMedCrossRefGoogle Scholar
  119. Oh SA, Park KS, Twell D, Park SK (2010) The SIDECAR POLLEN gene encodes a microspore-specific LOB/AS2 domain protein required for the correct timing and orientation of asymmetric cell division. Plant J 64(5):839–850.  https://doi.org/10.1111/j.1365-313X.2010.04374.x PubMedCrossRefGoogle Scholar
  120. Oh SA, Jeon J, Park HJ, Grini PE, Twell D, Park SK (2016) Analysis of gemini pollen 3 mutant suggests a broad function of AUGMIN in microtubule organization during sexual reproduction in Arabidopsis. Plant J 87(2):188–201.  https://doi.org/10.1111/tpj.13192 PubMedCrossRefGoogle Scholar
  121. Okada T, Endo M, Singh MB, Bhalla PL (2005) Analysis of the histone H3 gene family in Arabidopsis and identification of the male-gamete-specific variant AtMGH3. Plant J 44(4):557–568.  https://doi.org/10.1111/j.1365-313X.2005.02554.x PubMedCrossRefGoogle Scholar
  122. Ono S, Liu H, Tsuda K, Fukai E, Tanaka K, Sasaki T, Nonomura KI (2018) EAT1 transcription factor, a non-cell-autonomous regulator of pollen production, activates meiotic small RNA biogene sis in rice anther tapetum. PLoS Genet (in press).Google Scholar
  123. Osman F, Bjoras M, Alseth I, Morland I, McCready S, Seeberg E, Tsaneva I (2003) A new Schizosaccharomyces pombe base excision repair mutant, nth1, reveals overlapping pathways for repair of DNA base damage. Mol Microbiol 48(2):465–480PubMedCrossRefGoogle Scholar
  124. Overmyer K, Brosché M, Kangasjärvi J (2003) Reactive oxygen species and hormonal control of cell death. Trends Plant Sci 8(7):335–342.  https://doi.org/10.1016/s1360-1385(03)00135-3 PubMedCrossRefGoogle Scholar
  125. Palmer RG (1971) Cytological studies of ameiotic and normal maize with reference to premeiotic pairing. Chromosoma 35:233–246CrossRefGoogle Scholar
  126. Pawlowski WP, Wang CJ, Golubovskaya IN, Szymaniak JM, Shi L, Hamant O, Zhu T, Harper L, Sheridan WF, Cande WZ (2009) Maize AMEIOTIC1 is essential for multiple early meiotic processes and likely required for the initiation of meiosis. Proc Natl Acad Sci U S A 106(9):3603–3608. doi:0810115106PubMedPubMedCentralCrossRefGoogle Scholar
  127. Peters B, Casey J, Aidley J, Zohrab S, Borg M, Twell D, Brownfield L (2017) A conserved cis-regulatory module determines germline fate through activation of the transcription factor DUO1 promoter. Plant Physiol 173(1):280–293.  https://doi.org/10.1104/pp.16.01192 PubMedCrossRefGoogle Scholar
  128. Prieto P, Santos AP, Moore G, Shaw P (2004) Chromosomes associate premeiotically and in xylem vessel cells via their telomeres and centromeres in diploid rice (Oryza sativa). Chromosoma 112(6):300–307.  https://doi.org/10.1007/s00412-004-0274-8 PubMedCrossRefGoogle Scholar
  129. Raghavan V (1988) Anther and pollen development in rice (Oryza sativa). Amer J Bot 75(2):183–196CrossRefGoogle Scholar
  130. Rey MD, Calderon MC, Prieto P (2015) The use of the ph1b mutant to induce recombination between the chromosomes of wheat and barley. Front Plant Sci 6:160.  https://doi.org/10.3389/fpls.2015.00160 PubMedPubMedCentralCrossRefGoogle Scholar
  131. Rotman N, Durbarry A, Wardle A, Yang WC, Chaboud A, Faure JE, Berger F, Twell D (2005) A novel class of MYB factors controls sperm-cell formation in plants. Curr Biol 15(3):244–248.  https://doi.org/10.1016/j.cub.2005.01.013 PubMedCrossRefGoogle Scholar
  132. Sakane I, Kamataki C, Takizawa Y, Nakashima M, Toki S, Ichikawa H, Ikawa S, Shibata T, Kurumizaka H (2008) Filament formation and robust strand exchange activities of the rice DMC1A and DMC1B proteins. Nucleic Acids Res 36(13):4266–4276.  https://doi.org/10.1093/nar/gkn405 PubMedPubMedCentralCrossRefGoogle Scholar
  133. Schiefthaler U, Balasubramanian S, Sieber P, Chevalier D, Wisman E, Schneitz K (1999) Molecular analysis of NOZZLE, a gene involved in pattern formation and early sporogenesis during sex organ development in Arabidopsis thaliana. Proc Natl Acad Sci U S A 96(20):11664–11669PubMedPubMedCentralCrossRefGoogle Scholar
  134. Schwartz EK, Wright WD, Ehmsen KT, Evans JE, Stahlberg H, Heyer WD (2012) Mus81-Mms4 functions as a single heterodimer to cleave nicked intermediates in recombinational DNA repair. Mol Cell Biol 32(15):3065–3080.  https://doi.org/10.1128/MCB.00547-12 PubMedPubMedCentralCrossRefGoogle Scholar
  135. Shao T, Tang D, Wang K, Wang M, Che L, Qin B, Yu H, Li M, Gu M, Cheng Z (2011) OsREC8 is essential for chromatid cohesion and metaphase I monopolar orientation in rice meiosis. Plant Physiol 156(3):1386–1396.  https://doi.org/10.1104/pp.111.177428 PubMedPubMedCentralCrossRefGoogle Scholar
  136. Shen Y, Tang D, Wang K, Wang M, Huang J, Luo W, Luo Q, Hong L, Li M, Cheng Z (2012) ZIP4 in homologous chromosome synapsis and crossover formation in rice meiosis. J Cell Sci 125(Pt 11):2581–2591.  https://doi.org/10.1242/jcs.090993 PubMedCrossRefGoogle Scholar
  137. Shi J, Tan H, Yu XH, Liu Y, Liang W, Ranathunge K, Franke RB, Schreiber L, Wang Y, Kai G, Shanklin J, Ma H, Zhang D (2011) Defective pollen wall is required for anther and microspore development in rice and encodes a fatty acyl carrier protein reductase. Plant Cell 23(6):2225–2246.  https://doi.org/10.1105/tpc.111.087528 PubMedPubMedCentralCrossRefGoogle Scholar
  138. Shingu Y, Tokai T, Agawa Y, Toyota K, Ahamed S, Kawagishi-Kobayashi M, Komatsu A, Mikawa T, Yamamoto MT, Wakasa K, Shibata T, Kusano K (2012) The double-stranded break-forming activity of plant SPO11s and a novel rice SPO11 revealed by a Drosophila bioassay. BMC Mol Biol 13:1.  https://doi.org/10.1186/1471-2199-13-1 PubMedPubMedCentralCrossRefGoogle Scholar
  139. Si W, Yuan Y, Huang J, Zhang X, Zhang Y, Zhang Y, Tian D, Wang C, Yang Y, Yang S (2015) Widely distributed hot and cold spots in meiotic recombination as shown by the sequencing of rice F2 plants. New Phytol 206(4):1491–1502.  https://doi.org/10.1111/nph.13319 PubMedCrossRefGoogle Scholar
  140. Spillane C, Curtis MD, Grossniklaus U (2004) Apomixis technology development-virgin births in farmers’ fields? Nat Biotechnol 22(6):687–691.  https://doi.org/10.1038/nbt976 PubMedCrossRefGoogle Scholar
  141. Sumiyoshi M, Inamura T, Nakamura A, Aohara T, Ishii T, Satoh S, Iwai H (2015) UDP-arabinopyranose mutase 3 is required for pollen wall morphogenesis in rice (Oryza sativa). Plant Cell Physiol 56(2):232–241.  https://doi.org/10.1093/pcp/pcu132 PubMedCrossRefGoogle Scholar
  142. Suzuki K, Aoki N, Matsumura H, Okamura M, Ohsugi R, Shimono H (2015) Cooling water before panicle initiation increases chilling-induced male sterility and disables chilling-induced expression of genes encoding OsFKBP65 and heat shock proteins in rice spikelets. Plant Cell Environ 38(7):1255–1274.  https://doi.org/10.1111/pce.12498 PubMedCrossRefGoogle Scholar
  143. Szostak JW, Orr-Weaver TL, Rothstein RJ, Stahl FW (1983) The double-strand-break repair model for recombination. Cell 33(1):25–35PubMedCrossRefGoogle Scholar
  144. Tan H, Liang W, Hu J, Zhang D (2012) MTR1 encodes a secretory fasciclin glycoprotein required for male reproductive development in rice. Dev Cell 22(6):1127–1137.  https://doi.org/10.1016/j.devcel.2012.04.011 PubMedCrossRefGoogle Scholar
  145. Tanaka N, Uraguchi S, Saito A, Kajikawa M, Kasai K, Sato Y, Nagamura Y, Fujiwara T (2013) Roles of pollen-specific boron efflux transporter, OsBOR4, in the rice fertilization process. Plant Cell Physiol 54(12):2011–2019.  https://doi.org/10.1093/pcp/pct136 PubMedCrossRefGoogle Scholar
  146. Tang D, Miao C, Li Y, Wang H, Liu X, Yu H, Cheng Z (2014) OsRAD51C is essential for double-strand break repair in rice meiosis. Front Plant Sci 5:167.  https://doi.org/10.3389/fpls.2014.00167 PubMedPubMedCentralCrossRefGoogle Scholar
  147. Tsubouchi H, Ogawa H (1998) A novel mre11 mutation impairs processing of double-strand breaks of DNA during both mitosis and meiosis. Mol Cell Biol 18(1):260–268PubMedPubMedCentralCrossRefGoogle Scholar
  148. Tsuji H, Aya K, Ueguchi-Tanaka M, Shimada Y, Nakazono M, Watanabe R, Nishizawa NK, Gomi K, Shimada A, Kitano H, Ashikari M, Matsuoka M (2006) GAMYB controls different sets of genes and is differentially regulated by microRNA in aleurone cells and anthers. Plant J 47(3):427–444.  https://doi.org/10.1111/j.1365-313X.2006.02795.x PubMedCrossRefGoogle Scholar
  149. Twell D, Park SK, Hawkins TJ, Schubert D, Schmidt R, Smertenko A, Hussey PJ (2002) MOR1/GEM1 has an essential role in the plant-specific cytokinetic phragmoplast. Nat Cell Biol 4(9):711–714.  https://doi.org/10.1038/ncb844 PubMedPubMedCentralCrossRefGoogle Scholar
  150. Ueda K, Ono M, Iwashita J, Wabiko H, Inoue M (2012) Generative cell-specific activation of the histone gH2A gene promoter of Lilium longiflorum in tobacco. Sex Plant Reprod 25(4):247–255.  https://doi.org/10.1007/s00497-012-0194-3 PubMedCrossRefGoogle Scholar
  151. Ueda K, Yoshimura F, Miyao A, Hirochika H, Nonomura KI, Wabiko H (2013) Collapsed abnormal pollen1 gene encoding the Arabinokinase-like protein is involved in pollen development in rice. Plant Physiol 162(2):858–871.  https://doi.org/10.1104/pp.113.216523 PubMedPubMedCentralCrossRefGoogle Scholar
  152. Vongs A, Kakutani T, Martienssen RA, Richards EJ (1993) Arabidopsis thaliana DNA methylation mutants. Science 260(5116):1926–1928PubMedCrossRefGoogle Scholar
  153. Wang A, Xia Q, Xie W, Dalta R, Selvaraj G (2003) The classical Ubisch bodies carry a sporophytically produced structural protein (RAFTIN) that is essential for pollen development. Proc Natl Acad Sci U S A 100(24):11487–11492CrossRefGoogle Scholar
  154. Wang Y, Magnard JL, McCormick S, Yang M (2004) Progression through meiosis I and meiosis II in Arabidopsis anthers is regulated by an A-type cyclin predominately expressed in prophase I. Plant Physiol 136(4):4127–4135.  https://doi.org/10.1104/pp.104.051201 PubMedPubMedCentralCrossRefGoogle Scholar
  155. Wang K, Tang D, Wang M, Lu J, Yu H, Liu J, Qian B, Gong Z, Wang X, Chen J, Gu M, Cheng Z (2009) MER3 is required for normal meiotic crossover formation, but not for presynaptic alignment in rice. J Cell Sci 122(Pt 12):2055–2063.  https://doi.org/10.1242/jcs.049080 PubMedCrossRefGoogle Scholar
  156. Wang M, Wang K, Tang D, Wei C, Li M, Shen Y, Chi Z, Gu M, Cheng Z (2010) The central element protein ZEP1 of the synaptonemal complex regulates the number of crossovers during meiosis in rice. Plant Cell 22(2):417–430.  https://doi.org/10.1105/tpc.109.070789 PubMedPubMedCentralCrossRefGoogle Scholar
  157. Wang K, Wang M, Tang D, Shen Y, Qin B, Li M, Cheng Z (2011a) PAIR3, an axis-associated protein, is essential for the recruitment of recombination elements onto meiotic chromosomes in rice. Mol Biol Cell 22(1):12–19.  https://doi.org/10.1091/mbc.E10-08-0667
  158. Wang M, Tang D, Wang K, Shen Y, Qin B, Miao C, Li M, Cheng Z (2011b) OsSGO1 maintains synaptonemal complex stabilization in addition to protecting centromeric cohesion during rice meiosis. Plant J 67(4):583–594.  https://doi.org/10.1111/j.1365-313X.2011.04615.x PubMedCrossRefGoogle Scholar
  159. Wang K, Wang M, Tang D, Shen Y, Miao C, Hu Q, Lu T, Cheng Z (2012a) The role of rice HEI10 in the formation of meiotic crossovers. PLoS Genet 8(7):e1002809.  https://doi.org/10.1371/journal.pgen.1002809 PubMedPubMedCentralCrossRefGoogle Scholar
  160. Wang M, Tang D, Luo Q, Jin Y, Shen Y, Wang K, Cheng Z (2012b) BRK1, a Bub1-related kinase, is essential for generating proper tension between homologous kinetochores at metaphase I of rice meiosis. Plant Cell 24(12):4961–4973.  https://doi.org/10.1105/tpc.112.105874 PubMedPubMedCentralCrossRefGoogle Scholar
  161. Wang H, Hu Q, Tang D, Liu X, Du G, Shen Y, Li Y, Cheng Z (2016) OsDMC1 is not required for homologous pairing in rice meiosis. Plant Physiol 171(1):230–241.  https://doi.org/10.1104/pp.16.00167 PubMedPubMedCentralCrossRefGoogle Scholar
  162. Wang C, Higgins JD, He Y, Lu P, Zhang D, Liang W (2017) Resolvase OsGEN1 mediates DNA repair by homologous recombination. Plant Physiol 173(2):1316–1329.  https://doi.org/10.1104/pp.16.01726 PubMedPubMedCentralCrossRefGoogle Scholar
  163. Wilson ZA, Zhang DB (2009) From Arabidopsis to rice: pathways in pollen development. J Exp Bot 60(5):1479–1492.  https://doi.org/10.1093/jxb/erp095 PubMedCrossRefGoogle Scholar
  164. Wojtasz L, Daniel K, Roig I, Bolcun-Filas E, Xu H, Boonsanay V, Eckmann CR, Cooke HJ, Jasin M, Keeney S, McKay MJ, Toth A (2009) Mouse HORMAD1 and HORMAD2, two conserved meiotic chromosomal proteins, are depleted from synapsed chromosome axes with the help of TRIP13 AAA-ATPase. PLoS Genet 5(10):e1000702.  https://doi.org/10.1371/journal.pgen.1000702 PubMedPubMedCentralCrossRefGoogle Scholar
  165. Wold MS (1997) Replication protein A: a heterotrimeric, single-stranded DNA-binding protein required for eukaryotic DNA metabolism. Annu Rev Biochem 66:61–92.  https://doi.org/10.1146/annurev.biochem.66.1.61 PubMedCrossRefGoogle Scholar
  166. Wu L, Guan Y, Wu Z, Yang K, Lv J, Converse R, Huang Y, Mao J, Zhao Y, Wang Z, Min H, Kan D, Zhang Y (2014) OsABCG15 encodes a membrane protein that plays an important role in anther cuticle and pollen exine formation in rice. Plant Cell Rep 33(11):1881–1899.  https://doi.org/10.1007/s00299-014-1666-8 PubMedPubMedCentralCrossRefGoogle Scholar
  167. Yamaki S, Nagato Y, Kurata N, Nonomura KI (2011) Ovule is a lateral organ finally differentiated from the terminating floral meristem in rice. Dev Biol 351(1):208–216.  https://doi.org/10.1016/j.ydbio.2010.12.006 PubMedCrossRefGoogle Scholar
  168. Yang WC, Ye D, Xu J, Sundaresan V (1999) The SPOROCYTELESS gene of Arabidopsis is required for initiation of sporogenesis and encodes a novel nuclear protein. Genes Dev 13(16):2108–2117PubMedPubMedCentralCrossRefGoogle Scholar
  169. Yang SL, Xie LF, Mao HZ, Puah CS, Yang WC, Jiang L, Sundaresan V, Ye D (2003) Tapetum determinant1 is required for cell specialization in the Arabidopsis anther. Plant Cell 15(12):2792–2804.  https://doi.org/10.1105/tpc.016618 PubMedPubMedCentralCrossRefGoogle Scholar
  170. Yang SL, Jiang L, Puah CS, Xie LF, Zhang XQ, Chen LQ, Yang WC, Ye D (2005) Overexpression of TAPETUM DETERMINANT1 alters the cell fates in the Arabidopsis carpel and tapetum via genetic interaction with excess microsporocytes1/extra sporogenous cells. Plant Physiol 139(1):186–191.  https://doi.org/10.1104/pp.105.063529 PubMedPubMedCentralCrossRefGoogle Scholar
  171. Yang Y, Ishino S, Yamagami T, Kumamaru T, Satoh H, Ishino Y (2012) The OsGEN-L protein from Oryza sativa possesses Holliday junction resolvase activity as well as 5′-flap endonuclease activity. J Biochem 151(3):317–327.  https://doi.org/10.1093/jb/mvr145 PubMedCrossRefGoogle Scholar
  172. Yang X, Wu D, Shi J, He Y, Pinot F, Grausem B, Yin C, Zhu L, Chen M, Luo Z, Liang W, Zhang D (2014) Rice CYP703A3, a cytochrome P450 hydroxylase, is essential for development of anther cuticle and pollen exine. J Integr Plant Biol 56(10):979–994.  https://doi.org/10.1111/jipb.12212 PubMedCrossRefGoogle Scholar
  173. Yang X, Liang W, Chen M, Zhang D, Zhao X, Shi J (2017) Rice fatty acyl-CoA synthetase OsACOS12 is required for tapetum programmed cell death and male fertility. Planta.  https://doi.org/10.1007/s00425-017-2691-y
  174. Yi J, An S, An G (2014) OsMLO12, encoding seven transmembrane proteins, is involved with pollen hydration in rice. Plant Reprod 27(4):169–180.  https://doi.org/10.1007/s00497-014-0249-8 PubMedCrossRefGoogle Scholar
  175. Yi J, Moon S, Lee YS, Zhu L, Liang W, Zhang D, Jung KH, An G (2016) Defective Tapetum cell death 1 (DTC1) regulates ROS levels by binding to metallothionein during tapetum degeneration. Plant Physiol 170(3):1611–1623.  https://doi.org/10.1104/pp.15.01561 PubMedGoogle Scholar
  176. Yoshimoto K (2012) Beginning to understand autophagy, an intracellular self-degradation system in plants. Plant Cell Physiol 53(8):1355–1365.  https://doi.org/10.1093/pcp/pcs099 PubMedCrossRefGoogle Scholar
  177. Yu H, Wang M, Tang D, Wang K, Chen F, Gong Z, Gu M, Cheng Z (2010) OsSPO11-1 is essential for both homologous chromosome pairing and crossover formation in rice. Chromosoma 119(6):625–636.  https://doi.org/10.1007/s00412-010-0284-7 PubMedCrossRefGoogle Scholar
  178. Zhai J, Zhang H, Arikit S, Huang K, Nan GL, Walbot V, Meyers BC (2015) Spatiotemporally dynamic, cell-type-dependent premeiotic and meiotic phasiRNAs in maize anthers. Proc Natl Acad Sci U S A 112(10):3146–3151.  https://doi.org/10.1073/pnas.1418918112 PubMedPubMedCentralCrossRefGoogle Scholar
  179. Zhang Z, Lu Y, Feng J (2005) Nuclear and cell migration during pollen development in rice (Oryza sativa L.) Sex Plant Reprod 17:297–302CrossRefGoogle Scholar
  180. Zhang L, Tao J, Wang S, Chong K, Wang T (2006) The rice OsRad21-4, an orthologue of yeast Rec8 protein, is required for efficient meiosis. Plant Mol Biol 60(4):533–554.  https://doi.org/10.1007/s11103-005-4922-z PubMedCrossRefGoogle Scholar
  181. Zhang D, Liang W, Yin C, Zong J, Gu F, Zhang D (2010) OsC6, encoding a lipid transfer protein, is required for postmeiotic anther development in rice. Plant Physiol 154(1):149–162.  https://doi.org/10.1104/pp.110.158865 PubMedPubMedCentralCrossRefGoogle Scholar
  182. Zhang J, Pawlowski WP, Han F (2013) Centromere pairing in early meiotic prophase requires active centromeres and precedes installation of the synaptonemal complex in maize. Plant Cell 25(10):3900–3909.  https://doi.org/10.1105/tpc.113.117846 PubMedPubMedCentralCrossRefGoogle Scholar
  183. Zhang B, Wang M, Tang D, Li Y, Xu M, Gu M, Cheng Z, Yu H (2015) XRCC3 is essential for proper double-strand break repair and homologous recombination in rice meiosis. J Exp Bot 66(19):5713–5725.  https://doi.org/10.1093/jxb/erv253 PubMedCrossRefGoogle Scholar
  184. Zhao DZ, Wang GF, Speal B, Ma H (2002) The excess microsporocytes1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. Genes Dev 16(15):2021–2031.  https://doi.org/10.1101/gad.997902 PubMedPubMedCentralCrossRefGoogle Scholar
  185. Zhao X, de Palma J, Oane R, Gamuyao R, Luo M, Chaudhury A, Herve P, Xue Q, Bennett J (2008) OsTDL1A binds to the LRR domain of rice receptor kinase MSP1, and is required to limit sporocyte numbers. Plant J 54(3):375–387. doi:TPJ3426PubMedPubMedCentralCrossRefGoogle Scholar
  186. Zhao G, Shi J, Liang W, Xue F, Luo Q, Zhu L, Qu G, Chen M, Schreiber L, Zhang D (2015) Two ATP binding cassette G transporters, rice ATP binding cassette G26 and ATP binding cassette G15, collaboratively regulate rice male reproduction. Plant Physiol 169(3):2064–2079.  https://doi.org/10.1104/pp.15.00262 PubMedPubMedCentralGoogle Scholar
  187. Zickler D, Kleckner N (2016) A few of our favorite things: pairing, the bouquet, crossover interference and evolution of meiosis. Semin Cell Dev Biol 54:135–148.  https://doi.org/10.1016/j.semcdb.2016.02.024 PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  1. 1.Experimental FarmNational Institute of GeneticsMishimaJapan
  2. 2.Department of Life ScienceGraduate University for Advanced Studies/SOKENDAIMishimaJapan
  3. 3.Department of Biological Production, Faculty of Bioresource SciencesAkita Prefectural UniversityAkitaJapan

Personalised recommendations