1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Plant Biology
  4. Volume 67, 2016
  5. Article

Annual Review of Plant Biology

Volume 67, 2016

Pre-Meiotic Anther Development: Cell Fate Specification and Differentiation

Abstract

Research into anther ontogeny has been an active and developing field, transitioning from a strictly lineage-based view of cellular differentiation events to a more complex understanding of cell fate specification. Here we describe the modern interpretation of pre-meiotic anther development, from the earliest cell specifications within the anther lobes through /-, -, and -dependent pathways as well as the initial setup of the abaxial and adaxial axes and outgrowth of the anther lobes. We then continue with a look at the known information regarding further differentiation of the somatic layers of the anther (the epidermis, endothecium, middle layer, and tapetum), with an emphasis on male-sterile mutants identified as defective in somatic cell specification. We also describe the differences in developmental stages among species and use this information to discuss molecular studies that have analyzed transcriptome, proteome, and small-RNA information in the anther.

Keyword(s): archesporial cell, lineage, parietal cell, periclinal division, transcriptome

[Erratum, Closure]

An erratum has been published for this article:
Pre-Meiotic Anther Development: Cell Fate Specification and Differentiation
Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-043015-111804
2016-04-29
2024-05-04
Loading full text...

Full text loading...

/deliver/fulltext/arplant/67/1/annurev-arplant-043015-111804.html?itemId=/content/journals/10.1146/annurev-arplant-043015-111804&mimeType=html&fmt=ahah

Literature Cited

  1. Albertsen M, Fox T, Trimnell M, Wu Y, Lowe K. 1.  et al. 2011. MSCA1 nucleotide sequences impacting male fertility and method of using same US Patent No. 7915478 B2
  2. Albrecht C, Russinova E, Hecht V, Baaijens E, de Vries S. 2.  2005. The Arabidopsis thaliana SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASES1 and 2 control male sporogenesis. Plant Cell 17:3337–49 [Google Scholar]
  3. Aya K, Suzuki G, Suwabe K, Hobo T, Takahashi H. 3.  et al. 2011. Comprehensive network analysis of anther-expressed genes in rice by the combination of 33 laser microdissection and 143 spatiotemporal microarrays. PLOS ONE 6:e26162 [Google Scholar]
  4. Bedinger P, Fowler J. 4.  2009. The maize male gametophyte. Handbook of Maize: Its Biology JL Bennetzen, SC Hake 57–77 New York: Springer [Google Scholar]
  5. Berger F, Twell D. 5.  2011. Germline specification and function in plants. Annu. Rev. Plant Biol. 62:461–84 [Google Scholar]
  6. Boateng K, Yang X, Dong F, Owen H, Makaroff C. 6.  2008. SWI1 is required for meiotic chromosome remodeling events. Mol. Plant 1:620–33 [Google Scholar]
  7. Bommert P, Satoh-Nagasawa N, Jackson D, Hirano HY. 7.  2005. Genetics and evolution of inflorescence and flower development in grasses. Plant Cell Physiol. 46:69–78 [Google Scholar]
  8. Borg M, Berger F. 8.  2015. Chromatin remodelling during male gametophyte development. Plant J. 83:177–88 [Google Scholar]
  9. Borg M, Brownfield L, Twell D. 9.  2009. Male gametophyte development: a molecular perspective. J. Exp. Bot. 60:1465–78 [Google Scholar]
  10. Bowman JL, Drews GN, Meyerowitz EM. 10.  1991. Expression of the Arabidopsis floral homeotic gene AGAMOUS is restricted to specific cell types late in flower development. Plant Cell 3:749–58 [Google Scholar]
  11. Bowman JL, Smyth DR, Meyerowitz EM. 11.  2012. The ABC model of flower development: then and now. Development 139:4095–98 [Google Scholar]
  12. Canales C, Bhatt AM, Scott R, Dickinson H. 12.  2002. EXS, a putative LRR receptor kinase, regulates male germline cell number and tapetal identity and promotes seed development in Arabidopsis. Curr. Biol. 12:1718–27 [Google Scholar]
  13. Chang F, Wang Y, Wang S, Ma H. 13.  2011. Molecular control of microsporogenesis in Arabidopsis. Curr. Opin. Plant Biol. 14:66–73 [Google Scholar]
  14. Chaubal R, Anderson JR, Trimnell MR, Fox TW, Albertsen MC, Bedinger P. 14.  2003. The transformation of anthers in the msca1 mutant of maize. Planta 216:778–88 [Google Scholar]
  15. Chaubal R, Zanella C, Trimnell MR, Fox TW, Albertsen MC, Bedinger P. 15.  2000. Two male-sterile mutants of Zea mays (Poaceae) with an extra cell division in the anther wall. Am. J. Bot. 87:1193–1201 [Google Scholar]
  16. Clement C, Burrus M, Audran J. 16.  2015. Floral organ growth and carbohydrate content during pollen development in Lillium. Am. J. Bot. 83:459–69 [Google Scholar]
  17. Colcombet J, Boisson-Dernier A, Ros-Palau R, Vera CE, Schroeder JI. 17.  2005. Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASES1 and 2 are essential for tapetum development and microspore maturation. Plant Cell 17:3350–61 [Google Scholar]
  18. Couteau F, Belzile F, Horlow C, Grandjean O, Vezon D, Doutriaux MP. 18.  1999. Random chromosome segregation without meiotic arrest in both male and female meiocytes of a dmc1 mutant of Arabidopsis. Plant Cell 11:1623–34 [Google Scholar]
  19. D'Arcy WG, Keating R. 19.  1996. The Anther: Form, Function, Phylogeny Cambridge, UK: Cambridge Univ. Press
  20. Deveshwar P, Bovill WD, Sharma R, Able J, Kapoor S. 20.  2011. Analysis of anther transcriptomes to identify genes contributing to meiosis and male gametophyte development in rice. BMC Plant Biol. 11:78 [Google Scholar]
  21. Ding J, Lu Q, Ouyang Y, Mao H, Zhang P. 21.  et al. 2012. A long noncoding RNA regulates photoperiod-sensitive male sterility, an essential component of hybrid rice. PNAS 109:2654–59 [Google Scholar]
  22. Dinneny JR, Weigel D, Yanofsky MF. 22.  2006. NUBBIN and JAGGED define stamen and carpel shape in Arabidopsis. Development 133:1645–55 [Google Scholar]
  23. Feng B, Lu D, Ma X, Peng Y, Sun Y. 23.  et al. 2012. Regulation of the Arabidopsis anther transcriptome by DYT1 for pollen development. Plant J. 72:612–24 [Google Scholar]
  24. Feng X, Dickinson HG. 24.  2007. Packaging the male germline in plants. Trends Genet. 23:503–10 [Google Scholar]
  25. Feng X, Dickinson HG. 25.  2010. Tapetal cell fate, lineage and proliferation in the Arabidopsis anther. Development 137:2409–16 [Google Scholar]
  26. Fu Z, Yu J, Cheng X, Zong X, Xu J. 26.  et al. 2014. The rice basic helix-loop-helix transcription factor TDR INTERACTING PROTEIN2 is a central switch in early anther development. Plant Cell 26:1512–24 [Google Scholar]
  27. Golubovskaya IN, Hamant O, Timofejeva L, Wang CJR, Braun D. 27.  et al. 2006. Alleles of afd1 dissect REC8 functions during meiotic prophase I. J. Cell Sci. 119:3306–15 [Google Scholar]
  28. Grandont L, Jenczewski E, Lloyd A. 28.  2013. Meiosis and its deviations in polyploid plants. Cytogenet. Genome Res. 140:171–84 [Google Scholar]
  29. Grelon M. 29.  2014. The molecular biology of meiosis in plants. Annu. Rev. Plant Biol. 66:297–327 [Google Scholar]
  30. Hamant O, Ma H, Cande WZ. 30.  2006. Genetics of meiotic prophase I in plants. Annu. Rev. Plant Biol. 57:267–302 [Google Scholar]
  31. Hong L, Tang D, Shen Y, Hu Q, Wang K. 31.  et al. 2012. MIL2 (MICROSPORELESS2) regulates early cell differentiation in the rice anther. New Phytol. 196:402–13 [Google Scholar]
  32. Hong L, Tang D, Zhu K, Wang K, Li M, Cheng Z. 32.  2012. Somatic and reproductive cell development in rice anther is regulated by a putative glutaredoxin. Plant Cell 24:577–88 [Google Scholar]
  33. Honys D, Twell D. 33.  2004. Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol. 5:R85 [Google Scholar]
  34. Hord CLH, Chen C, Deyoung BJ, Clark SE. 34.  2006. The BAM1/BAM2 receptor-like kinases are important regulators of Arabidopsis early anther development. Plant Cell 18:1667–80 [Google Scholar]
  35. Hord CLH, Sun YJ, Pillitteri LJ, Torii KU, Wang H. 35.  et al. 2008. Regulation of Arabidopsis early anther development by the mitogen-activated protein kinases, MPK3 and MPK6, and the ERECTA and related receptor-like kinases. Mol. Plant 1:645–58 [Google Scholar]
  36. Ischebeck T, Valledor L, Lyon D, Gingl S, Nagler M. 36.  et al. 2014. Comprehensive cell-specific protein analysis in early and late pollen development from diploid microsporocytes to pollen tube growth. Mol. Cell. Proteom. 13:295–310 [Google Scholar]
  37. Ito T, Wellmer F, Yu H, Das P, Ito N. 37.  et al. 2004. The homeotic protein AGAMOUS controls microsporogenesis by regulation of SPOROCYTELESS. Nature 430:356–60 [Google Scholar]
  38. Ji C, Li H, Chen L, Xie M, Wang F, Liu Y. 38.  2013. A novel rice bHLH transcription factor, DTD, acts coordinately with TDR in controlling tapetum function and pollen development. Mol. Plant 6:1715–18 [Google Scholar]
  39. Jia G, Liu X, Owen H, Zhao D. 39.  2008. Signaling of cell fate determination by the TPD1 small protein and EMS1 receptor kinase. PNAS 105:2220–25 [Google Scholar]
  40. Johnson C, Kasprzewska A, Tennessen K, Fernandes J, Nan GL. 40.  et al. 2009. Clusters and superclusters of phased small RNAs in the developing inflorescence of rice. Genome Res. 19:1429–40 [Google Scholar]
  41. Jung K-H, Han M-J, Lee Y-S, Kim Y-W, Hwang I. 41.  et al. 2005. Rice Undeveloped Tapetum1 is a major regulator of early tapetum development. Plant Cell 17:2705–22 [Google Scholar]
  42. Kelliher T, Egger RL, Zhang H, Walbot V. 42.  2014. Unresolved issues in pre-meiotic anther development. Front. Plant Sci. 5:347 [Google Scholar]
  43. Kelliher T, Walbot V. 43.  2011. Emergence and patterning of the five cell types of the Zea mays anther locule. Dev. Biol. 350:32–49 [Google Scholar]
  44. Kelliher T, Walbot V. 44.  2012. Hypoxia triggers meiotic fate acquisition in maize. Science 337:345–48 [Google Scholar]
  45. Kelliher T, Walbot V. 45.  2014. Maize germinal cell initials accommodate hypoxia and precociously express meiotic genes. Plant J. 77:639–52 [Google Scholar]
  46. Ko S-S, Li M-J, Ku MS-B, Ho Y-C, Lin Y-J. 46.  et al. 2014. The bHLH142 transcription factor coordinates with TDR1 to modulate the expression of EAT1 and regulate pollen development in rice. Plant Cell 26:2486–504 [Google Scholar]
  47. Komiya R, Ohyanagi H, Niihama M, Watanabe T, Nakano M. 47.  et al. 2014. Rice germline-specific Argonaute MEL1 protein binds to phasiRNAs generated from more than 700 lincRNAs. Plant J. 78:385–97 [Google Scholar]
  48. Li N, Zhang D-S, Liu H-S, Yin C-S, Li X. 48.  et al. 2006. The rice Tapetum Degeneration Retardation gene is required for tapetum degradation and anther development. Plant Cell 18:2999–3014 [Google Scholar]
  49. Li S, Lauri A, Ziemann M, Busch A, Bhave M, Zachgo S. 49.  2009. Nuclear activity of ROXY1, a glutaredoxin interacting with TGA factors, is required for petal development in Arabidopsis thaliana. Plant Cell 21:429–41 [Google Scholar]
  50. Liu J, Pang C, Wei H, Song M, Meng Y. 50.  et al. 2015. iTRAQ-facilitated proteomic profiling of anthers from a photosensitive male sterile mutant and wild-type cotton (Gossypium hirsutum L.). J. Proteom. 126:68–81 [Google Scholar]
  51. Liu X, Huang J, Parameswaran S, Ito T, Seubert B. 51.  et al. 2009. The SPOROCYTELESS/NOZZLE gene is involved in controlling stamen identity in Arabidopsis. Plant Physiol. 151:1401–11 [Google Scholar]
  52. Liu Z, Bao W, Liang W, Yin J, Zhang D. 52.  2010. Identification of gamyb-4 and analysis of the regulatory role of GAMYB in rice anther development. J. Integr. Plant Biol. 52:670–78 [Google Scholar]
  53. Lu XC, Gong HQ, Huang ML, Bai SL, He YB. 53.  et al. 2006. Molecular analysis of early rice stamen development using organ-specific gene expression profiling. Plant Mol. Biol. 61:845–61 [Google Scholar]
  54. Ma H. 54.  2005. Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu. Rev. Plant Biol. 56:393–434 [Google Scholar]
  55. Ma J, Duncan D, Morrow DJ, Fernandes J, Walbot V. 55.  2007. Transcriptome profiling of maize anthers using genetic ablation to analyze pre-meiotic and tapetal cell types. Plant J. 50:637–48 [Google Scholar]
  56. Ma J, Morrow DJ, Fernandes J, Walbot V. 56.  2006. Comparative profiling of the sense and antisense transcriptome of maize lines. Genome Biol. 7:R22 [Google Scholar]
  57. Ma J, Skibbe DS, Fernandes J, Walbot V. 57.  2008. Male reproductive development: gene expression profiling of maize anther and pollen ontogeny. Genome Biol. 9:R181 [Google Scholar]
  58. Ma X, Feng B, Ma H. 58.  2012. AMS-dependent and independent regulation of anther transcriptome and comparison with those affected by other Arabidopsis anther genes. BMC Plant Biol. 12:23 [Google Scholar]
  59. Mandaokar A, Thines B, Shin B, Lange BM, Choi G. 59.  et al. 2006. Transcriptional regulators of stamen development in Arabidopsis identified by transcriptional profiling. Plant J. 46:984–1008 [Google Scholar]
  60. Mercier R, Armstrong SJ, Horlow C, Jackson NP, Makaroff C. 60.  et al. 2003. The meiotic protein SWI1 is required for axial element formation and recombination initiation in Arabidopsis. Development 130:3309–18 [Google Scholar]
  61. Millar A, Gubler F. 61.  2005. The Arabidopsis GAMYB-LIKE genes, MYB33 and MYB65, are microRNA-regulated genes that redundantly facilitate anther development. Plant Cell 17:705–21 [Google Scholar]
  62. Moon J, Skibbe D, Timofejeva L, Wang CJR, Kelliher T. 62.  et al. 2013. Regulation of cell divisions and differentiation by MALE STERILITY32 is required for anther development in maize. Plant J. 76:592–602 [Google Scholar]
  63. Murmu J, Bush MJ, DeLong C, Li S, Xu M. 63.  et al. 2010. Arabidopsis bZIP transcription factors TGA9 and TGA10 interact with floral glutaredoxins ROXY1 and ROXY2 and are redundantly required for anther development. Plant Physiol. 154:1492–1504 [Google Scholar]
  64. Murphy KM, Egger RL, Walbot V. 64.  2015. Chloroplasts in anther endothecium of Zea mays (Poaceae). Am. J. Bot. 102:1931–37 [Google Scholar]
  65. Nan G-L, Ronceret A, Wang RC, Fernandes JF, Cande WZ, Walbot V. 65.  2011. Global transcriptome analysis of two ameiotic1 alleles in maize anthers: defining steps in meiotic entry and progression through prophase I. BMC Plant Biol. 11:120 [Google Scholar]
  66. Niu N, Liang W, Yang X, Jin W, Wilson Z. 66.  et al. 2013. EAT1 promotes tapetal cell death by regulating aspartic proteases during male reproductive development in rice. Nat. Commun. 4:1445 [Google Scholar]
  67. Nonomura K-I, Miyoshi K, Eiguchi M, Suzuki T, Miyao A. 67.  et al. 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 15:1728–39 [Google Scholar]
  68. Nonomura K-I, Morohoshi A, Nakano M, Eiguchi M, Miyao A. 68.  et al. 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 19:2583–94 [Google Scholar]
  69. Parish RW, Li SF. 69.  2010. Death of a tapetum: a programme of developmental altruism. Plant Sci. 178:73–89 [Google Scholar]
  70. Pearce S, Ferguson A, King J, Wilson ZA. 70.  2015. FlowerNet: a gene expression correlation network for anther and pollen development. Plant Physiol. 167:1717–30 [Google Scholar]
  71. Raghavan V. 71.  1988. Anther and pollen development in rice (Oryza sativa). Am. J. Bot. 75:183–96 [Google Scholar]
  72. Risso D, Ngai J, Speed TP, Dudoit S. 72.  2014. Normalization of RNA-seq data using factor analysis of control genes or samples. Nat. Biotechnol. 32:1–10 [Google Scholar]
  73. Rogers K, Chen X. 73.  2013. Biogenesis, turnover, and mode of action of plant microRNAs. Plant Cell 25:2383–99 [Google Scholar]
  74. Ronceret A, Doutriaux M-P, Golubovskaya IN, Pawlowski WP. 74.  2009. PHS1 regulates meiotic recombination and homologous chromosome pairing by controlling the transport of RAD50 to the nucleus. PNAS 106:20121–26 [Google Scholar]
  75. Russell SD, Jones DS. 75.  2015. The male germline of angiosperms: repertoire of an inconspicuous but important cell lineage. Front. Plant Sci. 6:173 [Google Scholar]
  76. Sanders PM, Bui AQ, Weterings K, McIntire KN, Hsu YC. 76.  et al. 1999. Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex. Plant Reprod. 11:297–322 [Google Scholar]
  77. Schiefthaler U, Balasubramanian S, Sieber P, Chevalier D, Wisman E, Schneitz K. 77.  1999. Molecular analysis of NOZZLE, a gene involved in pattern formation and early sporogenesis during sex organ development in Arabidopsis thaliana. PNAS 96:11664–69 [Google Scholar]
  78. Scott RJ, Spielman M, Dickinson HG. 78.  2004. Stamen structure and function. Plant Cell 16:Suppl.S46–60 [Google Scholar]
  79. Sessions A, Nemhauser JL, McColl A, Roe JL, Feldmann KA, Zambryski PC. 79.  1997. ETTIN patterns the Arabidopsis floral meristem and reproductive organs. Development 124:4481–91 [Google Scholar]
  80. Sheridan WF, Golubeva E, Abrhamova LI, Golubovskaya IN. 80.  1999. The mac1 mutation alters the developmental fate of the hypodermal cells and their cellular progeny in the maize anther. Genetics 153:933–41 [Google Scholar]
  81. Skibbe DS, Doehlemann G, Fernandes J, Walbot V. 81.  2010. Maize tumors caused by Ustilago maydis require organ-specific genes in host and pathogen. Science 328:89–92 [Google Scholar]
  82. Skibbe DS, Fernandes JF, Medzihradszky KF, Burlingame AL, Walbot V. 82.  2009. Mutator transposon activity reprograms the transcriptomes and proteomes of developing maize anthers. Plant J. 59:622–33 [Google Scholar]
  83. Slotkin RK, Vaughn M, Borges F, Tanurdžić M, Becker JD. 83.  et al. 2009. Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136:461–72 [Google Scholar]
  84. Smyth DR, Bowman JL, Meyerowitz EM. 84.  1990. Early flower development in Arabidopsis. Plant Cell 2:755–67 [Google Scholar]
  85. Song X, Li P, Zhai J, Zhou M, Ma L. 85.  et al. 2012. Roles of DCL4 and DCL3B in rice phased small RNA biogenesis. Plant J. 69:462–74 [Google Scholar]
  86. Sorensen AM, Kröber S, Unte US, Huijser P, Dekker K, Saedler H. 86.  2003. The Arabidopsis ABORTED MICROSPORES (AMS) gene encodes a MYC class transcription factor. Plant J. 33:413–23 [Google Scholar]
  87. Suwabe K, Suzuki G, Takahashi H, Shiono K, Endo M. 87.  et al. 2008. Separated transcriptomes of male gametophyte and tapetum in rice: validity of a laser microdissection (LM) microarray. Plant Cell Physiol. 49:1407–16 [Google Scholar]
  88. Tanaka W, Pautler M, Jackson D, Hirano HY. 88.  2013. Grass meristems II: inflorescence architecture, flower development and meristem fate. Plant Cell Physiol. 54:313–24 [Google Scholar]
  89. Tang X, Zhang Z-Y, Zhang W-J, Zhao X-M, Li X. 89.  et al. 2010. Global gene profiling of laser-captured pollen mother cells indicates molecular pathways and gene subfamilies involved in rice meiosis. Plant Physiol. 154:1855–70 [Google Scholar]
  90. Timmermans MC, Schultes NP, Jankovsky JP, Nelson T. 90.  1998. Leafbladeless1 is required for dorsoventrality of lateral organs in maize. Development 125:2813–23 [Google Scholar]
  91. Timofejeva L, Skibbe DS, Lee S, Golubovskaya I, Wang R. 91.  et al. 2013. Cytological characterization and allelism testing of anther developmental mutants identified in a screen of maize male sterile lines. G3 3:231–49 [Google Scholar]
  92. Toriba T, Suzaki T, Yamaguchi T, Ohmori Y, Tsukaya H, Hirano H-Y. 92.  2010. Distinct regulation of adaxial-abaxial polarity in anther patterning in rice. Plant Cell 22:1452–62 [Google Scholar]
  93. Vernoud V, Laigle G, Rozier F, Meeley RB, Perez P, Rogowsky PM. 93.  2009. The HD-ZIP IV transcription factor OCL4 is necessary for trichome patterning and anther development in maize. Plant J. 59:883–94 [Google Scholar]
  94. Wang CJR, Nan GL, Kelliher T, Timofejeva L, Vernoud V. 94.  et al. 2012. Maize multiple archesporial cells 1 (mac1), an ortholog of rice TDL1A, modulates cell proliferation and identity in early anther development. Development 139:2594–603 [Google Scholar]
  95. Wang D, Adams CM, Fernandes JF, Egger RL, Walbot V. 95.  2012. A low molecular weight proteome comparison of fertile and male sterile 8 anthers of Zea mays. Plant Biotechnol. J. 10:925–35 [Google Scholar]
  96. Wang D, Oses-Prieto JA, Li KH, Fernandes JF, Burlingame AL, Walbot V. 96.  2010. The male sterile 8 mutation of maize disrupts the temporal progression of the transcriptome and results in the mis-regulation of metabolic functions. Plant J. 63:939–51 [Google Scholar]
  97. Wang D, Skibbe DS, Walbot V. 97.  2011. Maize csmd1 exhibits pre-meiotic somatic and post-meiotic microspore and somatic defects but sustains anther growth. Sex. Plant Reprod. 24:297–306 [Google Scholar]
  98. Wang D, Skibbe DS, Walbot V. 98.  2013. Maize male sterile 8 (ms8), a putative β-1,3-galactosyltransferase, modulates cell division, expansion, and differentiation during early maize anther development. Plant Reprod. 26:329–38 [Google Scholar]
  99. Wei B, Zhang J, Pang C, Yu H, Guo D. 99.  et al. 2014. The molecular mechanism of SPOROCYTELESS/NOZZLE in controlling Arabidopsis ovule development. Cell Res. 25:121–34 [Google Scholar]
  100. Wellmer F, Riechmann L, Alves-Ferreira M, Meyerowitz EM. 100.  2004. Genome-wide analysis of spatial gene expression in Arabidopsis flowers. Plant Cell 16:1314–26 [Google Scholar]
  101. Wilson ZA, Zhang DB. 101.  2009. From Arabidopsis to rice: pathways in pollen development. J. Exp. Bot. 60:1479–92 [Google Scholar]
  102. Xing S, Salinas M, Huijser P. 102.  2011. New players unveiled in early anther development. Plant Signal. Behav. 6:934–38 [Google Scholar]
  103. Xing S, Zachgo S. 103.  2008. ROXY1 and ROXY2, two Arabidopsis glutaredoxin genes, are required for anther development. Plant J. 53:790–801 [Google Scholar]
  104. Xu J, Ding Z, Vizcay-Barrena G, Shi J, Liang W. 104.  et al. 2014. ABORTED MICROSPORES acts as a master regulator of pollen wall formation in Arabidopsis. Plant Cell 26:1544–56 [Google Scholar]
  105. Yan J, Tian H, Wang S, Shao J, Zheng Y. 105.  et al. 2014. Pollen developmental defects in ZD-CMS rice line explored by cytological, molecular and proteomic approaches. J. Proteom. 108:110–23 [Google Scholar]
  106. Yang S-L, Jiang L, Puah CS, Xie L-F, Zhang X-Q. 106.  et al. 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. 139:186–91 [Google Scholar]
  107. Yang S-L, Xie L, Mao H, Puah CS, Yang W. 107.  et al. 2003. TAPETUM DETERMINANT1 is required for cell specialization in the Arabidopsis anther. Plant Cell 15:2792–804 [Google Scholar]
  108. Yang W-C, Ye D, Xu J, Sundaresan V. 108.  1999. The SPOROCYTELESS gene of Arabidopsis is required for initation of sporogenesis and encodes a novel nuclear protein. Genes Dev. 13:2108–17 [Google Scholar]
  109. Yi J, Kim SR, Lee DY, Moon S, Lee YS. 109.  et al. 2012. The rice gene DEFECTIVE TAPETUM AND MEIOCYTES 1 (DTM1) is required for early tapetum development and meiosis. Plant J. 70:256–70 [Google Scholar]
  110. Zhai J, Zhang H, Arikit S, Huang K, Nan G-L. 110.  et al. 2015. Spatiotemporally dynamic, cell-type-dependent premeiotic and meiotic phasiRNAs in maize anthers. PNAS 112:3146–51 [Google Scholar]
  111. Zhang D, Luo X, Zhu L. 111.  2011. Cytological analysis and genetic control of rice anther development. J. Genet. Genom. 38:379–90 [Google Scholar]
  112. Zhang D, Yang L. 112.  2014. Specification of tapetum and microsporocyte cells within the anther. Curr. Opin. Plant Biol. 17:49–55 [Google Scholar]
  113. Zhang DS, Liang WQ, Yuan Z, Li N, Shi J. 113.  et al. 2008. Tapetum Degeneration Retardation is critical for aliphatic metabolism and gene regulation during rice pollen development. Mol. Plant 1:599–610 [Google Scholar]
  114. Zhang H, Egger RL, Kelliher T, Morrow D, Fernandes J. 114.  et al. 2014. Transcriptomes and proteomes define gene expression progression in pre-meiotic maize anthers. G3 4:993–1010 [Google Scholar]
  115. Zhang W, Sun Y, Timofejeva L, Chen C, Grossniklaus U, Ma H. 115.  2006. Regulation of Arabidopsis tapetum development and function by DYSFUNCTIONAL TAPETUM1 (DYT1) encoding a putative bHLH transcription factor. Development 133:3085–95 [Google Scholar]
  116. Zhao DZ. 116.  2009. Control of anther cell differentiation: a teamwork of receptor-like kinases. Sex. Plant Reprod. 22:221–28 [Google Scholar]
  117. Zhao DZ, Wang GF, Speal B, Ma H. 117.  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. 16:2021–31 [Google Scholar]
  118. Zhao X, De Palma J, Oane R, Gamuyao R, Luo M. 118.  et al. 2008. OsTDL1A binds to the LRR domain of rice receptor kinase MSP1, and is required to limit sporocyte numbers. Plant J. 54:375–87 [Google Scholar]
  119. Zhu E, You C, Wang S, Cui J, Niu B. 119.  et al. 2015. The DYT1-interacting proteins bHLH010, bHLH089, and bHLH091 are redundantly required for Arabidopsis anther development and transcriptome. Plant J. 83:976–90 [Google Scholar]
  120. Zhu J, Chen H, Li H, Gao JF, Jiang H. 120.  et al. 2008. Defective in Tapetal Development and Function 1 is essential for anther development and tapetal function for microspore maturation in Arabidopsis. Plant J. 55:266–77 [Google Scholar]
/content/journals/10.1146/annurev-arplant-043015-111804
Loading
Pre-Meiotic Anther Development: Cell Fate Specification and Differentiation
Annual Review of Plant Biology 67, 365 (2016); https://doi.org/10.1146/annurev-arplant-043015-111804
/content/journals/10.1146/annurev-arplant-043015-111804
/content/journals/10.1146/annurev-arplant-043015-111804
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error