1932

Abstract

The grass family is one of the largest families in angiosperms and has evolved a characteristic inflorescence morphology, with complex branches and specialized spikelets. The origin and development of the highly divergent inflorescence architecture in grasses have recently received much attention. Increasing evidence has revealed that numerous factors, such as transcription factors and plant hormones, play key roles in determining reproductive meristem fate and inflorescence patterning in grasses. Moreover, some molecular switches that have been implicated in specifying inflorescence shapes contribute significantly to grain yields in cereals. Here, we review key genetic and molecular switches recently identified from two model grass species, rice () and maize (), that regulate inflorescence morphology specification, including meristem identity, meristem size and maintenance, initiation and outgrowth of axillary meristems, and organogenesis. Furthermore, we summarize emerging networks of genes and pathways in grass inflorescence morphogenesis and emphasize their evolutionary divergence in comparison with the model eudicot We also discuss the agricultural application of genes controlling grass inflorescence development.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-050213-040104
2014-04-29
2024-06-25
Loading full text...

Full text loading...

/deliver/fulltext/arplant/65/1/annurev-arplant-050213-040104.html?itemId=/content/journals/10.1146/annurev-arplant-050213-040104&mimeType=html&fmt=ahah

Literature Cited

  1. Abbe E, Phinney B. 1.  1951. The growth of the shoot apex in maize: external features.. Am. J. Bot. 38:737–44 [Google Scholar]
  2. Argueso CT, Raines T, Kieber JJ. 2.  2010. Cytokinin signaling and transcriptional networks. Curr. Opin. Plant Biol. 13:533–39 [Google Scholar]
  3. Ashikari M, Sakakibara H, Lin S, Yamamoto T, Takashi T. 3.  et al. 2005. Cytokinin oxidase regulates rice grain production. Science 309:741–45 [Google Scholar]
  4. Bates C. 4.  2007. Thiamine. Handbook of Vitamins J Zempleni, R Rucker, D McCormick, J Suttie 252–88 Boca Raton, FL: CRC [Google Scholar]
  5. Barazesh S, McSteen P. 5.  2008. Hormonal control of grass inflorescence development. Trends Plant Sci. 13:656–62 [Google Scholar]
  6. Benjamins R, Scheres B. 6.  2008. Auxin: the looping star in plant development. Annu. Rev. Plant Biol. 59:443–65 [Google Scholar]
  7. Benlloch R, Berbel A, Serrano-Mislata A, Madueño F. 7.  2007. Floral initiation and inflorescence architecture: a comparative view. Ann. Bot. 100:659–76 [Google Scholar]
  8. Bolduc N, Hake S. 8.  2009. The maize transcription factor KNOTTED1 directly regulates the gibberellin catabolism gene ga2ox1. Plant Cell 21:1647–58 [Google Scholar]
  9. Bolduc N, Yilmaz A, Mejia-Guerra MK, Morohashi K, O'Connor D. 9.  et al. 2012. Unraveling the KNOTTED1 regulatory network in maize meristems. Genes Dev. 26:1685–90 [Google Scholar]
  10. Bomblies K, Wang R-L, Ambrose BA, Schmidt RJ, Meeley RB, Doebley J. 10.  2003. Duplicate FLORICAULA/LEAFY homologs zfl1 and zfl2 control inflorescence architecture and flower patterning in maize. Development 130:2385–95 [Google Scholar]
  11. Bommert P, Je BI, Goldshmidt A, Jackson D. 11.  2013. The maize Gα gene COMPACT PLANT2 functions in CLAVATA signalling to control shoot meristem size. Nature 502:555–58 [Google Scholar]
  12. Bommert P, Nagasawa NS, Jackson D. 12.  2013. Quantitative variation in maize kernel row number is controlled by the FASCIATED EAR2 locus. Nat. Genet. 45:334–37 [Google Scholar]
  13. Bommert P, Nardmann J, Vollbrecht E, Running M, Jackson D. 13.  et al. 2005. thick tassel dwarf1 encodes a putative maize ortholog of the Arabidopsis CLAVATA1 leucine-rich repeat receptor-like kinase. Development 132:1235–45 [Google Scholar]
  14. Bommert P, Satoh-Nagasawa N, Jackson D, Hirano H-Y. 14.  2005. Genetics and evolution of inflorescence and flower development in grasses. Plant Cell Physiol. 46:69–78 [Google Scholar]
  15. Bortiri E, Chuck G, Vollbrecht E, Rocheford T, Martienssen R, Hake S. 15.  2006. ramosa2 encodes a LATERAL ORGAN BOUNDARY domain protein that determines the fate of stem cells in branch meristems of maize. Plant Cell 18:574–85 [Google Scholar]
  16. Carmona MJ, Calonje M, Martínez-Zapater JM. 16.  2007. The FT/TFL1 gene family in grapevine. Plant Mol. Biol. 63:637–50 [Google Scholar]
  17. Carraro N, Forestan C, Canova S, Traas J, Varotto S. 17.  2006. ZmPIN1a and ZmPIN1b encode two novel putative candidates for polar auxin transport and plant architecture determination of maize. Plant Physiol. 142:254–64 [Google Scholar]
  18. Chen A, Dubcovsky J. 18.  2012. Wheat TILLING mutants show that the vernalization gene VRN1 down-regulates the flowering repressor VRN2 in leaves but is not essential for flowering. PLoS Genet. 8:e1003134 [Google Scholar]
  19. Cheng Y, Zhao Y. 19.  2007. A role for auxin in flower development. J. Integr. Plant Biol. 49:99–104 [Google Scholar]
  20. Chu H, Liang W, Li J, Hong F, Wu Y. 20.  et al. 2013. A CLE–WOX signalling module regulates root meristem maintenance and vascular tissue development in rice. J. Exp. Bot 64:5359–69 [Google Scholar]
  21. Chu H, Qian Q, Liang W, Yin C, Tan H. 21.  et al. 2006. The FLORAL ORGAN NUMBER4 gene encoding a putative ortholog of Arabidopsis CLAVATA3 regulates apical meristem size in rice. Plant Physiol. 142:1039–52 [Google Scholar]
  22. Chu H, Zhang D. 22.  2007. The shoot apical meristem size regulated by FON4 in rice. Plant Signal. Behav. 2:115–16 [Google Scholar]
  23. Chuck G, Cigan AM, Saeteurn K, Hake S. 23.  2007. The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA. Nat. Genet. 39:544–49 [Google Scholar]
  24. Chuck G, Meeley RB, Hake S. 24.  1998. The control of maize spikelet meristem fate by the APETALA2-like gene indeterminate spikelet1. Genes Dev. 12:1145–54 [Google Scholar]
  25. Chuck G, Meeley RB, Hake S. 25.  2008. Floral meristem initiation and meristem cell fate are regulated by the maize AP2 genes ids1 and sid1. Development 135:3013–19 [Google Scholar]
  26. Chuck G, Muszynski M, Kellogg E, Hake S, Schmidt RJ. 26.  2002. The control of spikelet meristem identity by the branched silkless1 gene in maize. Science 298:1238–41 [Google Scholar]
  27. Chuck G, Whipple C, Jackson D, Hake S. 27.  2010. The maize SBP-box transcription factor encoded by tasselsheath4 regulates bract development and the establishment of meristem boundaries. Development 137:1243–50 [Google Scholar]
  28. Ciaffi M, Paolacci AR, Tanzarella OA, Porceddu E. 28.  2011. Molecular aspects of flower development in grasses. Sex. Plant Reprod. 24:247–82 [Google Scholar]
  29. Clark SE, Williams RW, Meyerowitz EM. 29.  1997. The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89:575–85 [Google Scholar]
  30. Colasanti J, Coneva V. 30.  2009. Mechanisms of floral induction in grasses: something borrowed, something new. Plant Physiol. 149:56–62 [Google Scholar]
  31. Colasanti J, Yuan Z, Sundaresan V. 31.  1998. The indeterminate gene encodes a zinc finger protein and regulates a leaf-generated signal required for the transition to flowering in maize. Cell 93:593–603 [Google Scholar]
  32. Danilevskaya ON, Meng X, Ananiev EV. 32.  2010. Concerted modification of flowering time and inflorescence architecture by ectopic expression of TFL1-like genes in maize. Plant Physiol. 153:238–51 [Google Scholar]
  33. Danilevskaya ON, Meng X, Selinger DA, Deschamps S, Hermon P. 33.  et al. 2008. Involvement of the MADS-box gene ZMM4 in floral induction and inflorescence development in maize. Plant Physiol. 147:2054–69 [Google Scholar]
  34. Derbyshire P, Byrne ME. 34.  2013. MORE SPIKELETS1 is required for spikelet fate in the inflorescence of Brachypodium. Plant Physiol. 161:1291–302 [Google Scholar]
  35. Devos KM, Gale MD. 35.  2000. Genome relationships: the grass model in current research. Plant Cell 12:637–46 [Google Scholar]
  36. Doi K, Izawa T, Fuse T, Yamanouchi U, Kubo T. 36.  et al. 2004. Ehd1, a B-type response regulator in rice, confers short-day promotion of flowering and controls FT-like gene expression independently of Hd1. Genes Dev. 18:926–36 [Google Scholar]
  37. Doust AN. 37.  2007. Architectural evolution and its implications for domestication in grasses. Ann. Bot. 100:941–50 [Google Scholar]
  38. Doust AN, Devos KM, Gadberry MD, Gale MD, Kellogg EA. 38.  2005. The genetic basis for inflorescence variation between foxtail and green millet (Poaceae). Genetics 169:1659–72 [Google Scholar]
  39. Endo-Higashi N, Izawa T. 39.  2011. Flowering time genes Heading date 1 and Early heading date 1 together control panicle development in rice. Plant Cell Physiol. 52:1083–94 [Google Scholar]
  40. Fletcher JC, Brand U, Running MP, Simon R, Meyerowitz EM. 40.  1999. Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283:1911–14 [Google Scholar]
  41. Forestan C, Varotto S. 41.  2012. The role of PIN auxin efflux carriers in polar auxin transport and accumulation and their effect on shaping maize development. Mol. Plant 5:787–98 [Google Scholar]
  42. Gallavotti A, Barazesh S, Malcomber S, Hall D, Jackson D. 42.  et al. 2008. sparse inflorescence1 encodes a monocot-specific YUCCA-like gene required for vegetative and reproductive development in maize. Proc. Natl. Acad. Sci. USA 105:15196–201 [Google Scholar]
  43. Gallavotti A, Long JA, Stanfield S, Yang X, Jackson D. 43.  et al. 2010. The control of axillary meristem fate in the maize ramosa pathway. Development 137:2849–56 [Google Scholar]
  44. Gallavotti A, Malcomber S, Gaines C, Stanfield S, Whipple C. 44.  et al. 2011. BARREN STALK FASTIGIATE1 is an AT-hook protein required for the formation of maize ears. Plant Cell 23:1756–71 [Google Scholar]
  45. Gallavotti A, Yang Y, Schmidt RJ, Jackson D. 45.  2008. The relationship between auxin transport and maize branching. Plant Physiol. 147:1913–23 [Google Scholar]
  46. Gallavotti A, Zhao Q, Kyozuka J, Meeley RB, Ritter MK. 46.  et al. 2004. The role of barren stalk1 in the architecture of maize. Nature 432:630–35 [Google Scholar]
  47. Gao H, Zheng X-M, Fei G, Chen J, Jin M. 47.  et al. 2013. Ehd4 encodes a novel and Oryza-genus-specific regulator of photoperiodic flowering in rice. PLoS Genet. 9:e1003281 [Google Scholar]
  48. Gao X, Liang W, Yin C, Ji S, Wang H. 48.  et al. 2010. The SEPALLATA-like gene OsMADS34 is required for rice inflorescence and spikelet development. Plant Physiol. 153:728–40 [Google Scholar]
  49. Giulini A, Wang J, Jackson D. 49.  2004. Control of phyllotaxy by the cytokinin-inducible response regulator homologue ABPHYL1. Nature 430:1031–34 [Google Scholar]
  50. 50. Grass Phylogeny Work. Group 2001. Phylogeny and subfamilial classification of the grasses (Poaceae). Ann. Mo. Bot. Gard. 88:373–457 [Google Scholar]
  51. Harder LD, Prusinkiewicz P. 51.  2013. The interplay between inflorescence development and function as the crucible of architectural diversity. Ann. Bot. 112:1477–93 [Google Scholar]
  52. Hirose N, Makita N, Kojima M, Kamada-Nobusada T, Sakakibara H. 52.  2007. Overexpression of a type-A response regulator alters rice morphology and cytokinin metabolism. Plant Cell Physiol. 48:523–39 [Google Scholar]
  53. Hong L, Qian Q, Zhu K, Tang D, Huang Z. 53.  et al. 2010. ELE restrains empty glumes from developing into lemmas. J. Genet. Genomics 37:101–15 [Google Scholar]
  54. Horigome A, Nagasawa N, Ikeda K, Ito M, Itoh JI, Nagato Y. 54.  2009. Rice OPEN BEAK is a negative regulator of class 1 knox genes and a positive regulator of class B floral homeotic gene. Plant J. 58:724–36 [Google Scholar]
  55. Huang X, Qian Q, Liu Z, Sun H, He S. 55.  et al. 2009. Natural variation at the DEP1 locus enhances grain yield in rice. Nat. Genet. 41:494–97 [Google Scholar]
  56. Ikeda K, Ito M, Nagasawa N, Kyozuka J, Nagato Y. 56.  2007. Rice ABERRANT PANICLE ORGANIZATION 1, encoding an F-box protein, regulates meristem fate. Plant J. 51:1030–40 [Google Scholar]
  57. Ikeda K, Nagasawa N, Nagato Y. 57.  2005. ABERRANT PANICLE ORGANIZATION 1 temporally regulates meristem identity in rice. Dev. Biol. 282:349–60 [Google Scholar]
  58. Ikeda K, Sunohara H, Nagato Y. 58.  2004. Developmental course of inflorescence and spikelet in rice. Breed. Sci. 54:147–56 [Google Scholar]
  59. Ikeda-Kawakatsu K, Maekawa M, Izawa T, Itoh JI, Nagato Y. 59.  2012. ABERRANT PANICLE ORGANIZATION 2/RFL, the rice ortholog of Arabidopsis LEAFY, suppresses the transition from inflorescence meristem to floral meristem through interaction with APO1. Plant J. 69:168–80 [Google Scholar]
  60. Ishii T, Numaguchi K, Miura K, Yoshida K, Thanh PT. 60.  et al. 2013. OsLG1 regulates a closed panicle trait in domesticated rice. Nat. Genet. 45:462–65 [Google Scholar]
  61. Itoh Ji, Hibara Ki, Kojima M, Sakakibara H, Nagato Y. 61.  2012. Rice DECUSSATE controls phyllotaxy by affecting the cytokinin signaling pathway. Plant J. 72:869–81 [Google Scholar]
  62. Izawa T, Oikawa T, Sugiyama N, Tanisaka T, Yano M, Shimamoto K. 62.  2002. Phytochrome mediates the external light signal to repress FT orthologs in photoperiodic flowering of rice. Genes Dev. 16:2006–20 [Google Scholar]
  63. Izawa T, Takahashi Y, Yano M. 63.  2003. Comparative biology comes into bloom: genomic and genetic comparison of flowering pathways in rice and Arabidopsis. Curr. Opin. Plant Biol. 6:113–20 [Google Scholar]
  64. Jackson D, Hake S. 64.  1999. Control of phyllotaxy in maize by the abphyl1 gene. Development 126:315–23 [Google Scholar]
  65. Jasinski S, Piazza P, Craft J, Hay A, Woolley L. 65.  et al. 2005. KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Curr. Biol. 15:1560–65 [Google Scholar]
  66. Jeong S, Trotochaud AE, Clark SE. 66.  1999. The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required for the stability of the CLAVATA1 receptor-like kinase. Plant Cell 11:1925–33 [Google Scholar]
  67. Jiang Y, Cai Z, Xie W, Long T, Yu H, Zhang Q. 67.  2012. Rice functional genomics research: progress and implications for crop genetic improvement. Biotechnol. Adv. 30:1059–70 [Google Scholar]
  68. Jiao Y, Wang Y, Xue D, Wang J, Yan M. 68.  et al. 2010. Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat. Genet. 42:541–44 [Google Scholar]
  69. Kayes JM, Clark SE. 69.  1998. CLAVATA2, a regulator of meristem and organ development in Arabidopsis. Development 125:3843–51 [Google Scholar]
  70. Kellogg EA. 70.  2007. Floral displays: genetic control of grass inflorescences. Curr. Opin. Plant Biol. 10:26–31 [Google Scholar]
  71. Kim J-Y. 71.  2005. Regulation of short-distance transport of RNA and protein. Curr. Opin. Plant Biol. 8:45–52 [Google Scholar]
  72. Kim J-Y, Yuan Z, Jackson D. 72.  2003. Developmental regulation and significance of KNOX protein trafficking in Arabidopsis. Development 130:4351–62 [Google Scholar]
  73. Kobayashi K, Maekawa M, Miyao A, Hirochika H, Kyozuka J. 73.  2010. PANICLE PHYTOMER2 (PAP2), encoding a SEPALLATA subfamily MADS-box protein, positively controls spikelet meristem identity in rice. Plant Cell Physiol. 51:47–57 [Google Scholar]
  74. Kobayashi K, Yasuno N, Sato Y, Yoda M, Yamazaki R. 74.  et al. 2012. Inflorescence meristem identity in rice is specified by overlapping functions of three AP1/FUL-like MADS box genes and PAP2, a SEPALLATA MADS box gene. Plant Cell 24:1848–59 [Google Scholar]
  75. Komatsu K, Maekawa M, Ujiie S, Satake Y, Furutani I. 75.  et al. 2003. LAX and SPA: major regulators of shoot branching in rice. Proc. Natl. Acad. Sci. USA 100:11765–70 [Google Scholar]
  76. Komiya R, Ikegami A, Tamaki S, Yokoi S, Shimamoto K. 76.  2008. Hd3a and RFT1 are essential for flowering in rice. Development 135:767–74 [Google Scholar]
  77. Komiya R, Yokoi S, Shimamoto K. 77.  2009. A gene network for long-day flowering activates RFT1 encoding a mobile flowering signal in rice. Development 136:3443–50 [Google Scholar]
  78. Kurakawa T, Ueda N, Maekawa M, Kobayashi K, Kojima M. 78.  et al. 2007. Direct control of shoot meristem activity by a cytokinin-activating enzyme. Nature 445:652–55 [Google Scholar]
  79. Kyozuka J. 79.  2007. Control of shoot and root meristem function by cytokinin. Curr. Opin. Plant Biol. 10:442–46 [Google Scholar]
  80. LeClere S, Schmelz EA, Chourey PS. 80.  2010. Sugar levels regulate tryptophan-dependent auxin biosynthesis in developing maize kernels. Plant Physiol. 153:306–18 [Google Scholar]
  81. Lee B, Johnston R, Yang Y, Gallavotti A, Kojima M. 81.  et al. 2009. Studies of aberrant phyllotaxy1 mutants of maize indicate complex interactions between auxin and cytokinin signaling in the shoot apical meristem. Plant Physiol. 150:205–16 [Google Scholar]
  82. Lee DY, An G. 82.  2012. Two AP2 family genes, SUPERNUMERARY BRACT (SNB) and OsINDETERMINATE SPIKELET 1 (OsIDS1), synergistically control inflorescence architecture and floral meristem establishment in rice. Plant J. 69:445–61 [Google Scholar]
  83. Lee DY, Lee J, Moon S, Park SY, An G. 83.  2007. The rice heterochronic gene SUPERNUMERARY BRACT regulates the transition from spikelet meristem to floral meristem. Plant J. 49:64–78 [Google Scholar]
  84. Li F, Liu W, Tang J, Chen J, Tong H. 84.  et al. 2010. Rice DENSE AND ERECT PANICLE 2 is essential for determining panicle outgrowth and elongation. Cell Res. 20:838–49 [Google Scholar]
  85. Li M, Tang D, Wang K, Wu X, Lu L. 85.  et al. 2011. Mutations in the F-box gene LARGER PANICLE improve the panicle architecture and enhance the grain yield in rice. Plant Biotechnol. J. 9:1002–13 [Google Scholar]
  86. Li S, Zhao B, Yuan D, Duan M, Qian Q. 86.  et al. 2013. Rice zinc finger protein DST enhances grain production through controlling Gn1a/OsCKX2 expression. Proc. Natl. Acad. Sci. USA 110:3167–72 [Google Scholar]
  87. Li X, Qian Q, Fu Z, Wang Y, Xiong G. 87.  et al. 2003. Control of tillering in rice. Nature 422:618–21 [Google Scholar]
  88. Liu C, Teo ZWN, Bi Y, Song S, Xi W. 88.  et al. 2013. A conserved genetic pathway determines inflorescence architecture in Arabidopsis and rice. Dev. Cell 24:612–22 [Google Scholar]
  89. Liu C, Thong Z, Yu H. 89.  2009. Coming into bloom: the specification of floral meristems. Development 136:3379–91 [Google Scholar]
  90. Long JA, Moan EI, Medford JI, Barton MK. 90.  1996. A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379:66–69 [Google Scholar]
  91. Long JA, Ohno C, Smith ZR, Meyerowitz EM. 91.  2006. TOPLESS regulates apical embryonic fate in Arabidopsis. Science 312:1520–23 [Google Scholar]
  92. Malcomber ST, Kellogg EA. 92.  2005. SEPALLATA gene diversification: brave new whorls. Trends Plant Sci. 10:427–35 [Google Scholar]
  93. Malcomber ST, Preston JC, Reinheimer R, Kossuth J, Kellogg EA. 93.  2006. Developmental gene evolution and the origin of grass inflorescence diversity. Adv. Bot. Res. 44:425–81 [Google Scholar]
  94. Matsubara K, Yamanouchi U, Nonoue Y, Sugimoto K, Wang ZX. 94.  et al. 2011. Ehd3, encoding a plant homeodomain finger-containing protein, is a critical promoter of rice flowering. Plant J. 66:603–12 [Google Scholar]
  95. Matsubara K, Yamanouchi U, Wang Z-X, Minobe Y, Izawa T, Yano M. 95.  2008. Ehd2, a rice ortholog of the maize INDETERMINATE1 gene, promotes flowering by up-regulating Ehd1. Plant Physiol. 148:1425–35 [Google Scholar]
  96. McSteen P. 96.  2009. Hormonal regulation of branching in grasses. Plant Physiol. 149:46–55 [Google Scholar]
  97. McSteen P, Hake S. 97.  2001. barren inflorescence2 regulates axillary meristem development in the maize inflorescence. Development 128:2881–91 [Google Scholar]
  98. McSteen P, Leyser O. 98.  2005. Shoot branching. Annu. Rev. Plant Biol. 56:353–74 [Google Scholar]
  99. Meng X, Muszynski MG, Danilevskaya ON. 99.  2011. The FT-like ZCN8 gene functions as a floral activator and is involved in photoperiod sensitivity in maize. Plant Cell 23:942–60 [Google Scholar]
  100. Miura K, Ikeda M, Matsubara A, Song X-J, Ito M. 100.  et al. 2010. OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat. Genet. 42:545–49 [Google Scholar]
  101. Moubayidin L, Di Mambro R, Sabatini S. 101.  2009. Cytokinin–auxin crosstalk. Trends Plant Sci. 14:557–62 [Google Scholar]
  102. Müller R, Bleckmann A, Simon R. 102.  2008. The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1. Plant Cell 20:934–46 [Google Scholar]
  103. Muszynski MG, Dam T, Li B, Shirbroun DM, Hou Z. 103.  et al. 2006. delayed flowering1 encodes a basic leucine zipper protein that mediates floral inductive signals at the shoot apex in maize. Plant Physiol. 142:1523–36 [Google Scholar]
  104. Nakagawa M, Shimamoto K, Kyozuka J. 104.  2002. Overexpression of RCN1 and RCN2, rice TERMINAL FLOWER 1/CENTRORADIALIS homologs, confers delay of phase transition and altered panicle morphology in rice. Plant J. 29:743–50 [Google Scholar]
  105. Nardmann J, Werr W. 105.  2006. The shoot stem cell niche in angiosperms: expression patterns of WUS orthologues in rice and maize imply major modifications in the course of mono- and dicot evolution. Mol. Biol. Evol. 23:2492–504 [Google Scholar]
  106. Ogawa M, Shinohara H, Sakagami Y, Matsubayashi Y. 106.  2008. Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319:294 [Google Scholar]
  107. Ohyama K, Shinohara H, Ogawa-Ohnishi M, Matsubayashi Y. 107.  2009. A glycopeptide regulating stem cell fate in Arabidopsis thaliana. Nat. Chem. Biol. 5:578–80 [Google Scholar]
  108. Oikawa T, Kyozuka J. 108.  2009. Two-step regulation of LAX PANICLE1 protein accumulation in axillary meristem formation in rice. Plant Cell 21:1095–108 [Google Scholar]
  109. Ongaro V, Leyser O. 109.  2008. Hormonal control of shoot branching. J. Exp. Bot. 59:67–74 [Google Scholar]
  110. Park SJ, Kim SL, Lee S, Je BI, Piao HL. 110.  et al. 2008. Rice Indeterminate 1 (OsId1) is necessary for the expression of Ehd1 (Early heading date 1) regardless of photoperiod. Plant J. 56:1018–29 [Google Scholar]
  111. Pautler M, Tanaka W, Hirano H-Y, Jackson D. 111.  2013. Grass meristems I: shoot apical meristem maintenance, axillary meristem determinacy and the floral transition. Plant Cell Physiol. 54:302–12 [Google Scholar]
  112. Phillips KA, Skirpan AL, Liu X, Christensen A, Slewinski TL. 112.  et al. 2011. vanishing tassel2 encodes a grass-specific tryptophan aminotransferase required for vegetative and reproductive development in maize. Plant Cell 23:550–66 [Google Scholar]
  113. Pnueli L, Gutfinger T, Hareven D, Ben-Naim O, Ron N. 113.  et al. 2001. Tomato SP-interacting proteins define a conserved signaling system that regulates shoot architecture and flowering. Plant Cell 13:2687–702 [Google Scholar]
  114. Preston JC, Kellogg EA. 114.  2006. Reconstructing the evolutionary history of paralogous APETALA1/FRUITFULL-like genes in grasses (Poaceae). Genetics 174:421–37 [Google Scholar]
  115. Putterill J, Robson F, Lee K, Simon R, Coupland G. 115.  1995. The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell 80:847–57 [Google Scholar]
  116. Qiao Y, Piao R, Shi J, Lee S-I, Jiang W. 116.  et al. 2011. Fine mapping and candidate gene analysis of dense and erect panicle 3, DEP3, which confers high grain yield in rice (Oryza sativa L.). Theor. Appl. Genet. 122:1439–49 [Google Scholar]
  117. Rao NN, Prasad K, Kumar PR, Vijayraghavan U. 117.  2008. Distinct regulatory role for RFL, the rice LFY homolog, in determining flowering time and plant architecture. Proc. Natl. Acad. Sci. USA 105:3646–51 [Google Scholar]
  118. Ren D, Li Y, Zhao F, Sang X, Shi J. 118.  et al. 2013. MULTI-FLORET SPIKELET1, which encodes an AP2/ERF protein, determines spikelet meristem fate and sterile lemma identity in rice. Plant Physiol. 162:872–84 [Google Scholar]
  119. Ritter MK, Padilla CM, Schmidt RJ. 119.  2002. The maize mutant barren stalk1 is defective in axillary meristem development. Am. J. Bot. 89:203–10 [Google Scholar]
  120. Sakamoto T, Sakakibara H, Kojima M, Yamamoto Y, Nagasaki H. 120.  et al. 2006. Ectopic expression of KNOTTED1-like homeobox protein induces expression of cytokinin biosynthesis genes in rice. Plant Physiol. 142:54–62 [Google Scholar]
  121. Satoh-Nagasawa N, Nagasawa N, Malcomber S, Sakai H, Jackson D. 121.  2006. A trehalose metabolic enzyme controls inflorescence architecture in maize. Nature 441:227–30 [Google Scholar]
  122. Sazuka T, Kamiya N, Nishimura T, Ohmae K, Sato Y. 122.  et al. 2009. A rice tryptophan deficient dwarf mutant, tdd1, contains a reduced level of indole acetic acid and develops abnormal flowers and organless embryos. Plant J. 60:227–41 [Google Scholar]
  123. Schoof H, Lenhard M, Haecker A, Mayer KFX, Jürgens G. 123.  et al. 2000. The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100:635–44 [Google Scholar]
  124. Scofield S, Dewitte W, Nieuwland J, Murray JAH. 124.  2013. The Arabidopsis homeobox gene SHOOT MERISTEMLESS has cellular and meristem-organisational roles with differential requirements for cytokinin and CYCD3 activity. Plant J. 75:53–66 [Google Scholar]
  125. Simons KJ, Fellers JP, Trick HN, Zhang Z, Tai Y-S. 125.  et al. 2006. Molecular characterization of the major wheat domestication gene Q. Genetics 172:547–55 [Google Scholar]
  126. Skirpan A, Culler AH, Gallavotti A, Jackson D, Cohen JD, McSteen P. 126.  2009. BARREN INFLORESCENCE2 interaction with ZmPIN1a suggests a role in auxin transport during maize inflorescence development. Plant Cell Physiol. 50:652–57 [Google Scholar]
  127. Skirpan A, Wu X, McSteen P. 127.  2008. Genetic and physical interaction suggest that BARREN STALK1 is a target of BARREN INFLORESCENCE2 in maize inflorescence development. Plant J. 55:787–97 [Google Scholar]
  128. Smyth DR, Bowman JL, Meyerowitz EM. 128.  1990. Early flower development in Arabidopsis. Plant Cell 2:755–67 [Google Scholar]
  129. Suzaki T, Sato M, Ashikari M, Miyoshi M, Nagato Y, Hirano H-Y. 129.  2004. The gene FLORAL ORGAN NUMBER1 regulates floral meristem size in rice and encodes a leucine-rich repeat receptor kinase orthologous to Arabidopsis CLAVATA1. Development 131:5649–57 [Google Scholar]
  130. Suzaki T, Toriba T, Fujimoto M, Tsutsumi N, Kitano H, Hirano H-Y. 130.  2006. Conservation and diversification of meristem maintenance mechanism in Oryza sativa: function of the FLORAL ORGAN NUMBER2 gene. Plant Cell Physiol. 47:1591–602 [Google Scholar]
  131. Tabuchi H, Zhang Y, Hattori S, Omae M, Shimizu-Sato S. 131.  et al. 2011. LAX PANICLE2 of rice encodes a novel nuclear protein and regulates the formation of axillary meristems. Plant Cell 23:3276–87 [Google Scholar]
  132. Taguchi-Shiobara F, Yuan Z, Hake S, Jackson D. 132.  2001. The fasciated ear2 gene encodes a leucine-rich repeat receptor-like protein that regulates shoot meristem proliferation in maize. Genes Dev. 15:2755–66 [Google Scholar]
  133. Tanaka W, Pautler M, Jackson D, Hirano H-Y. 133.  2013. Grass meristems II: inflorescence architecture, flower development and meristem fate. Plant Cell Physiol. 54:313–24 [Google Scholar]
  134. Tanaka W, Toriba T, Ohmori Y, Yoshida A, Kawai A. 134.  et al. 2012. The YABBY gene TONGARI-BOUSHI1 is involved in lateral organ development and maintenance of meristem organization in the rice spikelet. Plant Cell 24:80–95 [Google Scholar]
  135. Taoka K, Ohki I, Tsuji H, Furuita K, Hayashi K. 135.  et al. 2011. 14-3-3 proteins act as intracellular receptors for rice Hd3a florigen. Nature 476:332–35 [Google Scholar]
  136. Thompson BE, Hake S. 136.  2009. Translational biology: from Arabidopsis flowers to grass inflorescence architecture. Plant Physiol. 149:38–45 [Google Scholar]
  137. Tsuda K, Ito Y, Sato Y, Kurata N. 137.  2011. Positive autoregulation of a KNOX gene is essential for shoot apical meristem maintenance in rice. Plant Cell 23:4368–81 [Google Scholar]
  138. Turner A, Beales J, Faure S, Dunford RP, Laurie DA. 138.  2005. The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science 310:1031–34 [Google Scholar]
  139. Vollbrecht E, Reiser L, Hake S. 139.  2000. Shoot meristem size is dependent on inbred background and presence of the maize homeobox gene, knotted1. Development 127:3161–72 [Google Scholar]
  140. Vollbrecht E, Springer PS, Goh L, Buckler ES IV, Martienssen R. 140.  2005. Architecture of floral branch systems in maize and related grasses. Nature 436:1119–26 [Google Scholar]
  141. Wang Y, Li J. 141.  2011. Branching in rice. Curr. Opin. Plant Biol. 14:94–99 [Google Scholar]
  142. Wei X, Xu J, Guo H, Jiang L, Chen S. 142.  et al. 2010. DTH8 suppresses flowering in rice, influencing plant height and yield potential simultaneously. Plant Physiol. 153:1747–58 [Google Scholar]
  143. Woodward JB, Abeydeera ND, Paul D, Phillips K, Rapala-Kozik M. 143.  et al. 2010. A maize thiamine auxotroph is defective in shoot meristem maintenance. Plant Cell 22:3305–17 [Google Scholar]
  144. Wu C, You C, Li C, Long T, Chen G. 144.  et al. 2008. RID1, encoding a Cys2/His2-type zinc finger transcription factor, acts as a master switch from vegetative to floral development in rice. Proc. Natl. Acad. Sci. USA 105:12915–20 [Google Scholar]
  145. Wu X, McSteen P. 145.  2007. The role of auxin transport during inflorescence development in maize (Zea mays, Poaceae). Am. J. Bot. 94:1745–55 [Google Scholar]
  146. Xu M, Zhu L, Shou H, Wu P. 146.  2005. A PIN1 family gene, OsPIN1, involved in auxin-dependent adventitious root emergence and tillering in rice. Plant Cell Physiol. 46:1674–81 [Google Scholar]
  147. Xu XM, Wang J, Xuan Z, Goldshmidt A, Borrill PG. 147.  et al. 2011. Chaperonins facilitate KNOTTED1 cell-to-cell trafficking and stem cell function. Science 333:1141–44 [Google Scholar]
  148. Xue W, Xing Y, Weng X, Zhao Y, Tang W. 148.  et al. 2008. Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat. Genet. 40:761–67 [Google Scholar]
  149. Yan L, Loukoianov A, Blechl A, Tranquilli G, Ramakrishna W. 149.  et al. 2004. The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science 303:1640–44 [Google Scholar]
  150. Yan W-H, Wang P, Chen H-X, Zhou H-J, Li Q-P. 150.  et al. 2011. A major QTL, Ghd8, plays pleiotropic roles in regulating grain productivity, plant height, and heading date in rice. Mol. Plant 4:319–30 [Google Scholar]
  151. Yanai O, Shani E, Dolezal K, Tarkowski P, Sablowski R. 151.  et al. 2005. Arabidopsis KNOXI proteins activate cytokinin biosynthesis. Curr. Biol. 15:1566–71 [Google Scholar]
  152. Yano M, Katayose Y, Ashikari M, Yamanouchi U, Monna L. 152.  et al. 2000. Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell 12:2473–83 [Google Scholar]
  153. Yoshida A, Ohmori Y, Kitano H, Taguchi-Shiobara F, Hirano HY. 153.  2012. ABERRANT SPIKELET AND PANICLE1, encoding a TOPLESS-related transcriptional co-repressor, is involved in the regulation of meristem fate in rice. Plant J. 70:327–39 [Google Scholar]
  154. Yoshida A, Sasao M, Yasuno N, Takagi K, Daimon Y. 154.  et al. 2013. TAWAWA1, a regulator of rice inflorescence architecture, functions through the suppression of meristem phase transition. Proc. Natl. Acad. Sci. USA 110:767–72 [Google Scholar]
  155. Yoshida A, Suzaki T, Tanaka W, Hirano H-Y. 155.  2009. The homeotic gene long sterile lemma (G1) specifies sterile lemma identity in the rice spikelet. Proc. Natl. Acad. Sci. USA 106:20103–8 [Google Scholar]
  156. Yoshida H, Nagato Y. 156.  2011. Flower development in rice. J. Exp. Bot. 62:4719–30 [Google Scholar]
  157. Yuan Z, Gao S, Xue D-W, Luo D, Li L-T. 157.  et al. 2009. RETARDED PALEA1 controls palea development and floral zygomorphy in rice. Plant Physiol. 149:235–44 [Google Scholar]
  158. Zahn LM, Kong H, Leebens-Mack JH, Kim S, Soltis PS. 158.  et al. 2005. The evolution of the SEPALLATA subfamily of MADS-box genes: a preangiosperm origin with multiple duplications throughout angiosperm history. Genetics 169:2209–23 [Google Scholar]
  159. Zalewski W, Galuszka P, Gasparis S, Orczyk W, Nadolska-Orczyk A. 159.  2010. Silencing of the HvCKX1 gene decreases the cytokinin oxidase/dehydrogenase level in barley and leads to higher plant productivity. J. Exp. Bot. 61:1839–51 [Google Scholar]
  160. Zhang D, Yuan Z, An G, Dreni L, Hu JP, Kater M. 160.  2013. Panicle development. Genetics and Genomics of Rice Q Zhang, RA Wing 279–95 Plant Genet. Genomics Crops Models 5 New York: Springer [Google Scholar]
  161. Zhang L, Zhao YL, Gao LF, Zhao GY, Zhou RH. 161.  et al. 2012. TaCKX6-D1, the ortholog of rice OsCKX2, is associated with grain weight in hexaploid wheat. New Phytol. 195:574–84 [Google Scholar]
  162. Zhang S, Hu W, Wang L, Lin C, Cong B. 162.  et al. 2005. TFL1/CEN-like genes control intercalary meristem activity and phase transition in rice. Plant Sci. 168:1393–408 [Google Scholar]
  163. Zhao Y. 163.  2008. The role of local biosynthesis of auxin and cytokinin in plant development. Curr. Opin. Plant Biol. 11:16–22 [Google Scholar]
  164. Zhao Y. 164.  2010. Auxin biosynthesis and its role in plant development. Annu. Rev. Plant Biol. 61:49–64 [Google Scholar]
  165. Zhu K, Tang D, Yan C, Chi Z, Yu H. 165.  et al. 2010. ERECT PANICLE2 encodes a novel protein that regulates panicle erectness in indica rice. Genetics 184:343–50 [Google Scholar]
  166. Zhu Q-H, Hoque MS, Dennis ES, Upadhyaya NM. 166.  2003. Ds tagging of BRANCHED FLORETLESS 1 (BFL1) that mediates the transition from spikelet to floret meristem in rice (Oryza sativa L). BMC Plant Biol. 3:6 [Google Scholar]
  167. Zhu Q-H, Upadhyaya NM, Gubler F, Helliwell CA. 167.  2009. Over-expression of miR172 causes loss of spikelet determinacy and floral organ abnormalities in rice (Oryza sativa). BMC Plant Biol. 9:149 [Google Scholar]
/content/journals/10.1146/annurev-arplant-050213-040104
Loading
/content/journals/10.1146/annurev-arplant-050213-040104
Loading

Data & Media loading...

Supplementary Data

  • Article Type: Review Article
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