1932

Abstract

The size of seeds affects not only evolutionary fitness but also grain yield of crops. Understanding the mechanisms controlling seed size has become an important research field in plant science. Seed size is determined by the integrated signals of maternal and zygotic tissues, which control the coordinated growth of the embryo, endosperm, and seed coat. Recent advances have identified several signaling pathways that control seed size through maternal tissues, including or involving the ubiquitin-proteasome pathway, G-protein signaling, mitogen-activated protein kinase (MAPK) signaling, phytohormone perception and homeostasis, and some transcriptional regulators. Meanwhile, growth of the zygotic tissues is regulated in part by the HAIKU (IKU) pathway and phytohormones. This review provides a general overview of current findings in seed size control and discusses the emerging molecular mechanisms and regulatory networks found to be involved.

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2019-04-29
2024-04-15
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Literature Cited

  1. 1.  Adamski NM, Anastasiou E, Eriksson S, O'Neill CM, Lenhard M 2009. Local maternal control of seed size by KLUH/CYP78A5-dependent growth signaling. PNAS 106:20115–20
    [Google Scholar]
  2. 2.  Ashikari M, Sakakibara H, Lin S, Yamamoto T, Takashi T et al. 2005. Cytokinin oxidase regulates rice grain production. Science 309:741–45
    [Google Scholar]
  3. 3.  Ashikari M, Wu J, Yano M, Sasaki T, Yoshimura A 1999. Rice gibberellin-insensitive dwarf mutant gene Dwarf 1 encodes the α-subunit of GTP-binding protein. PNAS 96:10284–89
    [Google Scholar]
  4. 4.  Aya K, Hobo T, Sato-Izawa K, Ueguchi-Tanaka M, Kitano H, Matsuoka M 2014. A novel AP2-type transcription factor, SMALL ORGAN SIZE1, controls organ size downstream of an auxin signaling pathway. Plant Cell Physiol 55:897–912
    [Google Scholar]
  5. 5.  Bartels S, Gonzalez Besteiro MA, Lang D, Ulm R 2010. Emerging functions for plant MAP kinase phosphatases. Trends Plant Sci 15:322–29
    [Google Scholar]
  6. 6.  Bartrina I, Otto E, Strnad M, Werner T, Schmülling T 2011. Cytokinin regulates the activity of reproductive meristems, flower organ size, ovule formation, and thus seed yield in Arabidopsis thaliana. Plant Cell 23:69–80
    [Google Scholar]
  7. 7.  Botella JR 2012. Can heterotrimeric G proteins help to feed the world. ? Trends Plant Sci 17:563–68
    [Google Scholar]
  8. 8.  Chakravorty D, Trusov Y, Zhang W, Acharya BR, Sheahan MB et al. 2011. An atypical heterotrimeric G-protein γ-subunit is involved in guard cell K+-channel regulation and morphological development in Arabidopsis thaliana. Plant J 67:840–51
    [Google Scholar]
  9. 9.  Che R, Tong H, Shi B, Liu Y, Fang S et al. 2015. Control of grain size and rice yield by GL2-mediated brassinosteroid responses. Nat. Plants 2:15195
    [Google Scholar]
  10. 10.  Cheng Z, Li JF, Niu Y, Zhang XC, Woody OZ et al. 2015. Pathogen-secreted proteases activate a novel plant immune pathway. Nature 521:213–16
    [Google Scholar]
  11. 11.  Cheng ZJ, Zhao XY, Shao XX, Wang F, Zhou C et al. 2014. Abscisic acid regulates early seed development in Arabidopsis by ABI5-mediated transcription of SHORT HYPOCOTYL UNDER BLUE1. Plant Cell 26:1053–68Shows that abscisic acid acts through the HAIKU pathway to control seed size by regulating endosperm development.
    [Google Scholar]
  12. 12.  Chujo T, Miyamoto K, Ogawa S, Masuda Y, Shimizu T et al. 2014. Overexpression of phosphomimic mutated OsWRKY53 leads to enhanced blast resistance in rice. PLOS ONE 9:e98737
    [Google Scholar]
  13. 13.  Disch S, Anastasiou E, Sharma VK, Laux T, Fletcher JC, Lenhard M 2006. The E3 ubiquitin ligase BIG BROTHER controls Arabidopsis organ size in a dosage-dependent manner. Curr. Biol. 16:272–79
    [Google Scholar]
  14. 14.  Dong H, Dumenil J, Lu FH, Na L, Vanhaeren H et al. 2017. Ubiquitylation activates a peptidase that promotes cleavage and destabilization of its activating E3 ligases and diverse growth regulatory proteins to limit cell proliferation in Arabidopsis. Genes Dev 31:197–208Shows that the ubiquitin-dependent protease DA1 is activated by DA2 and ENHANCER OF DA1/BIG BROTHER and cleaves downstream targets to control seed size.
    [Google Scholar]
  15. 15.  Du L, Li N, Chen L, Xu Y, Li Y et al. 2014. The ubiquitin receptor DA1 regulates seed and organ size by modulating the stability of the ubiquitin-specific protease UBP15/SOD2 in Arabidopsis. Plant Cell 26:665–77
    [Google Scholar]
  16. 16.  Duan P, Ni S, Wang J, Zhang B, Xu R et al. 2015. Regulation of OsGRF4 by OsmiR396 controls grain size and yield in rice. Nat. Plants 2:15203Identified the OsmiR396-OsGRF4-OsGIFs regulatory module.
    [Google Scholar]
  17. 17.  Duan P, Rao Y, Zeng D, Yang Y, Xu R et al. 2014. SMALL GRAIN 1, which encodes a mitogen-activated protein kinase kinase 4, influences grain size in rice. Plant J 77:547–57
    [Google Scholar]
  18. 18.  Duan P, Xu J, Zeng D, Zhang B, Geng M et al. 2017. Natural variation in the promoter of GSE5 contributes to grain size diversity in rice. Mol. Plant 10:685–94
    [Google Scholar]
  19. 19.  Eloy NB, Gonzalez N, Van Leene J, Maleux K, Vanhaeren H et al. 2012. SAMBA, a plant-specific anaphase-promoting complex/cyclosome regulator is involved in early development and A-type cyclin stabilization. PNAS 109:13853–58
    [Google Scholar]
  20. 20.  Fan C, Xing Y, Mao H, Lu T, Han B et al. 2006. GS3, a major QTL for grain length and weight and minor QTL for grain width and thickness in rice, encodes a putative transmembrane protein. Theor. Appl. Genet. 112:1164–71
    [Google Scholar]
  21. 21.  Fang N, Xu R, Huang L, Zhang B, Duan P et al. 2016. SMALL GRAIN 11 controls grain size, grain number and grain yield in rice. Rice 9:64
    [Google Scholar]
  22. 22.  Fang W, Wang Z, Cui R, Li J, Li Y 2012. Maternal control of seed size by EOD3/CYP78A6 in Arabidopsis thaliana. Plant J 70:929–39
    [Google Scholar]
  23. 23.  Feng Z, Wu C, Wang C, Roh J, Zhang L et al. 2016. SLG controls grain size and leaf angle by modulating brassinosteroid homeostasis in rice. J. Exp. Bot. 67:4241–53
    [Google Scholar]
  24. 24.  Figueiredo DD, Batista RA, Roszak PJ, Hennig L, Köhler C 2016. Auxin production in the endosperm drives seed coat development in Arabidopsis. eLife 5:e20542
    [Google Scholar]
  25. 25.  Fujisawa Y, Kato T, Ohki S, Ishikawa A, Kitano H et al. 1999. Suppression of the heterotrimeric G protein causes abnormal morphology, including dwarfism, in rice. PNAS 96:7575–80
    [Google Scholar]
  26. 26.  Garcia D, Fitz Gerald JN, Berger F 2005. Maternal control of integument cell elongation and zygotic control of endosperm growth are coordinated to determine seed size in Arabidopsis. Plant Cell 17:52–60
    [Google Scholar]
  27. 27.  Garcia D, Saingery V, Chambrier P, Mayer U, Jurgens G, Berger F 2003. Arabidopsis haiku mutants reveal new controls of seed size by endosperm. Plant Physiol 131:1661–70
    [Google Scholar]
  28. 28.  Ge L, Yu J, Wang H, Luth D, Bai G et al. 2016. Increasing seed size and quality by manipulating BIG SEEDS1 in legume species. PNAS 113:12414–19
    [Google Scholar]
  29. 29.  Gehring M, Satyaki PR 2017. Endosperm and imprinting, inextricably linked. Plant Physiol 173:143–54
    [Google Scholar]
  30. 30.  Gonzalez N, Pauwels L, Baekelandt A, De Milde L, Van Leene J et al. 2015. A repressor protein complex regulates leaf growth in Arabidopsis. Plant Cell 27:2273–87
    [Google Scholar]
  31. 31.  Gu Y, Li W, Jiang H, Wang Y, Gao H et al. 2017. Differential expression of a WRKY gene between wild and cultivated soybeans correlates to seed size. J. Exp. Bot. 68:2717–29
    [Google Scholar]
  32. 32.  Guo T, Chen K, Dong NQ, Shi CL, Ye WW et al. 2018. GRAIN SIZE AND NUMBER1 negatively regulates the OsMKKK10-OsMKK4-OsMPK6 cascade to coordinate the trade-off between grain number per panicle and grain size in rice. Plant Cell 30:871–88Shows that OsMKP1 negatively regulates grain size by dephosphorylating OsMAPK6.
    [Google Scholar]
  33. 33.  He Z, Zeng J, Ren Y, Chen D, Li W et al. 2017. OsGIF1 positively regulates the sizes of stems, leaves, and grains in rice. Front. Plant Sci. 8:1730
    [Google Scholar]
  34. 34.  Hicke L, Schubert HL, Hill CP 2005. Ubiquitin-binding domains. Nat. Rev. Mol. Cell Biol. 6:610–21
    [Google Scholar]
  35. 35.  Hirano K, Yoshida H, Aya K, Kawamura M, Hayashi M et al. 2017. SMALL ORGAN SIZE 1 and SMALL ORGAN SIZE 2/DWARF AND LOW-TILLERING form a complex to integrate auxin and brassinosteroid signaling in rice. Mol. Plant 10:590–604
    [Google Scholar]
  36. 36.  Hong Z, Ueguchi-Tanaka M, Fujioka S, Takatsuto S, Yoshida S et al. 2005. The rice brassinosteroid-deficient dwarf2 mutant, defective in the rice homolog of Arabidopsis DIMINUTO/DWARF1, is rescued by the endogenously accumulated alternative bioactive brassinosteroid, dolichosterone. Plant Cell 17:2243–54
    [Google Scholar]
  37. 37.  Hu J, Wang Y, Fang Y, Zeng L, Xu J et al. 2015. A rare allele of GS2 enhances grain size and grain yield in rice. Mol. Plant 8:1455–65
    [Google Scholar]
  38. 38.  Hu L, Ye M, Li R, Zhang T, Zhou G et al. 2015. The rice transcription factor WRKY53 suppresses herbivore-induced defenses by acting as a negative feedback modulator of mitogen-activated protein kinase activity. Plant Physiol 169:2907–21
    [Google Scholar]
  39. 39.  Hu Z, Lu SJ, Wang MJ, He H, Sun L et al. 2018. A novel QTL qTGW3 encodes the GSK3/SHAGGY-Like Kinase OsGSK5/OsSK41 that interacts with OsARF4 to negatively regulate grain size and weight in rice. Mol. Plant 11:736–49
    [Google Scholar]
  40. 40.  Huang K, Wang D, Duan P, Zhang B, Xu R et al. 2017. WIDE AND THICK GRAIN 1, which encodes an otubain-like protease with deubiquitination activity, influences grain size and shape in rice. Plant J 91:849–60
    [Google Scholar]
  41. 41.  Huang X, Qian Q, Liu Z, Sun H, He S et al. 2009. Natural variation at the DEP1 locus enhances grain yield in rice. Nat. Genet. 41:494–97
    [Google Scholar]
  42. 42.  Hughes R, Spielman M, Schruff MC, Larson TR, Graham IA, Scott RJ 2008. Yield assessment of integument-led seed growth following targeted repair of auxin response factor 2. Plant Biotechnol. J 6:758–69
    [Google Scholar]
  43. 43.  Hutchison CE, Li J, Argueso C, Gonzalez M, Lee E et al. 2006. The Arabidopsis histidine phosphotransfer proteins are redundant positive regulators of cytokinin signaling. Plant Cell 18:3073–87
    [Google Scholar]
  44. 44.  Hwang I, Sheen J, Müller B 2012. Cytokinin signaling networks. Annu. Rev. Plant Biol. 63:353–80
    [Google Scholar]
  45. 45.  Ishimaru K, Hirotsu N, Madoka Y, Murakami N, Hara N et al. 2013. Loss of function of the IAA-glucose hydrolase gene TGW6 enhances rice grain weight and increases yield. Nat. Genet. 45:707–11
    [Google Scholar]
  46. 46.  Jiang WB, Huang HY, Hu YW, Zhu SW, Wang ZY, Lin WH 2013. Brassinosteroid regulates seed size and shape in Arabidopsis. Plant Physiol 162:1965–77
    [Google Scholar]
  47. 47.  Jiang Y, Bao L, Jeong SY, Kim SK, Xu C et al. 2012. XIAO is involved in the control of organ size by contributing to the regulation of signaling and homeostasis of brassinosteroids and cell cycling in rice. Plant J 70:398–408
    [Google Scholar]
  48. 48.  Jiao Y, Wang Y, Xue D, Wang J, Yan M et al. 2010. Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat. Genet. 42:541–44
    [Google Scholar]
  49. 49.  Jin J, Hua L, Zhu Z, Tan L, Zhao X et al. 2016. GAD1 encodes a secreted peptide that regulates grain number, grain length, and awn development in rice domestication. Plant Cell 28:2453–63
    [Google Scholar]
  50. 50.  Jofuku KD, den Boer BG, Van Montagu M, Okamuro JK 1994. Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell 6:1211–25
    [Google Scholar]
  51. 51.  Jofuku KD, Omidyar PK, Gee Z, Okamuro JK 2005. Control of seed mass and seed yield by the floral homeotic gene APETALA2. PNAS 102:3117–22
    [Google Scholar]
  52. 52.  Johnson CS, Kolevski B, Smyth DR 2002. TRANSPARENT TESTA GLABRA2, a trichome and seed coat development gene of Arabidopsis, encodes a WRKY transcription factor. Plant Cell 14:1359–75
    [Google Scholar]
  53. 53.  Kang X, Li W, Zhou Y, Ni M 2013. A WRKY transcription factor recruits the SYG1-like protein SHB1 to activate gene expression and seed cavity enlargement. PLOS Genet 9:e1003347
    [Google Scholar]
  54. 54.  Kang X, Ni M 2006. Arabidopsis SHORT HYPOCOTYL UNDER BLUE1 contains SPX and EXS domains and acts in cryptochrome signaling. Plant Cell 18:921–34
    [Google Scholar]
  55. 55.  Kurepa J, Wang S, Li Y, Zaitlin D, Pierce AJ, Smalle JA 2009. Loss of 26S proteasome function leads to increased cell size and decreased cell number in Arabidopsis shoot organs. Plant Physiol 150:178–89
    [Google Scholar]
  56. 56.  Lee YK, Kim GT, Kim IJ, Park J, Kwak SS et al. 2006. LONGIFOLIA1 and LONGIFOLIA2, two homologous genes, regulate longitudinal cell elongation in Arabidopsis. Development 133:4305–14
    [Google Scholar]
  57. 57.  Leon-Kloosterziel KM, Keijzer CJ, Koornneef M 1994. A seed shape mutant of Arabidopsis that is affected in integument development. Plant Cell 6:385–92
    [Google Scholar]
  58. 58.  Li J, Nie X, Tan JL, Berger F 2013. Integration of epigenetic and genetic controls of seed size by cytokinin in Arabidopsis. PNAS 110:15479–84Shows that cytokinin acts downstream of the HAIKU pathway to control seed size.
    [Google Scholar]
  59. 59.  Li N, Li Y 2016. Signaling pathways of seed size control in plants. Curr. Opin. Plant Biol. 33:23–32
    [Google Scholar]
  60. 60.  Li N, Liu Z, Wang Z, Ru L, Gonzalez N et al. 2018. STERILE APETALA modulates the stability of a repressor protein complex to control organ size in Arabidopsis thaliana. PLOS Genet 14:e1007218
    [Google Scholar]
  61. 61.  Li Q, Li L, Yang X, Warburton ML, Bai G et al. 2010. Relationship, evolutionary fate and function of two maize co-orthologs of rice GW2 associated with kernel size and weight. BMC Plant Biol 10:143
    [Google Scholar]
  62. 62.  Li S, Gao F, Xie K, Zeng X, Cao Y et al. 2016. The OsmiR396c-OsGRF4-OsGIF1 regulatory module determines grain size and yield in rice. Plant Biotechnol. J. 14:2134–46
    [Google Scholar]
  63. 63.  Li S, Liu Y, Zheng L, Chen L, Li N et al. 2012. The plant-specific G protein γ subunit AGG3 influences organ size and shape in Arabidopsis thaliana. New Phytologist 194:690–703
    [Google Scholar]
  64. 64.  Li W, Wu J, Weng S, Zhang Y, Zhang D, Shi C 2010. Identification and characterization of dwarf 62, a loss-of-function mutation in DLT/OsGRAS-32 affecting gibberellin metabolism in rice. Planta 232:1383–96
    [Google Scholar]
  65. 65.  Li Y, Fan C, Xing Y, Jiang Y, Luo L et al. 2011. Natural variation in GS5 plays an important role in regulating grain size and yield in rice. Nat. Genet. 43:1266–69
    [Google Scholar]
  66. 66.  Li Y, Zheng L, Corke F, Smith C, Bevan MW 2008. Control of final seed and organ size by the DA1 gene family in Arabidopsis thaliana. Genes Dev 22:1331–36Demonstrates the role of the DA1 gene family in seed size control.
    [Google Scholar]
  67. 67.  Liang G, He H, Li Y, Wang F, Yu D 2014. Molecular mechanism of miR396 mediating pistil development in Arabidopsis. Plant Physiol 164:249–58
    [Google Scholar]
  68. 68.  Liu J, Chen J, Zheng X, Wu F, Lin Q et al. 2017. GW5 acts in the brassinosteroid signalling pathway to regulate grain width and weight in rice. Nat. Plants 3:17043
    [Google Scholar]
  69. 69.  Liu J, Deng M, Guo H, Raihan S, Luo J et al. 2015. Maize orthologs of rice GS5 and their trans-regulator are associated with kernel development. J. Integr. Plant Biol. 57:943–53
    [Google Scholar]
  70. 70.  Liu J, Hua W, Hu Z, Yang H, Zhang L et al. 2015. Natural variation in ARF18 gene simultaneously affects seed weight and silique length in polyploid rapeseed. PNAS 112:E5123–32
    [Google Scholar]
  71. 71.  Liu L, Tong H, Xiao Y, Che R, Xu F et al. 2015. Activation of Big Grain1 significantly improves grain size by regulating auxin transport in rice. PNAS 112:11102–7
    [Google Scholar]
  72. 72.  Liu Q, Han R, Wu K, Zhang J, Ye Y et al. 2018. G-protein βγ subunits determine grain size through interaction with MADS-domain transcription factors in rice. Nat. Commun. 9:852Shows that DEP1 and GRAIN SIZE 3 interact with MADS1 to promote the transcription of downstream genes to repress grain growth.
    [Google Scholar]
  73. 73.  Liu S, Hua L, Dong S, Chen H, Zhu X et al. 2015. OsMAPK6, a mitogen-activated protein kinase, influences rice grain size and biomass production. Plant J 84:672–81
    [Google Scholar]
  74. 74.  Lu X, Xiong Q, Cheng T, Li QT, Liu XL et al. 2017. A PP2C-1 allele underlying a quantitative trait locus enhances soybean 100-seed weight. Mol. Plant 10:670–84
    [Google Scholar]
  75. 75.  Luo J, Liu H, Zhou T, Gu B, Huang X et al. 2013. An-1 encodes a basic helix-loop-helix protein that regulates awn development, grain size, and grain number in rice. Plant Cell 25:3360–76
    [Google Scholar]
  76. 76.  Luo M, Dennis ES, Berger F, Peacock WJ, Chaudhury A 2005. MINISEED3 (MINI3), a WRKY family gene, and HAIKU2 (IKU2), a leucine-rich repeat (LRR) KINASE gene, are regulators of seed size in Arabidopsis. PNAS 102:17531–36
    [Google Scholar]
  77. 77.  Mao H, Sun S, Yao J, Wang C, Yu S et al. 2010. Linking differential domain functions of the GS3 protein to natural variation of grain size in rice. PNAS 107:19579–84
    [Google Scholar]
  78. 78.  Meng LS, Wang ZB, Yao SQ, Liu A 2015. The ARF2–ANT–COR15A gene cascade regulates ABA-signaling-mediated resistance of large seeds to drought in Arabidopsis. J. Cell Sci 128:3922–32
    [Google Scholar]
  79. 79.  Miao J, Yang Z, Zhang D, Wang Y, Xu M et al. 2019. Mutation of RGG2, which encodes a type B heterotrimeric G protein γ subunit, increases grain size and yield production in rice. Plant Biotechnol. J. 17:650–64
    [Google Scholar]
  80. 80.  Miura K, Ikeda M, Matsubara A, Song XJ, Ito M et al. 2010. OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat. Genet. 42:545–49
    [Google Scholar]
  81. 81.  Morinaka Y, Sakamoto T, Inukai Y, Agetsuma M, Kitano H et al. 2006. Morphological alteration caused by brassinosteroid insensitivity increases the biomass and grain production of rice. Plant Physiol 141:924–31
    [Google Scholar]
  82. 82.  Nagasawa N, Hibara K, Heppard EP, Vander Velden KA, Luck S et al. 2013. GIANT EMBRYO encodes CYP78A13, required for proper size balance between embryo and endosperm in rice. Plant J 75:592–605
    [Google Scholar]
  83. 83.  Noguero M, Le Signor C, Vernoud V, Bandyopadhyay K, Sanchez M et al. 2015. DASH transcription factor impacts Medicago truncatula seed size by its action on embryo morphogenesis and auxin homeostasis. Plant J 81:453–66
    [Google Scholar]
  84. 84.  Ohto MA, Fischer RL, Goldberg RB, Nakamura K, Harada JJ 2005. Control of seed mass by APETALA2. PNAS 102:3123–28
    [Google Scholar]
  85. 85.  Okushima Y, Mitina I, Quach HL, Theologis A 2005. AUXIN RESPONSE FACTOR 2 (ARF2): a pleiotropic developmental regulator. Plant J 43:29–46
    [Google Scholar]
  86. 86.  Orozco-Arroyo G, Paolo D, Ezquer I, Colombo L 2015. Networks controlling seed size in Arabidopsis. Plant Reprod 28:17–32
    [Google Scholar]
  87. 87.  Pandey S, Vijayakumar A 2018. Emerging themes in heterotrimeric G-protein signaling in plants. Plant Sci 270:292–300
    [Google Scholar]
  88. 88.  Peng Y, Chen L, Li S, Zhang Y, Xu R et al. 2018. BRI1 and BAK1 interact with G proteins and regulate sugar-responsive growth and development in Arabidopsis. Nat. Commun 9:1522
    [Google Scholar]
  89. 89.  Qi P, Lin YS, Song XJ, Shen JB, Huang W et al. 2012. The novel quantitative trait locus GL3.1 controls rice grain size and yield by regulating Cyclin-T1;3. Cell Res 22:1666–80
    [Google Scholar]
  90. 90.  Riefler M, Novak O, Strnad M, Schmülling T 2006. Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. Plant Cell 18:40–54
    [Google Scholar]
  91. 91.  Rodriguez RE, Mecchia MA, Debernardi JM, Schommer C, Weigel D, Palatnik JF 2010. Control of cell proliferation in Arabidopsis thaliana by microRNA miR396. Development 137:103–12
    [Google Scholar]
  92. 92.  Schruff MC, Spielman M, Tiwari S, Adams S, Fenby N, Scott RJ 2006. The AUXIN RESPONSE FACTOR 2 gene of Arabidopsis links auxin signalling, cell division, and the size of seeds and other organs. Development 133:251–61
    [Google Scholar]
  93. 93.  Segami S, Kono I, Ando T, Yano M, Kitano H et al. 2012. Small and round seed 5 gene encodes alpha-tubulin regulating seed cell elongation in rice. Rice 5:4
    [Google Scholar]
  94. 94.  Segami S, Takehara K, Yamamoto T, Kido S, Kondo S et al. 2017. Overexpression of SRS5 improves grain size of brassinosteroid-related dwarf mutants in rice (Oryza sativa L.). Breed Sci 67:393–97
    [Google Scholar]
  95. 95.  Shomura A, Izawa T, Ebana K, Ebitani T, Kanegae H et al. 2008. Deletion in a gene associated with grain size increased yields during rice domestication. Nat. Genet. 40:1023–28
    [Google Scholar]
  96. 96.  Si L, Chen J, Huang X, Gong H, Luo J et al. 2016. OsSPL13 controls grain size in cultivated rice. Nat. Genet. 48:447–56
    [Google Scholar]
  97. 97.  Smalle J, Vierstra RD 2004. The ubiquitin 26S proteasome proteolytic pathway. Annu. Rev. Plant Biol. 55:555–90
    [Google Scholar]
  98. 98.  Song XJ, Huang W, Shi M, Zhu MZ, Lin HX 2007. A QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase. Nat. Genet. 39:623–30
    [Google Scholar]
  99. 99.  Song XJ, Kuroha T, Ayano M, Furuta T, Nagai K et al. 2015. Rare allele of a previously unidentified histone H4 acetyltransferase enhances grain weight, yield, and plant biomass in rice. PNAS 112:76–81
    [Google Scholar]
  100. 100.  Su Z, Hao C, Wang L, Dong Y, Zhang X 2011. Identification and development of a functional marker of TaGW2 associated with grain weight in bread wheat (Triticum aestivum L.). Theor. Appl. Genet. 122:211–23
    [Google Scholar]
  101. 101.  Sun H, Qian Q, Wu K, Luo J, Wang S et al. 2014. Heterotrimeric G proteins regulate nitrogen-use efficiency in rice. Nat. Genet. 46:652–56
    [Google Scholar]
  102. 102.  Sun L, Li X, Fu Y, Zhu Z, Tan L et al. 2013. GS6, a member of the GRAS gene family, negatively regulates grain size in rice. J. Integr. Plant Biol. 55:938–49
    [Google Scholar]
  103. 103.  Sun P, Zhang W, Wang Y, He Q, Shu F et al. 2016. OsGRF4 controls grain shape, panicle length and seed shattering in rice. J. Integr. Plant Biol. 58:836–47
    [Google Scholar]
  104. 104.  Sun S, Wang L, Mao H, Shao L, Li X et al. 2018. A G-protein pathway determines grain size in rice. Nat. Commun. 9:851Demonstrates that GRAIN SIZE 3 acts antagonistically with DEP1 and GGC2 to regulate grain size by competitively binding Gβ.
    [Google Scholar]
  105. 105.  Sun X, Shantharaj D, Kang X, Ni M 2010. Transcriptional and hormonal signaling control of Arabidopsis seed development. Curr. Opin. Plant Biol. 13:611–20
    [Google Scholar]
  106. 106.  Sun Y, Wang C, Wang N, Jiang X, Mao H et al. 2017. Manipulation of Auxin Response Factor 19 affects seed size in the woody perennial Jatropha curcas. Sci. Rep 7:40844
    [Google Scholar]
  107. 107.  Takano-Kai N, Jiang H, Kubo T, Sweeney M, Matsumoto T et al. 2009. Evolutionary history of GS3, a gene conferring grain length in rice. Genetics 182:1323–34
    [Google Scholar]
  108. 108.  Tanabe S, Ashikari M, Fujioka S, Takatsuto S, Yoshida S et al. 2005. A novel cytochrome P450 is implicated in brassinosteroid biosynthesis via the characterization of a rice dwarf mutant, dwarf11, with reduced seed length. Plant Cell 17:776–90
    [Google Scholar]
  109. 109.  Tang W, Wu T, Ye J, Sun J, Jiang Y et al. 2016. SNP-based analysis of genetic diversity reveals important alleles associated with seed size in rice. BMC Plant Biol 16:93
    [Google Scholar]
  110. 110.  Tian X, Li X, Zhou W, Ren Y, Wang Z et al. 2017. Transcription factor OsWRKY53 positively regulates brassinosteroid signaling and plant architecture. Plant Physiol 175:1337–49
    [Google Scholar]
  111. 111.  Tong H, Liu L, Jin Y, Du L, Yin Y et al. 2012. DWARF AND LOW-TILLERING acts as a direct downstream target of a GSK3/SHAGGY-like kinase to mediate brassinosteroid responses in rice. Plant Cell 24:2562–77
    [Google Scholar]
  112. 112.  Utsunomiya Y, Samejima C, Takayanagi Y, Izawa Y, Yoshida T et al. 2011. Suppression of the rice heterotrimeric G protein β-subunit gene, RGB1, causes dwarfism and browning of internodes and lamina joint regions. Plant J 67:907–16
    [Google Scholar]
  113. 113.  Vanhaeren H, Inzé D, Gonzalez N 2016. Plant growth beyond limits. Trends Plant Sci 21:102–9
    [Google Scholar]
  114. 114.  Wan X, Weng J, Zhai H, Wang J, Lei C et al. 2008. Quantitative trait loci (QTL) analysis for rice grain width and fine mapping of an identified QTL allele gw-5 in a recombination hotspot region on chromosome 5. Genetics 179:2239–52
    [Google Scholar]
  115. 115.  Wang A, Garcia D, Zhang H, Feng K, Chaudhury A et al. 2010. The VQ motif protein IKU1 regulates endosperm growth and seed size in Arabidopsis. Plant J 63:670–79
    [Google Scholar]
  116. 116.  Wang J, Nakazaki T, Chen S, Chen W, Saito H et al. 2009. Identification and characterization of the erect-pose panicle gene EP conferring high grain yield in rice (Oryza sativa L.). Theor. Appl. Genet. 119:85–91
    [Google Scholar]
  117. 117.  Wang JL, Tang MQ, Chen S, Zheng XF, Mo HX et al. 2017. Down-regulation of BnDA1, whose gene locus is associated with the seeds weight, improves the seeds weight and organ size in Brassica napus. Plant Biotechnol. J 15:1024–33
    [Google Scholar]
  118. 118.  Wang S, Li S, Liu Q, Wu K, Zhang J et al. 2015. The OsSPL16-GW7 regulatory module determines grain shape and simultaneously improves rice yield and grain quality. Nat. Genet. 47:949–54
    [Google Scholar]
  119. 119.  Wang S, Wu K, Qian Q, Liu Q, Li Q et al. 2017. Non-canonical regulation of SPL transcription factors by a human OTUB1-like deubiquitinase defines a new plant type rice associated with higher grain yield. Cell Res 27:1142–56
    [Google Scholar]
  120. 120.  Wang S, Wu K, Yuan Q, Liu X, Liu Z et al. 2012. Control of grain size, shape and quality by OsSPL16 in rice. Nat. Genet. 44:950–54
    [Google Scholar]
  121. 121.  Wang X, Li Y, Zhang H, Sun G, Zhang W, Qiu L 2015. Evolution and association analysis of GmCYP78A10 gene with seed size/weight and pod number in soybean. Mol. Biol. Rep. 42:489–96
    [Google Scholar]
  122. 122.  Wang Y, Xiong G, Hu J, Jiang L, Yu H et al. 2015. Copy number variation at the GL7 locus contributes to grain size diversity in rice. Nat. Genet. 47:944–48
    [Google Scholar]
  123. 123.  Wang Z, Li N, Jiang S, Gonzalez N, Huang X et al. 2016. SCFSAP controls organ size by targeting PPD proteins for degradation in Arabidopsis thaliana. Nat. Commun 7:11192
    [Google Scholar]
  124. 124.  Weijers D, Friml J 2009. SnapShot: auxin signaling and transport. Cell 136:1172–72.E1
    [Google Scholar]
  125. 125.  Weng J, Gu S, Wan X, Gao H, Guo T et al. 2008. Isolation and initial characterization of GW5, a major QTL associated with rice grain width and weight. Cell Res 18:1199–209
    [Google Scholar]
  126. 126.  Werner T, Motyka V, Laucou V, Smets R, Van Onckelen H, Schmülling T 2003. Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell 15:2532–50
    [Google Scholar]
  127. 127.  White DW 2006. PEAPOD regulates lamina size and curvature in Arabidopsis. PNAS 103:13238–43
    [Google Scholar]
  128. 128.  Wu Y, Fu Y, Zhao S, Gu P, Zhu Z et al. 2016. CLUSTERED PRIMARY BRANCH 1, a new allele of DWARF11, controls panicle architecture and seed size in rice. Plant Biotechnol. J. 14:377–86
    [Google Scholar]
  129. 129.  Xia D, Zhou H, Liu R, Dan W, Li P et al. 2018. GL3.3, a novel QTL encoding a GSK3/SHAGGY-like Kinase, epistatically interacts with GS3 to form extra-long grains in rice. Mol. Plant 11:754–56
    [Google Scholar]
  130. 130.  Xia T, Li N, Dumenil J, Li J, Kamenski A et al. 2013. The ubiquitin receptor DA1 interacts with the E3 ubiquitin ligase DA2 to regulate seed and organ size in Arabidopsis. Plant Cell 25:3347–59
    [Google Scholar]
  131. 131.  Xiang J, Tang S, Zhi H, Jia G, Wang H, Diao X 2017. Loose Panicle1 encoding a novel WRKY transcription factor, regulates panicle development, stem elongation, and seed size in foxtail millet [Setaria italica (L.) P. Beauv.]. PLOS ONE 12:e0178730
    [Google Scholar]
  132. 132.  Xiao YG, Sun QB, Kang XJ, Chen CB, Ni M 2016. SHORT HYPOCOTYL UNDER BLUE1 or HAIKU2 mixepression alters canola and Arabidopsis seed development. New Phytol 209:636–49
    [Google Scholar]
  133. 133.  Xie G, Li Z, Ran Q, Wang H, Zhang J 2018. Over-expression of mutated ZmDA1 or ZmDAR1 gene improves maize kernel yield by enhancing starch synthesis. Plant Biotechnol. J. 16:234–44
    [Google Scholar]
  134. 134.  Xing Y, Zhang Q 2010. Genetic and molecular bases of rice yield. Annu. Rev. Plant Biol. 61:421–42
    [Google Scholar]
  135. 135.  Xu C, Liu Y, Li Y, Xu X, Li X et al. 2015. Differential expression of GS5 regulates grain size in rice. J. Exp. Bot. 66:2611–23
    [Google Scholar]
  136. 136.  Xu F, Fang J, Ou S, Gao S, Zhang F et al. 2015. Variations in CYP78A13 coding region influence grain size and yield in rice. Plant Cell Environ 38:800–11
    [Google Scholar]
  137. 137.  Xu J, Zhang S 2015. Mitogen-activated protein kinase cascades in signaling plant growth and development. Trends Plant Sci 20:56–64
    [Google Scholar]
  138. 138.  Xu R, Duan P, Yu H, Zhou Z, Zhang B et al. 2018. Control of grain size and weight by the OsMKKK10-OsMKK4-OsMAPK6 signaling pathway in rice. Mol. Plant 11:860–73Demonstrates that OsMKKK10, OsMKK4, and OsMAPK6 act as a cascade to regulate grain size.
    [Google Scholar]
  139. 139.  Xu R, Yu H, Wang J, Duan P, Zhang B et al. 2018. A mitogen-activated protein kinase phosphatase influences grain size and weight in rice. Plant J 95:937–46Shows that OsMKP1 negatively regulates grain size by dephosphorylating OsMAPK6.
    [Google Scholar]
  140. 140.  Yang W, Gao M, Yin X, Liu J, Xu Y et al. 2013. Control of rice embryo development, shoot apical meristem maintenance, and grain yield by a novel cytochrome p450. Mol. Plant 6:1945–60
    [Google Scholar]
  141. 141.  Ye J, Liu P, Zhu C, Qu J, Wang X et al. 2014. Identification of candidate genes JcARF19 and JcIAA9 associated with seed size traits in Jatropha. Funct. Integr. Genom. 14:757–66
    [Google Scholar]
  142. 142.  Yi X, Zhang Z, Zeng S, Tian C, Peng J et al. 2011. Introgression of qPE9–1 allele, conferring the panicle erectness, leads to the decrease of grain yield per plant in japonica rice (Oryza sativa L.). J. Genet. Genom. 38:217–23
    [Google Scholar]
  143. 143.  Ying JZ, Ma M, Bai C, Huang X, Liu JL et al. 2018. TGW3, a major QTL that negatively modulates grain length and weight in rice. Mol. Plant 11:750–53
    [Google Scholar]
  144. 144.  Yoo SJ, Kim SH, Kim MJ, Ryu CM, Kim YC et al. 2014. Involvement of the OsMKK4-OsMPK1 cascade and its downstream transcription factor OsWRKY53 in the wounding response in rice. Plant Pathol. J. 30:168–77
    [Google Scholar]
  145. 145.  Yu J, Miao J, Zhang Z, Xiong H, Zhu X et al. 2018. Alternative splicing of OsLG3b controls grain length and yield in japonica rice. Plant Biotechnol. J. 16:1667–78
    [Google Scholar]
  146. 146.  Yuan GL, Li HJ, Yang WC 2017. The integration of Gβ and MAPK signaling cascade in zygote development. Sci. Rep. 7:8732
    [Google Scholar]
  147. 147.  Yuan H, Fan S, Huang J, Zhan S, Wang S et al. 2017. 08SG2/OsBAK1 regulates grain size and number, and functions differently in Indica and Japonica backgrounds in rice. Rice 10:25
    [Google Scholar]
  148. 148.  Zhang M, Wu H, Su J, Wang H, Zhu Q et al. 2017. Maternal control of embryogenesis by MPK6 and its upstream MKK4/MKK5 in Arabidopsis. Plant J 92:1005–19
    [Google Scholar]
  149. 149.  Zhang X, Wang J, Huang J, Lan H, Wang C et al. 2012. Rare allele of OsPPKL1 associated with grain length causes extra-large grain and a significant yield increase in rice. PNAS 109:21534–39
    [Google Scholar]
  150. 150.  Zhang Y, Du L, Xu R, Cui R, Hao J et al. 2015. Transcription factors SOD7/NGAL2 and DPA4/NGAL3 act redundantly to regulate seed size by directly repressing KLU expression in Arabidopsis thaliana. Plant Cell 27:620–32
    [Google Scholar]
  151. 151.  Zhao B, Dai A, Wei H, Yang S, Wang B et al. 2016. Arabidopsis KLU homologue GmCYP78A72 regulates seed size in soybean. Plant Mol. Biol. 90:33–47
    [Google Scholar]
  152. 152.  Zhao D-S, Li Q-F, Zhang C-Q, Zhang C, Yang Q-Q et al. 2018. GS9 acts as a transcriptional activator to regulate rice grain shape and appearance quality. Nat. Commun. 9:1240
    [Google Scholar]
  153. 153.  Zhou Y, Miao J, Gu H, Peng X, Leburu M et al. 2015. Natural variations in SLG7 regulate grain shape in rice. Genetics 201:1591–99
    [Google Scholar]
  154. 154.  Zhou Y, Tao Y, Zhu J, Miao J, Liu J et al. 2017. GNS4, a novel allele of DWARF11, regulates grain number and grain size in a high-yield rice variety. Rice 10:34
    [Google Scholar]
  155. 155.  Zhou Y, Zhang X, Kang X, Zhao X, Ni M 2009. SHORT HYPOCOTYL UNDER BLUE1 associates with MINISEED3 and HAIKU2 promoters in vivo to regulate Arabidopsis seed development. Plant Cell 21:106–17
    [Google Scholar]
  156. 156.  Zhou Y, Zhu J, Li Z, Yi C, Liu J et al. 2009. Deletion in a quantitative trait gene qPE9-1 associated with panicle erectness improves plant architecture during rice domestication. Genetics 183:315–24
    [Google Scholar]
  157. 157.  Zuo J, Li J 2014. Molecular genetic dissection of quantitative trait loci regulating rice grain size. Annu. Rev. Genet. 48:99–118
    [Google Scholar]
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