An evolutionarily conserved gene, FUWA, plays a role in determining panicle architecture, grain shape and grain weight in rice

Plant Journal

Volumn 83, Issue 3, 2015, Pages 427-438

  Chen, Jun ^a   Gao, He ^b,c   Zheng, Xiao Ming ^a   Jin, Mingna ^a   Weng, Jian Feng ^a   Ma, Jin ^a   Ren, Yulong ^a   Zhou, Kunneng ^b   Wang, Qi ^b   Wang, Jie ^a   Wang, Jiu Lin ^a   Zhang, Xin ^a   Cheng, Zhijun ^a   Wu, Chuanyin ^a   Wang, Haiyang ^a   Wan, Jian Min ^a,b  

^a INSTITUTE OF PLANT PROTECTION   (China)

^b NANJING AGRICULTURAL UNIVERSITY   (China)

^c MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

Author keywords

cell division; domestication; FUWA; grain size; panicle architecture; rice

Indexed keywords

AGRONOMY; ARCHITECTURE; CELL PROLIFERATION; CROPS; GRAIN SIZE AND SHAPE; PLANTS (BOTANY); TRANSCRIPTION;

CELL DIVISIONS; DOMESTICATION; FUWA; GRAIN SIZE; RICE;

GRAIN (AGRICULTURAL PRODUCT);

JAPONICA; ZEA MAYS;

VEGETABLE PROTEIN;

GENE EXPRESSION REGULATION; GENETICS; GERMLINE MUTATION; GROWTH, DEVELOPMENT AND AGING; MAIZE; MOLECULAR GENETICS; ORYZA; PLANT GENE; SORGHUM;

GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GERM-LINE MUTATION; MOLECULAR SEQUENCE DATA; ORYZA; PLANT PROTEINS; SORGHUM; ZEA MAYS;

EID: 84938065068     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12895     Document Type: Article

References (64)

1. Ashikari, M., Sakakibara, H., Lin, S.Y., Yamamoto, T., Takashi, T., Nishimura, A., Angeles, E.R., Qian, Q., Kitano, H., and, Matsuoka, M., (2005) Cytokinin oxidase regulates rice grain production. Science, 309, 741-745.
2. Bart, R., Chern, M., Park, C.-J., Bartley, L., and, Ronald, P.C., (2006) A novel system for gene silencing using siRNAs in rice leaf and stem-derived protoplasts. Plant Methods, 2, 13.
3. Bradley, D., Carpenter, R., Sommer, H., Hartley, N., and, Coen, E., (1993) Complementary floral homeotic phenotypes result from opposite orientations of a transposon at the plena locus of antirrhinum. Cell, 72, 85-95.
4. Dewitte, W., and, Murray, J.A.H., (2003) The plant cell cycle. Annu. Rev. Plant Biol. 54, 235-264.
5. Frank, D.J., Edgar, B.A., and, Roth, M.B., (2002) The Drosophila melanogaster gene brain tumor negatively regulates cell growth and ribosomal RNA synthesis. Development, 129, 399-407.
6. Garris, A.J., Tai, T.H., Coburn, J., Kresovich, S., and, McCouch, S., (2005) Genetic structure and diversity in Oryza sativa L. Genetics, 169, 1631-1638.
7. Godfray, H.C.J., Beddington, J.R., Crute, I.R., Haddad, L., Lawrence, D., Muir, J.F., Pretty, J., Robinson, S., Thomas, S.M., and, Toulmin, C., (2010) Food security: the challenge of feeding 9 billion people. Science, 327, 812-818.
8. Goff, S.A., Ricke, D., Lan, T.-H., Presting, G., Wang, R., Dunn, M., Glazebrook, J., Sessions, A., Oeller, P., and, Varma, H., (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science, 296, 92-100.
9. Harlan, J.R., (1975) Crops and Man. Madison, WI: American Society of Agronomy/Crop Science Society.
10. Hong, Z., Ueguchi-Tanaka, M., Fujioka, S., Takatsuto, S., Yoshida, S., Hasegawa, Y., Ashikari, M., Kitano, H., and, Matsuoka, M., (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, 2243-2254.
11. Huang, X., Qian, Q., Liu, Z., Sun, H., He, S., Luo, D., Xia, G., Chu, C., Li, J., and, Fu, X., (2009) Natural variation at the DEP1 locus enhances grain yield in rice. Nat. Genet. 41, 494-497.
12. Huang, X.H., Yang, S.H., Gong, J.Y., et al. (2015) Genomic analysis of hybrid rice varieties reveals numerous superior alleles that contribute to heterosis. Nat. Commun. 6, 6258.
13. Hudson, R.R., Kreitman, M., and, Aguadé, M., (1987) A test of neutral molecular evolution based on nucleotide data. Genetics, 116, 153-159.
14. Ikeda, K., Sunohara, H., and, Nagato, Y., (2004) Developmental course of inflorescence and spikelet in rice. Breeding Sci. 54, 147-156.
15. Inze, D., and, De Veylder, L., (2006) Cell cycle regulation in plant development. Annu. Rev. Genet. 40, 77-105.
16. Ishimaru, K., Hirotsu, N., Madoka, Y., Murakami, N., Hara, N., Onodera, H., Kashiwagi, T., Ujiie, K., Shimizu, B.-I., and, Onishi, A., (2013) Loss of function of the IAA-glucose hydrolase gene TGW6 enhances rice grain weight and increases yield. Nat. Genet. 45, 707-711.
17. Jiang, Y., Bao, L., Jeong, S.Y., Kim, S.K., Xu, C., Li, X., and, Zhang, Q., (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.
18. Jiao, Y., Wang, Y., Xue, D., Wang, J., Yan, M., Liu, G., Dong, G., Zeng, D., Lu, Z., and, Zhu, X., (2010) Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat. Genet. 42, 541-544.
19. Juliano, B.O., and, Villareal, C., (1993) Grain Quality Evaluation of World Rices. Manila, Philippines: International Rice Research Institute.
20. Komatsu, K., Maekawa, M., Ujiie, S., Satake, Y., Furutani, I., Okamoto, H., Shimamoto, K., and, Kyozuka, J., (2003a) LAX and SPA: major regulators of shoot branching in rice. Proc. Natl. Acad. Sci. USA, 100, 11765-11770.
21. Komatsu, M., Chujo, A., Nagato, Y., Shimamoto, K., and, Kyozuka, J., (2003b) FRIZZY PANICLE is required to prevent the formation of axillary meristems and to establish floral meristem identity in rice spikelets. Development, 130, 3841-3850.
22. Kono, A., Umeda-Hara, C., Lee, J., Ito, M., Uchimiya, H., and, Umeda, M., (2003) Arabidopsis D-type cyclin CYCD4;1 is a novel cyclin partner of B2-type cyclin-dependent kinase. Plant Physiol. 132, 1315-1321.
23. Kovach, M.J., Sweeney, M.T., and, McCouch, S.R., (2007) New insights into the history of rice domestication. Trends Genet. 23, 578-587.
24. Li, F., Liu, W., Tang, J., Chen, J., Tong, H., Hu, B., Li, C., Fang, J., Chen, M., and, Chu, C., (2010) Rice DENSE AND ERECT PANICLE 2 is essential for determining panicle outgrowth and elongation. Cell Res. 20, 838-849.
25. Li, M., Tang, D., Wang, K.J., Wu, X.R., Lu, L.L., Yu, H.X., Gu, M.H., Yan, C.J., and, Cheng, Z.K., (2011a) Mutations in the F-box gene LARGER PANICLE improve the panicle architecture and enhance the grain yield in rice. Plant Biotechnol. J. 9, 1002-1013.
26. Li, Y., Fan, C., Xing, Y., Jiang, Y., Luo, L., Sun, L., Shao, D., Xu, C., Li, X., and, Xiao, J., (2011b) Natural variation in GS5 plays an important role in regulating grain size and yield in rice. Nat. Genet. 43, 1266-1269.
27. Li, H., Jiang, L., Youn, J.H., Sun, W., Cheng, Z., Jin, T., Ma, X., Guo, X., Wang, J., and, Zhang, X., (2013a) A comprehensive genetic study reveals a crucial role of CYP90D2/D2 in regulating plant architecture in rice (Oryza sativa). New Phytol. 200, 1076-1088.
28. Li, S., Zhao, B., Yuan, D., Duan, M., Qian, Q., Tang, L., Wang, B., Liu, X., Zhang, J., and, Wang, J., (2013b) Rice zinc finger protein DST enhances grain production through controlling Gn1a/OsCKX2 expression. Proc. Natl. Acad. Sci. USA, 110, 3167-3172.
29. Loedige, I., and, Filipowicz, W., (2009) TRIM-NHL proteins take on miRNA regulation. Cell, 136, 818-820.
30. Mao, H., Sun, S., Yao, J., Wang, C., Yu, S., Xu, C., Li, X., and, Zhang, Q., (2010) Linking differential domain functions of the GS3 protein to natural variation of grain size in rice. Proc. Natl. Acad. Sci. USA, 107, 19579-19584.
31. McCouch, S., (2004) Diversifying selection in plant breeding. PLoS Biol. 2, e347.
32. Miura, K., Ikeda, M., Matsubara, A., Song, X.-J., Ito, M., Asano, K., Matsuoka, M., Kitano, H., and, Ashikari, M., (2010) OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat. Genet. 42, 545-549.
33. Mori, M., Nomura, T., Ooka, H., et al. (2002) Isolation and characterization of a rice dwarf mutant with a defect in brassinosteroid biosynthesis. Plant Physiol. 130, 1152-1161.
34. Nakagawa, H., Tanaka, A., Tanabata, T., Ohtake, M., Fujioka, S., Nakamura, H., Ichikawa, H., and, Mori, M., (2012) SHORT GRAIN1 decreases organ elongation and brassinosteroid response in rice. Plant Physiol. 158, 1208-1219.
35. Neumuller, R.A., Betschinger, J., Fischer, A., Bushati, N., Poernbacher, I., Mechtler, K., Cohen, S.M., and, Knoblich, J.A., (2008) Mei-P26 regulates microRNAs and cell growth in the Drosophila ovarian stem cell lineage. Nature, 454, 241-245.
36. Piao, R., Jiang, W., Ham, T.H., et al. (2009) Map-based cloning of the ERECT PANICLE 3 gene in rice. Theor. Appl. Genet. 119, 1497-1506.
37. Qi, P., Lin, Y.-S., Song, X.-J., Shen, J.-B., Huang, W., Shan, J.-X., Zhu, M.-Z., Jiang, L., Gao, J.-P., and, Lin, H.-X., (2012) The novel quantitative trait locus GL3.1 controls rice grain size and yield by regulating Cyclin-T1;3. Cell Res. 22, 1666-1680.
38. Rosegrant, M.W., and, Cline, S.A., (2003) Global food security: challenges and policies. Science, 302, 1917-1919.
39. Rozas, J., Sánchez-DelBarrio, J.C., Messeguer, X., and, Rozas, R., (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics, 19, 2496-2497.
40. Sang, T., (2009) Genes and mutations underlying domestication transitions in grasses. Plant Physiol. 149, 63-70.
41. Shomura, A., Izawa, T., Ebana, K., Ebitani, T., Kanegae, H., Konishi, S., and, Yano, M., (2008) Deletion in a gene associated with grain size increased yields during rice domestication. Nat. Genet. 40, 1023-1028.
42. Slack, F.J., and, Ruvkun, G., (1998) A novel repeat domain that is often associated with RING finger and B-box motifs. Trends Biochem. Sci. 23, 474-475.
43. Song, X.-J., Huang, W., Shi, M., Zhu, M.-Z., and, Lin, H.-X., (2007) A QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase. Nat. Genet. 39, 623-630.
44. Song, X.J., Kuroha, T., Ayano, M., et al. (2015) Rare allele of a previously unidentified histone H4 acetyltransferase enhances grain weight, yield, and plant biomass in rice. Proc. Natl Acad. Sci. USA, 112, 76-81.
45. Sonoda, J., and, Wharton, R.P., (2001) Drosophila brain tumor is a translational repressor. Genes Dev. 15, 762-773.
46. Surridge, C., (2002) Agricultural biotech: the rice squad. Nature, 416, 576-578.
47. Tajima, F., (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123, 585-595.
48. Tanabe, S., Ashikari, M., Fujioka, 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, 776-790.
49. Tanksley, S.D., and, McCouch, S.R., (1997) Seed banks and molecular maps: unlocking genetic potential from the wild. Science, 277, 1063-1066.
50. Unnevehr, L., Duff, B., and, Juliano, B.O., (1992) Consumer Demand for Rice Grain Quality: Terminal Report of IDRC Projects National Grain Quality (Asia) and International Grain Quality Economics (Asia). Manila, Philippines: International Rice Research Institute.
51. Wang, E., Wang, J., Zhu, X., Hao, W., Wang, L., Li, Q., Zhang, L., He, W., Lu, B., and, Lin, H., (2008) Control of rice grain-filling and yield by a gene with a potential signature of domestication. Nat. Genet. 40, 1370-1374.
52. Wang, S., Wu, K., Yuan, Q., Liu, X., Liu, Z., Lin, X., Zeng, R., Zhu, H., Dong, G., and, Qian, Q., (2012) Control of grain size, shape and quality by OsSPL16 in rice. Nat. Genet. 44, 950-954.
53. Weingartner, M., Pelayo, H.R., Binarova, P., Zwerger, K., Melikant, B., de la Torre, C., Heberle-Bors, E., and, Bogre, L., (2003) A plant cyclin B2 is degraded early in mitosis and its ectopic expression shortens G2 phase and alleviates the DNA-damage checkpoint. J. Cell Sci. 116, 487-498.
54. Weng, J., Gu, S., Wan, X., Gao, H., Guo, T., Su, N., Lei, C., Zhang, X., Cheng, Z., and, Guo, X., (2008) Isolation and initial characterization of GW5, a major QTL associated with rice grain width and weight. Cell Res. 18, 1199-1209.
55. Wright, S.I., and, Charlesworth, B., (2004) The HKA test revisited: a maximum-likelihood ratio test of the standard neutral model. Genetics, 168, 1071-1076.
56. Xing, Y.Z., and, Zhang, Q.F., (2010) Genetic and molecular bases of rice yield. Annu. Rev. Plant Biol. 61, 421-442.
57. Xu, X., Liu, X., Ge, S., et al. (2012) Resequencing 50 accessions of cultivated and wild rice yields markers for identifying agronomically important genes. Nat. Biotechnol. 30, 105-111.
58. Yoshida, A., Sasao, M., Yasuno, N., et al. (2013) TAWAWA1, a regulator of rice inflorescence architecture, functions through the suppression of meristem phase transition. Proc. Natl Acad. Sci. USA, 110, 767-772.
59. Yu, J., Hu, S., Wang, J., Wong, G.K.-S., Li, S., Liu, B., Deng, Y., Dai, L., Zhou, Y., and, Zhang, X., (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science, 296, 79-92.
60. Zhang, X., Wang, J., Huang, J., Lan, H., Wang, C., Yin, C., Wu, Y., Tang, H., Qian, Q., and, Li, J., (2012) Rare allele of OsPPKL1 associated with grain length causes extra-large grain and a significant yield increase in rice. Proc. Natl. Acad. Sci. USA, 109, 21534-21539.
61. Zhu, Q., Zheng, X., Luo, J., Gaut, B.S., and, Ge, S., (2007) Multilocus analysis of nucleotide variation of Oryza sativa and its wild relatives: severe bottleneck during domestication of rice. Mol. Biol. Evol. 24, 875-888.
62. Zhu, K.M., Tang, D., Yan, C.J., Chi, Z.C., Yu, H.X., Chen, J.M., Liang, J.S., Gu, M.H., and, Cheng, Z.K., (2010) ERECT PANICLE2 encodes a novel protein that regulates panicle erectness in indica rice. Genetics, 184, 343-350.
63. Zuo, J., and, Li, J., (2013) Molecular dissection of complex agronomic traits of rice: a team effort by Chinese scientists in recent years. Natl. Sci. Rev. 48, 99-118.
64. Zuo, J.R., and, Li, J.Y., (2014) Molecular genetic dissection of quantitative trait loci regulating rice grain size. Annu. Rev. Genet. 48, 99-118.