Advances in the Molecular Mechanism and Genetic Regulation of Grain-filling Rate in Rice

doi:10.11983/CBB20157

Abstract

Abstract: High yield and good quality of rice are important guarantees for food security in China, as well as the objective which breeders are pursuing. Grain-filling rate (GFR) is an important and complex agronomic trait in rice, directly affecting grain plumpness, weight, and quality. To date, elite rice germplasm with rapid GFR is rare, and valuable gene resources for breeding remain limited, which has become a bottleneck for further improvement of yield and quality in rice breeding. Comparing with other rice agronomic traits, GFR is highly complex for its spatio-temporal dynamics and environment- dependent variability, the research of which has long been concentrated on the physiological and biochemical characteristics and cultivation measure control of grain-filling period. The study on the molecular mechanism and genetic regulation of GFR has arisen relatively recently. Here, focusing on the GFR-related genes in rice identified recently, we reviewed the preliminarily known molecular mechanism and genetic regulation of GFR, including the influence of sugar metabolism and transport-related genes on GFR, the transcriptional and translational regulatory genes in GFR, the function of grain size and weight-related quantitative trait loci (QTLs) of GFR, and the analysis of GFR-related QTLs; we also discussed the future perspective of the research strategies for GFR, especially the application potential of phenomics-related technologies for GFR research, in order to promote the foundational research and application in rice breeding.

Key words: rice, grain-filling rate, molecular mechanism, genetic regulation, quantitative trait locus

Sunlu Chen, Chengfang Zhan, Hong Jiang, Linhan Li, Hongsheng Zhang. Advances in the Molecular Mechanism and Genetic Regulation of Grain-filling Rate in Rice[J]. Chinese Bulletin of Botany, 2021, 56(1): 80-89.

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URL: https://www.chinbullbotany.com/EN/10.11983/CBB20157

https://www.chinbullbotany.com/EN/Y2021/V56/I1/80

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References 75

[1]	贾小丽, 叶江华, 苗利国, 林红梅, 林文雄 (2012). 水稻重组自交群体灌浆速率的遗传分析. 中国农学通报 28(21), 22-26.
[2]	施伟, 朱国永, 孙明法, 王爱民, 陈中兵, 严国红 (2020). 水稻籽粒灌浆的影响因子及其机制研究进展. 中国农学通报 36(8), 1-7.
[3]	Aoki N, Hirose T, Scofield GN, Whitfeld PR, Furbank RT (2003). The sucrose transporter gene family in rice. Plant Cell Physiol 44, 223-232. DOI URL PMID
[4]	Cai YC, Li SF, Jiao GA, Sheng ZH, Wu YW, Shao GN, Xie LH, Peng C, Xu JF, Tang SQ, Wei XJ, Hu PS (2018). OsPK2 encodes a plastidic pyruvate kinase involved in rice endosperm starch synthesis, compound granule formation and grain filling. Plant Biotechnol J 16, 1878-1891. URL PMID
[5]	Che RH, Tong HN, Shi BH, Liu YQ, Fang SR, Liu DP, Xiao YH, Hu B, Liu LC, Wang HR, Zhao MF, Chu CC (2016). Control of grain size and rice yield by GL2-mediated brassinosteroid responses. Nat Plants 2, 15195. DOI URL PMID
[6]	Chen C, He BS, Liu XX, Ma XD, Liu YJ, Yao HY, Zhang P, Yin JL, Wei X, Koh HJ, Yang C, Xue HW, Fang ZW, Qiao YL (2020). Pyrophosphate-fructose 6-phosphate 1-phosphotransferase (PFP1) regulates starch biosynthesis and seed development via heterotetramer formation in rice (Oryza sativa L.). Plant Biotechnol J 18, 83-95. DOI URL PMID
[7]	Chen XL, Jiang LR, Zheng JS, Chen FY, Wang TS, Wang ML, Tao Y, Wang HC, Hong ZL, Huang YM, Huang RY (2019). A missense mutation in Large Grain Size 1 increases grain size and enhances cold tolerance in rice. J Exp Bot 70, 3851-3866. DOI URL PMID
[8]	Cheng XJ, Pan MY, E ZG, Zhou Y, Niu BX, Chen C (2020). Functional divergence of two duplicated Fertilization Independent Endosperm genes in rice with respect to seed development. Plant J 104, 124-137. URL PMID
[9]	Dong NQ, Sun YW, Guo T, Shi CL, Zhang YM, Kan Y, Xiang YH, Zhang H, Yang YB, Li YC, Zhao HY, Yu HX, Lu ZQ, Wang Y, Ye WW, Shan JX, Lin HX (2020). UDP-glucosyltransferase regulates grain size and abiotic stress tolerance associated with metabolic flux redirection in rice. Nat Commun 11, 2629. URL PMID
[10]	Duan EC, Wang YH, Liu LL, Zhu JP, Zhong MS, Zhang H, Li SF, Ding BX, Zhang X, Guo XP, Jiang L, Wan JM (2016a). Pyrophosphate: fructose-6-phosphate 1-phosphotransferase (PFP) regulates carbon metabolism during grain filling in rice. Plant Cell Rep 35, 1321-1331. URL PMID
[11]	Duan PG, Ni S, Wang JM, Zhang BL, Xu R, Wang YX, Chen HQ, Zhu XD, Li YH (2016b). Regulation of OsGRF4 by OsmiR396 controls grain size and yield in rice. Nat Plants 2, 15203. URL PMID
[12]	Eom JS, Cho JI, Reinders A, Lee SW, Yoo Y, Tuan PQ, Choi SB, Bang G, Park YI, Cho MH, Bhoo SH, An G, Hahn TR, Ward JM, Jeon JS (2011). Impaired function of the tonoplast-localized sucrose transporter in rice, OsSUT2, limits the transport of vacuolar reserve sucrose and affects plant growth. Plant Physiol 157, 109-119. URL PMID
[13]	Fu FF, Xue HW (2010). Coexpression analysis identifies Rice Starch Regulator 1, a rice AP2/EREBP family transcription factor, as a novel rice starch biosynthesis regulator. Plant Physiol 154, 927-938. URL PMID
[14]	Gao XY, Zhang JQ, Zhang XJ, Zhou J, Jiang ZS, Huang P, Tang ZB, Bao YM, Cheng JP, Tang HJ, Zhang WH, Zhang HS, Huang J (2019). Rice qGL3/OsPPKL1 functions with the GSK3/SHAGGY-like kinase OsGSK3 to modulate brassinosteroid signaling. Plant Cell 31, 1077-1093. DOI URL PMID
[15]	Hirose T, Takano M, Terao T (2002). Cell wall invertase in developing rice caryopsis: molecular cloning of OsCIN1 and analysis of its expression in relation to its role in grain filling. Plant Cell Physiol 43, 452-459. URL PMID
[16]	Hu J, Wang YX, Fang YX, Zeng LJ, Xu J, Yu HP, Shi ZY, Pan JJ, Zhang D, Kang SJ, Zhu L, Dong GJ, Guo LB, Zeng DL, Zhang GH, Xie LH, Xiong GS, Li JY, Qian Q (2015). A rare allele of GS2 enhances grain size and grain yield in rice. Mol Plant 8, 1455-1465. URL PMID
[17]	Hu L, Tu B, Yang W, Yuan H, Li JL, Guo L, Zheng L, Chen WL, Zhu XB, Wang YP, Qin P, Ma BT, Li SG (2020a). Mitochondria-associated pyruvate kinase complexes regulate grain filling in rice. Plant Physiol 183, 1073-1087. URL PMID
[18]	Hu WJ, Zhang C, Jiang YQ, Huang CL, Liu Q, Xiong LZ, Yang WN, Chen F ( 2020b). Nondestructive 3D image analysis pipeline to extract rice grain traits using X-ray computed tomography. Plant Phenom 2020,3414926.
[19]	Ishimaru K, Hirose T, Aoki N, Takahashi S, Ono K, Yamamoto S, Wu JZ, Saji S, Baba T, Ugaki M, Matsumoto T, Ohsugi R (2001). Antisense expression of a rice sucrose transporter OsSUT1 in rice (Oryza sativa L.). Plant Cell Physiol 42, 1181-1185. DOI URL PMID
[20]	Ishimaru K, Hirotsu N, Madoka Y, Murakami N, Hara N, Onodera H, Kashiwagi T, Ujiie K, Shimizu BI, Onishi A, Miyagawa H, Katoh E (2013). Loss of function of the IAA-glucose hydrolase gene TGW6 enhances rice grain weight and increases yield. Nat Genet 45, 707-711.
[21]	Jones DB, Peterson ML, Geng S (1979). Association between grain filling rate and duration and yield components in rice. Crop Sci 19, 641-644.
[22]	Jongkaewwattana S, Geng S (2001). Inter-relationships amongst grain characteristics, grain-filling parameters and rice (Oryza sativa L.) milling quality. J Agron Crop Sci 187, 223-229.
[23]	Kawakatsu T, Yamamoto MP, Touno SM, Yasuda H, Takaiwa F (2009). Compensation and interaction between RISBZ1 and RPBF during grain filling in rice. Plant J 59, 908-920. DOI URL PMID
[24]	Li S, Tian YH, Wu K, Ye YF, Yu JP, Zhang JQ, Liu Q, Hu MY, Li H, Tong YP, Harberd NP, Fu XD (2018). Modulating plant growth-metabolism coordination for sustainable agriculture. Nature 560, 595-600. DOI URL PMID
[25]	Li SC, Gao FY, Xie KL, Zeng XH, Cao Y, Zeng J, He ZS, Ren Y, Li WB, Deng QM, Wang SQ, Zheng AP, Zhu J, Liu HN, Wang LX, Li P (2016). The OsmiR396c- OsGRF4-OsGIF1 regulatory module determines grain size and yield in rice. Plant Biotechnol J 14, 2134-2146.
[26]	Li SS, Zhou B, Peng XB, Kuang Q, Huang XL, Yao JL, Du B, Sun MX (2014). OsFIE2 plays an essential role in the regulation of rice vegetative and reproductive development. New Phytol 201, 66-79. URL PMID
[27]	Li YB, Fan CC, Xing YZ, Jiang YH, Luo LJ, Sun L, Shao D, Xu CJ, Li XH, Xiao JH, He YQ, Zhang QF (2011). Natural variation in GS5 plays an important role in regulating grain size and yield in rice. Nat Genet 43, 1266-1269. DOI URL PMID
[28]	Liu EB, Liu XL, Zeng SY, Zhao KM, Zhu CF, Liu Y, Breria MC, Zhang BJ, Hong DL (2015). Time-course association mapping of the grain-filling rate in rice (Oryza sativa L.). PLoS One 10, e0119959. URL PMID
[29]	Liu EB, Zeng SY, Zhu SS, Liu Y, Wu GC, Zhao KM, Liu XL, Liu QM, Dong ZY, Dang XJ, Xie H, Li DL, Hu XX, Hong DL (2019). Favorable alleles of GRAIN-FILLING RATE 1 increase the grain-filling rate and yield of rice. Plant Physiol 181, 1207-1222. URL PMID
[30]	Liu XB, Wei XJ, Sheng ZH, Jiao GA, Tang SQ, Luo J, Hu PS (2016). Polycomb protein OsFIE2 affects plant height and grain yield in rice. PLoS One 11, e0164748. DOI URL PMID
[31]	Ma L, Zhang DC, Miao QS, Yang J, Xuan YH, Hu YB (2017). Essential role of sugar transporter OsSWEET11 during the early stage of rice grain filling. Plant Cell Physiol 58, 863-873. DOI URL PMID
[32]	Na JK, Seo MH, Yoon IS, Lee YH, Lee KO, Kim DY (2012). Involvement of rice polycomb protein OsFIE2 in plant growth and seed size. Plant Biotechnol Rep 6, 339-346. DOI URL
[33]	Nagata K, Shimizu H, Terao T (2002). Quantitative trait loci for nonstructural carbohydrate accumulation in leaf sheaths and culms of rice (Oryza sativa L.) and their effects on grain filling. Breed Sci 52, 275-283.
[34]	Nallamilli BRR, Zhang J, Mujahid H, Malone BM, Bridges SM, Peng ZH (2013). Polycomb group gene OsFIE2 regulates rice (Oryza sativa) seed development and grain filling via a mechanism distinct from Arabidopsis. PLoS Genet 9, e1003322. DOI URL PMID
[35]	Onodera Y, Suzuki A, Wu CY, Washida H, Takaiwa F (2001). A rice functional transcriptional activator, RISBZ1, responsible for endosperm-specific expression of storage protein genes through GCN4 motif. J Biol Chem 276, 14139-14152. DOI URL PMID
[36]	Peng C, Wang YH, Liu F, Ren YL, Zhou KN, Lv J, Zheng M, Zhao SL, Zhang L, Wang CM, Jiang L, Zhang X, Guo XP, Bao YQ, Wan JM (2014a). FLOURY ENDOSPERM 6 encodes a CBM48 domain-containing protein involved in compound granule formation and starch synthesis in rice endosperm. Plant J 77, 917-930. DOI URL PMID
[37]	Peng T, Sun HZ, Du YX, Zhang J, Li JZ, Liu YX, Zhao YF, Zhao QZ (2013). Characterization and expression patterns of microRNAs involved in rice grain filling. PLoS One 8, e54148. URL PMID
[38]	Peng T, Sun HZ, Qiao MM, Zhao YF, Du YX, Zhang J, Li JZ, Tang GL, Zhao QZ (2014b). Differentially expressed microRNA cohorts in seed development may contribute to poor grain filling of inferior spikelets in rice. BMC Plant Biol 14, 196. DOI URL PMID
[39]	Qi P, Lin YS, Song XJ, Shen JB, Huang W, Shan JX, Zhu MZ, Jiang LW, Gao JP, Lin HX (2012). The novel quantitative trait locus GL3.1 controls rice grain size and yield by regulating Cyclin-T1;3. Cell Res 22, 1666-1680. DOI URL PMID
[40]	Schmidt R, Schippers JHM, Mieulet D, Watanabe M, Hoefgen R, Guiderdoni E, Mueller-Roeber B (2014). SALT-RESPONSIVE ERF 1 is a negative regulator of grain filling and gibberellin-mediated seedling establishment in rice. Mol Plant 7, 404-421. DOI URL PMID
[41]	Scofield GN, Hirose T, Aoki N, Furbank RT (2007). Involvement of the sucrose transporter, OsSUT1, in the long-distance pathway for assimilate transport in rice. J Exp Bot 58, 3155-3169. DOI URL PMID
[42]	Scofield GN, Hirose T, Gaudron JA, Furbank RT, Upadhyaya NM, Ohsugi R (2002). Antisense suppression of the rice transporter gene, OsSUT1, leads to impaired grain filling and germination but does not affect photosynthesis. Funct Plant Biol 29, 815-826. URL PMID
[43]	Shi CL, Ren YL, Liu LL, Wang F, Zhang H, Tian P, Pan T, Wang YF, Jing RN, Liu TZ, Wu FQ, Lin QB, Lei CL, Zhang X, Zhu SS, Guo XP, Wang JL, Zhao ZC, Wang J, Zhai HQ, Cheng ZJ, Wan JM (2019). Ubiquitin Specific Protease 15 has an important role in regulating grain width and size in rice. Plant Physiol 180, 381-391. DOI URL PMID
[44]	Si LZ, Chen JY, Huang XH, Gong H, Luo JH, Hou QQ, Zhou TY, Lu TT, Zhu JJ, Shangguan YY, Chen EW, Gong CX, Zhao Q, Jing YF, Zhao Y, Li Y, Cui LL, Fan DL, Lu YQ, Weng QJ, Wang YC, Zhan QL, Liu KY, Wei XH, An K, An G, Han B (2016). OsSPL13 controls grain size in cultivated rice. Nat Genet 48, 447-456. URL PMID
[45]	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, 623-630. DOI URL PMID
[46]	Song XJ, Kuroha T, Ayano M, Furuta T, Nagai K, Komeda N, Segami S, Miura K, Ogawa D, Kamura T, Suzuki T, Higashiyama T, Yamasaki M, Mori H, Inukai Y, Wu JZ, Kitano H, Sakakibara H, Jacobsen SE, Ashikari M (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. DOI URL PMID
[47]	Sosso D, Luo DP, Li QB, Sasse J, Yang JL, Gendrot G, Suzuki M, Koch KE, McCarty DR, Chourey PS, Rogowsky PM, Ross-Ibarra J, Yang B, Frommer WB (2015). Seed filling in domesticated maize and rice depends on SWEET-mediated hexose transport. Nat Genet 47, 1489-1493. DOI URL PMID
[48]	Sturm A, Tang GQ (1999). The sucrose-cleaving enzymes of plants are crucial for development, growth and carbon partitioning. Trends Plant Sci 4, 401-407. DOI URL PMID
[49]	Sun PY, Zhang WH, Wang YH, He Q, Shu F, Liu H, Wang J, Wang JM, Yuan LP, Deng HF (2016). OsGRF4 controls grain shape, panicle length and seed shattering in rice. J Integr Plant Biol 58, 836-847. DOI URL PMID
[50]	Takai T, Fukuta Y, Shiraiwa T, Horie T (2005). Time- related mapping of quantitative trait loci controlling grain- filling in rice (Oryza sativa L.). J Exp Bot 56, 2107-2118. DOI URL PMID
[51]	Tsukaguchi T, Horie T, Ohnishi M (1996). Filling percentage of rice spikelets as affected by availability of non- structural carbohydrates at the initial phase of grain filling. Jpn J Crop Sci 65, 445-452.
[52]	Wang ET, Wang JJ, Zhu XD, Hao W, Wang LY, Li Q, Zhang LX, He W, Lu BR, Lin HX, Ma H, Zhang GQ, He ZH (2008). Control of rice grain-filling and yield by a gene with a potential signature of domestication. Nat Genet 40, 1370-1374. DOI URL PMID
[53]	Wang ET, Xu X, Zhang L, Zhang H, Lin L, Wang Q, Li Q, Ge S, Lu BR, Wang W, He ZH (2010). Duplication and independent selection of cell-wall invertase genes GIF1 and OsCIN1 during rice evolution and domestication. BMC Evol Biol 10, 108. DOI URL PMID
[54]	Wang JC, Xu H, Zhu Y, Liu QQ, Cai XL (2013). OsbZIP58, a basic leucine zipper transcription factor, regulates starch biosynthesis in rice endosperm. J Exp Bot 64, 3453-3466. URL PMID
[55]	Wang SK, Li S, Liu Q, Wu K, Zhang JQ, Wang SS, Wang Y, Chen XB, Zhang Y, Gao CX, Wang F, Huang HX, Fu XD (2015a). The OsSPL16-GW7 regulatory module determines grain shape and simultaneously improves rice yield and grain quality. Nat Genet 47, 949-954. DOI URL PMID
[56]	Wang SK, Wu K, Yuan QB, Liu XY, Liu ZB, Lin XY, Zeng RZ, Zhu HT, Dong GJ, Qian Q, Zhang GQ, Fu XD (2012). Control of grain size, shape and quality by OsSPL16 in rice. Nat Genet 44, 950-954. DOI URL PMID
[57]	Wang YX, Xiong GS, Hu J, Jiang L, Yu H, Xu J, Fang YX, Zeng LJ, Xu EB, Xu J, Ye WJ, Meng XB, Liu RF, Chen HQ, Jing YH, Wang YH, Zhu XD, Li JY, Qian Q (2015b). Copy number variation at the GL7 locus contributes to grain size diversity in rice. Nat Genet 47, 944-948. DOI URL PMID
[58]	Wei XJ, Jiao GA, Lin HY, Sheng ZH, Shao GN, Xie LH, Tang SQ, Xu QG, Hu PS (2017). GRAIN INCOMPLETE FILLING 2 regulates grain filling and starch synthesis during rice caryopsis development. J Integr Plant Biol 59, 134-153. DOI URL PMID
[59]	Wu Y, Wang Y, Mi XF, Shan JX, Li XM, Xu JL, Lin HX (2016). The QTL GNP1 encodes GA20ox1, which increases grain number and yield by increasing cytokinin activity in rice panicle meristems. PLoS Genet 12, e1006386. DOI URL PMID
[60]	Wu YF, Lee SK, Yoo Y, Wei JH, Kwon SY, Lee SW, Jeon JS, An G (2018). Rice transcription factor OsDOF11 modulates sugar transport by promoting expression of Sucrose Transporter and SWEET genes. Mol Plant 11, 833-845. DOI URL PMID
[61]	Xiong YF, Ren Y, Li W, Wu FS, Yang WJ, Huang XL, Yao JL (2019). NF-YC12 is a key multi-functional regulator of accumulation of seed storage substances in rice. J Exp Bot 70, 3765-3780. DOI URL PMID
[62]	Xu CJ, Liu Y, Li YB, Xu XD, Xu CG, Li XH, Xiao JH, Zhang QF (2015). Differential expression of GS5 regulates grain size in rice. J Exp Bot 66, 2611-2623. URL PMID
[63]	Xu JJ, Zhang XF, Xue HW (2016). Rice aleurone layer specific OsNF-YB1 regulates grain filling and endosperm development by interacting with an ERF transcription factor. J Exp Bot 67, 6399-6411. URL PMID
[64]	Yang J, Luo DP, Yang B, Frommer WB, Eom JS (2018). SWEET11 and 15 as key players in seed filling in rice. New Phytol 218, 604-615. DOI URL PMID
[65]	Yang JC, Zhang JH (2006). Grain filling of cereals under soil drying. New Phytol 169, 223-236. DOI URL PMID
[66]	Yang JC, Zhang JH (2010). Grain-filling problem in ‘super’ rice. J Exp Bot 61, 1-5. DOI URL PMID
[67]	Yang JC, Zhang JH, Wang ZQ, Zhu QS, Wang W (2001). Hormonal changes in the grains of rice subjected to water stress during grain filling. Plant Physiol 127, 315-323. DOI URL PMID
[68]	Yi R, Zhu ZX, Hu JH, Qian Q, Dai JC, Ding Y (2013). Identification and expression analysis of microRNAs at the grain filling stage in rice (Oryza sativa L.) via deep sequencing. PLoS One 8, e57863. DOI URL PMID
[69]	Yin LL, Xue HW (2012). The MADS29 transcription factor regulates the degradation of the nucellus and the nucellar projection during rice seed development. Plant Cell 24, 1049-1065. DOI URL PMID
[70]	Zhai LY, Wang F, Yan A, Liang CW, Wang S, Wang Y, Xu JL (2020). Pleiotropic effect of GNP1 underlying grain number per panicle on sink, source and flow in rice. Front Plant Sci 11, 933. DOI URL PMID
[71]	Zhang J, Nallamilli BR, Mujahid H, Peng ZH (2010). OsMADS6 plays an essential role in endosperm nutrient accumulation and is subject to epigenetic regulation in rice (Oryza sativa). Plant J 64, 604-617. DOI URL PMID
[72]	Zhang XJ, Wang JF, Huang J, Lan HX, Wang CL, Yin CF, Wu YY, Tang HJ, Qian Q, Li JY, Zhang HS (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. DOI URL PMID
[73]	Zhang Y, Xiong Y, Liu RY, Xue HW, Yang ZB (2019a). The Rho-family GTPase OsRac1 controls rice grain size and yield by regulating cell division. Proc Natl Acad Sci USA 116, 16121-16126. DOI URL PMID
[74]	Zhang ZX, Zhao H, Huang FL, Long JF, Song G, Lin WX (2019b). The 14-3-3 protein GF14f negatively affects grain filling of inferior spikelets of rice (Oryza sativa L.). Plant J 99, 344-358. DOI URL PMID
[75]	Zhao YF, Peng T, Sun HZ, Teotia S, Wen HL, Du YX, Zhang J, Li JZ, Tang GL, Xue HW, Zhao QZ (2019). miR1432- OsACOT (Acyl-CoA thioesterase) module determines grain yield via enhancing grain filling rate in rice. Plant Biotechnol J 17, 712-723. DOI URL PMID