Research Progress on the Molecular Mechanism of Starch Accumulation in Rice Endosperm

doi:10.11983/CBB22071

Abstract

Abstract: Starch is the major storage material of rice (Oryza sativa) endosperm, and its accumulation process affects the subsequent growth and development of plants. As one of the main nutrients absorbed by human beings from rice, the synthesis and accumulation process of starch in rice has attracted increasing attention. This review mainly discusses the latest progress of endogenous factors affecting starch synthesis and accumulation, such as sucrose unloading from phloem, key enzymes of starch synthesis and hormones, and points out the unsettled questions in the field of endosperm starch accumulation to provide some reference ideas for further research in the future.

Key words: starch, endosperm, sucrose unloading, starch synthase, hormone

Ziwen Tang, Dongping Zhang. Research Progress on the Molecular Mechanism of Starch Accumulation in Rice Endosperm[J]. Chinese Bulletin of Botany, 2023, 58(4): 612-621.

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URL: https://www.chinbullbotany.com/EN/10.11983/CBB22071

https://www.chinbullbotany.com/EN/Y2023/V58/I4/612

Figures/Tables 3

Figure 1 Unloading process of sucrose during rice caryopsis development (A) Schematic diagram of cross section of rice at the stage of nutrient accumulation; (B) Sucrose transport from maternal tissue to maternal-filial interface in early caryopsis development of rice. DV: Dorsal vascular bundle; NT: Nucellar tissue; SV: Style vascular bundle; Pe: Peel; ES: Endosperm; AL: Aleurone layer; SE: Sieve element; CC: Companion cell; NP: Nucellar protrusion; P: Phloem parenchyma cell

Figure 2 Expression patterns of sucrose transporters SUTs and SWEETs in different parts and stages of rice

Figure 3 Regulation of several main enzymes in rice starch synthesis Glc-1-P: Glucose-1-phosphate; ADP-Glc: ADP-glucose; Glc- 6-P: Glucose-6-phosphate; AGPase: ADP glucose pyrophosphorylase; PGM: Phosphoglucomutase; GBSSI: Granule bound starch synthase I; SS: Soluble starch synthase; BE: Starch branching enzyme; DBE: Starch debranching enzyme; BT1: ADP-glucose transporter; G1PT: Putative Glc-1-P transporter; GPT: Glc-6-P transporter; PTST1: Protein targeting starch 1

References 68

[1]	包颖, 杜家潇, 景翔, 徐思 (2015). 药用野生稻叶中淀粉合成酶基因家族的序列分化和特异表达. 植物学报 50, 683-690. DOI
[2]	陈观杰, 郑殿峰, 冯乃杰, 马国辉, 周行, 母德伟, 冯胜杰 (2022). 盐胁迫下ABA对水稻萌芽期及孕穗期生长、生理代谢的影响. 杂交水稻 37(2), 100-108.
[3]	高秀华, 傅向东 (2018). 赤霉素信号转导及其调控植物生长发育的研究进展. 生物技术通报 34(7), 1-13. DOI
[4]	郭韬, 余泓, 邱杰, 李家洋, 韩斌, 林鸿宣 (2019). 中国水稻遗传学研究进展与分子设计育种. 中国科学: 生命科学 49, 1185-1212.
[5]	黄升谋, 邹应斌 (2006). 赤霉素和脱落酸对水稻籽粒灌浆及结实的影响. 安徽农业大学学报 33, 293-296.
[6]	李静, 吴翼, 弓淑芳, 杨耀东 (2021). E3泛素连接酶调控GA、ABA影响种子萌发综述. 热带农业科学 41, 108-116.
[7]	刘春明, 程佑发, 刘永秀, 孙蒙祥, 薛红卫 (2016). 植物种子发育的分子机理. 中国基础科学 18(2), 1-13.
[8]	潘鹏屹, 朱建平, 王云龙, 郝媛媛, 蔡跃, 张文伟, 江玲, 王益华, 万建民 (2016). 水稻粉质胚乳突变体ws的表型分析及基因克隆. 中国水稻科学 30, 447-457. DOI
[9]	杨建昌, 王志琴, 朱庆森, 苏宝林 (1999). ABA与GA对水稻籽粒灌浆的调控. 作物学报 25, 341-348.
[10]	张娟, 牛百晓, 鄂志国, 陈忱 (2021). 水稻胚乳发育遗传调控的研究进展. 中国水稻科学 35, 326-341. DOI
[11]	郑云飞 (2021). 中国考古改变稻作起源和中华文明认知. 中国稻米 27(4), 12-16. DOI
[12]	周述波, 林伟, 萧浪涛 (2011). 外源GA₃、ABA处理对杂交稻亲本产量及种子贮藏性的影响. 湖南农业科学 (3), 9-11.
[13]	Aloni R, Aloni E, Langhans M, Ullrich CI (2006). Role of auxin in regulating Arabidopsis flower development. Planta 223, 315-328. DOI PMID
[14]	Armenta-Medina A, Gillmor CS, Gao P, Mora-Macias J, Kochian LV, Xiang DQ, Datla R (2021). Developmental and genomic architecture of plant embryogenesis: from model plant to crops. Plant Commun 2, 100136. DOI URL
[15]	Bai AN, Lu XD, Li DQ, Liu JX, Liu CM (2016). NF-YB1- regulated expression of sucrose transporters in aleurone facilitates sugar loading to rice endosperm. Cell Res 26, 384-388. DOI
[16]	Basunia MA, Nonhebel HM (2019). Hormonal regulation of cereal endosperm development with a focus on rice (Oryza sativa). Funct Plant Biol 46, 493-506. DOI PMID
[17]	Bertoft E (2017). Understanding starch structure: recent progress. Agronomy 7, 56. DOI URL
[18]	Burton RA, Jenner H, Carrangis L, Fahy B, Fincher GB, Hylton C, Laurie DA, Parker M, Waite D, Van Wegen S, Verhoeven T, Denyer K (2002). Starch granule initiation and growth are altered in barley mutants that lack isoamylase activity. Plant J 31, 97-112.
[19]	Cao X, Yang HL, Shang CQ, Ma S, Liu L, Cheng JL (2019). The roles of auxin biosynthesis YUCCA gene family in plants. Int J Mol Sci 20, 6343. DOI URL
[20]	Chen J, Yi Q, Cao Y, Wei B, Zheng LJ, Xiao QL, Xie Y, Gu Y, Li YP, Huang HH, Wang YB, Hou XB, Long TD, Zhang JJ, Liu HM, Liu YH, Yu GW, Huang YB (2016). ZmbZIP91 regulates expression of starch synthesis-related genes by binding to ACTCAT elements in their promoters. J Exp Bot 67, 1327-1338. DOI PMID
[21]	Chen TT, Li GY, Islam MR, Fu WM, Feng BH, Tao LX, Fu GF (2019). Abscisic acid synergizes with sucrose to enhance grain yield and quality of rice by improving the source-sink relationship. BMC Plant Biol 19, 525. DOI PMID
[22]	Cheng YF, Dai XH, Zhao YD (2007). Auxin synthesized by the YUCCA flavin monooxygenases is essential for embryogenesis and leaf formation in Arabidopsis. Plant Cell 19, 2430-2439. DOI URL
[23]	Fei HH, Yang ZP, Lu QT, Wen XG, Zhang Y, Zhang AH, Lu CM (2021). OsSWEET14 cooperates with OsSWEET11 to contribute to grain filling in rice. Plant Sci 306, 110851. DOI URL
[24]	Fu FF, Xue HW (2010). Coexpression analysis identifies rice starch regulator1, a rice AP2/EREBP family transcription factor, as a novel rice starch biosynthesis regulator. Plant Physiol 154, 927-938. DOI URL
[25]	Gibon Y, Pyl ET, Sulpice R, Lunn JE, Höhne M, Günther M, Stitt M (2009). Adjustment of growth, starch turnover, protein content and central metabolism to a decrease of the carbon supply when Arabidopsis is grown in very short photoperiods. Plant Cell Environ 32, 859-874. DOI URL
[26]	Hedden P, Thomas SG (2012). Gibberellin biosynthesis and its regulation. Biochem J 444, 11-25. DOI PMID
[27]	Huang XH, Kurata N, Wei XH, Wang ZX, Wang AH, Zhao Q, Zhao Y, Liu KY, Lu HY, Li WJ, Guo YL, Lu YQ, Zhou CC, Fan DL, Weng QJ, Zhu CR, Huang T, Zhang L, Wang YC, Feng L, Furuumi H, Kubo T, Miyabayashi T, Yuan XP, Xu Q, Dong GJ, Zhan QL, Li CY, Fujiyama A, Toyoda A, Lu TT, Feng Q, Qian Q, Li JY, Han B (2012). A map of rice genome variation reveals the origin of cultivated rice. Nature 490, 497-501. DOI
[28]	Huang XL, Zhang YY, Wang LL, Dong XY, Hu WX, Jiang M, Chen G, An G, Xiong F, Wu YF (2021). OsDOF11 affects nitrogen metabolism by sucrose transport signaling in rice (Oryza sativa L.). Front Plant Sci 12, 703034. DOI URL
[29]	Jin SK, Zhang MQ, Leng YJ, Xu LN, Jia SW, Wang SL, Song T, Wang RA, Yang QQ, Tao T, Cai XL, Gao JP (2022). OsNAC129 regulates seed development and plant growth and participates in the brassinosteroid signaling pathway. Front Plant Sci 13, 905148. DOI URL
[30]	Khan SU, Gurmani AR, Jalal-Ud-Din, Qayyum A, Abbasi KS, Liaquat M, Ahmad Z (2016). Exogenously applied gibberellic acid, indole acetic acid and kinetin as potential regulators of source-sink relationship, physiological and yield attributes in rice (Oryza sativa L.) genotypes under water deficit conditions. Int J Agric Biol 18, 139-145.
[31]	Kubo A, Rahman S, Utsumi Y, Li ZY, Mukai Y, Yamamoto M, Ugaki M, Harada K, Satoh H, Konik-Rose C, Morell M, Nakamura Y (2005). Complementation of sugary-1 phenotype in rice endosperm with the wheat isoamylase1 gene supports a direct role for isoamylase1 in amylopectin biosynthesis. Plant Physiol 137, 43-56. DOI URL
[32]	Lee SK, Hwang SK, Han M, Eom JS, Kang HG, Han Y, Choi SB, Cho MH, Bhoo SH, An G, Hahn TR, Okita TW, Jeon JS (2007). Identification of the ADP-glucose pyrophosphorylase isoforms essential for starch synthesis in the leaf and seed endosperm of rice (Oryza sativa L.). Plant Mol Biol 65, 531-546. DOI URL
[33]	Li C, Powell PO, Gilbert RG (2017). Recent progress toward understanding the role of starch biosynthetic enzymes in the cereal endosperm. Amylase 1, 59-74.
[34]	Liu LC, Tong HN, Xiao YH, Che RH, Xu F, Hu B, Liang CZ, Chu JF, Li JY, Chu CC (2015). Activation of big grain1 significantly improves grain size by regulating auxin transport in rice. Plant Biol 112, 11102-11107.
[35]	Locascio A, Roig-Villanova I, Bernardi J, Varotto S (2014). Current perspectives on the hormonal control of seed development in Arabidopsis and maize: a focus on auxin. Front Plant Sci 5, 412.
[36]	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 PMID
[37]	Ohdan T, Francisco PB Jr, Sawada T, Hirose T, Terao T, Satoh H, Nakamura Y (2005). Expression profiling of genes involved in starch synthesis in sink and source organs of rice. J Exp Bot 422, 3229-3244.
[38]	Olsen OA (2004). Nuclear endosperm development in cereals and Arabidopsis thaliana. Plant Cell 16, S214-S227.
[39]	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 (2014). FLOURY ENDOSPERM6 encodes a CBM48 domain-containing protein involved in compound granule formation and starch synthesis in rice endosperm. Plant J 77, 917-930. DOI URL
[40]	Ramadoss BR, Gangola MP, Agasimani S, Jaiswal S, Venkatesan T, Sundaram GR, Chibbar RN (2019). Starch granule size and amylopectin chain length influence starch in vitro enzymatic digestibility in selected rice mutants with similar amylose concentration. J Food Sci Technol 56, 391-400. DOI
[41]	Ren Y, Huang ZQ, Jiang H, Wang Z, Wu FS, Xiong YF, Yao JL (2021). A heat stress responsive NAC transcription factor heterodimer plays key roles in rice grain filling. J Exp Bot 72, 2947-2964. DOI PMID
[42]	Sabelli PA, Larkins BA (2009). The development of endosperm in grasses. Plant Physiol 149, 14-26. DOI PMID
[43]	Sawada T, Itoh M, Nakamura Y (2018). Contributions of three starch branching enzyme isozymes to the fine structure of amylopectin in rice endosperm. Front Plant Sci 9, 1536. DOI PMID
[44]	Schmidt R, Schippers JHM, Mieulet D, Watanabe M, Hoefgen R, Guiderdoni E, Mueller-Roeber B (2014). SALT-RESPONSIVE ERF1 is a negative regulator of grain filling and gibberellin-mediated seedling establishment in rice. Mol Plant 7, 404-421. DOI PMID
[45]	Smith AM, Denyer K, Martin CR (1995). What controls the amount and structure of starch in storage organs? Plant Physiol 107, 673-677. DOI PMID
[46]	Tappiban P, Ying YN, Xu FF, Bao JS (2021). Proteomics and post-translational modifications of starch biosynthesis-related proteins in developing seeds of rice. Int J Mol Sci 22, 5901. DOI URL
[47]	Tetlow IJ, Bertoft E (2020). A review of starch biosynthesis in relation to the building block-backbone model. Int J Mol Sci 21, 7011. DOI URL
[48]	Tian ZX, Qian Q, Liu QQ, Yan MX, Liu XF, Yan CJ, Liu GF, Gao ZY, Tang SZ, Zeng DL, Wang YH, Yu JM, Gu MH, Li JY (2009). Allelic diversities in rice starch biosynthesis lead to a diverse array of rice eating and cooking qualities. Proc Natl Acad Sci USA 106, 21760-21765. DOI PMID
[49]	Tuncel A, Kawaguchi J, Ihara Y, Matsusaka H, Nishi A, Nakamura T, Kuhara S, Hirakawa H, Nakamura Y, Cakir B, Nagamine A, Okita TW, Hwang SK, Satoh H (2014). The rice endosperm ADP-glucose pyrophosphorylase large subunit is essential for optimal catalysis and allosteric regulation of the heterotetrameric enzyme. Plant Cell Physiol 55, 1169-1183. DOI PMID
[50]	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 PMID
[51]	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
[52]	Wang J, Chen ZC, Zhang Q, Meng SS, Wei CX (2020a). The NAC transcription factors OsNAC20 and OsNAC26 regulate starch and storage protein synthesis. Plant Physiol 184, 1775-1791. DOI URL
[53]	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. DOI URL
[54]	Wang W, Wei XJ, Jiao GA, Chen WQ, Wu YW, Sheng ZH, Hu SK, Xie LH, Wang JY, Tang SQ, Hu PS (2020b). GBSS-BINDING PROTEIN, encoding a CBM48 domain- containing protein, affects rice quality and yield. J Integr Plant Biol 62, 948-966. DOI URL
[55]	Wang XK (2022). Managing land carrying capacity: key to achieving sustainable production systems for food security. Land 11, 484. DOI URL
[56]	Wang ZQ, Xu YJ, Chen TT, Zhang H, Yang JC, Zhang JH (2015). Abscisic acid and the key enzymes and genes in sucrose-to-starch conversion in rice spikelets in response to soil drying during grain filling. Planta 241, 1091-1107. DOI PMID
[57]	Wu XB, Liu JX, Li DQ, Liu CM (2016). Rice caryopsis development II: dynamic changes in the endosperm. J Integr Plant Biol 58, 786-798. DOI
[58]	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
[59]	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. DOI URL
[60]	Xu XY, E ZG, Zhang DP, Yun QB, Zhou Y, Niu BX, Chen C (2021). OsYUC11-mediated auxin biosynthesis is essential for endosperm development of rice. Plant Physiol 185, 934-950. DOI URL
[61]	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 PMID
[62]	Yang JC, Zhang JH, Wang ZQ, Liu K, Wang P (2006). Post-anthesis development of inferior and superior spikelets in rice in relation to abscisic acid and ethylene. J Exp Bot 57, 149-160. PMID
[63]	Zhang DP, Zhang MY, Liang JS (2021a). RGB1 regulates grain development and starch accumulation through its effect on OsYUC11-mediated auxin biosynthesis in rice endosperm cells. Front Plant Sci 12, 585174. DOI URL
[64]	Zhang DP, Zhang MY, Wang YZ, Liang JS (2021b). RGB1 regulates rice panicle architecture and grain filling through monitoring cytokinin level in inflorescence meristem and grain abscisic acid level during filling stage. Rice Sci 28, 317-321. DOI URL
[65]	Zhang JJ, Chen J, Yi Q, Hu YF, Liu HM, Liu YH, Huang YB (2014). Novel role of ZmaNAC36 in co-expression of starch synthetic genes in maize endosperm. Plant Mol Biol 84, 359-369. PMID
[66]	Zhang XF, Tong JH, Bai AN, Liu CM, Xiao LT, Xue HW (2020). Phytohormone dynamics in developing endosperm influence rice grain shape and quality. J Integr Plant Biol 62, 1625-1637. DOI
[67]	Zhu JH, Yu WW, Zhang CQ, Zhu YJ, Xu JL, Li EP, Gilbert RG, Liu QQ (2020). New insights into amylose and amylopectin biosynthesis in rice endosperm. Carbohydr Polym 230, 115656.
[68]	Zhu Y, Cai XL, Wang ZY, Hong MM (2003). An interaction between a MYC protein and an EREBP protein is involved in transcriptional regulation of the rice Wx gene. J Biol Chem 278, 47803-47811. DOI URL