谷物糊粉层发育的调控机制及其育种应用

doi:10.16819/j.1001-7216.2023.230105

摘要/Abstract

摘要：

植物最外层胚乳细胞在种子发育过程中分化为糊粉层细胞，其在形态和生理功能上均显著区别于内胚乳细胞。与淀粉胚乳不同，糊粉层富含蛋白质、脂类、维生素、膳食纤维、矿质元素和抗氧化物等多种营养物质。同时，在种子萌发过程中，糊粉层细胞能够分泌淀粉酶和蛋白酶分解种子内积累的储藏物质，为种子萌发提供能量。目前利用突变体材料，克隆了一些控制糊粉层细胞分化的关键基因，相关研究极大深化了我们对糊粉层细胞命运决定的认识。同时，由于糊粉层富含各种营养物质，增加糊粉层细胞层数可以作为改良谷物营养品质的一个重要手段。本文主要以水稻及其他谷类作物为例，系统介绍了糊粉层细胞分化和发育的过程，并对其遗传调控机制进行总结梳理，同时对利用糊粉层相关性状进行稻米品质改良可能存在的问题及其对策进行了探讨。

关键词: 糊粉层, 糊粉层细胞, 分化, 遗传调控, 营养品质改良

Abstract:

The outmost layer of endosperm cells differentiates into alleurone cells during seed development, which distinguish themselves from the inner endosperm cells morphologically and physiologically. For example, the aleurone layer is rich in proteins, lipids, vitamins, dietary fibers and mineral elements. The aleurone cells secrete amylase and protease for hydrolyzing reserves accumulated in the endosperm. Several key genes involved in the regulation of aleurone cell differentiation and development have been identified with the mutants showing aleurone defects, deepening our understanding of the aleurone cell fate determination. It has been proposed that increasing the number of aleurone layers may help improve nutritional quality of cereals. In this review, taking rice as an example, we summarized the differentiation and development regulations of aleurone in cereals. We also discussed the potentials, issues and possible solutions for breeding high-nutrition cereals by improving the aleurone-related traits.

Key words: aleurone layer, aleurone cell, cell differentiation, genetic regulation, nutrition improvement

王腾蛟, 陈忱. 谷物糊粉层发育的调控机制及其育种应用[J]. 中国水稻科学, 2023, 37(5): 459-469.

WANG Tengjiao, CHEN Chen. Mechanisms Behind Aleurone Development in Cereals and Its Application in Breeding[J]. Chinese Journal OF Rice Science, 2023, 37(5): 459-469.

图/表 1

图1 糊粉层细胞分化和发育的分子调控模式图箭头表示正调控，“T”表示负调控，实线表示已有充分证据支持该调控作用，虚线表示该调控路径尚不明确或缺少实验证据。红色和蓝色分别表示从水稻和玉米中克隆的糊粉层发育调控因子；橙色表示未克隆或作用机制未知的糊粉层发育调控因子。

Fig. 1. Schematic illustration of the molecular regulations of aleurone differentiation and development. Arrows indicate positive regulations; “T” bars indicate negative regulations; Solid lines indicate the regulations are well supported by different studies; Dash lines indicate the possible regulations that require further study. The aleurone regulators identified from rice and maize are indicated in red and blue, respectively. The possible regulators uncloned or with unknown mechanism are indicated in orange.

参考文献 98

[1]	张娟, 牛百晓, 鄂志国, 陈忱. 水稻胚乳发育遗传调控的研究进展[J]. 中国水稻科学, 2021, 35(4): 326-341.
	Zhang J, Niu B, E Z, Chen C. Towards understanding the genetic regulations of endosperm development in rice[J]. Chinese Journal of Rice Science, 2021, 35(4): 326-341. (in Chinese with English abstract)
[2]	Becraft P W, Yi G. Regulation of aleurone development in cereal grains[J]. Journal of Experimental Botany, 2011, 62(5): 1669-1675.
[3]	Olsen O A. Nuclear endosperm development in cereals and Arabidopsis thaliana[J]. The Plant Cell, 2004, 16 (Suppl): S214-S227.
[4]	Becraft P W, Stinard P S, McCarty D R. CRINKLY4: A TNFR-like receptor kinase involved in maize epidermal differentiation[J]. Science, 1996, 273(5280): 1406-1409.
[5]	Becraft P W, Li K, Dey N, Asuncion-Crabb Y. The maize dek1 gene functions in embryonic pattern formation and cell fate specification[J]. Development (Cambridge, England), 2002, 129(22): 5217-5225.
[6]	He Y, Yang Q, Yang J, Wang Y-F, Sun X, Wang S, Qi W, Ma Z, Song R. shrunken4 is a mutant allele of ZmYSL2 that affects aleurone development and starch synthesis in maize[J]. Genetics, 2021, 218(2): iyab070.
[7]	Li D Q, Wu X B, Wang H F, Feng X, Yan S J, Wu S Y, Liu J X, Yao X F, Bai A N, Zhao H, Song X F, Guo L, Zhang S Y, Liu C M. Defective mitochondrial function by mutation in THICK ALEURONE 1 encoding a mitochondrion-targeted single-stranded DNA-binding protein leads to increased aleurone cell layers and improved nutrition in rice[J]. Molecular Plant, 2021, 14(8): 1343-1361.
[8]	Liu J, Wu X, Yao X, Yu R, Larkin P J, Liu C M. Mutations in the DNA demethylase OsROS1 result in a thickened aleurone and improved nutritional value in rice grains[J]. Proceedings of the National Academy of Sciences, 2018, 115(44): 11327-11332.
[9]	Gontarek B C, Becraft P W. Aleurone[A]// Maize Kernel Development[M]. CABI, 2017: 68-80.
[10]	McClintock B. The origin and behavior of mutable loci in maize[J]. Proceedings of the National Academy of Sciences of the United States of America, 1950, 36(6): 344-355.
[11]	Brink R A. A genetic change associated with the r locus in maize which is directed and potentially reversible[J]. Genetics, 1956, 41(6): 872-889.
[12]	Kermicle J L. Dependence of the R-mottled aleurone phenotype in maize on mode of sexual transmission[J]. Genetics, 1970, 66(1): 69-85.
[13]	Bethke P C, Schuurink R, Jones R L. Hormonal signalling in cereal aleurone[J]. Journal of Experimental Botany, 1997, 48(312): 1337-1356.
[14]	Yamaguchi J, Itoh S, Saitoh T, Ikeda A, Tashiro T, Nagato Y. Characterization of β-amylase and its deficiency in various rice cultivars[J]. Theoretical and Applied Genetics, 1999, 98(1): 32-38.
[15]	Ritchie S, Swanson S J, Gilroy S. Physiology of the aleurone layer and starchy endosperm during grain development and early seedling growth: New insights from cell and molecular biology[J]. Seed Science Research, 2000, 10(3): 193-212.
[16]	Aubert M K, Coventry S, Shirley N J, Betts N S, Würschum T, Burton R A, Tucker M R. Differences in hydrolytic enzyme activity accompany natural variation in mature aleurone morphology in barley (Hordeum vulgare L.)[J]. Scientific Reports, 2018, 8(1): 1-14.
[17]	Meziani S, Nadaud I, Tasleem-Tahir A, Nurit E, Benguella R, Branlard G. Wheat aleurone layer: A site enriched with nutrients and bioactive molecules with potential nutritional opportunities for breeding[J]. Journal of Cereal Science, 2021, 100: 103225.
[18]	Yu R, Wu X, Liu J, Howitt C A, Bird A R, Liu C M, Larkin P J. Rice with multilayer aleurone: A larger sink for multiple micronutrients[J]. Rice, 2021, 14(1): 102.
[19]	Wu J, Chen J, Liu W, Liu C, Zhong Y, Luo D, Li Z, Guo X. Effects of aleurone layer on rice cooking: A histological investigation[J]. Food Chemistry, 2016, 191: 28-35.
[20]	Olsen O A. ENDOSPERM DEVELOPMENT: Cellularization and cell fate specification[J]. Annual Review of Plant Physiology and Plant Molecular Biology, 2001, 52(1): 233-267.
[21]	Wu X, Liu J, Li D, Liu C M. Rice caryopsis development. Ⅱ: Dynamic changes in the endosperm[J]. Journal of Integrative Plant Biology, 2016, 58(9): 786-798.
[22]	Ishimaru K, Hirotsu N, Madoka Y, Murakami N, Hara N, Onodera H, Kashiwagi T, Ujiie K, Shimizu B I, Onishi A, Miyagawa H, Katoh E. Loss of function of the IAA-glucose hydrolase gene TGW6 enhances rice grain weight and increases yield[J]. Nature Genetics, 2013, 45(6): 707-711.
[23]	王忠, 顾蕴洁, 郑彦坤, 王慧慧. 水稻胚乳细胞发育的结构观察及其矿质元素[J]. 中国水稻科学, 2012, 26(6): 693-705.
	Wang Z, Gu Y J, Zheng Y K, Wang H H. Structure observation of rice endosperm cell development and its mineral element analysis[J]. Chinese Journal of Rice Science, 2012, 26(6): 693-705. (in Chinese with English abstract)
[24]	Hoshikawa K. Studies on the development of endosperm in rice : 4. Differentiation and development of the aleuron layer[J]. Japanese Journal of Crop Science, 1967, 36(3): 216-220.
[25]	Khin O M, Sato M, Li-Tao T, Matsue Y, Yoshimura A, Mochizuki T. Close association between aleurone traits and lipid contents of rice grains observed in widely different genetic resources of Oryza sativa[J]. Plant Production Science, 2013, 16(1): 41-49.
[26]	Kim M S, Ko S R, Le V T, Jee M G, Jung Y J, Kang K K, Cho Y G. Development of snp markers from GWAS for selecting seed coat and aleurone layers in brown rice (Oryza sativa L.)[J]. Genes, 2022, 13(10): 1805.
[27]	Wolf M J, Cutler H C, Zuber M S, Khoo U. Maize with multilayer aleurone of high protein content[J]. Crop Science, 1972, 12(4): 440-442.
[28]	Olsen O A. The Modular control of cereal endosperm development[J]. Trends in Plant Science, 2020, 25(3): 279-290.
[29]	Iwai T, Takahashi M, Oda K, Terada Y, Yoshida K T. Dynamic changes in the distribution of minerals in relation to phytic acid accumulation during rice seed development[J]. Plant Physiology, 2012, 160(4): 2007-2014.
[30]	Perera I, Seneweera S, Hirotsu N. Manipulating the phytic acid content of rice grain toward improving micronutrient bioavailability[J]. Rice, 2018, 11(1): 4.
[31]	郑岩, 李江, 杨鹏, 陈惠萍. 水稻糊粉层PCD过程细胞形态观察[J]. 热带作物学报, 2016, 37(2): 298-303.
	Zheng Y, Li J, Yang P, Chen H P. The cell morphology of rice aleurone layers during programmed cell death[J]. Chinese Journal of Tropical Crops, 2016, 37(2): 298-303. (in Chinese with English abstract)
[32]	Becraft P W, Asuncion-Crabb Y. Positional cues specify and maitain aleurone cell fate in maize endosperm development[J]. Development, 2000, 127(18): 4039-4048.
[33]	Gruis D, Guo H, Selinger D, Tian Q, Olsen O A. Surface position, not signaling from surrounding maternal tissues, specifies aleurone epidermal cell fate in maize[J]. Plant Physiology, 2006, 141(3): 898-909.
[34]	Geisler-Lee J, Gallie D R. Aleurone cell identity is suppressed following connation in maize kernels[J]. Plant Physiology, 2005, 139(1): 204-212.
[35]	Lid S E, Gruis D, Jung R, Lorentzen J A, Ananiev E, Chamberlin M, Niu X, Meeley R, Nichols S, Olsen O A. The defective kernel 1 (dek1) gene required for aleurone cell development in the endosperm of maize grains encodes a membrane protein of the calpain gene superfamily[J]. Proceedings of the National Academy of Sciences of the United States of America, 2002, 99(8): 5460-5465.
[36]	王忠, 顾蕴洁, 李卫芳, 黄山, 李克武. 水稻糊粉层的形成及其在萌发过程中的变化[J]. 扬州大学学报, 1998, 1(1): 19-24.
	Wang Z, Gu Y J, Li W F, Huang S, Li K W. Formation of rice aleurone layer and its changes during germination[J]. Journal of Yangzhou University, 1998, 1(1): 19-24. (in Chinese with English abstract)
[37]	Penfield S, Rylott E L, Gilday A D, Graham S, Larson T R, Graham I A. Reserve mobilization in the Arabidopsis endosperm fuels hypocotyl elongation in the dark, is independent of abscisic acid, and requires phosphoenolpyruvate carboxykinase1[J]. Plant Cell, 2004, 16(10): 2705-2718.
[38]	Eastmond P J, Germain V, Lange P R, Bryce J H, Smith S M, Graham I A. Postgerminative growth and lipid catabolism in oilseeds lacking the glyoxylate cycle[J]. Proceedings of the National Academy of Sciences of the United States of America, 2000, 97(10): 5669-5674.
[39]	Footitt S. Control of germination and lipid mobilization by COMATOSE, the Arabidopsis homologue of human ALDP[J]. The EMBO Journal, 2002, 21(12): 2912-2922.
[40]	Takafuji Y, Shimizu-Sato S, Ta K N, Suzuki T, Nosaka-Takahashi M, Oiwa T, Kimura W, Katoh H, Fukai M, Takeda S, Sato Y, Hattori T. High-resolution spatiotemporal transcriptome analyses during cellularization of rice endosperm unveil the earliest gene regulation critical for aleurone and starchy endosperm cell fate specification[J]. Journal of Plant Research, 2021, 134(5): 1061-1081.
[41]	Gontarek B C, Neelakandan A K, Wu H, Becraft P W. NKD transcription factors are central regulators of maize endosperm development[J]. Plant Cell, 2016, 28(12): 2916-2936.
[42]	Bethke P C, Libourel I G L, Aoyama N, Chung Y Y, Still D W, Jones R L. The Arabidopsis aleurone layer responds to nitric oxide, gibberellin, and abscisic acid and is sufficient and necessary for seed dormancy[J]. Plant Physiology, 2007, 143(3): 1173-1188.
[43]	Gehring M. Genomic imprinting: insights from plants[J]. Annual Review of Genetics, 2013, 47: 187-208.
[44]	Köhler C, Wolff P, Spillane C. Epigenetic mechanisms underlying genomic imprinting in plants[J]. Annual Review of Plant Biology, 2012, 63(1): 331-352.
[45]	Piskurewicz U, Iwasaki M, Susaki D, Megies C, Kinoshita T, Lopez-Molina L. Dormancy-specific imprinting underlies maternal inheritance of seed dormancy in Arabidopsis thaliana[J]. eLife, 2016, 5: 1-23.
[46]	Iwasaki M, Hyvärinen L, Piskurewicz U, Lopez-Molina L. Non-canonical RNA-directed DNA methylation participates in maternal and environmental control of seed dormancy[J]. eLife, 2019, 8: 1-17.
[47]	Sato H, Santos-González J, Köhler C. Combinations of maternal-specific repressive epigenetic marks in the endosperm control seed dormancy[J]. eLife, 2021, 10: e64593.
[48]	Sato H, Köhler C. Genomic imprinting regulates establishment and release of seed dormancy[J]. Current Opinion in Plant Biology, 2022, 69: 102264.
[49]	Kaneko M, Itoh H, Inukai Y, Sakamoto T, Ueguchi-Tanaka M, Ashikari M, Matsuoka M. Where do gibberellin biosynthesis and gibberellin signaling occur in rice plants?[J]. Plant Journal, 2003, 35(1): 104-115.
[50]	Xiong M, Yu J, Wang J, Gao Q, Huang L, Chen C, Zhang C, Fan X, Zhao D, Liu Q Q, Li Q F. Brassinosteroids regulate rice seed germination through the BZR1-RAmy3D transcriptional module[J]. Plant Physiology, 2022, 189(1): 402-418.
[51]	Liu J, Wu M, Liu C. Cereal Endosperms: Development and storage product accumulation[J]. Annual Review of Plant Biology, 2022, 73(1): 255-291.
[52]	Olsen L T, Divon H H, Al R, Fosnes K, Lid S E, Opsahl-Sorteberg H G. The defective seed5 (des5) mutant: Effects on barley seed development and HvDek1, HvCr4, and HvSal1 gene regulation[J]. Journal of Experimental Botany, 2008, 59(13): 3753-3765.
[53]	Pu C X, Ma Y, Wang J, Zhang Y C, Jiao X W, Hu Y H, Wang L L, Zhu Z G, Sun D, Sun Y. Crinkly4 receptor-like kinase is required to maintain the interlocking of the palea and lemma, and fertility in rice, by promoting epidermal cell differentiation[J]. The Plant Journal, 2012, 70(6): 940-953.
[54]	Hibara K, Obara M, Hayashida E, Abe M, Ishimaru T, Satoh H, Itoh J, Nagato Y. The ADAXIALIZED LEAF1 gene functions in leaf and embryonic pattern formation in rice[J]. Developmental Biology, 2009, 334(2): 345-354.
[55]	He Y, Yang Q, Yang J, Wang Y F, Sun X, Wang S, Qi W, Ma Z, Song R. shrunken4 is a mutant allele of ZmYSL2 that affects aleurone development and starch synthesis in maize[J]. Genetics, 2021, 218(2): iyab070.
[56]	Zang J, Huo Y, Liu J, Zhang H, Liu J, Chen H. Maize YSL2 is required for iron distribution and development in kernels[J]. Journal of Experimental Botany, 2020, 71(19): 5896-5910.
[57]	Chao Z, Chen Y, Ji C, Wang Y, Huang X, Zhang C, Yang J, Song T, Wu J, Guo L, Liu C, Han M, Wu Y, Yan J, Chao D. A genome-wide association study identifies a transporter for zinc uploading to maize kernels[J]. EMBO Reports, 2023, 24(1): 1-19.
[58]	Shen B, Li C, Min Z, Meeley R B, Tarczynski M C, Olsen O A. Sal1 determines the number of aleurone cell layers in maize endosperm and encodes a class E vacuolar sorting protein[J]. Proceedings of the National Academy of Sciences of the United States of America, 2003, 100(11): 6552-6557.
[59]	Tian Q, Olsen L, Sun B, Lid S E, Brown R C, Lemmon B E, Fosnes K, Olsen O A. Subcellular localization and functional domain studies of DEFECTIVE KERNEL1 in maize and Arabidopsis suggest a model for aleurone cell fate specification involving CRINKLY4 and SUPERNUMERARY ALEURONE LAYER1[J]. Plant Cell, 2007, 19(10): 3127-3145.
[60]	Yi G, Lauter A M, Paul Scott M, Becraft P W. The thick aleurone1 mutant defines a negative regulation of maize aleurone cell fate that functions downstream of defective kernel[J]. Plant Physiology, 2011, 156(4): 1826-1836.
[61]	Wu H, Gontarek B C, Yi G, Beall B D, Neelakandan A K, Adhikari B, Chen R, McCarty D R, Severin A J, Becraft P W. The thick aleurone1 gene encodes a NOT1 subunit of the CCR4-NOT complex and regulates cell patterning in endosperm[J]. Plant Physiology, 2020, 184(2): 960-972.
[62]	Yi G, Neelakandan A K, Gontarek B C, Vollbrecht E, Becraft P W. The naked endosperm genes encode duplicate INDETERMINATE domain transcription factors required for maize endosperm cell patterning and differentiation[J]. Plant Physiology, 2015, 167(2): 443-456.
[63]	Qi X, Li S, Zhu Y, Zhao Q, Zhu D, Yu J. ZmDof3, a maize endosperm-specific Dof protein gene, regulates starch accumulation and aleurone development in maize endosperm[J]. Plant Molecular Biology, 2017, 93(1-2): 7-20.
[64]	Kawakatsu T, Yamamoto M P, Touno S M, Yasuda H, Takaiwa F. Compensation and interaction between RISBZ1 and RPBF during grain filling in rice[J]. The Plant Journal, 2009, 59(6): 908-920.
[65]	Huang X, Peng X, Sun M X. OsGCD1 is essential for rice fertility and required for embryo dorsal-ventral pattern formation and endosperm development[J]. New Phytologist, 2017, 215(3): 1039-1058.
[66]	Wang X, Zhou W, Lu Z, Ouyang Y, Chol S O, Yao J. A lipid transfer protein, OsLTPL36, is essential for seed development and seed quality in rice[J]. Plant Science, 2015, 239: 200-208.
[67]	Kim Y J, Yeu S Y, Park B S, Koh H-J, Song J T, Seo H S. Protein disulfide isomerase-like protein 1-1 controls endosperm development through regulation of the amount and composition of seed proteins in rice[J]. PLoS ONE, 2012, 7(9): e44493.
[68]	Achary V M M, Reddy M K. CRISPR-Cas9 mediated mutation in GRAIN WIDTH and WEIGHT2 (GW2) locus improves aleurone layer and grain nutritional quality in rice[J]. Scientific Reports, 2021, 11(1): 21941.
[69]	Lid S E, Al R H, Krekling T, Meeley R B, Ranch J, Opsahl-Ferstad H G, Olsen O A. The maize disorganized aleurone layer 1 and 2 [dil1, dil2] mutants lack control of the mitotic division plane in the aleurone layer of developing endosperm[J]. Planta, 2004, 218(3): 370-378.
[70]	Lewis D, Bacic A, Chandler P M, Newbigin E J. Aberrant cell expansion in the elongation mutants of barley[J]. Plant and Cell Physiology, 2009, 50(3): 554-571.
[71]	Costa L M, Gutierrez-Marcos J F, Brutnell T P, Greenland A J, Dickinson H G. The globby1-1 (glo1-1) mutation disrupts nuclear and cell division in the developing maize seed causing alterations in endosperm cell fate and tissue differentiation[J]. Development, 2003, 130(20): 5009-5017.
[72]	Kessler S, Seiki S, Sinha N. Xcl1 causes delayed oblique periclinal cell divisions in developing maize leaves, leading to cellular differentiation by lineage instead of position[J]. Development, 2002, 129(8): 1859-1869.
[73]	Suzuki M, Latshaw S, Sato Y, Settles A M, Koch K E, Hannah L C, Kojima M, Sakakibara H, McCarty D R. The maize Viviparous8 locus, encoding a putative ALTERED MERISTEM PROGRAM1-Like peptidase, regulates abscisic acid accumulation and coordinates embryo and endosperm development[J]. Plant Physiology, 2008, 146(3): 1193-1206.
[74]	Qin P, Zhang G, Hu B, Wu J, Chen W, Ren Z, Liu Y, Xie J, Yuan H, Tu B, Ma B, Wang Y, Ye L, Li L, Xiang C, Li S. Leaf-derived ABA regulates rice seed development via a transporter-mediated and temperature-sensitive mechanism[J]. Science Advances, 2021, 7(3): eabc8873.
[75]	Xu X, E Z, Zhang D, Yun Q, Zhou Y, Niu B, Chen C. OsYUC11-mediated auxin biosynthesis is essential for endosperm development of rice[J]. Plant Physiology, 2021, 185(3): 934-950.
[76]	Batista R A, Figueiredo D D, Santos-González J, Köhler C. Auxin regulates endosperm cellularization in Arabidopsis[J]. Genes & Development, 2019, 33(7-8): 466-476.
[77]	Figueiredo D D, Batista R A, Roszak P J, Köhler C. Auxin production couples endosperm development to fertilization[J]. Nature plants, 2015, 1: 15184.
[78]	Forestan C, Meda S, Varotto S. ZmPIN1-mediated auxin transport is related to cellular differentiation during maize embryogenesis and endosperm development[J]. Plant Physiology, 2010, 152(3): 1373-1390.
[79]	Basunia M A, Nonhebel H M, Backhouse D, McMillan M. Localised expression of OsIAA29 suggests a key role for auxin in regulating development of the dorsal aleurone of early rice grains[J]. Planta, 2021, 254(2): 40.
[80]	Wu H, Becraft P W. Comparative transcriptomics and network analysis define gene coexpression modules that control maize aleurone development and auxin signaling[J]. Plant Genome, 2021, 14(3): 1-14.
[81]	Chen W, Wang W, Lyu Y, Wu Y, Huang P, Hu S, Wei X, Jiao G, Shao G, Luo J. OsVP1 activates Sdr4 expression to control rice seed dormancy via the ABA signaling pathway[J]. The Crop Journal, 2021, 9(1): 68-78.
[82]	Miyoshi K, Kagaya Y, Ogawa Y, Nagato Y, Hattori T. Temporal and spatial expression pattern of the OSVP1 and OSEM genes during seed development in rice[J]. Plant & Cell Physiology, 2002, 43(3): 307-713.
[83]	Cao X, Costa L M, Biderre-Petit C, Kbhaya B, Dey N, Perez P, McCarty D R, Gutierrez-Marcos J F, Becraft P W. Abscisic acid and stress signals induce Viviparous1 expression in seed and vegetative tissues of maize[J]. Plant Physiology, 2007, 143(2): 720-731.
[84]	Wang X S, Zhu H B, Jin G L, Liu H L, Wu W R, Zhu J. Genome-scale identification and analysis of LEA genes in rice (Oryza sativa L.)[J]. Plant Science, 2007, 172(2): 414-420.
[85]	Zheng Y, Zhang H, Deng X, Liu J, Chen H. The relationship between vacuolation and initiation of PCD in rice (Oryza sativa) aleurone cells[J]. Scientific Reports, 2017, 7(1): 41245.
[86]	Zhang H, Xiao Y, Deng X, Feng H, Li Z, Zhang L, Chen H. OsVPE3 mediates GA-induced programmed cell death in rice aleurone layers via interacting with actin microfilaments[J]. Rice, 2020, 13(1): 22.
[87]	Laskowski W, Górska-Warsewicz H, Rejman K, Czeczotko M, Zwolińska J. How Important are cereals and cereal products in the average polish diet?[J]. Nutrients, 2019, 11(3): 679.
[88]	Juliano B O, Tuaño A P P. Gross structure and composition of the rice grain[A]//Rice[M]. Elsevier, 2019(1): 31-53.
[89]	Lebert L, Buche F, Sorin A, Aussenac T. The Wheat Aleurone layer: Optimisation of its benefits and application to bakery products[J]. Foods, 2022, 11(22): 3552.
[90]	Bhattacharya S. Chemical and Nutritional Properties of Brown Rice[A] // Manickavasagan A, Santhakumar C, Venkatachalapathy N. Brown Rice[M]. Cham: Springer International Publishing, 2017: 93-110.
[91]	Yang Y, Guo M, Sun S, Zou Y, Yin S, Liu Y, Tang S, Gu M, Yang Z, Yan C. Natural variation of OsGluA2 is involved in grain protein content regulation in rice[J]. Nature Communications, 2019, 10(1): 1949.
[92]	Hoshikawa K. Studies on the development of endosperm in rice : 5. The number of aleuron cell layers, its varietal difference and the influence of environmental factors[J]. Japanese Journal of Crop Science, 1967, 36(3): 221-227.
[93]	Khin O M, Matsue Y, Matsuo R, Yamagata Y, Yoshimura A, Mochizuki T. Identification of QTL for aleurone traits contributing to lipid content of rice (Oryza sativa L.)[J]. Japanese Journal of Crop Science, 2012, 234(Extra issue): 126-127.
[94]	Jestin L, Ravel C, Auroy S, Laubin B, Perretant M R, Pont C, Charmet G. Inheritance of the number and thickness of cell layers in barley aleurone tissue (Hordeum vulgare L.): An approach using F₂-F₃ progeny[J]. Theoretical and Applied Genetics, 2008, 116(7): 991-1002.
[95]	Nagato K, Ebata M. Effects of temperature in the ripening periods upon the development and qualities of lowland rice kernels[J]. Japanese Journal of Crop Science, 1960, 28(3): 275-278.
[96]	Nagato K, Ebata M. Effects of high temperature during ripening period on the development and the quality of rice kernels[J]. Japanese Journal of Crop Science, 1965, 34(1): 59-66.
[97]	Nagato K, Ebata M, Kishi Y. Effects of high temperature during ripening period on the qualities of indica rice[J]. Japanese Journal of Crop Science, 1966, 35(3-4): 239-244.
[98]	Nguyen T M P, Abiko T, Nakamura T, Mochizuki T. Development and application of a plate method for visualizing aleurone layers in mature rice grains[J]. Plant Production Science, 2022, 25(2): 260-267.