Molecular-Genetic Foundations of Rice Domestication: Control of Seed Shattering, Grain Size, and Pericarp Coloration
- Authors: Mirgorodskii N.A.1, Slezova S.A.1, Dobarkina N.A.1, Matveeva T.V.2,3, Andreeva E.A.2
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Affiliations:
- Sirius University of Science and Technology
- Saint Petersburg State University
- All-Russian Research Institute of Plant Protection
- Issue: Vol 23, No 2 (2025)
- Pages: 115-128
- Section: Genetic basis of ecosystems evolution
- Submitted: 12.12.2024
- Accepted: 21.03.2025
- Published: 27.06.2025
- URL: https://journals.eco-vector.com/ecolgenet/article/view/642867
- DOI: https://doi.org/10.17816/ecogen642867
- EDN: https://elibrary.ru/EWYUDE
- ID: 642867
Cite item
Abstract
Domestication of rice (Oryza sativa L.), one of the five earliest cereal crops, gave rise to a characteristic “domestication syndrome” marked by loss of natural seed dispersal, enlargement and colour change of the caryopsis, shortening of seed dormancy, and transition to an annual life cycle. Archaeological, physiological-genetic and molecular evidence is synthesised here to summarise the mechanisms underlying these key agronomic traits. Reduced seed shattering is linked to mutations andallelic diversification at loci SH4, qSH1, SH5, SHAT1, CPL1, OsSh1/ObSH3, ObSH11, NPC1, OSH15, GRF4 and OsLG1/SPR3, which govern formation and degradation of the spikelet abscission layer. Grain size is determined by QTL GW2, GS3, GS5 and TGW6, modulating cell division and endosperm development and thus shaping thousand-grain weight and yield. Pericarp pigmentation is controlled by Rc and Rd together with the Kala1–Kala3–Kala4 cassette; structural rearrangements in theKala4 promoter trigger ectopic expression of a bHLH factor and anthocyanin accumulation, whereas a 14-bp deletion in Rc converted most cultivars to the white-grained type and was later functionally restored via CRISPR/Cas9. Collectively, these findings provide a genetic foundation for targeted improvement of yield, harvestability and nutritional quality in modern rice breeding.
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About the authors
Nikita A. Mirgorodskii
Sirius University of Science and Technology
Author for correspondence.
Email: i@nmirgorodskij.ru
ORCID iD: 0009-0005-6662-0741
SPIN-code: 1057-6260
Russian Federation, 1 Olimpiiskii av., Sirius Federal Territory, 354340
Sofya A. Slezova
Sirius University of Science and Technology
Email: slezovas@mail.ru
Russian Federation, 1 Olimpiiskii av., Sirius Federal Territory, 354340
Nadezhda A. Dobarkina
Sirius University of Science and Technology
Email: n.dobarkina@yandex.ru
ORCID iD: 0009-0009-4283-519X
Russian Federation, 1 Olimpiiskii av., Sirius Federal Territory, 354340
Tatiana V. Matveeva
Saint Petersburg State University; All-Russian Research Institute of Plant Protection
Email: radishlet@gmail.com
ORCID iD: 0000-0001-8569-6665
SPIN-code: 3877-6598
Scopus Author ID: 7006494611
Dr. Sci. (Biology), Professor
Russian Federation, Saint Petersburg; Saint Petersburgcity, PushkinElena A. Andreeva
Saint Petersburg State University
Email: a.andreeva@spbu.ru
ORCID iD: 0000-0002-9326-3170
SPIN-code: 7269-8240
Cand. Sci. (Biology)
Russian Federation, Saint PetersburgReferences
- Fuller DQ. Contrasting patterns in crop domestication and domestication rates: recent archaeobotanical insights from the Old World. Ann Bot. 2007;100(5):903–924. doi: 10.1093/aob/mcm048
- Pankin A, von Korff M. Co-evolution of methods and thoughts in cereal domestication studies: a tale of barley (Hordeum vulgare). Curr Opin Plant Biol. 2017;36:15–21. doi: 10.1016/j.pbi.2016.12.001
- Khush GS. Productivity improvements in rice. Nutr Rev. 2003;61(S6): S114–S116. doi: 10.1301/nr.2003.jun.S114-S116
- Khush GS. Challenges for meeting the global food and nutrient needs in the new millennium. Proc Nutr Soc. 2001;60:15–26. doi: 10.1079/PNS200075
- Jiang LP, Liu L. New evidence for the origins of sedentism and rice domestication in the Lower Yangzi River, China. Antiquity. 2006;80(308):355–361. doi: 10.1017/S0003598X00093674
- Wu H, He Q, Wang Q. Advances in rice seed shattering. Int J Mol Sci. 2023;24(10):8889. doi: 10.3390/ijms24108889
- Ji H-S, Chu S-H, Jiang W, et al. Characterization and mapping of a shattering mutant in rice that corresponds to a block of domestication genes. Genetics. 2006;173(2):995–1005. doi: 10.1534/genetics.105.054031.
- Li Y, Fan C, Xing Y, et al. Natural variation in GS5 plays an important role in regulating grain size and yield in rice. Nat Genet. 2011;43(12):1266–1269. doi: 10.1038/ng.977
- Nkouaya Mbanjo EG, Jones H, Isaguirre Caguiat XG, et al. Exploring the genetic diversity within traditional Philippine pigmented rice. Rice. 2019;12:27. doi: 10.1186/s12284-019-0281-2
- Ishii T, Numaguchi K, Miura K, et al. OsLG1 regulates a closed panicle trait in domesticated rice. Nat Genet. 2013;45(4):462–465.doi: 10.1038/ng.2567
- Maity A, Lamichaney A, Joshi DC, et al. Seed shattering: A trait of evolutionary importance in plants. Front Plant Sci. 2021;12:657773. doi: 10.3389/fpls.2021.657773
- Fuller DQ, Qin L, Zheng Y. et al. The domestication process and domestication rate in rice: spikelet bases from the Lower Yangtze. Science. 2009;323(5921):1607–1610. doi: 10.1126/science.1166605
- Li C, Zhou A, Sang T. Rice domestication by reducing shattering. Science. 2006;311(5769):1936–1939. doi: 10.1126/science.1123604
- Thurber CS, Hepler PK, Caicedo AL. Timing is everything: early degradation of abscission layer is associated with increased seed shattering in U.S. weedy rice. BMC Plant Biol. 2011;11:14. doi: 10.1186/1471-2229-11-14
- Lin Z, Griffith ME, Li X, et al. Origin of seed shattering in rice (Oryza sativa L.). Planta. 2007;226(1):11–20. doi: 10.1007/s00425-006-0460-4
- Roeder AHK, Ferrándiz C, Yanofsky MF. The role of theREPLUMLESS homeodomain protein in patterning the Arabidopsis fruit.Curr Biol. 2003;13(18):1630–1635. doi: 10.1016/j.cub.2003.08.027
- Konishi S, Izawa T, Lin SY, et al. An SNP caused loss of seed shattering during rice domestication. Science. 2006;312(5778):1392–1396.doi: 10.1126/science.1126410
- Yoon J, Cho L-H, Kim SL, et al. The BEL1-type homeobox gene SH5 induces seed shattering by enhancing abscission-zone development and inhibiting lignin biosynthesis. Plant J. 2014;79(5):717–728. doi: 10.1111/tpj.12581
- Zhou Y, Lu D, Li C, et al. Genetic control of seed shattering in rice by the APETALA2 transcription factor SHATTERING ABORTION1. Plant Cell. 2012;24(3):1034–1048. doi: 10.1105/tpc.111.094383
- Jiang L, Ma X, Zhao S, et al. The APETALA2-like transcription factor SUPERNUMERARY BRACT controls rice seed shattering and seed size. Plant Cell. 2019;31(1):17–36. doi: 10.1105/tpc.18.00304
- Lin Z, Li X, Shannon LM, et al. Parallel domestication of the Shattering1 genes in cereals. Nat Genet. 2012;44(6):720–724. doi: 10.1038/ng.2281
- Lv S, Wu W, Wang M, et al. Genetic control of seed shattering during African rice domestication. Nat Plants. 2018;4(6):331–337.doi: 10.1038/s41477-018-0164-3
- Cao H, Zhuo L, Su Y, et al. Non-specific phospholipase C1 affects silicon distribution and mechanical strength in stem nodes of rice. Plant J. 2016;86(4):308–321. doi: 10.1111/tpj.13165
- Sun P, Zhang W, Wang Y, et al. OsGRF4 controls grain shape, panicle length and seed shattering in rice. J Integr Plant Biol. 2016;58(10):836–847. doi: 10.1111/jipb.12473
- Ning J, He W, Wu L, et al. The MYB transcription factor Seed Shattering 11 controls seed shattering by repressing lignin synthesis in African rice. Plant Biotechnol J. 2023;21(5):931–942. doi: 10.1111/pbi.14004
- Takeda S, Matsuoka M. Genetic approaches to crop improvement: responding to environmental and population changes. Nat Rev Genet. 2008;9(6):444–457. doi: 10.1038/nrg2342
- Fitzgerald MA, McCouch SR, Hall RD. Not just a grain of rice: the quest for quality. Trends Plant Sci. 2009;14(3):133–139.doi: 10.1016/j.tplants.2008.12.004
- Sakamoto T, Matsuoka M. Identifying and exploiting grain yield genes in rice. Curr Opin Plant Biol. 2008;11(2):209–214. doi: 10.1016/j.pbi.2008.01.009
- Harberd NP. Shaping taste: The molecular discovery of rice genes improving grain size, shape and quality. J Genet Genom. 2015;42(11):597–599. doi: 10.1016/j.jgg.2015.09.008
- Ishimaru K, Hirotsu N, Madoka Y, et al. Loss of function of theIAA-glucose hydrolase gene TGW6 enhances rice grain weight and increases yield. Nat Genet. 2013;45(6):707–711. doi: 10.1038/ng.2612
- Jakubowska A, Kowalczyk S. A specific enzyme hydrolyzing 6-O-(4-O)-indole-3-ylacetyl-β-d-glucose in immature kernels of Zea mays. J Plant Physiol. 2005;162(2):207–213. doi: 10.1016/j.jplph.2004.05.015
- Song X-J, Huang W, Shi M, et al. A QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase. Nat Genet. 2007;39(5):623–630. doi: 10.1038/ng2014
- Fan C, Xing Y, Mao H, et al. 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. 2006;112(6):1164–1171. doi: 10.1007/s00122-006-0218-1
- Liu JP, Van Eck J, Cong B, Tanksley SD. A new class of regulatory genes underlying the cause of pear-shaped tomato fruit. PNAS USA. 2002;99(20):13302–13306. doi: 10.1073/pnas.162485999
- O’Leary JM, Hamilton JM, Deane CM, et al. Solution structure and dynamics of a prototypical Chordin-like cysteine-rich repeat (von Willebrand factor type C module) from collagen IIA. J Biol Chem. 2004;279(51):53857–53866. doi: 10.1074/jbc.M409225200
- Kikuchi S, Satoh K, Nagata T, et al. Collection, mapping, and annotation of over 28,000 cDNA clones from japonica rice. Science. 2003;301(5631):376–379. doi: 10.1126/science.1081288
- Fan C, Xing Y, Mao H, et al. 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. 2006;112(6):1164–1171. doi: 10.1007/s00122-006-0218-1
- Mao H, Sun S, Yao J, et al. Linking differential domain functions of the GS3 protein to natural variation of grain size in rice. PNAS USA. 2010;107(45):19579–19584. doi: 10.1073/pnas.1014419107
- Shomura A, Izawa T, Ebana K, et al. Deletion in a gene associated with grain size increased yields during rice domestication. Nat Genet. 2008;40(8):1023–1028. doi: 10.1038/ng.169
- Winkel-Shirley B. Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol. 2001;126(2):485–493. doi: 10.1104/pp.126.2.485
- Nagata K, Yoshinaga S, Takanashi J-i, Terao T. Effects of dry matter production, translocation of nonstructural carbohydrates and nitrogen application on grain filling in rice cultivar Takanari, a cultivar bearing a large number of spikelets. Plant Prod Sci. 2001;4(3):173–183. doi: 10.1626/pps.4.173
- Yang J, Zhang J, Wang Z, et al. Grain and dry matter yields and partitioning of assimilates in japonica/indica hybrid rice. Crop Sci. 2002;42(3):766–772. doi: 10.2135/cropsci2002.7660
- Peng S, Khush GS, Virk P, et al. Progress in ideotype breeding to increase rice yield potential. Field Crops Res. 2008;108(1):32–38.doi: 10.1016/j.fcr.2008.04.001
- Holton TA, Cornish EC. Genetics and biochemistry of anthocyanin biosynthesis. Plant Cell. 1995;7(7):1071–1083. doi: 10.2307/3870058
- Brown RC, Lemmon BE, Olsen O-A. Development of the endosperm in rice (Oryza sativa L.): cellularization. J Plant Res. 1996;109(4):301–313. doi: 10.1007/BF02344477
- Mizutani M, Naganuma T, Tsutsumi K, Saitoh Y. The syncytium-specific expression of the Orysa; KRP3 CDK inhibitor: implication of its involvement in the cell cycle control in the rice (Oryza sativa L.) syncytial endosperm.J Exp Bot. 2010;61(3):791–798. doi: 10.1093/jxb/erp343
- Xia D, Zhang Y, Zhang H, et al. How rice organs are colored: The genetic basis of anthocyanin biosynthesis in rice. Crop J. 2021;9(3):598–608. doi: 10.1016/j.cj.2021.03.013
- Oikawa T, Maeda H, Oguchi T, et al. The birth of a black rice gene and its local spread by introgression. Plant Cell. 2015;27(9):2401–2414.doi: 10.1105/tpc.15.00310
- Ciulu M, de la Luz Cádiz-Gurrea M, Segura-Carretero A. Extraction and analysis of phenolic compounds in rice: a review. Molecules. 2018;23(11):2890. doi: 10.3390/molecules23112890
- Weng J, Gu S, Wan X, et al. Isolation and initial characterization of GW5, a major QTL associated with rice grain width and weight. Cell Res. 2008;18(12):1199–1209. doi: 10.1038/cr.2008.307
- Gonçalves AC, Campos G, Martins Z, et al. Dietary effects of anthocyanins in human health: A comprehensive review. Pharmaceuticals. 2021;14(7):690. doi: 10.3390/ph14070690
- Meng L, Qi C, Wang Z, et al. Determinant factors and regulatory systems for anthocyanin biosynthesis in rice apiculi and stigmas. Rice. 2021;14:45. doi: 10.1186/s12284-021-00480-1
- Furukawa T, Maekawa M, Oki T, et al. The Rc and Rd genes are involved in proanthocyanidin synthesis in rice pericarp. Plant J. 2007;49(1):91–102. doi: 10.1111/j.1365-313X.2006.02958.x
- Chachar ZA, Zhou J, Li W, et al. Cloned genes and genetic regulation of anthocyanin biosynthesis in maize, a comparative review. Front Plant Sci. 2023;15:1310634. doi: 10.3389/fpls.2024.1310634
- Nagata S, Takahashi M. Attempt to construct twelve linkage groups in Japanese rice. Japanese Journal of Genetics. 1963;38(1):10–15.
- Sweeney MT, Thomson MJ, Cho YG, et al. Caught red-handed: Rc encodes a basic helix-loop-helix protein conditioning red pericarp in rice. Plant Cell. 2006;18(2):283–294. doi: 10.1105/tpc.105.038430
- Vaughan LK, Ottis BV, Prazak-Havey AM, et al. Is all red rice found in commercial rice really Oryza sativa? Weed Sci. 2001;49(4):468–476. doi: 10.1614/0043-1745(2001)049[0468:IARRFI]2.0.CO;2
- Gu X-Y, Foley ME, Horvath DP, et al. Association between seed dormancy and pericarp color is controlled by a pleiotropic gene that regulates abscisic acid and flavonoid synthesis in weedy red rice. Genetics. 2011;189(4):1515–1524. doi: 10.1534/genetics.111.131169
- Raju RS, Sahoo C, Hanjagi PS, Samai KC. Physiological and biochemical traits regulating preharvest sprouting resistance in rice. ORYZA — Int J Rice. 2023;60(1):140–149. doi: 10.35709/ory.2023.60.1.5
- Gu X-Y, Kianian SF, Foley ME. Multiple loci and epistases control genetic variation for seed dormancy in weedy rice (Oryza sativa). Genetics. 2004;166(3):1503–1516. doi: 10.1534/genetics.166.3.1503
- Tokmakov SV, Mukhina ZM, Bogomaz DI, Matveeva TV. Development of molecular marker for assessment of intraspecific polymorphism of Rc gene conditioning red pericarp in rice Oryza sativa L. Ecological genetics. 2011;9(3):57–67. EDN: OKDPLB doi: 10.17816/ecogen9357-67
- Alekseev VI, Grigoriev AM, Silin AN, Kosikov EN. Early diagnostics of rice red blotch based on the application of DNA marking. In: VII Congress of the Vavilov Society of Geneticists and Breeders dedicated to the 100th anniversary of the Department of Genetics, SPSU. 2019. P. 1106. (In Russ.)
- Zhu Y, Lin Y, Chen S, et al. CRISPR/Cas9-mediated functional recovery of the recessive rc allele to develop red rice. Plant Biotechnol J. 2019;17(11):2096–2105. doi: 10.1111/pbi.13125
- Zelenskaya OV, Zelensky GL, Ostapenko NV, Tumanyan IG. Genetic resources of rice (Oryza sativa L.) with colored pericarp. Vavilov journal of genetics and breeding. 2018;22(3):296–303. doi: 10.18699/VJ18.363EDN: XMHVCP
- Maeda H, Yamaguchi T, Omoteno M, et al. Genetic dissection of black grain rice by the development of a near isogenic line. Breed Sci. 2014;64(2):134–141. doi: 10.1270/jsbbs.64.134
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