Abstract
Main conclusion
A novel QTL GS6.1 increases yield per plant by controlling kernel size, plant architecture, and kernel filling in rice.
Abstract
Kernel size and plant architecture are critical agronomic traits that greatly influence kernel yield in rice. Using the single-segment substitution lines (SSSLs) with an indica cultivar Huajingxian74 as a recipient parent and American Jasmine as a donor parent, we identified a novel quantitative trait locus (QTL), named GS6.1. Near isogenic line-GS6.1 (NIL-GS6.1) produces long and narrow kernels by regulating cell length and width in the spikelet hulls, thus increasing the 1000-kernel weight. Compared with the control, the plant height, panicles per plant, panicle length, kernels per plant, secondary branches per panicle, and yield per plant of NIL-GS6.1 are increased. In addition, GS6.1 regulates the kernel filling rate. GS6.1 controls kernel size by modulating the transcription levels of part of EXPANSINs, kernel filling-related genes, and kernel size-related genes. These results indicate that GS6.1 might be beneficial for improving kernel yield and plant architecture in rice breeding by molecular design.
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Data availability
Data will be made available on request.
References
Arseneau JR, Steeves R, Laflamme M (2017) Modified low-salt CTAB extraction of high-quality DNA from contaminant-rich tissues. Mol Ecol Resour 17(4):686–693. https://doi.org/10.1111/1755-0998.12616
Choi BS, Kim YJ, Markkandan K, Koo YJ, Song JT, Seo HS (2018) GW2 functions as an E3 ubiquitin ligase for rice expansin-like 1. Int J Mol Sci 19(7):1904. https://doi.org/10.3390/ijms19071904
Duan PG, Ni S, Wang JM, Zhang BL, Xu R, Wang YX, Chen HQ, Zhu XD, Li YH (2016) Regulation of OsGRF4 by OsmiR396 controls grain size and yield in rice. Nat Plants 2(1):15203. https://doi.org/10.1038/Nplants.2015.203
Eshed Y, Zamir D (1995) An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield-associated QTL. Genetics 141(3):1147–1162. https://doi.org/10.1093/genetics/141.3.1147
Fang CW, Li L, He RM, Wang DQ, Wang M, Hu Q, Ma QR, Qin KY, Feng XY, Zhang GQ, Fu XL, Liu ZQ (2019) Identification of S23 causing both interspecific hybrid male sterility and environment-conditioned male sterility in rice. Rice 12(1):10. https://doi.org/10.1186/s12284-019-0271-4
Hao JQ, Wang DK, Wu YB, Huang K, Duan PG, Li N, Xu R, Zeng DL, Dong GJ, Zhang BL, Zhang LM, Inze D, Qian Q, Li YH (2021) The GW2-WG1-OsbZIP47 pathway controls grain size and weight in rice. Mol Plant 14(8):1266–1280. https://doi.org/10.1016/j.molp.2021.04.011
He Y, Li LY, Shi WB, Tan JH, Luo XX, Zheng SY, Chen WT, Li J, Zhuang CX, Jiang DG (2022) Florigen repression complexes involving rice CENTRORADIALIS2 regulate grain size. Plant Physiol 190(2):1260–1274. https://doi.org/10.1093/plphys/kiac338
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(10):1455–1465. https://doi.org/10.1016/j.molp.2015.07.002
Li N, Li YH (2016) Signaling pathways of seed size control in plants. Curr Opin Plant Biol 33:23–32. https://doi.org/10.1016/j.pbi.2016.05.008
Li N, Xu R, Li YH (2019) Molecular networks of seed size control in plants. Annu Rev Plant Biol 70:435–463. https://doi.org/10.1146/annurev-arplant-050718-095851
Li J, Yang HX, Xu GY, Deng KL, Yu JJ, Xiang SQ, Zhou K, Zhang QL, Li RX, Li MM, Ling YH, Yang ZL, He GH, Zhao FM (2022) QTL analysis of Z414, a chromosome segment substitution line with short, wide grains, and substitution mapping of qGL11 in rice. Rice 15(1):25. https://doi.org/10.1186/s12284-022-00571-7
Lin SJ, Liu ZP, Zhang K, Yang WF, Zhan PL, Tan QY, Gou YJ, Ma SP, Luan X, Huang CB, Xiao ZL, Liu YY, Zhu BH, Liang RQ, Zhou WQ, Zhu HT, Bu SH, Liu GF, Zhang GQ, Wang SK (2023) GL9 from Oryza glumaepatula controls grain size and chalkiness in rice. Crop J 11(1):198–207. https://doi.org/10.1016/j.cj.2022.06.006
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. Proc Natl Acad Sci USA 112(35):11102–11107. https://doi.org/10.1073/pnas.1512748112
Liu ZP, Chen G, Gao F, Xu R, Li N, Zhang YY, Li YH (2019) Transcriptional repression of the APC/C activator genes CCS52A1/A2 by the mediator complex subunit MED16 controls endoreduplication and cell growth in Arabidopsis. Plant Cell 31(8):1899–1912. https://doi.org/10.1105/tpc.18.00811
Liu ZP, Li N, Zhang YY, Li YH (2020) Transcriptional repression of GIF1 by the KIX-PPD-MYC repressor complex controls seed size in Arabidopsis. Nat Commun 11(1):1846. https://doi.org/10.1038/s41467-020-15603-3
Lyu J, Wang DK, Duan PG, Lu YP, Huang K, Zeng DL, Zhang LM, Dong GJ, Li YJ, Xu R, Zhang BL, Huang XH, Li N, Wang YC, Qian Q, Li YH (2020) Control of grain size and weight by the GSK2-LARGE1/OML4 pathway in rice. Plant Cell 32(6):1905–1918. https://doi.org/10.1105/tpc.19.00468
Ma NN, Wang Y, Qiu SC, Kang ZH, Che SG, Wang GX, Huang JL (2013) Overexpression of OsEXPA8, a root-specific gene, improves rice growth and root system architecture by facilitating cell extension. PLoS ONE 8(10):e75997. https://doi.org/10.1371/journal.pone.0075997. (ARTN e75997)
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(5):863–873. https://doi.org/10.1093/pcp/pcx040
Prasad K, Parameswaran S, Vijayraghavan U (2005) OsMADS1, a rice MADS-box factor, controls differentiation of specific cell types in the lemma and palea and is an early-acting regulator of inner floral organs. Plant J 43(6):915–928. https://doi.org/10.1111/j.1365-313X.2005.02504.x
Shearman JR (2022) A single segment substitution line population for identifying traits relevant to drought tolerance and avoidance. Genomics 114(1):476–481. https://doi.org/10.1016/j.ygeno.2019.10.001
Sun CH, Wang Y, Yang XR, Tang L, Wan CM, Liu JQ, Chen CP, Zhang HS, He CC, Liu CQ, Wang Q, Zhang K, Zhang WF, Yang B, Li SC, Zhu J, Sun YJ, Li WT, Zhou YH, Wang PR, Deng XJ (2023) MATE transporter GFD1 cooperates with sugar transporters, mediates carbohydrate partitioning and controls grain-filling duration, grain size and number in rice. Plant Biotechnol J 21(3):621–634. https://doi.org/10.1111/pbi.13976
Tan QY, Bu SH, Chen GD, Yan ZG, Chang ZY, Zhu HT, Yang WF, Zhan PL, Lin SJ, Xiong L, Chen SL, Liu GF, Liu ZP, Wang SK, Zhang GQ (2022) Reconstruction of the high stigma exsertion rate trait in rice by pyramiding multiple QTLs. Front Plant Sci 13:921700. https://doi.org/10.3389/fpls.2022.921700
Tang XJ, Peng C, Zhang J, Cai Y, You XM, Kong F, Yan HG, Wang GX, Wang L, Jin J, Chen WW, Chen XG, Ma J, Wang P, Jiang L, Zhang WW, Wan JM (2016) ADP-glucose pyrophosphorylase large subunit 2 is essential for storage substance accumulation and subunit interactions in rice endosperm. Plant Sci 249:70–83. https://doi.org/10.1016/j.plantsci.2016.05.010
Tian XJ, Li XF, Zhou WJ, Ren YK, Wang ZY, Liu ZQ, Tang JQ, Tong HN, Fang J, Bu QY (2017) Transcription Factor OsWRKY53 positively regulates brassinosteroid signaling and plant architecture. Plant Physiol 175(3):1337–1349. https://doi.org/10.1104/pp.17.00946
Wang E, Wang J, 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(11):1370–1374. https://doi.org/10.1038/ng.220
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(8):950–954. https://doi.org/10.1038/ng.2327
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(8):949–954. https://doi.org/10.1038/ng.3352
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(8):944–948. https://doi.org/10.1038/ng.3346
Wang DW, Sun WQ, Yuan ZY, Sun Q, Fan K, Zhang CP, Yu SB (2021) Identification of a novel QTL and candidate gene associated with grain size using chromosome segment substitution lines in rice. Sci Rep-Uk 11(1):189. https://doi.org/10.1038/s41598-020-80667-6
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(2):134–153. https://doi.org/10.1111/jipb.12510
Weng JF, Gu SH, Wan XY, Gao H, Guo T, Su N, Lei CL, Zhang X, Cheng ZJ, Guo XP, Wang JL, Jiang L, Zhai HQ, Wan JM (2008) Isolation and initial characterization of GW5, a major QTL associated with rice grain width and weight. Cell Res 18(12):1199–1209. https://doi.org/10.1038/cr.2008.307
Wu MM, Ren YL, Cai MH, Wang YL, Zhu SS, Zhu JP, Hao YY, Teng X, Zhu XP, Jing RN, Zhang H, Zhong MS, Wang YF, Lei CL, Zhang X, Guo XP, Cheng ZJ, Lin QB, Wang J, Jiang L, Bao YQ, Wang YH, Wan JM (2019) Rice FLOURY ENDOSPERM10 encodes a pentatricopeptide repeat protein that is essential for the trans-splicing of mitochondrial nad1 intron 1 and endosperm development. New Phytol 223(2):736–750. https://doi.org/10.1111/nph.15814
Xi ZY, He FH, Zeng RZ, Zhang ZM, Ding XH, Li WT, Zhang GQ (2006) Development of a wide population of chromosome single-segment substitution lines in the genetic background of an elite cultivar of rice (Oryza sativa L.). Genome 49(5):476–484. https://doi.org/10.1139/G06-005
Xing YZ, Zhang QF (2010) Genetic and molecular bases of rice yield. Annu Rev Plant Biol 61(61):421–442. https://doi.org/10.1146/annurev-arplant-042809-112209
Yang JL, Luo DP, Yang B, Frommer WB, Eom JS (2018) SWEET11 and 15 as key players in seed filling in rice. New Phytol 218(2):604–615. https://doi.org/10.1111/nph.15004
Yang WF, Liang JY, Hao QW, Luan X, Tan QY, Lin SW, Zhu HT, Liu GF, Liu ZP, Bu SH, Wang SK, Zhang GQ (2021a) Fine mapping of two grain chalkiness QTLs sensitive to high temperature in rice. Rice 14(1):33. https://doi.org/10.1186/s12284-021-00476-x
Yang WF, Xiong L, Liang JY, Hao QW, Luan X, Tan QY, Lin SW, Zhu HT, Liu GF, Liu ZP, Bu SH, Wang SK, Zhang GQ (2021b) Substitution mapping of two closely linked QTLs on chromosome 8 controlling grain chalkiness in rice. Rice 14(1):85. https://doi.org/10.1186/s12284-021-00526-4
Yang WF, Hao QW, Liang JY, Tan QY, Luan X, Lin SJ, Zhu HT, Bu SH, Liu ZP, Liu GF, Wang SK, Zhang GQ (2022) Fine mapping of two major quantitative trait loci for rice chalkiness with high temperature-enhanced additive effects. Front Plant Sci 13:957863. https://doi.org/10.3389/fpls.2022.957863
Yuan RZ, Zhao N, Usman B, Luo L, Liao SY, Qin YF, Nawaz G, Li RB (2020) Development of chromosome segment substitution lines (CSSLs) derived from guangxi wild rice (Oryza rufipogon Griff.) under rice (Oryza sativa L.) background and the identification of QTLs for plant architecture, agronomic traits and cold tolerance. Genes-Basel 11(9):980. https://doi.org/10.3390/genes11090980
Zhan PL, Wei X, Xiao ZL, Wang XL, Ma SP, Lin SJ, Li FP, Bu SH, Liu ZP, Zhu HT, Liu GF, Zhang GQ, Wang SK (2021) GW10, a member of P450 subfamily regulates grain size and grain number in rice. Theor Appl Genet 134(12):3941–3950. https://doi.org/10.1007/s00122-021-03939-3
Zhan PL, Ma SP, Xiao ZL, Li FP, Wei X, Lin SJ, Wang XL, Ji Z, Fu Y, Pan JH, Zhou M, Liu Y, Chang ZY, Li L, Bu SH, Liu ZP, Zhu HT, Liu GF, Zhang GQ, Wang SK (2022) Natural variations in grain length 10 (GL10) regulate rice grain size. J Genet Genom 49(5):405–413. https://doi.org/10.1016/j.jgg.2022.01.008
Zhang GQ (2021) Target chromosome-segment substitution: a way to breeding by design in rice. Crop J 9(3):658–668. https://doi.org/10.1016/j.cj.2021.03.001
Zhang ZX, Zhao H, Huang FL, Long JF, Song G, Lin WX (2019) The 14–3–3 protein GF14f negatively affects grain filling of inferior spikelets of rice (Oryza sativa L,). Plant J 99(2):344–358. https://doi.org/10.1111/tpj.14329
Zhao DS, Li QF, Zhang CQ, Zhang C, Yang QQ, Pan LX, Ren XY, Lu J, Gu MH, Liu QQ (2018) GS9 acts as a transcriptional activator to regulate rice grain shape and appearance quality. Nat Commun 9(1):1240. https://doi.org/10.1038/s41467-018-03616-y
Zou HY, Wenwen YH, Zang GC, Kang ZH, Zhang ZY, Huang JL, Wang GX (2015) OsEXPB2, a beta-expansin gene, is involved in rice root system architecture. Mol Breed 35(1):135. https://doi.org/10.1007/s11032-015-0203-y. (ARTN 4)
Zuo JR, Li JY (2014) Molecular genetic dissection of quantitative trait loci regulating rice grain size. Annu Rev Genet 48:99–118. https://doi.org/10.1146/annurev-genet-120213-092138
Acknowledgements
This study was supported by the National Natural Science Foundation of China (32201742), the Major Science and Technology Research Projects of Guangdong Laboratory for Lingnan Modern Agriculture (NT2021001), the Natural Science Foundation of Guangdong Province (2023A1515012083), Science and Technology Planning Project of Guangzhou (2023A04J1962), the Youth Talent Support Programme of Guangdong Provincial Association for Science and Technology, China (SKXRC202208), the double first-class discipline promotion project (2021B10564001), and the Hainan Provincial Natural Science Foundation of China (320MS079).
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Zhao, H., Fu, Y., Zhang, G. et al. GS6.1 controls kernel size and plant architecture in rice. Planta 258, 42 (2023). https://doi.org/10.1007/s00425-023-04201-4
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DOI: https://doi.org/10.1007/s00425-023-04201-4