A genome-wide association study using a Vietnamese landrace panel of rice (Oryza sativa) reveals new QTLs controlling panicle morphological traits

. 2018 Nov 14 ; 18 (1) : 282. [epub] 20181114

Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid30428844

Grantová podpora
106-NN.02-2016.60 Nafosted
EVOREPRICE 1201-004 Agropolis Fondation

Odkazy

PubMed 30428844
PubMed Central PMC6234598
DOI 10.1186/s12870-018-1504-1
PII: 10.1186/s12870-018-1504-1
Knihovny.cz E-zdroje

CONTEXT: Yield improvement is an important issue for rice breeding. Panicle architecture is one of the key components of rice yield and exhibits a large diversity. To identify the morphological and genetic determinants of panicle architecture, we performed a detailed phenotypic analysis and a genome-wide association study (GWAS) using an original panel of Vietnamese landraces. RESULTS: Using a newly developed image analysis tool, morphological traits of the panicles were scored over two years: rachis length; primary, secondary and tertiary branch number; average length of primary and secondary branches; average length of internode on rachis and primary branch. We observed a high contribution of spikelet number and secondary branch number per panicle to the overall phenotypic diversity in the dataset. Twenty-nine stable QTLs associated with seven traits were detected through GWAS over the two years. Some of these QTLs were associated with genes already implicated in panicle development. Importantly, the present study revealed the existence of new QTLs associated with the spikelet number, secondary branch number and primary branch number traits. CONCLUSIONS: Our phenotypic analysis of panicle architecture variation suggests that with the panel of samples used, morphological diversity depends largely on the balance between indeterminate vs. determinate axillary meristem fate on primary branches, supporting the notion of differences in axillary meristem fate between rachis and primary branches. Our genome-wide association study led to the identification of numerous genomic sites covering all the traits studied and will be of interest for breeding programs aimed at improving yield. The new QTLs detected in this study provide a basis for the identification of new genes controlling panicle development and yield in rice.

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Xing Y, Zhang Q. Genetic and molecular bases of rice yield. Annu Rev Plant Biol. 2010;61:421–442. doi: 10.1146/annurev-arplant-042809-112209. PubMed DOI

Ikeda M, Miura K, Aya K, Kitano H, Matsuoka M. Genes offering the potential for designing yield-related traits in rice. Curr Opin Plant Biol. 2013;16:1–8. doi: 10.1016/j.pbi.2013.02.002. PubMed DOI

Bai X, Wu B, Xing Y. Yield-related QTLs and their applications in rice genetic improvement. J Integr Plant Biol. 2012;54:300–311. doi: 10.1111/j.1744-7909.2012.01117.x. PubMed DOI

Fujita D, Trijatmiko KR, Tagle AG, Sapasap MV, Koide Y, Sasaki K, et al. NAL1 allele from a rice landrace greatly increases yield in modern indica cultivars. Proc Natl Acad Sci U S A. 2013;110:20431–20436. doi: 10.1073/pnas.1310790110. PubMed DOI PMC

Takai T, Adachi S, Taguchi-Shiobara F, Sanoh-Arai Y, Iwasawa N, Yoshinaga S, et al. A natural variant of NAL1, selected in high-yield rice breeding programs, pleiotropically increases photosynthesis rate. Sci Rep. 2013;3:2149. doi: 10.1038/srep02149. PubMed DOI PMC

Zhu C, Gore M, Buckler ES, Yu J. Status and prospects of association mapping in plants. Plant Gen. 2008;1:5–20. doi: 10.3835/plantgenome2008.02.0089. DOI

Huang X, Wei X, Sang T, Zhao Q, Feng Q, Zhao Y, et al. Genome-wide association studies of 14 agronomic traits in rice landraces. Nat Genet. 2010;42:961–967. doi: 10.1038/ng.695. PubMed DOI

Chen W, Gao Y, Xie W, Gong L, Lu K, Wang W, et al. Genome-wide association analyses provide genetic and biochemical insights into natural variation in rice metabolism. Nat Genet. 2014;46:714–721. doi: 10.1038/ng.3007. PubMed DOI

Yonemaru J-I, Mizobuchi R, Kato H, Yamamoto T, Yamamoto E, Matsubara K, et al. Genomic regions involved in yield potential detected by genome-wide association analysis in Japanese high-yielding rice cultivars. BMC Genomics. 2014;15:346. doi: 10.1186/1471-2164-15-346. PubMed DOI PMC

Magwa RA, Zhao H, Xing Y. Genome-wide association mapping revealed a diverse genetic basis of seed dormancy across subpopulations in rice (Oryza sativa L.) BMC Genet. 2016;17:28. doi: 10.1186/s12863-016-0340-2. PubMed DOI PMC

Matsuda F, Nakabayashi R, Yang Z, Okazaki Y, Yonemaru J-I, Ebana K, et al. Metabolome-genome-wide association study dissects genetic architecture for generating natural variation in rice secondary metabolism. Plant J. 2014;81:13–23. doi: 10.1111/tpj.12681. PubMed DOI PMC

Phung NTP, Mai CD, Hoang GT, Truong HTM, Lavarenne J, Gonin M, et al. Genome-wide association mapping for root traits in a panel of rice accessions from Vietnam. BMC Plant Biol. 2016;16:64. doi: 10.1186/s12870-016-0747-y. PubMed DOI PMC

Kumar V, Singh A, Mithra SV, Krishnamurthy SL, Parida SK, Jain S, et al. Genome-wide association mapping of salinity tolerance in rice (Oryza sativa) DNA Res. 2015;22:133–145. doi: 10.1093/dnares/dsu046. PubMed DOI PMC

Famoso AN, Zhao K, Clark RT, Tung C-W, Wright MH, Bustamante C, et al. Genetic architecture of aluminum tolerance in rice (Oryza sativa) determined through genome-wide association analysis and QTL mapping. PLoS Genet. 2011;7:e1002221. doi: 10.1371/journal.pgen.1002221. PubMed DOI PMC

Begum H, Spindel JE, Lalusin A, Borromeo T, Gregorio G, Hernandez J, et al. Genome-wide association mapping for yield and other agronomic traits in an elite breeding population of tropical rice (Oryza sativa) PLoS One. 2015;10:e0119873. doi: 10.1371/journal.pone.0119873. PubMed DOI PMC

Huang X, Zhao Y, Wei X, Li C, Wang A, Zhao Q, et al. Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm. Nat Genet. 2011;44:32–39. doi: 10.1038/ng.1018. PubMed DOI

Zhao K, Tung C-W, Eizenga GC, Wright MH, Ali ML, Price AH, et al. Genome-wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativa. Nat Commun. 2011;2:467. doi: 10.1038/ncomms1467. PubMed DOI PMC

Crowell S, Korniliev P, Falcão A, Ismail A, Gregorio G, Mezey J, et al. Genome-wide association and high-resolution phenotyping link Oryza sativa panicle traits to numerous trait-specific QTL clusters. Nat Commun. 2016;7:10527. doi: 10.1038/ncomms10527. PubMed DOI PMC

Rebolledo MC, Peña AL, Duitama J, Cruz DF, Dingkuhn M, Grenier C, et al. Combining image analysis, genome wide association studies and different field trials to reveal stable genetic regions related to panicle architecture and the number of spikelets per panicle in rice. Front Plant Sci. 2016;7:122–112. doi: 10.3389/fpls.2016.01384. PubMed DOI PMC

Bai Xufeng, Zhao Hu, Huang Yong, Xie Weibo, Han Zhongmin, Zhang Bo, Guo Zilong, Yang Lin, Dong Haijiao, Xue Weiya, Li Guangwei, Hu Gang, Hu Yong, Xing Yongzhong. Genome-Wide Association Analysis Reveals Different Genetic Control in Panicle Architecture Between and Rice. The Plant Genome. 2016;9(2):0. doi: 10.3835/plantgenome2015.11.0115. PubMed DOI

AL-Tam Faroq, Adam Helene, Anjos António, Lorieux Mathias, Larmande Pierre, Ghesquière Alain, Jouannic Stefan, Shahbazkia Hamid. P-TRAP: a Panicle Trait Phenotyping tool. BMC Plant Biology. 2013;13(1):122. doi: 10.1186/1471-2229-13-122. PubMed DOI PMC

Phung NTP, Mai DC, Mournet P, Frouin J, Droc G, Ta KN, Jouannic S, et al. 2014. Characterization of a panel of Vietnamese rice varieties using DArT and SNP markers for association mapping purposes. BMC Plant biol. 2014;14:371. PubMed PMC

Fukuoka S, Alpatyeva NV, Ebana K, Luu NT, Nagamine T. Analysis of Vietnamese rice germplasm provides an insight into japonica rice differentiation. Plant Breed. 2003;122:497–502. doi: 10.1111/j.1439-0523.2003.00908.x. DOI

Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000;155:945–959. PubMed PMC

Patterson HD, Williams ER. A new class of resolvable incomplete block designs. Biometrika. 1976;63:83–92. doi: 10.1093/biomet/63.1.83. DOI

Yu J, Pressoir G, Briggs WH, Vroh Bi I, Yamasaki M, Doebley JF, et al. A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet. 2006;38:203–208. doi: 10.1038/ng1702. PubMed DOI

Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler E. TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics. 2007;23:2633–2635. doi: 10.1093/bioinformatics/btm308. PubMed DOI

Mei HW, Xu JL, Li ZK, Yu XQ, Guo LB, Wang YP, et al. QTLs influencing panicle size detected in two reciprocal introgressive line (IL) populations in rice (Oryza sativa L.) Theor Appl Genet. 2006;112:648–656. doi: 10.1007/s00122-005-0167-0. PubMed DOI

Itoh J, Nonomura K, Ikeda K, Yamaki S, Inukai Y, Yamagishi H, et al. Rice plant development: from zygote to spikelet. Plant Cell Physiol. 2005;46:23–47. doi: 10.1093/pcp/pci501. PubMed DOI

Kyozuka J, Tokunaga H, Yoshida A. Control of grass inflorescence form by the fine-tuning of meristem phase change. Curr Opin Plant Biol. 2014;17:110–115. doi: 10.1016/j.pbi.2013.11.010. PubMed DOI

Yoshida A., Sasao M., Yasuno N., Takagi K., Daimon Y., Chen R., Yamazaki R., Tokunaga H., Kitaguchi Y., Sato Y., Nagamura Y., Ushijima T., Kumamaru T., Iida S., Maekawa M., Kyozuka J. TAWAWA1, a regulator of rice inflorescence architecture, functions through the suppression of meristem phase transition. Proceedings of the National Academy of Sciences. 2012;110(2):767–772. doi: 10.1073/pnas.1216151110. PubMed DOI PMC

Kurakawa T, Ueda N, Maekawa M, Kobayashi K, Kojima M, Nagato Y, et al. Direct control of shoot meristem activity by a cytokinin-activating enzyme. Nature. 2007;445:652–655. doi: 10.1038/nature05504. PubMed DOI

Iwamoto M, Tagiri A. MicroRNA-targeted transcription factor gene RDD1 promotes nutrient ion uptake and accumulation in rice. Plant J. 2016;85:466–477. doi: 10.1111/tpj.13117. PubMed DOI

Jiang D, Fang J, Lou L, Zhao J, Yuan S, Yin L, Sun W, Peng L, Guo B, Li X. Characterization of a null allelic mutant of the rice NAL1 gene reveals its role in regulating cell division. PLoS One. 2015;10:e0118169. doi: 10.1371/journal.pone.0118169. PubMed DOI PMC

Adriani DE, Dingkuhn M, Dardou A, Adam H, Luquet D, Lafarge T. Rice panicle plasticity in near isogenic lines carrying a QTL for larger panicle is genotype and environment dependent. Rice (N Y) 2016;9:28. doi: 10.1186/s12284-016-0101-x. PubMed DOI PMC

Zhang GH, Li SY, Wang L, Ye WJ, Zeng DL, Rao YC, Peng YL, Hu J, Yang YL, Xu J, Ren DY, Gao ZY, Zhu L, Dong GJ, Hu XM, Yan MX, Guo LB, Li CY, Qian Q. LSCHL4 from japonica cultivar, which is allelic to NAL1, increases yield of indica super rice 93-11. Mol Plant. 2014;7:1350–1364. doi: 10.1093/mp/ssu055. PubMed DOI PMC

Yang R, Tang Q, Wang H, Zhang X, Pan G, Wang H, Tu J. Analyses of two rice (Oryza sativa) cyclin-dependent kinase inhibitors and effects of transgenic expression of OsiICK6 on plant growth and development. Ann Bot. 2011;107:1087–1101. doi: 10.1093/aob/mcr057. PubMed DOI PMC

Han SH, Yoo SC, Lee BD, An G, Paek NC. Rice FLAVIN-BINDING, KELCH REPEAT, F-BOX 1 (OsFKF1) promotes flowering independent of photoperiod. Plant Cell Environ. 2015;38:2527–2540. doi: 10.1111/pce.12549. PubMed DOI

Lee YS, Jeong DH, Lee DY, Yi J, Ryu CH, Kim SL, et al. OsCOL4 is a constitutive flowering repressor upstream of Ehd1 and downstream of OsphyB. Plant J. 2010;63:18–30. PubMed

Zhang LY, Bai MY, Wu J, Zhu JY, Wang H, Zhang Z, et al. Antagonistic HLH/bHLH transcription factors mediate brassinosteroid regulation of cell elongation and plant development in rice and Arabidopsis. Plant Cell. 2009;21:3767–3780. doi: 10.1105/tpc.109.070441. PubMed DOI PMC

Tanaka K, Murata K, Yamazaki M, Onosato K, Miyao A, Hirochika H. Three distinct rice cellulose synthase catalytic subunit genes required for cellulose synthesis in the secondary wall. Plant Physiol. 2003;133:73–83. doi: 10.1104/pp.103.022442. PubMed DOI PMC

Mohanta TK, Mohanta N, Bae H. Identification and expression analysis of PIN-like (PILS) gene family of rice treated with auxin and cytokinin. Genes. 2015;6:622–640. doi: 10.3390/genes6030622. PubMed DOI PMC

Wang D, Pei K, Fu Y, Sun Z, Li S, Liu H, et al. Genome-wide analysis of the auxin response factors (ARF) gene family in rice (Oryza sativa) Gene. 2007;394:13–24. doi: 10.1016/j.gene.2007.01.006. PubMed DOI

Sridhar VV, Surendrarao A, Gonzalez D, Conlan RS, Liu Z. Transcriptional repression of target genes by LEUNIG and SEUSS, two interacting regulatory proteins for Arabidopsis flower development. Proc Natl Acad Sci U S A. 2004;101:11494–11499. doi: 10.1073/pnas.0403055101. PubMed DOI PMC

Spielmeyer W, Ellis MH, Chandler PM. Semidwarf (sd-1), "green revolution" rice, contains a defective gibberellin 20-oxidase gene. Proc Natl Acad Sci U S A. 2002;99:9043–9048. doi: 10.1073/pnas.132266399. PubMed DOI PMC

Jiao Yongqing, Wang Yonghong, Xue Dawei, Wang Jing, Yan Meixian, Liu Guifu, Dong Guojun, Zeng Dali, Lu Zefu, Zhu Xudong, Qian Qian, Li Jiayang. Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nature Genetics. 2010;42(6):541–544. doi: 10.1038/ng.591. PubMed DOI

Huang J, Li Z, Zhao D. Deregulation of the osmiR160 target gene OsARF18 causes growth and developmental defects with an alteration of auxin signaling in rice. Sci Rep. 2016;6:29938. doi: 10.1038/srep29938. PubMed DOI PMC

Xie Z, Kasschau KD, Carrington JC. Negative feedback regulation of dicer-Like1 in Arabidopsis by microRNA-guided mRNA degradation. Curr Biol. 2003;13:784–789. doi: 10.1016/S0960-9822(03)00281-1. PubMed DOI

Fan T, Li X, Yang W, Xia K, Ouyang J, Zhang M. Rice Osa-miR171c mediates phase change from vegetative to reproductive development and shoot apical meristem maintenance by repressing four OsHAM transcription factors. PLoS One. 2015;10:e0125833. doi: 10.1371/journal.pone.0125833. PubMed DOI PMC

Zhu QH, Upadhyaya NM, Gubler F, Helliwell CA. Over-expression of miR172 causes loss of spikelet determinacy and floral organ abnormalities in rice (Oryza sativa) BMC Plant Biol. 2009;9:149. doi: 10.1186/1471-2229-9-149. PubMed DOI PMC

Wang L, Sun S, Jin J, Fu D, Yang X, Weng X, et al. Coordinated regulation of vegetative and reproductive branching in rice. Proc Natl Acad Sci U S A. 2015;112:15504–15509. doi: 10.1073/pnas.1521949112. PubMed DOI PMC

Zhang YC, Yu Y, Wang CY, Li ZY, Liu Q, Xu J, et al. Overexpression of microRNA OsmiR397 improves rice yield by increasing grain size and promoting panicle branching. Nat Biotechnol. 2013;31:848–852. doi: 10.1038/nbt.2646. PubMed DOI

Li S, Gao F, Xie K, Zeng X, Cao Y, Zeng J, et al. The OsmiR396c-OsGRF4-OsGIF1 regulatory module determines grain size and yield in rice. Plant Biotechnol J. 2016;14:2134–2146. doi: 10.1111/pbi.12569. PubMed DOI PMC

Wang Y, Shen D, Bo S, Chen H, Zheng J, Zhu QH, et al. Sequence variation and selection of small RNAs in domesticated rice. BMC Evol Biol. 2010;10:119. doi: 10.1186/1471-2148-10-119. PubMed DOI PMC

Wang Y, Bai X, Yan C, Gui Y, Wei X, Zhu QH, et al. Genomic dissection of small RNAs in wild rice (Oryza rufipogon): lessons for rice domestication. New Phytol. 2012;196:914–925. doi: 10.1111/j.1469-8137.2012.04304.x. PubMed DOI

Wang Y, Li J. Branching in rice. Curr Opin Plant Biol. 2011;14:94–99. doi: 10.1016/j.pbi.2010.11.002. PubMed DOI

Teo ZW, Song S, Wang YQ, Liu J, Yu H. New insights into the regulation of inflorescence architecture. Trends Plant Sci. 2014;19:158–165. doi: 10.1016/j.tplants.2013.11.001. PubMed DOI

Jang S, Lee Y, Lee G, Seo J, Lee D, Yu Y, et al. Association between sequence variants in panicle development genes and the number of spikelets per panicle in rice. BMC Genet. 2018;19:5. doi: 10.1186/s12863-017-0591-6. PubMed DOI PMC

Li M, Li X, Zhou Z, Wu P, Fang M, Pan X, et al. Reassessment of the four yield-related genes Gn1a, DEP1, GS3, and IPA1 in Rice using a CRISPR/Cas9 system. Front Plant Sci. 2016;7:377. PubMed PMC

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