Abstract
The identification of rice drought tolerant materials is crucial for the development of best performing cultivars for the upland cultivation system. This study aimed to identify markers and candidate genes associated with drought tolerance by Genome Wide Association Study analysis, in order to develop tools for use in rice breeding programs. This analysis was made with 175 upland rice accessions (Oryza sativa), evaluated in experiments with and without water restriction, and 150,325 SNPs. Thirteen SNP markers associated with yield under drought conditions were identified. Through stepwise regression analysis, eight SNP markers were selected and validated in silico, and when tested by PCR, two out of the eight SNP markers were able to identify a group of rice genotypes with higher productivity under drought. These results are encouraging for deriving markers for the routine analysis of marker assisted selection. From the drought experiment, including the genes inherited in linkage blocks, 50 genes were identified, from which 30 were annotated, and 10 were previously related to drought and/or abiotic stress tolerance, such as the transcription factors WRKY and Apetala2, and protein kinases.
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Abadie T, Cordeiro CMT, Fonseca JR, Alves RBN, Burle ML, Brondani C, Rangel PHN, Castro EM, Silva HT, Freire MS, Zimmermann FJP, Magalhães JR (2005) Construção de uma coleção nuclear de arroz para o Brasil. Pesqui Agropecu Bras 40:129–136
Alonso JM, Ecker JR (2006) Moving forward in reverse: genetic technologies to enable genome-wide phenomic screens in Arabidopsis. Nat Rev Genet 7:524–536
Barrett JC, Fry B, Maller J, Daly MJ (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21:263–265
Bernier J, Kumar A, Venuprasad R, Spaner D, Atlin GN (2007) A large-effect QTL for grain yield under reproductive-stage drought stress in upland rice. Crop Sci 47:507–516
Biffani S, Dimauro C, Macciotta N, Rossoni A, Stella A, Biscarini F (2015) Predicting haplotype carriers from SNP genotypes in Bos taurus through linear discriminant analysis. Genet Sel Evol 47:4
Biscarini F, Marini S, Stevanato P, Broccanello C, Bellazzi R, Nazzicari N (2015) Developing a parsimonius predictor for binary traits in sugar beet (Beta vulgaris). Mol Breed 35:10
Biscarini F, Cozzi P, Casella L, Riccardi P, Vattari A, Orasen G, Perrini R, Tacconi G, Tondelli A, Biselli C, Cattivelli L, Spindel J, McCouch S, Abbruscato P, Valé G, Piffanelli P, Greco R (2016) Genome-Wide Association Study for traits related to plant and grain morphology, and root architecture in temperate rice accessions. PLoS One 11:e0155425
Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 19:2633–2635
Chen L, Song Y, Li S, Zhang L, Zou C, Yu D (2012) The role of WRKY transcription factors in plant abiotic stresses. Biochim Biophys Acta 1819:120–128
Chen L, Wang QQ, Zhou L, Ren F, Li DD, Li XB (2013) Arabidopsis CBL-interacting protein kinase (CIPK6) is involved in plant response to salt/osmotic stress and ABA. Mol Biol Rep 40:4759–4767
Cosgrove DJ (2015) Plant expansins: diversity and interactions with plant cell walls. Curr Opin Plant Biol 25:162–172
Courtois B, Audebert A, Dardou A, Roques S, Ghneim-Herrera T, Droc G, Frouin J, Rouan L, Goz E, Kilian A, Ahmadi N, Dingkuhn M (2013) Genome-wide association mapping of root traits in a japonica rice panel. PLoS One. doi:10.1371/journal.pone.0078037
Earl DA, Vonholdt BM (2011) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361
Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SEA (2011) Robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One. doi:10.1371/journal.pone.0019379
Gabriel SB, Schaffner SF, Nguyen H, Moore JM, Roy J, Blumenstiel B, Higgins J, Defelice M, Lochner A, Faggart M, Liu-Cordero SN, Rotimi C, Adeyemo A, Cooper R, Ward R, Lander ES, Daly MJ, Altshuler D (2002) The structure of haplotype blocks in the human genome. Science 296:2225–2229
He J, Zhao X, Laroche A, Lu ZX, Liu H, Li Z (2014) Genotyping-by-Sequencing (GBS), an ultimate marker-assisted selection (MAS) tool to accelerate plant breeding. Front Plant Sci 5:484
Henry R (2014) Genomics strategies for germplasm characterization and the development of climate resilient crops. Front Plant Sci 5:68. doi:10.3389/fpls.2014.00068
Jain M, Aashima N, Arora R, Agarwal P, Ray S, Sharma P, Kapoor S, Tyagi AK, Khurana P (2007) F-box proteins in rice. Genome-wide analysis, classification, temporal and spatial gene expression during panicle and seed development, and regulation by light and abiotic stress. Plant Physiol 143:1467–1483
Jiang SY, Ma Z, Ramachandran R (2010) Evolutionary history and stress regulation of the lectin superfamily in higher plants. BMC Evol Biol 10:79. doi:10.1186/1471-2148-10-79
Jing Y, Lin R (2015) The VQ motif-containing protein family of plant-specific transcriptional regulators. Plant Physiol 169:371–378
Jisha V, Dampanaboina L, Vadassery J, Mithöfer A, Kappara S, Ramanan R (2015) Overexpression of an AP2/ERF type transcription factor OsEREBP1 confers biotic and abiotic stress tolerance in rice. PLoS One. doi:10.1371/journal.pone.0127831
Kang Y, Sakiroglu M, Krom N, Stanton-Geddes J, Wang M, Lee YC, Young ND, Udvardi M (2015) Genome-wide association of drought-related and biomass traits with HapMap SNPs in Medicago truncatula. Plant, Cell Environ 38:1997–2011. doi:10.1111/pce.12520
Kawahara Y, Bastide MDL, Hamilton JP, Kanamori H, Mccombie WR, Ouyang S, Schwartz DC, Tanaka T, Wu J, Zhou S, Childs KL, Davidson RM, Lin H, Quesada-Ocampo L, Vaillancourt B, Sakai H, Lee SS, Kim J, Numa H, Itoh T, Buell CR, Matsumoto T (2013) Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data. Rice 6:1–10
Kilian J, Whitehead K, Horak J, Wanke D, Weinl S, Batistic O, D’Angelo C, Bauer EB, Kudla J, Harter K (2007) The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J 50:347–363
Kole C, Muthamilarasan M, Henry R, Edwards D et al (2015) Application of genomics-assisted breeding for generation of climate resilient crops: progress and prospects. Front Plant Sci 6:563. doi:10.3389/fpls.2015.00563
Kumar K, Rao KP, Sharma P, Sinha AK (2008) Differential regulation of rice mitogen activated protein kinase kinase (MKK) by abiotic stress. Plant Physiol Biochem 46:891–897
Kumar A, Dixit S, Ram T, Yadaw RB, Mishra KK, Mandal NP (2014) Breeding high-yielding drought-tolerant rice: genetic variations and conventional and molecular approaches. J Exp Bot 65:6265–6278
Licausi F, Ohme-Takagi M, Perata P (2013) Apetala2/ethylene responsive factor (AP2/ERF) transcription factors: mediators of stress responses and developmental programs. New Phytol 199:639–649
Ma N, Wang Y, Qiu S, Kang Z, Che S, Wang G, Huang J (2013) Overexpression of OsEXPA8, a root-specific gene, improves rice growth and root system architecture by facilitating cell extension. PLoS One. doi:10.1371/journal.pone.0075997
Morillo SA, Tax RE (2006) Functional analysis of receptor-like kinases in monocots and dicots. Curr Opinion Plant Biol 9:460–469
Perez-Clemente RM, Vives V, Zandalinas SI, Lopez-Climent MF, Munoz V, Gomez-Cadenas A (2013) Biotechnological approaches to study plant responses to stress. Biomed Res Int 2013:654120. doi:10.1155/2013/654120
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Rebolledo MC, Dingkuhn M, Courtois B, Gibon Y, Clément-Vidal A, Cruz DF, Duitama J, Lorieux M, Luquet D (2015) Phenotypic and genetic dissection of component traits for early vigour in rice using plant growth modelling, sugar content analyses and association mapping. J Exp Bot 66:5555–5566
Scheet P, Stephens M (2006) A fast and flexible statistical model for large-scale population genotype data: applications to inferring missing genotypes and haplotypic phase. Am J Hum Genet 78:629–644
Shamsudin NAZ, Swamy BPM, Ratnam W, Sta Cruz MT, Raman A, Kumar A (2016) Marker assisted pyramiding of drought yield QTLs into a popular Malaysian rice cultivar, MR219. BMC Genet 17:30. doi:10.1186/s12863-016-0334-0
Shen H, Liu C, Zhang Y, Meng X, Zhou X, Chu C, Wang X (2012) OsWRKY30 is activated by MAP kinases to confer drought tolerance in rice. Plant Mol Biol 80:241–253
Sinha AK, Jaggi M, Raghuram B, Tuteja N (2011) Mitogen-activated protein kinase signaling in plants under abiotic stress. Plant Signal Behav 6:196–203
Skirycz A, Claeys H, Bodt S, Oikawa A, Shinoda S, Andriankaja M, Maleux K, Eloy NB, Coppens F, Yoo SD, Saito K, Inzé D (2011) Pause-and-stop: the effects of osmotic stress on cell proliferation during early leaf development in Arabidopsis and a role for ethylene signaling in cell cycle arrest. Plant Cell 23:1876–1888
Srivastava S, Vishwakarma RK, Arafat YA, Gupta SK, Khan BM (2015) Abiotic stress induces change in Cinnamoyl CoA Reductase (CCR) protein abundance and lignin deposition in developing seedlings of Leucaena leucocephala. Physiol Mol Biol Plants 21:197–205
The R Foundation for statistical computing (2016) R: a language and environment for statistical computing. R Core Team, Vienna. http://www.R-project.org. Accessed 30 March 2016
Todaka D, Shinozaki K, Yamaguchi-Shinozaki K (2015) Recent advances in the dissection of drought-stress regulatory networks and strategies for development of drought-tolerant transgenic rice plants. Front Plant Sci 6:84. doi:10.3389/fpls.2015.00084
Vikram P, Swamy MB, Dixit S, Ahmed UH, Sta Cruz MT, Singh AK, Kumar A (2011) qDTY1.1, a major QTL for rice grain yield under reproductive-stage drought stress with a consistent effect in multiple elite genetic backgrounds. BMC Genet 12:89. doi:10.1186/1471-2156-12-89
Vikram P, Swamy BP, Dixit S, Singh R, Singh BP, Miro B, Kohli A, Henry A, Singh NK, Kumar A (2015) Drought susceptibility of modern rice varieties: an effect of linkage of drought tolerance with undesirable traits. Sci Rep 5:14799. doi:10.1038/srep14799
Wang Y, Ma N, Qiu S, Zou H, Zang G, Kang Z, Wang G, Huang J (2014) Regulation of the alpha-expansin gene OsEXPA8 expression affects root system architecture in transgenic rice plants. Mol Breed 34:47–57
Wankhede DP, Misra M, Singh P, Sinha AK (2013) Rice mitogen activated protein kinase kinase and mitogen activated protein kinase interaction network revealed by in silico docking and yeast two-hybrid approaches. PLoS One 8:e65011. doi:10.1371/journal.pone.0065011
Wu Y, Wei W, Pang X, Wang X, Zhang H, Dong B, Xing Y, Li X, Wang M (2014) Comparative transcriptome profiling of adesert evergreen shrub, Ammopiptanthus mongolicus, in response to drought and cold stresses. BMC Genom 15:671. doi:10.1186/1471-2164-15-671
Yang J, Lee SH, Goddard ME, Visscher PM (2011) GCTA: a tool for genome-wide complex trait analysis. Am J Hum Genet 88:76–82
Zhang Z, Ersoz E, Lai CQ, Todhunter RJ, Tiwari HK, Gore MA, Bradbury PJ, Yu J, Arnett DK, Ordovas JM, Buckler ES (2010) Mixed linear model approach adapted for genome-wide association studies. Nat Genet 42:355–360
Zhang Z, Ober U, Erbe M, Zhang H, Gao N, He J, Li J, Simianer H (2014) Improving the accuracy of whole genome prediction for complex traits using the results of genome wide association studies. PLoS One 9:e93017
Acknowledgments
National Council for Scientific and Technological Development (CNPq) for the grants to CB and RPV; the Coordination for the Improvement of Higher Education Personnel/Ministry of Education (CAPES/MEC) for the grants to GFP; and the Brazilian Agricultural Research Corporation (EMBRAPA) for financial support for this research.
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10709_2016_9932_MOESM1_ESM.docx
List of rice accessions drought-evaluated in field (Porangatu, F) and greenhouse (Sitis platform, S) experiments (DOCX 31 kb)
10709_2016_9932_MOESM2_ESM.docx
Putative annotation of rice transcripts identified by SNP markers related to yield in drought and control experiments (DOCX 22 kb)
10709_2016_9932_MOESM3_ESM.docx
Arabidopsis, Brachypodium, maize and sorghum transcripts homologous of rice transcripts identified by SNP markers related to yield in drought and control experiments (DOCX 21 kb)
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Pantalião, G.F., Narciso, M., Guimarães, C. et al. Genome wide association study (GWAS) for grain yield in rice cultivated under water deficit. Genetica 144, 651–664 (2016). https://doi.org/10.1007/s10709-016-9932-z
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DOI: https://doi.org/10.1007/s10709-016-9932-z