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Loci and alleles for submergence responses revealed by GWAS and transcriptional analysis in rice

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Abstract

The low seedling rate of rice caused by submergence in the process of rice direct seeding has always been an important factor limiting the popularization of rice direct seeding technology. Improving the tolerance of rice to submergence stress will benefit the production of rice and the promotion of direct seeding technology. In this study, we determined the submergence coleoptile length (SCL), submergence shoot length (SSL), and submergence tolerance index (STI) of 166 different cultivated rice seedlings as the phenotypes. Through the genome-wide association analysis (GWAS) of SCL, SSL, and STI, we found multiple quantitative trait locus (QTL) locations, including nine reported QTL locations. To narrow down the candidate gene numbers, we combined data from GWAS, transcriptomic analysis, gene function annotation, and reported QTL locations, and 50 candidate genes for submergence stress were obtained. Some reported genes had been firstly found to play certain roles in submergence-mediated growth response. Combining with reported RNA-seq data and expression profile data, we focused on four adjacent genes (LOC_Os11g47550, LOC_Os11g47570, LOC_Os11g47590, and LOC_Os11g47610) located in qAG11. RNA-seq and expression profile suggested the expression of these genes in sensitive and tolerant types differs hundreds of times (146~510 fold). Based on the diverse germplasms, we determined the natural haplotype of these genes. The haplotype analysis of these four genes showed a large genetic difference between indica and japonica. These results help us to better understand the molecular mechanism of natural variations in submergence tolerance among diverse germplasms and provide materials and new genes for further selection of new submergence tolerance varieties.

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References

  • Angaji SA, Septiningsih EM, Mackill D, Ismail AM (2010) QTLs associated with tolerance of flooding during germination in rice (Oryza sativa L.). Euphytica 172:159–168

    Google Scholar 

  • Bailey-Serres J, Voesenek LA (2010) Life in the balance: a signaling network controlling survival of flooding. Curr Opin Plant Biol 13:489–494

    CAS  PubMed  Google Scholar 

  • Baltazar MD, Ignacio JCI, Thomson MJ, Ismail AM, Mendioro MS, Septiningsih EM (2014) QTL mapping for tolerance of anaerobic germination from IR64 and the aus landrace Nanhi using SNP genotyping. Euphytica 197:251–260

    CAS  Google Scholar 

  • Benjamini Y, Drai D, Elmer G, Kafkafi N, Golani I (2001) Controlling the false discovery rate in behavior genetics research. Behav Brain Res 125:279–284

    CAS  PubMed  Google Scholar 

  • Bourne Y, Henrissat B (2001) Glycoside hydrolases and glycosyltransferases: families and functional modules. Curr Opin Struct Biol 11:593–600

    CAS  PubMed  Google Scholar 

  • Carbon S, Ireland A, Mungall CJ, Shu S, Marshall B, Lewis S, Hub A, Group WPW (2009) AmiGO: online access to ontology and annotation data. Bioinformatics 25:288–289

    CAS  PubMed  Google Scholar 

  • Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861

    CAS  PubMed  Google Scholar 

  • Ella ES, Setter TL (1999) Importance of seed carbohydrates in rice seedling establishment under anoxia. In: VI Symposium on Stand Establishment and ISHS Seed Symposium 504, pp 209–218

    Google Scholar 

  • Fukao T, Bailey-Serres J (2008) Submergence tolerance conferred by Sub1A is mediated by SLR1 and SLRL1 restriction of gibberellin responses in rice. Proceedings of the National Academy of Sciences 105:16814–16819

    CAS  Google Scholar 

  • Fukao T, Xu K, Ronald PC, Bailey-Serres J (2006) A variable cluster of ethylene response factor–like genes regulates metabolic and developmental acclimation responses to submergence in rice. The Plant Cell 18:2021–2034

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gibbs J, Morrell S, Valdez A, Setter T, Greenway H (2000) Regulation of alcoholic fermentation in coleoptiles of two rice cultivars differing in tolerance to anoxia. J Exp Bot 51:785–796

    CAS  PubMed  Google Scholar 

  • Hattori Y, Nagai K, Furukawa S, Song X-J, Kawano R, Sakakibara H, Wu J, Matsumoto T, Yoshimura A, Kitano H (2009) The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. Nature 460:1026–1030

    CAS  PubMed  Google Scholar 

  • Henrissat B (1997) Structural and sequence-based classification of glycoside hydrolases. Curr Opin Struct Biol:7

  • Hsu S-K, Tung C-W (2015) Genetic mapping of anaerobic germination-associated QTLs controlling coleoptile elongation in rice. Rice 8:1–12

    Google Scholar 

  • Hsu S-K, Tung C-W (2017) RNA-Seq analysis of diverse rice genotypes to identify the genes controlling coleoptile growth during submerged germination. Frontiers in plant science 8:762

    PubMed  PubMed Central  Google Scholar 

  • Huang X, Sang T, Zhao Q, Feng Q, Zhao Y, Li C, Zhu C, Lu T, Zhang Z, Li M (2010) Genome-wide association studies of 14 agronomic traits in rice landraces. Nat Genet 42:961–967

    CAS  PubMed  Google Scholar 

  • Ismail AM, Ella ES, Vergara GV, Mackill DJ (2009) Mechanisms associated with tolerance to flooding during germination and early seedling growth in rice (Oryza sativa). Ann Bot 103:197–209

    CAS  PubMed  Google Scholar 

  • Jiang L, Hou M-Y, Wang C-M, Wan J-M (2004) Quantitative trait loci and epistatic analysis of seed anoxia germinability in rice (Oryza sativa). Rice Sci 11:238–244

  • Kang HM, Sul JH, Service SK, Zaitlen NA, Kong S-Y, Freimer NB, Sabatti C, Eskin E (2010) Variance component model to account for sample structure in genome-wide association studies. Nat Genet 42:348–354

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kato-Noguchi H, Morokuma M (2007) Ethanolic fermentation and anoxia tolerance in four rice cultivars. J Plant Physiol 164:168–173

    CAS  PubMed  Google Scholar 

  • Kretzschmar T, Pelayo MAF, Trijatmiko KR, Gabunada LFM, Alam R, Jimenez R, Mendioro MS, Slamet-Loedin IH, Sreenivasulu N, Bailey-Serres J (2015) A trehalose-6-phosphate phosphatase enhances anaerobic germination tolerance in rice. Nature Plants 1:1–5

    Google Scholar 

  • Kuroha T, Nagai K, Gamuyao R, Wang DR, Furuta T, Nakamori M, Kitaoka T, Adachi K, Minami A, Mori Y (2018) Ethylene-gibberellin signaling underlies adaptation of rice to periodic flooding. Science 361:181–186

    CAS  PubMed  Google Scholar 

  • Kurusu T, Hamada J, Nokajima H, Kitagawa Y, Kiyoduka M, Takahashi A, Hanamata S, Ohno R, Hayashi T, Okada K (2010) Regulation of microbe-associated molecular pattern-induced hypersensitive cell death, phytoalexin production, and defense gene expression by calcineurin B-like protein-interacting protein kinases, OsCIPK14/15, in rice cultured cells. Plant Physiol 153:678–692

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lasanthi-Kudahettige R, Magneschi L, Loreti E, Gonzali S, Licausi F, Novi G, Beretta O, Vitulli F, Alpi A, Perata P (2007) Transcript profiling of the anoxic rice coleoptile. Plant Physiol 144:218–231

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee K-W, Chen P-W, Lu C-A, Chen S, Ho T-HD YS-M (2009) Coordinated responses to oxygen and sugar deficiency allow rice seedlings to tolerate flooding. Sci Signal 2:ra61-ra61

    Google Scholar 

  • Li J-Y, Wang J, Zeigler RS (2014) The 3,000 rice genomes project: new opportunities and challenges for future rice research. Gigascience 3:2047-2217X-3-8

    Google Scholar 

  • Lv Y, Yang M, Hu D, Yang Z, Ma S, Li X, Xiong L (2017) The OsMYB30 transcription factor suppresses cold tolerance by interacting with a JAZ protein and suppressing β-amylase expression. Plant Physiol 173(2):1475-1491

  • Magneschi L, Perata P (2009) Rice germination and seedling growth in the absence of oxygen. Ann Bot 103:181–196

    CAS  PubMed  Google Scholar 

  • Magneschi L, Kudahettige R, Alpi A, Perata P (2009) Comparative analysis of anoxic coleoptile elongation in rice varieties: relationship between coleoptile length and carbohydrate levels, fermentative metabolism and anaerobic gene expression. Plant Biol 11:561–573

    CAS  PubMed  Google Scholar 

  • Miro B, Ismail AM (2013) Tolerance of anaerobic conditions caused by flooding during germination and early growth in rice (Oryza sativa L.). Frontiers in plant science 4:269

    PubMed  PubMed Central  Google Scholar 

  • Nagai K, Hattori Y, Ashikari M (2010) Stunt or elongate? Two opposite strategies by which rice adapts to floods. J Plant Res 123:303–309

    PubMed  Google Scholar 

  • Nghi KN, Tondelli A, Valè G, Tagliani A, Marè C, Perata P, Pucciariello C (2019) Dissection of coleoptile elongation in japonica rice under submergence through integrated genome-wide association mapping and transcriptional analyses. Plant, Cell Environ 42:1832–1846

    CAS  Google Scholar 

  • Sasidharan R, Hartman S, Liu Z, Martopawiro S, Sajeev N, van Veen H, Yeung E, Voesenek LA (2018) Signal dynamics and interactions during flooding stress. Plant Physiol 176:1106–1117

    CAS  PubMed  Google Scholar 

  • Sedbrook JC, Kronebusch PJ, Borisy GG, Trewavas AJ, Masson PH (1996) Transgenic AEQUORIN reveals organ-specific cytosolic Ca2+ responses to anoxia in Arabidopsis thaliana seedlings. Plant Physiol 111:243–257

    CAS  PubMed  PubMed Central  Google Scholar 

  • Septiningsih EM, Pamplona AM, Sanchez DL, Neeraja CN, Vergara GV, Heuer S, Ismail AM, Mackill DJ (2009) Development of submergence-tolerant rice cultivars: the Sub1 locus and beyond. Ann Bot 103:151–160

    CAS  PubMed  Google Scholar 

  • Septiningsih EM, Ignacio JCI, Sendon PM, Sanchez DL, Ismail AM, Mackill DJ (2013) QTL mapping and confirmation for tolerance of anaerobic conditions during germination derived from the rice landrace Ma-Zhan Red. Theor Appl Genet 126:1357–1366

    PubMed  Google Scholar 

  • Setter TL, Ella ES (1994) Relationship between Coleoptile Elongation and Alcoholic Fermentation in Rice Exposed to Anoxia. I. Importance of Treatment Conditions and Different Tissues. Ann Bot 74(3):265-271

  • Setter T, Ella E, Valdez A (1994) Relationship between coleoptile elongation and alcoholic fermentation in rice exposed to anoxia. II Cultivar differences Ann Bot 74:273–279

    Google Scholar 

  • Singh A, Septiningsih EM, Balyan HS, Singh NK, Rai V (2017) Genetics, physiological mechanisms and breeding of flood-tolerant rice (Oryza sativa L.). Plant Cell Physiol 58:185–197

    CAS  PubMed  Google Scholar 

  • Subbaiah CC, Zhang J, Sachs MM (1994) Involvement of intracellular calcium in anaerobic gene expression and survival of maize seedlings. Plant Physiol 105:369–376

    CAS  PubMed  PubMed Central  Google Scholar 

  • Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2014) Correction: corrigendum: differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 9(10):2513–2513

    CAS  Google Scholar 

  • Wang W, Mauleon R, Hu Z, Chebotarov D, Tai S, Wu Z, Li M, Zheng T, Fuentes RR, Zhang F (2018) Genomic variation in 3,010 diverse accessions of Asian cultivated rice. Nature 557:43–49

    CAS  PubMed  PubMed Central  Google Scholar 

  • Watanabe H, Hase S, Saigusa M (2007) Effects of the combined application of ethephon and gibberellin on growth of rice (Oryza sativa L.) seedlings. Plant production science 10:468–472

    CAS  Google Scholar 

  • Xie W, Wang G, Yuan M, Yao W, Lyu K, Zhao H, Yang M, Li P, Zhang X, Yuan J (2015) Breeding signatures of rice improvement revealed by a genomic variation map from a large germplasm collection. Proceedings of the National Academy of Sciences 112:E5411–E5419

    CAS  Google Scholar 

  • Yamauchi M, Biswas J (1997) Rice cultivar difference in seedling establishment in flooded soil. Plant Soil 189:145–153

    Google Scholar 

  • Yan H, Xu W, Xie J, Gao Y, Wu L, Sun L, Feng L, Chen X, Zhang T, Dai C, Li T, Lin X, Zhang Z, Wang X, Li F, Zhu X, Li J, Li Z, Chen C, Ma M, Zhang H, He Z (2019) Author correction: variation of a major facilitator superfamily gene contributes to differential cadmium accumulation between rice subspecies. Nat Commun 10(1):3301

    PubMed  PubMed Central  Google Scholar 

  • Yang J, Sun K, Li D, Luo L, Liu Y, Huang M, Yang G, Liu H, Wang H, Chen Z (2019) Identification of stable QTLs and candidate genes involved in anaerobic germination tolerance in rice via high-density genetic mapping and RNA-Seq BMC. Genomics 20:355

    PubMed  Google Scholar 

  • Zhang M, Lu Q, Wu W, Niu X, Wang C, Feng Y, Xu Q, Wang S, Yuan X, Yu H (2017) Association mapping reveals novel genetic loci contributing to flooding tolerance during germination in indica rice. Frontiers in plant science 8:678

    PubMed  PubMed Central  Google Scholar 

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Funding

This work was supported by grants from the Agricultural Science and Technology Innovation Program, Shenzhen Science and Technology Program (Nos. KQTD2016113010482651, 2017050414212249, JCYJ20170303154506881, and JCYJ20170303154319837), National Natural Science Foundation of China (31700524), Natural Science Foundation of Shandong Province of China (ZR2016CB48), and Guangdong Basic and Applied Basic Research Foundation (2019A1515110557).

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  1. Hongsheng Gao, Chao Zhang and Huiying He contributed equally to this work.

Authors and Affiliations

  1. College of Agriculture, Ludong University, Yantai, 264025, China

    Hongsheng Gao, Chao Zhang & Chunyan Yu

  2. Shenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China

    Hongsheng Gao, Chao Zhang, Huiying He, Tianjiao Liu, Bin Zhang, Hai Lin, Xiaoxia Li, Zhaoran Wei, Qiaoling Yuan, Quan Wang & Lianguang Shang

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  1. Hongsheng Gao
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Correspondence to Chunyan Yu or Lianguang Shang.

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Gao, H., Zhang, C., He, H. et al. Loci and alleles for submergence responses revealed by GWAS and transcriptional analysis in rice. Mol Breeding 40, 75 (2020). https://doi.org/10.1007/s11032-020-01160-6

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