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Global identification of quantitative trait loci and candidate genes for cold stress and chilling acclimation in rice through GWAS and RNA-seq

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Abstract

Main conclusion

Associated analysis of GWAS with RNA-seq had detected candidate genes responsible for cold stress and chilling acclimation in rice. Haplotypes of two candidate genes and geographic distribution were analyzed.

Abstract

To explore new candidate genes and genetic resources for cold tolerance improvement in rice, genome-wide association study (GWAS) mapping experiments with 351 rice core germplasms was performed for three traits (survival rate, shoot length and chlorophyll content) under three temperature conditions (normal temperature, cold stress and chilling acclimation), yielding a total of 134 QTLs, of which 54, 59 and 21 QTLs were responsible for normal temperature, cold stress and chilling acclimation conditions, respectively. Integrated analysis of significant SNPs in 134 QTLs further identified 116 QTLs for three temperature treatments, 53, 43 and 18 QTLs responsible for normal temperature, cold stress and chilling acclimation, respectively, and 2 QTLs were responsible for both cold stress and chilling acclimation. Matching differentially expressed genes from RNA-seq to 43 and 18 QTLs for cold stress and chilling acclimation, we identified 69 and 44 trait-associated candidate genes, respectively, to be classified into six and five groups, particularly involved in metabolisms, reactive oxygen species scavenging and hormone signaling. Interestingly, two candidate genes LOC_Os01g04814, encoding a vacuolar protein sorting-associating protein 4B, and LOC_Os01g48440, encoding glycosyltransferase family 43 protein, showed the highest expression levels under chilling acclimation. Haplotype analysis revealed that both genes had a distinctive differentiation with subpopulation. Haplotypes of both genes with more japonica accessions have higher latitude distribution and higher chilling tolerance than the chilling sensitive indica accessions. These findings reveal the new insight into the molecular mechanism and candidate genes for cold stress and chilling acclimation in rice.

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Data availability

Additional data are provided as supporting information in the online version of this article.

Abbreviations

GWAS:

Genome-wide association study

QTL:

Quantitative trait loci

QTN:

Quantitative trait nucleotide

ROS:

Reactive oxygen species

SNP:

Single-nucleotide polymorphism

References

  • Agalou A, Purwantomo S, Overnäs E, Johannesson H, Zhu X, Estiati A, de Kam RJ, Engström P, Slamet-Loedin IH, Zhu Z, Wang M, Xiong L, Meijer AH, Ouwerkerk PBF (2008) A genome-wide survey of HD-Zip genes in rice and analysis of drought-responsive family members. Plant Mol Biol 66(1–2):87–103

    CAS  PubMed  Google Scholar 

  • Agrawal GK, Jwa NS, Shibato J, Han O, Iwahashi H, Rakwal R (2003) Diverse environmental cues transiently regulate OsOPR1 of the “octadecanoid pathway” revealing its importance in rice defense/stress and development. Biochem Biophys Res Commun 310(4):1073–1082. https://doi.org/10.1016/j.bbrc.2003.09.123

    Article  CAS  PubMed  Google Scholar 

  • Alexandrov N, Tai S, Wang W, Mansueto L, Palis K, Fuentes RR, Ulat VJ, Chebotarov D, Zhang G, Li Z, Mauleon R, Hamilton RS, McNally KL (2015) SNP-seek database of SNPs derived from 3000 rice genomes. Nucleic Acids Res 43:1023–1027

    Google Scholar 

  • Andaya VC, Tai TH (2006) Fine mapping of the qCTS12 locus, a major QTL for seedling cold tolerance in rice. Theor Appl Genet 113(3):467–475

    CAS  PubMed  Google Scholar 

  • Andaya VC, Tai TH (2007) Fine mapping of the qCTS4 locus associated with seedling cold tolerance in rice (Oryza sativa L.). Mol Breed 20(4):349–358

    CAS  Google Scholar 

  • Anders S, Pyl PT, Huber W (2015) HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics 31(2):166–169

    CAS  PubMed  Google Scholar 

  • Aya K, Hobo T, Sato-Izawa K, Ueguchi-Tanaka M, Kitano H, Matsuoka M (2014) A novel AP2-type transcription factor, SMALL ORGAN SIZE1, controls organ size downstream of an auxin signaling pathway. Plant Cell Physiol 55(5):897–912. https://doi.org/10.1093/pcp/pcu023

    Article  CAS  PubMed  Google Scholar 

  • Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13(8):1194–1202

    CAS  PubMed  Google Scholar 

  • Chiniquy D, Varanasi P, Oh T, Harholt J, Katnelson J, Singh S, Auer M, Simmons B, Adams PD, Scheller HV (2013) Three novel rice genes closely related to the Arabidopsis IRX9, IRX9L, and IRX14 genes and their roles in xylan biosynthesis. Front Plant Sci 4:83. https://doi.org/10.3389/fpls.2013.00083

    Article  PubMed  PubMed Central  Google Scholar 

  • Chinnusamy V, Zhu J, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12(10):444–451

    CAS  PubMed  Google Scholar 

  • Cooper JW, Hu Y, Beyyoudh L, YildizDasgan H, Kunert K, Beveridge CA, Foyer CH (2018) Strigolactones positively regulate chilling tolerance in pea and in Arabidopsis. Plant Cell Environ 41(6):1298–1310

    CAS  PubMed  Google Scholar 

  • Ding Y, Li H, Zhang X, Xie Q, Gong Z, Yang S (2015) OST1 kinase modulates freezing tolerance by enhancing ICE1 stability in Arabidopsis. Dev Cell 32(3):278–289

    CAS  PubMed  Google Scholar 

  • Ding Y, Shi Y, Yang S (2019) Advances and challenges in uncovering cold tolerance regulatory mechanisms in plants. New Phytol 222(4):1690–1704

    PubMed  Google Scholar 

  • Garg R, Jhanwar S, Tyagi AK, Jain M (2010) Genome-wide survey and expression analysis suggest diverse roles of glutaredoxin gene family members during development and response to various stimuli in rice. DNA Res 17(6):353–367. https://doi.org/10.1093/dnares/dsq023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gaur A, Jindal Y, Singh V, Tiwari R, Kumar D, Kaushik D, Singh J, Narwal S, Jaiswal S, Iquebal MA, Angadi UB, Singh G, Rai A, Singh GP, Sheoran S (2022) GWAS to identify novel QTNs for WSCs accumulation in wheat peduncle under different water regimes. Front Plant Sci 13:825687

    PubMed  PubMed Central  Google Scholar 

  • Guan YJ, Jin HU, Wang XJ, Shao CX (2009) Seed priming with chitosan improves maize germination and seedling growth in relation to physiological changes under low temperature stress. J Zhejiang Univ Sci B 10(6):427–433

    CAS  PubMed  PubMed Central  Google Scholar 

  • Han S, Min MK, Lee SY, Lim CW, Bhatnagar N, Lee Y, Shin D, Chung KY, Lee SC, Kim BG, Lee S (2017) Modulation of ABA signaling by altering VxGPhiL motif of PP2Cs in Oryza sativa. Mol Plant 10(9):1190–1205. https://doi.org/10.1016/j.molp.2017.08.003

    Article  CAS  PubMed  Google Scholar 

  • Hossain MA, Cho JI, Han M, Ahn CH, Jeon JS, An G, Park PB (2010) The ABRE-binding bZIP transcription factor OsABF2 is a positive regulator of abiotic stress and ABA signaling in rice. J Plant Physiol 167(17):1512–1520

    CAS  PubMed  Google Scholar 

  • Huang X, Wei X, Sang T, Zhao Q, Feng Q, Zhao Y, Li C, Zhu C, Lu T, Zhang Z, Li M, Fan D, Guo Y, Wang A, Wang L, Deng L, Li W, Lu Y, Weng Q, Liu K, Huang T, Zhou T, Jing Y, Li W, Lin Z, Buckler ES, Qian Q, Zhang Q-F, Li J, Han B (2010) Genome-wide association studies of 14 agronomic traits in rice landraces. Nature Gen 42(11):961–967

    CAS  Google Scholar 

  • Huang R, Zhao J, Liu J, Wang Y, Han S, Zhao H (2017) Genome-wide analysis and expression profiles of NTMC2 family genes in Oryza sativa. Gene 637:130–137. https://doi.org/10.1016/j.gene.2017.09.046

    Article  CAS  PubMed  Google Scholar 

  • Huo C, Zhang B, Wang H, Wang F, Liu M, Gao Y, Zhang W, Deng Z, Sun D, Tang W (2016) Comparative study of early cold-regulated proteins by two-dimensional difference gel electrophoresis reveals a key role for phospholipase D alpha1 in mediating cold acclimation signaling pathway in rice. Mol Cell Proteomics 15(4):1397–1411

    CAS  PubMed  PubMed Central  Google Scholar 

  • Imai R, Ali A, Pramanik HR, Nakaminami K, Sentoku N, Kato H (2004) A distinctive class of spermidine synthase is involved in chilling response in rice. J Plant Physiol 161(7):883–886. https://doi.org/10.1016/j.jplph.2003.11.002

    Article  CAS  PubMed  Google Scholar 

  • Jiang S, Yang C, Xu Q, Wang L, Yang X, Song X, Wang J, Zhang X, Li B, Li H, Li Z, Li W (2020) Genetic dissection of germinability under low temperature by building a resequencing linkage map in japonica rice. Int J Mol Sci 21(4):1284

    CAS  PubMed Central  Google Scholar 

  • Kim JY, Kim WY, Kwak KJ, Oh SH, Han YS, Kang H (2010) Zinc finger-containing glycine-rich RNA-binding protein in Oryza sativa has an RNA chaperone activity under cold stress conditions. Plant Cell Environ 33(5):759–768. https://doi.org/10.1111/j.1365-3040.2009.02101.x

    Article  CAS  PubMed  Google Scholar 

  • Kim SI, Andaya VC, Tai TH (2011) Cold sensitivity in rice (Oryza sativa L.) is strongly correlated with a naturally occurring 199V mutation in the multifunctional glutathione transferase isoenzyme GSTZ2. Biochem J 435:373–380. https://doi.org/10.1042/Bj20101610

    Article  CAS  PubMed  Google Scholar 

  • Kim SM, Suh JP, Lee CK, Lee JH, Kim YG, Jena KK (2014) QTL mapping and development of candidate gene-derived DNA markers associated with seedling cold tolerance in rice (Oryza sativa L.). Mol Gen Genom 289(3):333–343

    CAS  Google Scholar 

  • Kim SY, Kim JS, Cho W, Jun KM, Du X, Kim KD, Kim Y-K, Lee G-S (2021) A cold-shock protein from the South Pole-dwelling soil bacterium Arthrobacter sp. confers cold tolerance to rice. Genes 12(10):1589

    CAS  PubMed  PubMed Central  Google Scholar 

  • Koseki M, Kitazawa N, Yonebayashi S, Maehara Y, Wang ZX, Minobe Y (2010) Identification and fine mapping of a major quantitative trait locus originating from wild rice, controlling cold tolerance at the seedling stage. Mol Gen Genom 284(1):45–54

    CAS  Google Scholar 

  • Le Gall H, Philippe F, Domon JM, Gillet F, Pelloux J, Rayon C (2015) Cell wall metabolism in response to abiotic stress. Plants (Basel) 4(1):112–166. https://doi.org/10.3390/plants4010112

    Article  Google Scholar 

  • Li J, Zhang Z, Chong K, Xu Y (2022) Chilling tolerance in rice: past and present. J Plant Physiol 268:153576

    CAS  PubMed  Google Scholar 

  • Lin D, Gong X, Jiang Q, Zheng K, Zhou H, Xu J, Teng S, Dong Y (2015) The rice ALS3 encoding a novel pentatricopeptide repeat protein is required for chloroplast development and seedling growth. Rice 8:17

    PubMed  PubMed Central  Google Scholar 

  • Liu JP, Sun XJ, Xu FY, Zhang YJ, Zhang Q, Miao R, Zhang JH, Liang JS, Xu WF (2018) Suppression of OsMDHAR4 enhances heat tolerance by mediating H2O2-induced stomatal closure in rice plants. Rice 11:38. https://doi.org/10.1186/s12284-018-0230-5

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Wang H, Jiang Z, Wang W, Xu R, Wang Q, Zhang Z, Li A, Liang Y, Ou S, Liu X, Cao S, Tong H, Wang Y, Zhou F, Liao H, Hu B, Chu C (2021) Genomic basis of geographical adaptation to soil nitrogen in rice. Nature 590(7847):600–605

    CAS  PubMed  Google Scholar 

  • Lou QJ, Guo HF, Li J, Han SC, Khan NU, Gu YS, Zhao WT, Zhang ZY, Zhang HL, Li ZC, Li JJ (2022) Cold-adaptive evolution at the reproductive stage in Geng/japonica subspecies reveals the role of OsMAPK3 and OsLEA9. Plant J 111(4):1032–1051. https://doi.org/10.1111/tpj.15870

    Article  CAS  PubMed  Google Scholar 

  • Lv Y, Guo Z, Li X, Ye H, Li X, Xiong L (2016) New insights into the genetic basis of natural chilling and cold shock tolerance in rice by genome-wide association analysis. Plant Cell Environ 39(3):556–570

    CAS  PubMed  Google Scholar 

  • Ma JF, Yamaji N, Mitani N, Xu XY, Su YH, McGrath SP, Zhao FJ (2008) Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proc Natl Acad Sci USA 105(29):9931–9935. https://doi.org/10.1073/pnas.0802361105

    Article  PubMed  PubMed Central  Google Scholar 

  • Ma Y, Dai X, Xu Y, Luo W, Zheng X, Zeng D, Pan Y, Lin X, Liu H, Zhang D, Xiao J, Guo X, Xu S, Niu Y, Jin J, Zhang H, Xu X, Li L, Wang W, Qian Q, Ge S, Chong K (2015) COLD1 confers chilling tolerance in rice. Cell 160(6):1209–1221

    CAS  PubMed  Google Scholar 

  • Man L, Xiang D, Wang L, Zhang W, Wang X, Qi G (2017) Stress-responsive gene RsICE1 from Raphanus sativus increases cold tolerance in rice. Protoplasma 254(2):945–956

    CAS  PubMed  Google Scholar 

  • Mansueto L, Fuentes RR, Borja FN, Detras J, Abriol-Santos JM, Chebotarov D, Sanciangco M, Palis K, Copetti D, Poliakov A, Dubchak I, Solovyev V, Wing RA, Hamilton RS, Mauleon R, McNally KL, Alexandrov N (2017) Rice SNP-seek database update: new SNPs, indels, and queries. Nucleic Acids Res 45(1):1075–1081

    Google Scholar 

  • Mao D, Chen C (2012) Colinearity and similar expression pattern of rice DREB1s reveal their functional conservation in the cold-responsive pathway. PLoS ONE 7(10):e47275

    CAS  PubMed  PubMed Central  Google Scholar 

  • Meng XB, Zhao WS, Lin RM, Wang M, Peng YL (2006) Molecular cloning and characterization of a rice blast-inducible RING-H2 type zinc finger gene. DNA Seq 17(1):41–48. https://doi.org/10.1080/10425170500476509

    Article  CAS  PubMed  Google Scholar 

  • Mittal D, Chakrabarti S, Sarkar A, Singh A, Grover A (2009) Heat shock factor gene family in rice: genomic organization and transcript expression profiling in response to high temperature, low temperature and oxidative stresses. Plant Physiol Biochem 47(9):785–795. https://doi.org/10.1016/j.plaphy.2009.05.003

    Article  CAS  PubMed  Google Scholar 

  • Mott R, Yuan W, Kaisaki P, Gan X, Cleak J, Edwards A, Baud A, Flint J (2014) The architecture of parent-of-origin effects in mice. Cell 156(1–2):332–342

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pan Y, Zhang H, Zhang D, Li J, Xiong H, Yu J, Li J, Rashid MAR, Li G, Ma X, Cao G, Han L, Li Z (2015) Genetic analysis of cold tolerance at the germination and booting stages in rice by association mapping. PLoS ONE 10(3):e0120590

    PubMed  PubMed Central  Google Scholar 

  • Phan H, Schläppi M (2021) Low temperature antioxidant activity QTL associate with genomic regions involved in physiological cold stress tolerance responses in rice (Oryza sativa L.). Genes 12(11):1700. https://doi.org/10.3390/genes12111700

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MAR, Bender D, Maller J, Sklar P, de Bakker PIW, Daly MJ, Sham PC (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Human Gen 81(3):559–575

    CAS  Google Scholar 

  • Qi YH, Kawano N, Yamauchi Y, Ling JQ, Li DB, Tanaka K (2005) Identification and cloning of a submergence-induced gene OsGGT (glycogenin glucosyltransferase) from rice (Oryza sativa L.) by suppression subtractive hybridization. Planta 221(3):437–445. https://doi.org/10.1007/s00425-004-1453-9

    Article  CAS  PubMed  Google Scholar 

  • Reyna NS, Yang Y (2006) Molecular analysis of the rice MAP kinase gene family in relation to Magnaporthe grisea infection. Mol Plant-Microbe Interact 19(5):530–540

    CAS  PubMed  Google Scholar 

  • Rosado A, Schapire AL, Bressan RA, Harfouche AL, Hasegawa PM, Valpuesta V, Botella MA (2006) The Arabidopsis tetratricopeptide repeat-containing protein TTL1 is required for osmotic stress responses and abscisic acid sensitivity. Plant Physiol 142(3):1113–1126. https://doi.org/10.1104/pp.106.085191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schläppi MR, Jackson AK, Eizenga GC, Wang A, Chu C, Shi Y, Shimoyama N, Boykin DL (2017) Assessment of five chilling tolerance traits and GWAS mapping in rice using the USDA Mini-Core collection. Front Plant Sci 8:957

    PubMed  PubMed Central  Google Scholar 

  • Shakiba E, Edwards JD, Jodari F, Duke SE, Baldo AM, Korniliev P, McCouch SR, Eizenga GC (2017) Genetic architecture of cold tolerance in rice (Oryza sativa) determined through high resolution genome-wide analysis. PLoS ONE 12(3):e0172133

    PubMed  PubMed Central  Google Scholar 

  • Sharma S, Kaur C, Singla-Pareek SL, Sopory SK (2016) OsSRO1a interacts with RNA binding domain-containing protein (OsRBD1) and functions in abiotic stress tolerance in yeast. Front Plant Sci 7:62. https://doi.org/10.3389/fpls.2016.00062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shimoyama N, Johnson M, Beaumont A, Schläppi M (2020) Multiple cold tolerance trait phenotyping reveals shared quantitative trait loci in Oryza sativa. Rice 13(1):57

    PubMed  PubMed Central  Google Scholar 

  • Shin JH, Kim SR, An G (2009) Rice aldehyde dehydrogenase7 is needed for seed maturation and viability. Plant Physiol 149(2):905–915

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shinkawa R, Morishita A, Amikura K, Machida R, Murakawa H, Kuchitsu K, Ishikawa M (2013) Abscisic acid induced freezing tolerance in chilling-sensitive suspension cultures and seedlings of rice. BMC Res Notes 6:351

    PubMed  PubMed Central  Google Scholar 

  • Sipaseuth BJ, Fukai S, Tc F, Senthonghae M, Sengkeo PS, Linquist B, Chanphengsay M (2007) Opportunities to increasing dry season rice productivity in low temperature affected areas. Field Crops Res 102(2):87–97

    Google Scholar 

  • Song J, Li J, Sun J, Hu T, Wu A, Liu S, Wang W, Ma D, Zhao M (2018) Genome-wide association mapping for cold tolerance in a core collection of rice (Oryza sativa L.) landraces by using high-density single nucleotide polymorphism markers from specific-locus amplified fragment sequencing. Front Plant Sci 9:875

    PubMed  PubMed Central  Google Scholar 

  • Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25(9):1105–1111

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang K, Li M, Hakonarson H (2010) ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res 38(16):164

    CAS  Google Scholar 

  • Wang F, Yang Y, Wang Z, Zhou J, Fan B, Chen Z (2015) A critical role of Lyst-Interacting Protein5, a positive regulator of multivesicular body biogenesis, in plant responses to heat and salt stresses. Plant Physiol 169(1):497–511. https://doi.org/10.1104/pp.15.00518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang D, Liu J, Li C, Kang H, Wang Y, Tan X, Liu M, Deng Y, Wang Z, Liu Y, Zhang D, Xiao Y, Wang G-L (2016) Genome-wide association mapping of cold tolerance genes at the seedling stage in rice. Rice 9(1):61

    PubMed  PubMed Central  Google Scholar 

  • Wang W, Mauleon R, Hu Z, Chebotarov D, Tai S, Wu Z, Li M, Zheng T et al (2018) Genomic variation in 3,010 diverse accessions of Asian cultivated rice. Nature 557(7703):43–49

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wei X, Zhou H, Xie D, Li J, Yang M, Chang T, Wang D, Hu L, Xie G, Wang J, Wang L (2021) Genome-wide association study in rice revealed a novel gene in determining plant height and stem development, by encoding a WRKY transcription factor. Int J Mol Sci 22(15):8192. https://doi.org/10.3390/ijms22158192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie G, Kato H, Sasaki K, Imai R (2009) A cold-induced thioredoxin h of rice, OsTrx23, negatively regulates kinase activities of OsMPK3 and OsMPK6 in vitro. FEBS Lett 583(17):2734–2738

    CAS  PubMed  Google Scholar 

  • Yang C, Li D, Mao D, Liu X, Ji C, Li X, Zhao X, Cheng Z, Chen C, Zhu L (2013) Overexpression of microRNA319 impacts leaf morphogenesis and leads to enhanced cold tolerance in rice (Oryza sativa L.). Plant Cell Environ 36(12):2207–2218

    CAS  PubMed  Google Scholar 

  • Yang LM, Wang JG, Han ZH, Lei L, Liu HL, Zheng HL, Xin W, Zou DT (2021) Combining QTL-seq and linkage mapping to fine map a candidate gene in qCTS6 for cold tolerance at the seedling stage in rice. BMC Plant Biol 21(1):278

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yin L, Zhang H, Tang Z, Xu J, Yin D, Zhang Z, Yuan X, Zhu M, Zhao S, Li X, Liu X (2021) rMVP: A memory-efficient, visualization-enhanced, and parallel-accelerated tool for genome-wide association study. Gen Proteomics Bioinform 19(4):619–628

    Google Scholar 

  • Zhai YJ, Wen ZH, Han Y, Zhuo WQ, Wang F, Xi C, Liu J, Gao P, Zhao HP, Wang YDA, Wang YJ, Han SC (2020) Heterogeneous expression of plasma-membrane-localised OsOSCA1.4 complements osmotic sensing based on hyperosmolality and salt stress in Arabidopsis osca1 mutant. Cell Calcium 91:102261. https://doi.org/10.1016/j.ceca.2020.102261

    Article  CAS  PubMed  Google Scholar 

  • Zhan XQ, Shen QW, Wang XM, Hong YY (2017) The sulfoquinovosyltransferase-like enzyme SQD2.2 is involved in flavonoid glycosylation, regulating sugar metabolism and seed setting in rice. Sci Rep 7:4685. https://doi.org/10.1038/s41598-017-04002-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Q, Chen Q, Wang S, Hong Y, Wang Z (2014) Rice and cold stress: methods for its evaluation and summary of cold tolerance-related quantitative trait loci. Rice 7(1):24

    PubMed  PubMed Central  Google Scholar 

  • Zhang Z, Li J, Li F, Liu H, Yang W, Chong K, Xu Y (2017) OsMAPK3 phosphorylates OsbHLH002/OsICE1 and inhibits its ubiquitination to activate OsTPP1 and enhances rice chilling tolerance. Dev Cell 43(6):731–743

    CAS  PubMed  Google Scholar 

  • Zhang C, Dong S-S, Xu J-Y, He W-M, Yang T-L (2019) PopLDdecay: a fast and effective tool for linkage disequilibrium decay analysis based on variant call format files. Bioinformatics 35(10):1786–1788

    CAS  PubMed  Google Scholar 

  • Zhang H, Wu T, Li Z, Huang K, Kim NE, Ma ZM, Kwon SW, Jiang WZ, Du XL (2021) OsGATA16, a GATA transcription factor, confers cold tolerance by repressing OsWRKY45-1 at the seedling stage in rice. Rice 14(1):42–42

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao J, Zhang S, Yang T, Zeng Z, Huang Z, Liu Q, Wang X, Leach J, Leung H, Liu B (2015) Global transcriptional profiling of a cold-tolerant rice variety under moderate cold stress reveals different cold stress response mechanisms. Physiol Plant 154(3):381–394

    CAS  PubMed  Google Scholar 

  • Zhao J, Zhang S, Dong J, Yang T, Mao X, Liu Q, Wang X, Liu B (2017) A novel functional gene associated with cold tolerance at the seedling stage in rice. Plant Biotechnol J 15(9):1141–1148

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu GH, Ye NH, Zhang JH (2009) Glucose-induced delay of seed germination in rice is mediated by the suppression of ABA catabolism rather than an enhancement of ABA biosynthesis. Plant Cell Physiol 50(3):644–651. https://doi.org/10.1093/pcp/pcp022

    Article  CAS  PubMed  Google Scholar 

  • Zhu G, Gao W, Song X, Sun F, Hou S, Liu N, Huang Y, Zhang D, Ni Z, Chen Q, Guo W (2020) Genome-wide association reveals genetic variation of lint yield components under salty field conditions in cotton (Gossypium hirsutum L.). BMC Plant Biol 20(1):23

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This study is supported by grants from the National Key Research and Development Program of China (2017YFD0300106) and funding from State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources of China (SKLCUSA-b202202).

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Author notes

  1. Ahmed Adel Khatab and Jianguo Li have contributed equally to this work.

Authors and Affiliations

  1. College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, 430070, China

    Ahmed Adel Khatab, Jianguo Li, Chuchuan Fan, Lingqiang Wang & Guosheng Xie

  2. State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, College of Agriculture, Guangxi University, Nanning, China

    Jianguo Li, Lihua Hu, Jiangyi Yang & Lingqiang Wang

  3. College of Life Science and Technology, Guangxi University, Nanning, 530004, China

    Lihua Hu & Jiangyi Yang

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  1. Ahmed Adel Khatab
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  2. Jianguo Li
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  3. Lihua Hu
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  4. Jiangyi Yang
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Correspondence to Lingqiang Wang or Guosheng Xie.

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Supplementary file1 (XLS 1384 KB)

Fig. S1

QQ-plot of different traits after normal temperature, cold stress and chilling accumulation. a QQ-plot of survival rate after normal temperature, cold stress and chilling acclimation, and relative survival rate after cold stress and chilling acclimation. b QQ-plot of shoot length after normal temperature, cold stress and chilling acclimation, and relative shoot length after cold stress and chilling acclimation.c QQ-plot of chlorophyll content after normal temperature, cold stress and chilling acclimation, and relative chlorophyll content after cold stress and chilling acclimation. Supplementary file2 (TIF 279 KB)

Fig. S2

GWAS of the relative survival rate, relative shoot length and relative chlorophyll contents after cold stress and chilling accumulation. a Manhattan plot of relative survival rate after cold stress (RSRCS). b Manhattan plot of relative survival rate after chilling acclimation (RSRCA). c Manhattan plot of relative shoot length after cold stress (RSLCS). d Manhattan plot of relative shoot length after chilling acclimation (RSLCA). e Manhattan plot of relative chlorophyll content after cold stress (RCHCS). f Manhattan plot of relative chlorophyll content after chilling acclimation (RCHCA). The arrow was linked to the significant SNPs and the high-confidence SNP were annotated. Supplementary file3 (TIF 454 KB)

Fig. S3

Comparison of up-regulated and down-regulated genes detected by RNA-seq after cold stress and chilling acclimation. a Venn diagram of up/down-regulated genes under 6℃, 12℃ for 6 h, CA (chilling acclimation exposure). b Venn diagram of up/down-regulated genes under 6℃, 12℃, CA (chilling acclimation exposure) for 24 h. Supplementary file4 (TIF 156 KB)

Fig. S4

Haplotype analysis and geographic distribution of the LOC_Os01g04814 and their geographic distribution. a Linkage disequilibrium (LD) block of SNPs in LOC_Os01g04814. b Haplotype analysis of the genes LOC_Os01g04814. Colors of points represented the different subpopulations. c Haplotype distribution analysis of the genes LOC_Os01g04814. Colors of column represented the different haplotypes. * and ** represent the significant differences at the levels of P = 0.05 and P = 0.01, respectively. Supplementary file5 (TIF 349 KB)

Fig. S5

Haplotype analysis and geographic distribution of the LOC_Os01g48440 and their geographic distribution. a Linkage disequilibrium (LD) block of SNPs in LOC_Os01g48440. b Haplotype analysis of the genes LOC_Os01g48440. Colors of points represented the different subpopulations. c Haplotype distribution analysis of the genes LOC_Os01g48840. Colors of column represented the different haplotypes. * and ** represent the significant differences at the levels of P = 0.05 and P = 0.01, respectively. Supplementary file6 (TIF 322 KB)

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Khatab, A.A., Li, J., Hu, L. et al. Global identification of quantitative trait loci and candidate genes for cold stress and chilling acclimation in rice through GWAS and RNA-seq. Planta 256, 82 (2022). https://doi.org/10.1007/s00425-022-03995-z

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