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Dissecting the genetics of cold tolerance in a multiparental maize population

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Abstract

Key message

We identify the largest amount of QTLs for cold tolerance in maize; mainly associated with photosynthetic efficiency, which opens new possibilities for genomic selection for cold tolerance in maize.

Abstract

Breeding for cold tolerance in maize is an important objective in temperate areas. The objective was to carry out a highly efficient study of quantitative trait loci (QTLs) for cold tolerance in maize. We evaluated 406 recombinant inbred lines from a multi-parent advanced generation intercross (MAGIC) population in a growth chamber under cold and control conditions, and in the field at early and normal sowing. We recorded cold tolerance-related traits, including the number of days from sowing to emergence, chlorophyll content and maximum quantum efficiency of photosystem II (Fv/Fm). Association mapping was based on genotyping with near one million single nucleotide polymorphism (SNP) markers. We found 858 SNPs significantly associated with all traits, most of them under cold conditions and early sowing. Most QTLs were associated with chlorophyll and Fv/Fm. Many candidate genes coincided between the current research and previous reports. These results suggest that (1) the MAGIC population is an efficient tool for identifying QTLs for cold tolerance; (2) most QTLs for cold tolerance were associated with Fv/Fm; (3) most of these QTLs were located in specific genomic regions, particularly bin 10.04; (4) the current study allows genetically improving cold tolerance with genome-wide selection.

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Abbreviations

BLUE:

Best linear unbiased estimators

GWAS:

Genome-wide association analyses

IBM:

Population of RIL released from the maize inbred lines B73 and Mo17

MAGIC:

Multi-parent advanced generations intercross population

QTLs:

Quantitative trait loci

SNP:

Single nucleotide polymorphism

SPAD:

Soil–plant analyses development is the relative amount of chlorophyll estimated by measuring the absorbance of the leaf in two wavelength regions

Fv/Fm :

Maximum quantum efficiency of photosystem II

References

  • Agarwal M, Hao Y, Kapoor A, Dong CH, Fujii H, Zheng X, Zhu JK (2006) A R2R3 type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance. J Biol Chem 281:37636–37645

    Article  CAS  PubMed  Google Scholar 

  • Allam M, Revilla P, Djemel A, Tracy WF, Ordás B (2016) Identification of QTLs involved in cold tolerance in sweet × field corn. Euphytica 208:353–365

    Article  CAS  Google Scholar 

  • Bandillo N, Raghavan C, Muyco PA, Sevilla MA, Lobina IT, Dilla-Ermita CJ, Tung CW, McCouch S, Thomson M, Mauleon R, Singh RK, Gregorio G, Redoña E, Leung H (2013) Multi-parent advanced generation inter-cross (MAGIC) populations in rice: progress and potential for genetics research and breeding. Rice 6(1):11

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 23:2633–2635

    Article  CAS  PubMed  Google Scholar 

  • Chen DH, Ronald PC (1999) A rapid DNA minipreparation method suitable for AFLP and other PCR applications. Plant Mol Biol Rep 17:53–57

    Article  CAS  Google Scholar 

  • Chinnusamy V, Ohta M, Kanrar S, Lee BH, Hong X, Agarwal M, Zhu JK (2003) ICE1: A regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Develop 17:1043–1054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dell’Acqua M, Gatti DM, Pea G, Cattonaro F, Coppens F, Magris G, Hlaing AL, Aung HH, Nelissen H, Baute J, Frascaroli E, Churchill GA, Inzé D, Morgante M, Pè ME (2015) Genetic properties of the MAGIC maize population: a new platform for high definition QTL mapping in Zea mays. Genome Biol 16:167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong CH, Agarwal M, Zhang Y, Xie Q, Zhu JK (2006) The negative regulator of plant cold responses, HOS1, is a RING E3 ligase that mediates the ubiquitination and degradation of ICE1. Proc Nat Acad Sci USA 103:8281–8286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Du H, Zhu J, Su H, Huang M, Wang H, Ding S, Zhang B, Luo A, Wei S, Tian X, Xu Y (2017) Bulked segregant RNA-seq reveals differential expression and SNPs of candidate genes associated with waterlogging tolerance in maize. Front Plant Sci 8:1022

    Article  PubMed  PubMed Central  Google Scholar 

  • Flint-Garcia SA, Thornsberry JM, Buckler SE IV (2003) Structure of linkage disequilibrium in plants. Ann Rev Plant Biol 54:357–374

    Article  CAS  Google Scholar 

  • Flint-Garcia SA, Thuillet AC, Yu J, Pressoir G, Romero SM, Mitchell SE, Doebley J, Kresovich S, Goodman MM, Buckler ES (2005) Maize association population: a high-resolution platform for quantitative trait locus dissection. Plant J 44:1054–1064

    Article  CAS  PubMed  Google Scholar 

  • Fracheboud Y, Ribaut JM, Messmer R, Stamp P (2002) Identification of quantitative trait loci for cold-tolerance of photosynthesis in maize (Zea mays L.). J Exp Bot 376:1967–1977

    Article  CAS  Google Scholar 

  • Fracheboud Y, Jompuk C, Ribaut JM, Stamp P, Leipner J (2004) Genetic analysis of cold-tolerance of photosynthesis in maize. Plant Mol Biol 56:241–253

    Article  CAS  PubMed  Google Scholar 

  • Frascaroli E, Revilla P (2018) Genomics of cold tolerance in maize. In: Bennetzen J, Flint-Garcia S, Hirsch C, Tuberosa R (eds) The maize genome. Springer Nature, Switzerland, pp 287–303

    Chapter  Google Scholar 

  • Guan H, Ali F, Pan Q (2017) Dissection of recombination attributes for multiple maize populations using a common SNP assay. Front Plant Sci 8:2063

    Article  PubMed  PubMed Central  Google Scholar 

  • Guerra-Peraza O, Leipner J, Reimer R, Thuy Nguyen H, Stamp P, Fracheboud Y (2011) Temperature at night affects the genetic control of acclimation to cold in maize seedlings. Maydica 56:366–377

    Google Scholar 

  • Holland JB, Nyquist WE, Cervantes-Martínez CT (2005) Estimated an interpreting heritability for plant breeding. In: Janick J (ed.) Plant Breeding Reviews. Hoboken, New Jersey, USA: Jonh Wiley & Sons press, Inc pp. 9–112

  • Hu S, Lübberstedt T, Zhao G, Lee M (2016) QTL mapping of low-temperature germination ability in the maize IBM Syn4 RIL population. PLoS ONE 11(3):e0152795

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu G, Li Z, Lu Y, Li C, Gong S, Yan S, Li G, Wang M, Ren H, Guan H, Zhang Z, Qin D, Chai M, Yu J, Li Y, Yang D, Wang T, Zhang Z (2017) Genome-wide association study identifed multiple genetic loci on chilling resistance during germination in maize. Sci Rep 7:10840

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang BE, George AW, Forrest KL, Kilian A, Hayden MJ, Morell MK, Cavanagh CR (2012) A multiparent advanced generation inter-cross population for genetic analysis in wheat. Plant Biotech J 10:826–839

    Article  CAS  Google Scholar 

  • Huang J, Zhang J, Li W, Hu W, Duan L, Feng Y, Que F, Yue B (2013) Genome wide association analysis of ten chilling tolerance indices at the germination and seedling stages in maize. J Integr Plant Biol 55:735–744

    Article  CAS  PubMed  Google Scholar 

  • Hund A, Fracheboud Y, Soldati A, Frascaroli E, Salvi S, Stamp P (2004) QTL controlling root and shoot traits of maize seedlings under cold stress. Theor Appl Genet 109:618–629

    Article  CAS  PubMed  Google Scholar 

  • Jiménez-Galindo JC, Malvar RA, Butrón A, Santiago R, Samayoa LF and Ordás B (2019) Mapping of resistance to Mediterranean corn borer in a MAGIC population of maize. BMC Plant Biol (accepted)

  • Jompuk C, Fracheboud Y, Stamp P, Leipner J (2005) Mapping of quantitative trait loci associated with chilling tolerance in maize (Zea mays L.) seedlings grown under field conditions. J Exp Bot 56:1153–1163

    Article  CAS  PubMed  Google Scholar 

  • Kim SH, Kim HS, Bahk S, An J, Yoo Y, Kim JY, Chung WS (2017) Phosphorylation of the transcriptional repressor MYB15 by mitogen activated protein kinase6 is required for freezing tolerance in Arabidopsis. Nuc Acids Res 45:6613–6627

    Article  CAS  Google Scholar 

  • Kover PX, Valdar W, Trakalo J, Scarcelli N, Ehrenreich IM, Purugganan MD, Durrant C, Mott R (2009) A multiparent advanced generation inter-cross to fine-map quantitative traits in Arabidopsis thaliana. PLoS Genet 5(7):e1000551

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kucharik CJ (2006) A multidecadal trend of earlier corn planting in the central USA. Agro J 98:1544–1550

    Article  Google Scholar 

  • Kurepin LV, Dahal KP, Savitch LV, Singh J, Bode R, Ivanov AG, Hurry V, Hüner NPA (2013) Role of CBFs as integrators of chloroplast redox, phytochrome and plant hormone signaling during cold acclimation. Int J Mol Sci 14:12729–12763

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leipner J, Stamp P (2009) Chilling stress in maize seedlings. In: Bennetzen JL, Hake SC (eds) Handbook of Maize: Its Biology. Springer Press, Inc., New York, pp 291–310

    Chapter  Google Scholar 

  • Li J, Ji L (2005) Adjusting multiple testing in multilocus analyses using the eigenvalues of a correlation matrix. Heredity 95:221–227

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Li C, Bradbury P, Liu X, Lu F, Romay CM, Glaubitz JC, Wu X, Peng B, Shi Y, Song Y, Zhang D, Buckler ES, Zhang Z, Li Y, Wang T (2016) Identification of genetic variants associated with maize flowering time using an extremely large multigenetic background population. Plant J 86:391–402

    Article  CAS  PubMed  Google Scholar 

  • Li H, Ding Y, Shi Y, Zhang X, Zhang S, Gong Z, Yang S (2017) MPK3- and MPK6-mediated ICE1 phosphorylation negatively regulates ICE1 stability and freezing tolerance in Arabidopsis. Develop Cell 43:630–642

    Article  CAS  Google Scholar 

  • Li P, Cao W, Fang H, Xu S, Yin S, Zhang Y, Lin D, Wang J, Chen Y, Xu C, Yang Z (2017a) Transcriptomic profiling of the maize (Zea mays L.) leaf response to abiotic stresses at the seedling stage. Front Plant Sci 8: 290

  • Li X, Wang G, Fu J, Li L, Jia G, Ren L, Lubberstedt T, Wang G, Wang J, Gu R (2018) QTL mapping in three connected populations reveals a set of consensus genomic regions for low temperature germination ability in Zea mays L. Front Plant Sci 9:65

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Zhou J (2018) MAPping kinase regulation of ICE1 in freezing tolerance. Trends Plant Sci 23:91–93

    Article  CAS  PubMed  Google Scholar 

  • McMullen MD, Kresovich S, Villeda HS, Bradbury P, Li H, Sun Q, Flint-Garcia S, Thornsberry J, Acharya C, Bottoms C, Brown P, Browne C, Eller M, Guill K, Harjes C, Kroon D, Lepak N, Mitchell SE, Peterson B, Pressoir G, Romero S, Oropeza Rosas M, Salvo S, Yates H, Hanson M, Jones E, Smith S, Glaubitz JC, Goodman M, Ware D, Holland JB, Buckler ES (2009) Genetic properties of the maize nested association mapping population. Science 325:737–740

    Article  CAS  PubMed  Google Scholar 

  • Olukolu B, Wang G, Vontimitta V, Venkata BP, Marla S, Ji J, Gachomo E, Chu K, Negeri A, Benson J, Nelson R, Bradbury P, Nielsen D, Holland JB, Balint-Kurti P, Johal G (2014) A genome-wide association study of the maize hypersensitive defense response identifies genes that cluster in related pathways. PLoS Genet 10:e1004562

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pan Q, Li L, Yang X, Tong H, Xu S, Li Z, Li W, Muehlbauer GJ, Li J, Yan J (2016) Genome-wide recombination dynamics are associated with phenotypic variation in maize. New Phytol 210:1083–1094

    Article  CAS  PubMed  Google Scholar 

  • Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Op Plant Biol 14:290–295

    Article  CAS  Google Scholar 

  • Qin F, Shinozaki K, Yamaguchi-Shinozaki K (2011) Achievements and challenges in understanding plant abiotic stress responses and tolerance. Plant Cell Physiol 52:1569–1582

    Article  CAS  PubMed  Google Scholar 

  • Rebetzke GJ, Verbyla AP, Verbyla KL, Morell MK, Cavanagh CR (2014) Use of a large multiparent wheat mapping population in genomic dissection of coleoptile and seedling growth. Plant Biotech J 12:219–230

    Article  CAS  Google Scholar 

  • Revilla P, Butrón A, Cartea ME, Malvar RA, Ordás A (2005) Breeding for cold tolerance. In: Ashraf M, Harris PJC (eds) Abiotic Stresses. Plant resistance through breeding and molecular approaches. The Haworth Press Inc, New York, pp 301–398

    Google Scholar 

  • Revilla P, Rodríguez VM, Ordás A, Rincent R, Charcosset A, Giauffret C, Melchinger AE, Schön CC, Bauer E, Altmann T, Brunel D, Moreno-González J, Campo L, Ouzunova M, Laborde J, Álvarez Á, Ruíz de Galarreta JI, Malvar RA (2014) Cold tolerance in two large maize inbred panels adapted to European climates. Crop Sci 54:1981–1991

    Article  Google Scholar 

  • Revilla P, Rodríguez VM, Ordás A, Rincent R, Charcosset A, Giauffret C, Melchinger AE, Schön CC, Bauer E, Altmann T, Brunel D, Moreno-González J, Campo L, Ouzunova M, Álvarez Á, Ruíz de Galarreta JI, Laborde J, Malvar RA (2016) Association mapping for cold tolerance in two large maize inbred panels. BMC Plant Biol 16:127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodríguez VM, Butrón A, Malvar RA, Ordás A, Revilla P (2008) QTLs for cold tolerance in the maize IBM population. Int J Plant Sci 169:551–556

    Article  Google Scholar 

  • Rodríguez VM, Velasco P, Garrido JL, Revilla P, Ordás A, Butrón A (2013) Genetic regulation of cold-induced albinism in the maize inbred line A661. J Exp Bot 64:3657–3667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodríguez VM, Butrón A, Rady MOA, Soengas P, Revilla P (2014) Identification of QTLs involved in the response to cold stress in maize (Zea mays L.). Mol Breed 33:363–371

    Article  CAS  Google Scholar 

  • Sen TZ, Harper LC, Schaeffer ML, Andorf CM, Seigfried TE, Campbell DA, Lawrence CJ (2010) Choosing a genome browser for a model organism database: surveying the maize community. Database 2010: baq007 http: //database. oxfordjournals.org/content/2010/baq007.abstract

  • Shi Y, Li G, Tian Z, Wang Z, Wang X, Zhu Y, Chen Y, Guo S, Qi J, Zhang X, Ku L (2016) Genetic dissection of seed vigour traits in maize (Zea mays L.) under low-temperature conditions. J Genet 95:1017–1022

    Article  PubMed  Google Scholar 

  • Strigens A, Grieder C, Haussmann BIG, Melchinger AE (2012) Genetic variation among inbred lines and testcrosses of maize for early growth parameters and their relationship to final dry matter yield. Crop Sci 52:1084–1092

    Article  Google Scholar 

  • Strigens A, Freitag NM, Gilbert X, Grieder C, Riedelsheimer C, Schrag TA, Messmer R, Melchinger AE (2013) Association mapping for chilling tolerance in elite flint and dent maize inbred lines evaluated in growth chamber and field experiments. Plant Cell Environ 36:1871–1887

    Article  CAS  PubMed  Google Scholar 

  • Tacke E, Korfhage C, Michel D, Maddaloni M, Motto M, Lanzini S, Salami S, Döring HP (1995) Transposon tagging of the maize Glossy2 locus with the transposable element En/Spm. Plant J 8:907–917

    Article  CAS  PubMed  Google Scholar 

  • Xiao Y, Tong H, Yang X, Xu S, Pan Q, Qiao F, Raihan MS, Luo Y, Liu H, Zhang X, Yang N, Wang X, Deng M, Jin M, Zhao L, Luo X, Zhou Y, Li X, Liu J, Zhan W, Liu N, Wang H, Chen G, Cai Y, Xu G, Wang W, Zheng D, Yan J (2016) Genome-wide dissection of the maize ear genetic architecture using multiple populations. New Phytol 210:1095–1106

    Article  CAS  PubMed  Google Scholar 

  • Xiao Y, Liu H, Wu L, Warburton M, Yan J (2017) Genome-wide association studies in maize: praise and stargaze. Mol Plant 10:359–374

    Article  CAS  PubMed  Google Scholar 

  • Xue D, Zhang X, Lu X, Chen G, Chen ZH (2017) Molecular and evolutionary mechanisms of cuticular wax for plant drought tolerance. Front Plant Sci 8:621

    Article  PubMed  PubMed Central  Google Scholar 

  • Yadav SK (2010) Cold stress tolerance mechanisms in plants. A review. Agron Sustain Develop 30:515–527

    Article  CAS  Google Scholar 

  • Yan J, Wu Y, Li W, Qin X, Wang Y, Yue B (2017) Genetic mapping with testcrossing associations and F2:3 populations reveals the importance of heterosis in chilling tolerance at maize seedling stage. Sci Rep 7:3232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang T, Shad Ali G, Yang L, Du L, Reddy AS, Poovaiah BW (2010) Calcium/calmodulin-regulated receptor-like kinase CRLK1 interacts with MEKK1 in plants. Plant Signal Behav 5:991–994

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu J, Pressoir G, Briggs WH, Vroh Bi I, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB, Kresovich S, Buckler ES (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nature Genet 38:203–208

    Article  CAS  PubMed  Google Scholar 

  • Yu X, Jiang L, Wu R, Meng X, Zhang A, Li N, Xia Q, Qi X, Pang J, Xu ZY, Liu B (2016) The core subunit of a chromatin-remodeling complex, ZmCHB101, plays essential roles in maize growth and development. Sci Rep 6:38504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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. Nature Genet 44:355–360

    Article  CAS  Google Scholar 

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Acknowledgements

This research was supported by the Spanish Plan for Research and Development (AGL2016-77628-R) and funded in part by the European Regional Development Fund (FEDER). The genotypic data were provided by the Biotechnological Institute of the Cornell University USA). Q Yi acknowledges a grant from the China Scholarship Council (CSC).

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Authors and Affiliations

  1. Misión Biológica de Galicia (CSIC), Apartado 28, 36080, Pontevedra, Spain

    Q. Yi, R. A. Malvar, L. Álvarez-Iglesias, B. Ordás & Pedro Revilla

  2. College of Agronomy, Sichuan Agricultural University, Chengdu, 611130, China

    Q. Yi

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  1. Q. Yi
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  2. R. A. Malvar
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  3. L. Álvarez-Iglesias
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  4. B. Ordás
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  5. Pedro Revilla
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Contributions

BO and PR have designed the experiments. LAI and PR have conducted the experiments. QY and RAM have made the statistical analyses. QY has written the text. PR has edited and submitted the final manuscript.

Corresponding author

Correspondence to Pedro Revilla.

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Communicated by Albrecht E. Melchinger.

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Supplementary file1 (XLSX 12 kb)

Supplementary file2 (XLSX 12 kb)

Supplementary file3 (XLSX 90 kb)

Supplementary file4 (XLSX 513 kb)

Supplementary Figure S1. Scheme for the development of the MAGIC population (Jiménez-Galindo et al. 2019) (JPG 413 kb)

122_2019_3482_MOESM6_ESM.jpg

Supplementary Figure S2. Max, Min, and Average Temperature for each day from the 24th April to the 30th June in 2016 at Pontevedra in Spain. The X- and Y- axes indicate the date and temperature (ºC) from the 24th April to the 30th June in 2016, respectively. Note: temperature data are available on the website “https://www.worldweatheronline.com/lang/es/pontevedra-weather-history/galicia/es.aspx” (JPG 358 kb)

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Supplementary Figure S3. Distribution of BLUEs for four seedling traits in a MAGIC maize population and its parents in a growth chamber under cold and control conditions, as well as in the field at early and normal sowing dates. Chamber-Cold, Chamber-Control, Field-Early Sowing, and Field-Normal Sowing indicate the chamber under cold condition, the chamber under control condition, the field at early sowing date, and the field at normal sowing date, respectively. The distribution of eight founders is indicated with different colors and arrows (JPG 1583 kb)

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Supplementary Figure S4. Manhattan plot from a mixed linear model for early seedling traits in a MAGIC maize population. SNPs above the orange horizontal line surpassed the threshold of p = 2.42×10-5. The different colors indicate the 10 different chromosomes of maize. A and B indicate Manhattan plots for days to emergence in a chamber under cold and control conditions, respectively. C and D indicate Manhattan plots for germination rate in the field at early and normal sowing dates, respectively. E, F, G, and H indicate Manhattan plots for early vigor in a chamber under cold and control conditions, as well as in the field at early and normal sowing dates, respectively. I, J, K, and L indicate Manhattan plots for chlorophyll in a chamber under cold and control conditions, as well as in the field at early and normal sowing dates, respectively. M and N indicate Manhattan plots for maximum quantum efficiency of photosystem II (Fv/Fm) in a chamber under control condition and in the field at early normal sowing date, respectively. O and P indicate Manhattan plots for dry weight in a chamber under cold and control conditions, respectively (JPG 1085 kb)

Supplementary file9 (JPG 1079 kb)

Supplementary file10 (JPG 1083

kb)

Supplementary file11 (JPG 570 kb)

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Supplementary Figure S5 Graphical results of eight significant gene ontology (GO) terms for 134 candidate genes containing the most significant SNPs within QTLs for five early seedling traits in GO enrichment analysis (PNG 50 kb)

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Supplementary Figure S6. Principal component analysis of the SNPs in the RILs of the MAGIC population (Jiménez-Galindo et al. 2019). The parental lines were shown in the presented Figure (JPG 396 kb)

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Yi, Q., Malvar, R.A., Álvarez-Iglesias, L. et al. Dissecting the genetics of cold tolerance in a multiparental maize population. Theor Appl Genet 133, 503–516 (2020). https://doi.org/10.1007/s00122-019-03482-2

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