Log in

QTL map** for flowering time in a maize-teosinte population under well-watered and water-stressed conditions

  • Published:
Molecular Breeding Aims and scope Submit manuscript

Abstract

Maize grain yield can be greatly reduced when flowering time coincides with drought conditions, which delays silking and consequently increases the anthesis-silking interval. Although the genetic basis of delayed flowering time under water-stressed conditions has been elucidated in maize-maize populations, little is known in this regard about maize-teosinte populations. Here, 16 quantitative trait loci (QTL) for three flowering-time traits, namely days to anthesis, days to silk, and the anthesis-silking interval, were identified in a maize-teosinte introgression population under well-watered and water-stressed conditions; these QTL explained 3.98–32.61% of phenotypic variations. Six of these QTL were considered to be sensitive to drought stress, and the effect of any individual QTL was small, indicating the complex genetic nature of drought resistance in maize. To resolve which genes underlie the six QTL, 11 candidate genes were identified via colocalization analysis of known associations with flowering-time-related drought traits. Among the 11 candidate genes, five were found to be differentially expressed in response to drought stress or under selection during maize domestication, and thus represented the most likely candidates underlying the drought-sensitive QTL. The results lay a foundation for further studies of the genetic mechanisms of drought resistance and provide valuable information for improving drought resistance during maize breeding.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Brazil)

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

All data generated or analyzed during this study are included in this article and its supplementary information files.

References

  • Almeida GD, Makumbi D, Magorokosho C, Nair S, Borem A, Ribaut JM, Banziger M, Prasanna BM, Crossa J, Babu R (2013) QTL map** in three tropical maize populations reveals a set of constitutive and adaptive genomic regions for drought tolerance. Theor Appl Genet 126(3):583–600

    Article  CAS  PubMed  Google Scholar 

  • Bruce WB, Edmeades GO, Barker TC (2002) Molecular and physiological approaches to maize improvement for drought tolerance. J Exp Bot 53(366):13–25

    Article  CAS  PubMed  Google Scholar 

  • Bukowski R, Guo X, Lu Y, Zou C, He B, Rong Z, Wang B, Xu D, Yang B, **e C (2018) Construction of the third-generation Zea mays haplotype map. Gigascience 7(4):gic134

    Article  Google Scholar 

  • Chen YH, Gols R, Benrey B (2015) Crop domestication and its impact on naturally selected trophic interactions. Annu Rev Entomol 60:35–58

    Article  CAS  PubMed  Google Scholar 

  • Chen W, Chen L, Zhang X, Yang N, Guo J, Wang M, Ji S, Zhao X, Yin P, Cai L, Xu J, Zhang L, Han Y, **ao Y, Xu G, Wang Y, Wang S, Wu S, Yang F, Jackson D, Cheng J, Chen S, Sun C, Qin F, Tian F, Fernie AR, Li J, Yan J, Yang X (2022) Convergent selection of a WD40 protein that enhances grain yield in maize and rice. Science 375(6587):eabg7985

    Article  CAS  PubMed  Google Scholar 

  • Chugh V, Kaur N, Gupta AK (2011) Evaluation of oxidative stress tolerance in maize (Zea mays L.) seedlings in response to drought. Indian J Biochem Bio 48:47–53

    CAS  Google Scholar 

  • Farfan IDB, De La Fuente GN, Murray SC, Isakeit T, Huang P, Warburton M, Williams P, Windham GL, Kolomiets M (2015) Genome wide association study for drought, aflatoxin resistance, and important agronomic traits of maize hybrids in the sub-tropics. PLoS ONE 10(2):e117737

    Article  Google Scholar 

  • Feng X, Jia L, Cai Y, Guan H, Zheng D, Zhang W, **ong H, Zhou H, Wen Y, Hu Y (2022) ABA-inducible DEEPER ROOTING 1 improves adaptation of maize to water deficiency. Plant Biotechnol J 20(11):2077–2088

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao H, Cui J, Liu S, Wang S, Lian Y, Bai Y, Zhu T, Wu H, Wang Y, Yang S (2022) Natural variations of ZmSRO1d modulate the trade-off between drought resistance and yield by affecting ZmRBOHC-mediated stomatal ROS production in maize. Mol Plant 15(10):1558–1574

    Article  CAS  PubMed  Google Scholar 

  • Guo L, Wang XH, Zhao M, Huang C, Li C, Li D, Yang CJ, York AM, Xue W, Xu GH, Liang YM, Chen QY, Doebley JF, Tian F (2018) Stepwise cis-regulatory changes in ZCN8 contribute to maize flowering-time adaptation. Curr Biol 28(18):3005–3015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo J, Li CH, Zhang XQ, Li YX, Zhang DF, Shi YS, Song YC, Li Y, Yang DG, Wang TY (2020) Transcriptome and GWAS analyses reveal candidate gene for seminal root length of maize seedlings under drought stress. Plant Sci 292:110380

    Article  CAS  PubMed  Google Scholar 

  • Gupta A, Rico-Medina A, Caño-Delgado AI (2020) The physiology of plant responses to drought. Science 368(6488):266–269

    Article  CAS  PubMed  Google Scholar 

  • Hao Z, Liu X, Li X, **e C, Xu Y (2009) Identification of quantitative trait loci for drought tolerance at seedling stage by screening a large number of introgression lines in maize. Plant Breeding 128(4):337–341

    Article  Google Scholar 

  • Hufford MB, Bilinski P, Pyhäjärvi T, Ross-Ibarra J (2012) Teosinte as a model system for population and ecological genomics. Trends Genet 28(12):606–615

    Article  CAS  PubMed  Google Scholar 

  • Jia H, Li M, Li W, Liu L, Jian Y, Yang Z, Shen X, Ning Q, Du Y, Zhao R (2020) A serine/threonine protein kinase encoding gene KERNEL NUMBER PER ROW6 regulates maize grain yield. Nat Commun 11(1):1–11

    Article  Google Scholar 

  • Kang J, Hwang J, Lee M, Kim Y, Assmann SM, Martinoia E, Lee Y (2010) PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid. Proc Natl Acad Sci 107(5):2355–2360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khan SU, Zheng Y, Chachar Z, Zhang X, Zhou G, Zong N, Leng P, Zhao J (2022) Dissection of maize drought tolerance at the flowering stage using genome-wide association studies. Genes 13(4):564

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim K, Song K, Park J, Kim J, Lee B (2021) RNA-Seq analysis of gene expression changes related to delay of flowering time under drought stress in tropical maize. Appl Sci 11(9):4273

    Article  CAS  Google Scholar 

  • Kuromori T, Miyaji T, Yabuuchi H, Shimizu H, Sugimoto E, Kamiya A, Moriyama Y, Shinozaki K (2010) ABC transporter AtABCG25 is involved in abscisic acid transport and responses. Proc Natl Acad Sci 107(5):2361–2366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuromori T, Sugimoto E, Shinozaki K (2011) Arabidopsis mutants of AtABCG22, an ABC transporter gene, increase water transpiration and drought susceptibility. Plant J 67(5):885–894

    Article  CAS  PubMed  Google Scholar 

  • Lander ES, Botstein D (1989) Map** mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121(1):185–199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li XH, Liu XD, Li M, Zhang SH (2003) Identification of quantitative trait loci for anthesis-silking interval and yield components under drought stress in maize. Acta Botanica Sinica 45(7):852–857

    Google Scholar 

  • Li C, Sun B, Li YX, Liu C, Wu X, Zhang DF, Shi YS, Song YC, Buckler ES, Zhang ZW, Yu WT, Li Y (2016) Numerous genetic loci identified for drought tolerance in the maize nested association map** populations. BMC Genomics 17(1):1–11

    Article  Google Scholar 

  • Li P, Zhang YY, Yin SY, Zhu PF, Pan T, Xu Y, Wang JY, Hao D, Fang HM, Xu CW, Yang ZF (2018) QTL-By-Environment interaction in the response of maize root and shoot traits to different water regimes. Front Plant Sci 9:229

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu S, Qin F (2021) Genetic dissection of maize drought tolerance for trait improvement. Mol Breeding 41(2):1–13

    Article  Google Scholar 

  • Liu Y, Subhash C, Yan JB, Song CP, Zhao JR, Li JS (2011) Maize leaf temperature responses to drought: thermal imaging and quantitative trait loci (QTL) map**. Environ Exp Bot 71(2):158–165

    Article  Google Scholar 

  • Liu SX, Wang XL, Wang HW, **n HB, Yang XH, Yan JB, Li JS, Tran LSP, Shinozaki K, Yamaguchi-Shinozaki K, Qin F (2013a) Genome-Wide Analysis of ZmDREB genes and their association with natural variation in drought tolerance at seedling stage of Zea mays L. PloS Genet 9(9):e1003790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu X, Zhai S, Zhao Y, Sun B, Liu C, Yang A, Zhang J (2013b) Overexpression of the phosphatidylinositol synthase gene (ZmPIS) conferring drought stress tolerance by altering membrane lipid composition and increasing ABA synthesis in maize. Plant, Cell Environ 36(5):1037–1055

    Article  CAS  PubMed  Google Scholar 

  • Liu Z, Cook J, Melia Hancock S, Guill K, Bottoms C, Garcia A, Ott O, Nelson R, Recker J, BalintKurti P (2016) Expanding maize genetic resources with predomestication alleles: maize–teosinte introgression populations. Plant Genome 9(1):e2015–e2017

    Article  Google Scholar 

  • Liu B, Zhang B, Yang Z, Liu Y, Yang S, Shi Y, Jiang C, Qin F (2021) Manipulating ZmEXPA4 expression ameliorates the drought-induced prolonged anthesis and silking interval in maize. Plant Cell 33(6):2058–2071

    Article  PubMed  PubMed Central  Google Scholar 

  • Lu Y, Zhang S, Shah T, ** is a powerful approach to detecting quantitative trait loci underlying drought tolerance in maize. Proc Natl Acad Sci USA 107(45):19585–19590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma H, Liu C, Li Z, Ran Q, **e G, Wang B, Fang S, Chu J, Zhang J (2018) ZmbZIP4 contributes to stress resistance in maize by regulating ABA synthesis and root development. Plant Physiol 178(2):753–770

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mao H, Wang H, Liu S, Li Z, Yang X, Yan J, Li J, Tran LP, Qin F (2015) A transposable element in a NAC gene is associated with drought tolerance in maize seedlings. Nat Commun 6(1):1–13

    Article  CAS  Google Scholar 

  • Matiu M, Ankerst DP, Menzel A (2017) Interactions between temperature and drought in global and regional crop yield variability during 1961–2014. PLoS ONE 12(5):e178339

    Article  Google Scholar 

  • Matsuda S, Takano S, Sato M, Furukawa K, Nagasawa H, Yoshikawa S, Kasuga J, Tokuji Y, Yazaki K, Nakazono M (2016) Rice stomatal closure requires guard cell plasma membrane ATP-binding cassette transporter RCN1/OsABCG5. Mol Plant 9(3):417–427

    Article  CAS  PubMed  Google Scholar 

  • Meng X, Muszynski MG, Danilevskaya ON (2011) The FT-like ZCN8 gene functions as a floral activator and is involved in photoperiod sensitivity in maize. Plant Cell 23(3):942–960

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Monneveux P, Sanchez C, Tiessen A (2008) Future progress in drought tolerance in maize needs new secondary traits and cross combinations. J Agric Sci 146(3):287–300

    Article  Google Scholar 

  • Nelson DE, Repetti PP, Adams TR, Creelman RA, Wu J, Warner DC, Anstrom DC, Bensen RJ, Castiglioni PP, Donnarummo MG (2007) Plant nuclear factor Y (NF-Y) B subunits confer drought tolerance and lead to improved corn yields on water-limited acres. Proc Natl Acad Sci 104(42):16450–16455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ngugi K, Cheserek J, Muchira C, Chemining’Wa G (2013) Anthesis to silking interval usefulness in develo** drought tolerant maize. J Renew Agric 1(5):84–90

    Google Scholar 

  • Osuman AS, Badu-Apraku B, Karikari B, Ifie BE, Tongoona P, Danquah EY (2022) Genome-wide association study reveals genetic architecture and candidate genes for yield and related traits under terminal drought, combined heat and drought in tropical maize germplasm. Genes 13(2):349

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pan QC, Li L, Yang XH, Tong H, Xu ST, Li ZG, Li WY, Muehlbauer GJ, Li JS, Yan JB (2016) Genome-wide recombination dynamics are associated with phenotypic variation in maize. New Phytol 210(3):1083–1094

    Article  CAS  PubMed  Google Scholar 

  • Ren Z, Wang X, Huahu BU, **ao J, Zhang N, Yang H (2019) Research progress in drought resistance breeding of maize. J Shanxi Agric Sci 47(7):1291–1294

    Google Scholar 

  • Ribaut JM, Hoisington DA, Deutsch JA, Jiang C, Gonzalez-de-Leon D (1996) Identification of quantitative trait loci under drought conditions in tropical maize. 1. Flowering parameters and the anthesis-silking interval. Theor Appl Genet 92(7):905–914

    Article  CAS  PubMed  Google Scholar 

  • Ruta N, Liedgens M, Fracheboud Y, Stamp P, Hund A (2010) QTLs for the elongation of axile and lateral roots of maize in response to low water potential. Theor Appl Genet 120(3):621–631

    Article  CAS  PubMed  Google Scholar 

  • Sadessa K, Beyene Y, Ifie BE, Suresh LM, Olsen MS, Ogugo V, Wegary D, Tongoona P, Danquah E, Offei SK, Prasanna BM, Gowda M (2022) Identification of genomic regions associated with agronomic and disease resistance traits in a large set of multiple DH populations. Genes 13(2):351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sánchez González JDJ, Ruiz Corral JA, García GM, Ojeda GR, Larios LDLC, Holland JB, Medrano RM, García Romero GE (2018) Ecogeography of teosinte. PLoS ONE 13(2):e192676

    Article  Google Scholar 

  • Semagn K, Beyene Y, Warburton ML, Tarekegne A, Prasanna BM (2013) Meta-analyses of QTL for grain yield and anthesis silking interval in 18 maize populations evaluated under water-stressed and well-watered environments. BMC Genomics 14(1):1–16

    Article  Google Scholar 

  • Setter TL, Yan J, Warburton M, Ribaut JM, Xu Y, Sawkins M, Buckler ES, Zhang Z, Gore MA (2011) Genetic association map** identifies single nucleotide polymorphisms in genes that affect abscisic acid levels in maize floral tissues during drought. J Exp Bot 62(2):701–716

    Article  CAS  PubMed  Google Scholar 

  • Silva LC, Wang S, Zeng ZB (2012) Composite interval map** and multiple interval map**: procedures and guidelines for using Windows QTL Cartographer. Methods Mol Biol 871:75–119

    Article  CAS  PubMed  Google Scholar 

  • Sun XP, **ang YL, Dou NN, Zhang H, Pei SR, Franco AV, Menon M, Monier B, Ferebee T, Liu T, Liu SY, Gao YC, Wang JB, Terzaghi WL, Yan JB, Hearne S, Li L, Li F, Dai MQ (2023) The role of transposon inverted repeats in balancing drought tolerance and yield-related traits in maize. Nat Biotechnol 41(1):120–127

    Article  CAS  PubMed  Google Scholar 

  • Tang HJ, Sun BC, Zhou FZ, Liu C (2015) Analysis of the hereditability of maize drought resistance characteristics. **njiang Agric Sci 52(11):2011–2015

    Google Scholar 

  • Thirunavukkarasu N, Hossain F, Arora K, Sharma R, Shiriga K, Mittal S, Mohan S, Namratha PM, Dogga S, Rani TS (2014) Functional mechanisms of drought tolerance in subtropical maize (Zea mays L.) identified using genome-wide association map**. BMC Genomics 15:1–12

    Article  Google Scholar 

  • Tian T, Wang SH, Yang SP, Yang ZR, Liu SX, Wang YJ, Gao HJ, Zhang SS, Yang XH, Jiang CF, Qin F (2023) Genome assembly and genetic dissection of a prominent drought-resistant maize germplasm. Nat Genet 55(3):496–506

    Article  CAS  PubMed  Google Scholar 

  • Virlouvet L, Jacquemot M, Gerentes D, Corti H, Bouton S, Gilard F, Valot B, Trouverie J, Tcherkez G, Falque M (2011) The ZmASR1 protein influences branched-chain amino acid biosynthesis and maintains kernel yield in maize under water-limited conditions. Plant Physiol 157(2):917–936

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wallace JG, Zhang X, Beyene Y, Semagn K, Olsen M, Prasanna BM, Buckler ES (2016) Genome-wide association for plant height and flowering time across 15 tropical maize populations under managed drought stress and well-watered conditions in Sub-Saharan Africa. Crop Sci 56(5):2365–2378

    Article  CAS  Google Scholar 

  • Wang C, Yang A, Yue G, Gao Q, Yin H, Zhang J (2008) Enhanced expression of phospholipase C 1 (ZmPLC1) improves drought tolerance in transgenic maize. Planta 227(5):1127–1140

    Article  CAS  PubMed  Google Scholar 

  • Wang XL, Wang HW, Liu SX, Ferjani A, Li JS, Yan JB, Yang XH, Qin F (2016) Genetic variation in ZmVPP1 contributes to drought tolerance in maize seedlings. Nat Genet 48(10):1233–1241

    Article  CAS  PubMed  Google Scholar 

  • Wu X, Feng H, Wu D, Yan S, Zhang P, Wang W, Zhang J, Ye J, Dai G, Fan Y, Li W, Song B, Geng Z, Yang W, Chen G, Qin F, Terzaghi W, Stitzer M, Li L, ** to decipher the genetic architecture of maize drought tolerance. Genome Biol 22(1):1–26

    Article  Google Scholar 

  • Xue YD, Warburton ML, Sawkins M, Zhang XH, Setter T, Xu YB, Grudloyma P, Gethi J, Ribaut JM, Li WC, Zhang XB, Zheng YL, Yan JB (2013) Genome-wide association analysis for nine agronomic traits in maize under well-watered and water-stressed conditions. Theor Appl Genet 126(10):2587–2596

    Article  CAS  PubMed  Google Scholar 

  • Yang N, Xu XW, Wang RR, Peng WL, Cai LC, Song JM, Li WQ, Luo X, Niu LY, Wang YB, ** M, Chen L, Luo JY, Deng M, Wang L, Pan QC, Liu F, Jackson D, Yang XH, Chen LL, Yan JB (2017) Contributions of Zea mays subspecies mexicana haplotypes to modern maize. Nat Commun 8(1):1–10

    Article  Google Scholar 

  • Yuan Y, Cairns JE, Babu R, Gowda M, Makumbi D, Magorokosho C, Zhang A, Liu Y, Wang N, Hao Z (2019) Genome-wide association map** and genomic prediction analyses reveal the genetic architecture of grain yield and flowering time under drought and heat stress conditions in maize. Front Plant Sci 9:1919

    Article  PubMed  PubMed Central  Google Scholar 

  • Zeng ZB (1994) Precision map** of quantitative trait loci. Genetics 136(4):1457–1468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Q, Yao YB, Li YH, Huang JP, Ma ZG, Wang ZL, Wang SP, Wang Y, Zhang Y (2020a) Progress and prospect on the study of causes and variation regularity of droughts in China. Acta Meteor Sin 78(3):500–521

    Article  Google Scholar 

  • Zhang XM, Mi Y, Mao H, Liu SX, Chen LM, Qin F (2020b) Genetic variation in ZmTIP1 contributes to root hair elongation and drought tolerance in maize. Plant Biotechnol J 18:1271–1283

    Article  CAS  PubMed  Google Scholar 

  • Zhu ZM, **ng XU, Mao GL (2018) Response of different maize inbred lines seedlings to water stress and drought tolerance evaluation. Agric Res Arid Areas 36(2):176–185

    Google Scholar 

Download references

Funding

This research was supported by the Project of Renovation Capacity Building for the Young Sci-Tech Talents Sponsored by **njiang Academy of Agricultural Sciences (xjnkq-2019004), the open funds of the Jiangsu Key Laboratory of Crop Genomics and Molecular Breeding (PL202002), and the Bei**g Outstanding Young Scientist Program (BJJWZYJH01201910019026).

Author information

Authors and Affiliations

Authors

Contributions

X. Y. and F. Q. conceived and designed the research. H. T., X. X., L. Z., C. L., and B. S. performed the experiments. H. T., R. Z., M. W., and X. Z. analyzed the data. H. T., R. Z., and X. Y. wrote the manuscript. F. Q. edited the manuscript. All authors read and approved the manuscript.

Corresponding authors

Correspondence to Feng Qin or **aohong Yang.

Ethics declarations

Ethics approval

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 440 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tang, H., Zhang, R., Wang, M. et al. QTL map** for flowering time in a maize-teosinte population under well-watered and water-stressed conditions. Mol Breeding 43, 67 (2023). https://doi.org/10.1007/s11032-023-01413-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11032-023-01413-0

Keywords

Navigation