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Association analysis of germination level cold stress tolerance and candidate gene identification in Upland cotton (Gossypium hirsutum L.)

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Abstract

Cotton originated from ancestors in the Gossypium genus that grew in semi-desert habitats. As a result, it is adversely affected by low temperatures especially during germination and the first weeks of growth. Despite this, there are relatively few molecular studies on cold stress in cotton. This limitation may present a future breeding handicap, as recent years have witnessed increased low temperature damage to cotton production. Cold tolerance is a sustainable approach to obtain good production in case of extreme cold. In the present study, 110 Upland cotton (Gossypium hirsutum) genotypes were evaluated for cold tolerance at the germination stage. We identified vigorous genotypes with cold-related parameters that outperformed the panel’s average performance (\(\overline{x}\) = 76.9% CG, 83.9% CSI, 167.5 CWVI). Molecular genetic diversity analysis with 101 simple sequence repeat (SSR) markers yielding 416 loci was used to select tolerant genotypes that could be important materials for breeding this trait. A total of 16 marker-cold tolerance trait associations (p < 0.005) were identified with 10 of them having major effects (PVE > 10%). Based on the positions of these markers, candidate genes for cold tolerance in the G. hirsutum genome were identified. Three of these markers (BNL0569, CIR081 and CIR202) are important candidates for use in marker-assisted breeding for cold tolerance because they mapped to genes previously associated with cold tolerance in other plant species such as Arabidopsis thaliana, rice and tomato.

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Data are available upon request.

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Abbreviations

ABHD:

Alpha/beta hydrolase domain

bZIP:

Basic leucine zipper protein

GLM:

General linear model

MLM:

Mixed linear model

QTL:

Quantitative trait loci

SSR:

Simple sequence repeat

TF:

Transcription factor

ZIP:

Zinc finger protein

References

  • Abdurakhmonov IY, Kohel RJ, Yu JZ, Pepper AE, Abdullaev AA, Kushanov FN, Salakhutdinov IB, Buriev ZT, Saha S, Scheffler BE, Jenkins JN, Abdukarimov A (2008) Molecular diversity and association mapping of fiber quality traits in exotic G. hirsutum L. germplasm. Genomics 92:478–487

    Article  CAS  PubMed  Google Scholar 

  • Allen DJ, Ort DR (2001) Impacts of chilling temperatures on photosynthesis in warm-climate plants. Trends Plant Sci 6:36–42

    Article  CAS  PubMed  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Ardlie KG, Kruglyak L, Seielstad M (2002) Patterns of linkage disequilibrium in the human genome. Nat Rev Genet 3:299–309

    Article  CAS  PubMed  Google Scholar 

  • Bai H, Lin P, Li X, Liao X, Wan L, Yang X, Luo Y, Zhang L, Zhang F, Liu S, Liu Q (2021) DgC3H1, a CCCH zinc finger protein gene, confers cold tolerance in transgenic chrysanthemum. Sci Hortic 281:109901. https://doi.org/10.1016/j.scienta.2021.109901

    Article  CAS  Google Scholar 

  • Balasubramanian V, Rai K, Thu S, Hii MM, Mendu V (2016) Genome-wide identification of multifunctional laccase gene family in cotton (Gossypium spp.); expression and biochemical analysis during fiber development. Sci Rep 6:34309. https://doi.org/10.1038/srep34309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baughman T, Boman R, Lemon R (1994) Cool warm test. Texas cooperative extension. The Texas A&M University System, College Station

    Google Scholar 

  • Baughman T, Boman, R Lemon, R (2011) Cotton seed quality where it all begins. The Texas A&M University, College Station, TX. http://lubbock.tamu.edu/cotton/pdf/cotseedqual.pdf

  • Baytar AA, Erdogan O, Frary A, Frary A, Doganlar S (2017) Molecular diversity and identification of alleles for Verticillium wilt resistance in elite cotton (Gossypium hirsutum L.) germplasm. Euphytica 213:31. https://doi.org/10.1007/s10681-016-1787-y

    Article  CAS  Google Scholar 

  • Baytar AA, Peynircioğlu C, Sezener V, Basal H, Frary A, Frary A, Doğanlar S (2018) Identification of stable QTLs for fiber quality and plant structure in Upland cotton (G. hirsutum L.) under drought stress. Ind Crop Prod 124:776–786. https://doi.org/10.1016/j.indcrop.2018.08.054

    Article  Google Scholar 

  • Bolek Y (2010a) Genetic variability among cotton genotypes for cold tolerance. Field Crops Res 119:59–67

    Article  Google Scholar 

  • Bolek Y (2010b) Predicting cotton seedling emergence for cold tolerance: Gossypium hirsutum L. Not Bot Hort Agrobot Cluj 38(1):134–138

    Google Scholar 

  • Bradbury PJ, Zhang Z, Kroon DE, Casstevens DM, 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 

  • Brubaker CL, Wendel JF (1994) Reevaluating the origin of domesticated cotton (Gossypium hirsutum; malvaceae) using nuclear restriction fragment length polymorphisms (RFLPs). Am J Bot 81(10):1309

    Article  Google Scholar 

  • Cai WT, Yang YL, Wang WW, Guo GY, Liu W, Bi CL (2018) Overexpression of a wheat (Triticum aestivum L.) bZIP transcription factor gene, TabZIP6, decreased the freezing tolerance of transgenic Arabidopsis seedlings by down-regulating the expression of CBFs. Plant Physiol Biochem 124:100–111

    Article  CAS  PubMed  Google Scholar 

  • Collard BCY, Jahufer MZZ, Brouwer JB, Pang ECK (2005) An introduction to markers, quantitative trait loci (QTL) mapping and marker-assisted selection for crop improvement: the basic concepts. Euphytica 142:169–196

    Article  CAS  Google Scholar 

  • Dabbert TA (2014) Genetic analysis of cotton evaluated under high temperature and water deficit. Doctor of Philosophy Thesis, the Faculty of the School of Plant Sciences, The University of Arizona, Arizona, United States

  • DeRidder BP, Crafts-Brandner SJ (2008) Chilling stress response of postemergent cotton seedlings. Physiol Plant 134:430–439. https://doi.org/10.1111/j.1399-3054.2008.01147.x

    Article  CAS  PubMed  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • Earl DA, vonHoldt BM (2002) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Article  Google Scholar 

  • Edmisten KL (2000) Cotton seed quality concerns for 2000. North Carolina State University. http://www.cotton.ncsu.edu/ccn/2000/ccn-00-4a.htm. Accessed 15 May 2011

  • Ekinci R (2018) The investigation of cold tolerance in cottonseed (Gossypium hirsutum L.) germination. Appl Ecol Environ Res 16(5):6857–6872

    Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Fang DD, Yu JZ (2012) Addition of 455 microsatellite marker loci to the high-density Gossypium hirsutum TM-1 x G. barbadense 3–79 genetic map. J Cotton Sci 16:229–248

    CAS  Google Scholar 

  • Fang DD, Hinze LL, Percy RG, Li P, Deng D, Thyssen G (2013) A microsatellite-based genome-wide analysis of genetic diversity and linkage disequilibrium in Upland cotton (Gossypium hirsutum L.) cultivars from major cotton-growing countries. Euphytica 191:391–401. https://doi.org/10.1007/s10681-013-0886-2

    Article  CAS  Google Scholar 

  • Fowler D, N’Diaye A, Laudencia-Chingcuanco D, Pozniak CJ (2016) Quantitative trait loci associated with phenological development, low temperature tolerance, grain quality, and agronomic characters in wheat (Triticum aestivum L.). PLoS ONE 11:e0152185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao SQ, Chen M, Xu ZS, Zhao CP, Li LC, Xu HJ, Tang YM, Zhao X, Ma YZ (2011) The soybean GmbZIP1 transcription factor enhances multiple abiotic stress tolerances in transgenic plants. Plant Mol Biol 75:537–553

    Article  CAS  PubMed  Google Scholar 

  • Ghosh AK, Neha C, Rajakumari S, Daum G, Rajasekharan R (2009) AT4G24160, a soluble acyl-coenzyme A-dependent lysophosphatidic acid acyltransferase. Plant Physiol 151:869–881

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gong SY, Huang GQ, Sun X, Li P, Zhao LL, Zhang DJ, Li XB (2012) GhAGP31, a cotton non-classical arabinogalactan protein, is involved in response to cold stress during early seedling development. Plant Biol 14:447–457

    Article  CAS  PubMed  Google Scholar 

  • Guo YH, Yu YP, Wang D, Wu CA, Yang GD, Huang JG, Zheng CC (2009) GhZFP1, a novel CCCH-type zinc finger protein from cotton, enhances salt stress tolerance and fungal disease resistance in transgenic tobacco by interacting with GZIRD21A and GZIPR5. New Phytol 183:62–75

    Article  CAS  PubMed  Google Scholar 

  • He Q, Jones D, Li W, Xie F, Ma J, Sun R, Wang Q, Zhu S, Zhang B (2016) Genome-wide identification of R2R3-MYB genes and expression analyses during abiotic stress in Gossypium raimondii. Sci Rep 6:22980. https://doi.org/10.1038/srep22980

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iqbal MJ, Reddy OUK, El-Zik KM, Pepper AE (2001) A genetic bottleneck in the ’evolution under domestication’ of upland cotton Gossypium hirsutum L. examined using DNA fingerprinting. Theor Appl Genet 103(4):547–554

    Article  CAS  Google Scholar 

  • James CN, Horn PJ, Case CR, Gidda SK, Zhang D, Mullen RT, Dyer JM, Anderson RG, Chapman KD (2010) Disruption of the Arabidopsis CGI-58 homologue produces Chanarin–Dorfman-like lipid droplet accumulation in plants. Proc Natl Acad Sci USA 107:17833–17838

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kargiotidou A, Kappas I, Tsaftaris A, Galanopoulou D, Farmaki T (2010) Cold acclimation and low temperature resistance in cotton: Gossypium hirsutum phospholipase Dα isoforms are differentially regulated by temperature and light. J Exp Bot 61:2991–3002

    Article  CAS  PubMed  Google Scholar 

  • Kruglyak L (1999) Prospects for whole-genome linkage disequilibrium mapping of common disease genes. Nat Genet 22:139–144

    Article  CAS  PubMed  Google Scholar 

  • Kushanov FN, Pepper AE, Yu JZ, Buriev ZT, Shermatov SE, Saha S, Ulloa M, Jenkins JN, Abdukarimov A, Abdurakhmonov IY (2016) Development, genetic mapping and QTL association of cotton PHYA, PHYB, and HY5-specific CAPS and dCAPS markers. BMC Genet 17:141

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lacape JM, Dessauw D, Rajab M, Noyer JL, Hau B (2006) Microsatellite diversity in tetraploid Gossypium germplasm: assembling a highly informative genotyping set of cotton SSRs. Mol Breed 19(1):45–58

    Article  CAS  Google Scholar 

  • Li DD, Tai FJ, Zhang ZT, Li Y, Zheng Y, Wu YF, Li XB (2009) A cotton gene encodes a tonoplast aquaporin that is involved in cell tolerance to cold stress. Gene 438:26–32

    Article  CAS  PubMed  Google Scholar 

  • Li ZB, Zeng XY, Xu JW, Zhao RH, Wei YN (2019) Transcriptomic profiling of cotton Gossypium hirsutum challenged with low-temperature gradients stress. Sci Data 6:197. https://doi.org/10.1038/s41597-019-0210-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lipka AE, Tian F, Wang Q, Peiffer J, Li M, Bradbury PJ, Gore MA, Buckler ES, Zhang Z (2011) GAPIT: genome association and prediction integrated tool. Bioinformatics 28(18):397–2399. https://doi.org/10.1093/bioinformatics/bts444

    Article  CAS  Google Scholar 

  • Liu C, Wu Y, Wang X (2011) bZIP transcription factor OsbZIP52/RISBZ5: a potential negative regulator of cold and drought stress response in rice. Planta 235:1157–1169

    Article  PubMed  CAS  Google Scholar 

  • Liu J, Meng Y, Chen J, Lv F, Yina Ma, Chen B, Wang Y, Zhou Z, Oosterhuis DM (2015) Effect of late planting and shading on cotton yield and fiber quality formation. Field Crops Res 183:1–13

    Article  Google Scholar 

  • Liu Y, Zhou T, Ge H, Pang W, Gao L, Ren L, Chen H (2016) SSR mapping of QTLs conferring cold tolerance in an interspecific cross of tomato. Int J Genom. https://doi.org/10.1155/2016/3219276

    Article  Google Scholar 

  • Liu CT, Schläppi MR, Mao BR, Wang W, Wang AJ, Chu CC (2019) The bZIP73 transcription factor controls rice cold tolerance at the reproductive stage. Plant Biotechnol J 17:1834–1849

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J, Magwanga RO, Xu Y, Wei T, Kirungu JN, Zheng J, Hou Y, Wang Y, Agong SG, Okutp E, Wang K, Zhou Z, Cai X, Liu F (2021) Functional characterization of cotton C-repeat binding factor genes reveal their potential role in cold stress tolerance. Front Plant Sci 12:766130–766130

    Article  PubMed  PubMed Central  Google Scholar 

  • Mei H, Zhu X, Zhang T (2013) Favorable QTL alleles for yield and its components identified by association mapping in Chinese Upland cotton cultivars. PLoS ONE 8(12):e82193

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mohamed H, Abdel-Hamid A (2013) Molecular and biochemical studies for heat tolerance on four cotton genotypes. Rom Biotechnol Lett 18:8823–8831

    CAS  Google Scholar 

  • Mukhopadhyay A, Vij S, Tyagi AK (2004) Overexpression of a zinc-finger protein gene from rice confers tolerance to cold, dehydration, and salt stress in transgenic tobacco. Proc Natl Acad Sci 101:6309–6314. https://doi.org/10.1073/pnas.0401572101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nabukalu P, Kong W, Cox TS, Paterson AH (2021) Detection of quantitative trait loci regulating seed yield potential in two interspecific S. bicolor2 × S. halepense subpopulations. Euphytica 217:13. https://doi.org/10.1007/s10681-020-02734-3

    Article  CAS  Google Scholar 

  • Paterson AH, Bowers JE, Burow MD, Draye X, Elsik GC, Jiang CX, Katsar CS, Lan TH, Lin YR, Ming R, Wright RJ (2000) Comparative genomics of plant chromosomes. Plant Cell 12:1523–1540. https://doi.org/10.1105/tpc.12.9.1523

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perrier X, Jacquemoud-Collet JP (2006) DARwin software. http://darwin.cirad.fr/

  • Pi B, He X, Ruan Y, Jang JC, Huang Y (2018) Genome-wide analysis and stress-responsive expression of CCCH zinc finger family genes in Brassica rapa. BMC Plant Biol 18:373. https://doi.org/10.1186/s12870-018-1608-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qin H, Chen M, Yi X, Bie S, Zhang C, Zhang Y, Lan J, Meng Y, Yuan Y, Jiao C (2015) Identification of associated SSR markers for yield component and fiber quality traits based on frame map and Upland cotton collections. PLoS ONE 10:e0118073

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • R Core Team (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  • Rihan HZ, Al-issawi M, Fuller MP (2017) Advances in physiological and molecular aspects of plant cold tolerance. J Plant Interact 12:143–157

    Article  CAS  Google Scholar 

  • Rungis D, Llewellyn D, Dennis ES, Lyon BR (2005) Simple sequence repeat (ssr) markers reveal low levels of polymorphism between cotton (Gossypium hirsutum L.) cultivars”. Aust J Agric Res 56(3):301–307

    Article  CAS  Google Scholar 

  • Salih H, Gong W, He S, Sun G, Sun J, Du X (2016) Genome-wide characterization and expression analysis of MYB transcription factors in Gossypium hirsutum. BMC Genet 17:129. https://doi.org/10.1186/s12863-016-0436-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scotti-Campos P, Pais IP, Ribeiro-Barros AI, Martins LD, Tomaz MA, Rodrigues WP, Eliemar C, Semedo JN, Fortunato AS, Martins MQ, Partelli FL, Lidon FC, DaMatta FM, Ramalho JC (2019) Lipid profile adjustments may contribute to warming acclimation and to heat impact mitigation by elevated [CO2] in Coffea spp. Environ Exp Bot. https://doi.org/10.1016/j.envexpbot.2019.103856

    Article  Google Scholar 

  • Shan DP, Huang JG, Yang YT, Guo YH, Wu CA, Yang GD, Gao Z, Zheng CC (2007) Cotton GhDREB1 increases plant tolerance to low temperature and is negatively regulated by gibberellic acid. New Phytol 176:70–81

    Article  CAS  PubMed  Google Scholar 

  • Shim J, Gannaban RB, de los Reyes BG, Angeles-Shim RB (2019) Identification of novel sources of genetic variation for the improvement of cold germination ability in upland cotton (Gossypium hirsutum). Euphytica 215:190. https://doi.org/10.1007/s10681-019-2510-6

    Article  CAS  Google Scholar 

  • Smith CW, Varvil JJ (1984) Standard and cool germination test compared with field emergence in upland cotton. Agronomy J 76:587–589

    Article  Google Scholar 

  • Speed TR, Jividen DR, Jividen G (1996) Relationship between cotton seedling cold tolerance and physical and chemical properties T.R. Texas Tech University and Cotton Incorporated Lubbock, TX Raleigh, NC. Reprinted from the Proceedings of the Beltwide Cotton Conference, vol 2. National Cotton Council, Memphis TN, pp 1170–1171

  • Staus HC, Hopper NW (1983) Evaluation of several tests to determine seed quality of cotton. Proc Beltwide Cotton Prod Res Conf 1983:38

    Google Scholar 

  • Storey JD (2002) A direct approach to false discovery rates. J R Stat Soc Ser B Stat Methodol 64:479–498

    Article  Google Scholar 

  • Sun H, Meng M, Yan Z, Lin Z, Nie X, Yang X (2019) Genome-wide association mapping of stress-tolerance traits in cotton. Crop J 7:77–88

    Article  Google Scholar 

  • Tolliver J, Savoy BR, Drummond EA (1997) Cool germination test on cotton variability between seed testing laboratories. Proc Beltwide Cotton Conf 1997:442–443

    Google Scholar 

  • Turlapati PV, Kim KW, Davin LB, Lewis NG (2011) The laccase multigene family in Arabidopsis thaliana: towards addressing the mystery of their gene function(s). Planta 233:439–470

    Article  CAS  PubMed  Google Scholar 

  • Tyagi P, Gore MA, Bowman DT, Campbell BT, Udall JA, Kuraparthy V (2013) Genetic diversity and population structure in the US Upland cotton (Gossypium hirsutum L.). Theor Appl Genet 127:283–295

    Article  PubMed  Google Scholar 

  • Ulloa M, Cantrell RG, Percy RG, Zeiger E, Lu Z (2000) QTL analysis of stomatal conductance and relationship to lint yield in an interspecific cotton. J Cotton Sci 4:10–18

    CAS  Google Scholar 

  • Vijayakumar A, Rajasekharan R (2016) Distinct roles of alpha/beta hydrolase domain containing proteins. Biochem Mol Biol J 2:3

    Article  Google Scholar 

  • Vijayakumar A, Panneerselvam V, Vijayakumar AK, Rajasekharan R (2016) The Arabidopsis ABHD11 mutant accumulates polar lipids in leaves as a consequence of absent acylhydrolase activity. Plant Physiol 170:180–193

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Cao HL, Qian WJ, Yao LN, Hao XY, Li N, Yang Y, Wang X (2017) Identification of a novel bZIP transcription factor in Camellia sinensis as a negative regulator of freezing tolerance in transgenic Arabidopsis. Ann Bot London 119:1195–1209

    Article  CAS  Google Scholar 

  • Wright R, Thaxton P, Paterson AH, El-Zik K (1998) Polyploid formation in Gossypium has created novel avenues for response to selection for disease resistance. Genetics 149:1987–1996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu Z, Yu J, Kohel RJ, Percy RG, Beavis WD, Main D, Yu JZ (2015) Distribution and evolution of cotton fiber development genes in the fibreless Gossypium raimondii genome. Genomics 106:61–69

    Article  CAS  PubMed  Google Scholar 

  • Yan LJ (2013) Responses to cold stress of six cotton varieties in initial growth stage. Acta Laser Biol Sinica 22:557–563

    Google Scholar 

  • Yao L, Hao X, Cao H, Ding C, Yang Y, Wang L, Wang X (2020) ABA dependent bZIP transcription factor, CsbZIP18, from Camellia sinensis negatively regulates freezing tolerance in Arabidopsis. Plant Cell Rep 39:553–565

    Article  CAS  PubMed  Google Scholar 

  • Yu Y, Qian Y, Jiang M, Xu J, Yang J, Zhang T, Gou L, Pi E (2020) Regulation mechanisms of plant basic leucine zippers to various abiotic stresses. Front Plant Sci 11:1258

    Article  PubMed  PubMed Central  Google Scholar 

  • Zafar SA, Noor MA, Waqas MA, Wang X, Shaheen T, Raza M, Rahman MU (2018) Temperature extremes in cotton production and mitigation strategies. Past Present Future Trends Cotton Breed. https://doi.org/10.5772/intechopen.74648

    Article  Google Scholar 

  • Zhang J, Lu Y, Cantrell RG, Hughs E (2005) Molecular marker diversity and field performance in commercial cotton cultivars evaluated in the southwestern USA. Crop Sci 45:1483–1490

    Article  CAS  Google Scholar 

  • Zhang LN, Zhang L, Xia C, Zhao GY, Liu J, Jia JZ, Kong X (2015) A novel wheat bZIP transcription factor, TabZIP60, confers multiple abiotic stress tolerances in transgenic Arabidopsis. Physiol Plantarum 153:538–554

    Article  CAS  Google Scholar 

  • Zhang LN, Zhang LC, Xia C, Gao LF, Hao CY, Zhao GY, Jia J, Kong X (2017) A novel wheat C-bZIP gene, TabZIP14-B, participates in salt and freezing tolerance in transgenic plants. Front Plant Sci 8:710

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu Y, Chen K, Mi X, Chen T, Ali J, Ye G, Xu J, Li Z (2015) Identification and fine mapping of a stably expressed QTL for cold tolerance at the booting stage using an interconnected breeding population in rice. PLoS ONE 10:e0145704

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhu M, Meng X, Cai J, Li G, Dong T, Li Z (2018) Basic leucine zipper transcription factor SlbZIP1 mediates salt and drought stress tolerance in tomato. BMC Plant Biol 18:83. https://doi.org/10.1186/s12870-018-1299-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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This work was supported by a research grant (317O179) from The Scientific and Technological Research Council of Turkey.

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Authors and Affiliations

  1. Department of Molecular Biology and Genetics, Izmir Institute of Technology, Izmir, Turkey

    Asena Akkose Baytar, Anne Frary & Sami Doğanlar

  2. Özaltın Agricultural Enterprises Industry and Commerce Inc., Aydın, Turkey

    Ceng Peynircioğlu

  3. Nazilli Cotton Research Institute, Nazilli, Aydın, Turkey

    Volkan Sezener

  4. Plant Science and Technology Applied Research Center, Izmir Institute of Technology, Izmir, Turkey

    Sami Doğanlar

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  1. Asena Akkose Baytar
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  2. Ceng Peynircioğlu
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  3. Volkan Sezener
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Molecular characterization, data analysis, interpretation of data, manuscript drafting and revision: AAB; Phenotyping experiments: CP and VS; Conception and design, interpretation of data, manuscript revision: AF; Conception and design, manuscript revision: SD. All: final approval of the version to be published.

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Correspondence to Sami Doğanlar.

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Baytar, A.A., Peynircioğlu, C., Sezener, V. et al. Association analysis of germination level cold stress tolerance and candidate gene identification in Upland cotton (Gossypium hirsutum L.). Physiol Mol Biol Plants 28, 1049–1060 (2022). https://doi.org/10.1007/s12298-022-01184-6

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