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Journal of Integrative Agriculture  2023, Vol. 22 Issue (5): 1324-1337    DOI: 10.1016/j.jia.2022.08.034
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Association mapping of lignin response to Verticillium wilt through an eight-way MAGIC population in Upland cotton

TIAN Xiao-min1*, HAN Peng1*, WANG Jing2, SHAO Pan-xia1, AN Qiu-shuang1, Nurimanguli AINI1, YANG Qing-yong1, 2, YOU Chun-yuan3, LIN Hai-rong1, ZHU Long-fu1, 4#, PAN Zhen-yuan1#, NIE Xin-hui1#

1 Key Laboratory of Oasis Eco-agricultural, Xinjiang Production and Construction Corps/Agricultural College, Shihezi University, Shihezi 832003, P.R.China

2 College of Informatics, Huazhong Agricultural University, Wuhan 430070, P.R.China

3 Cotton Research Institute, Shihezi Academy of Agricultural Sciences, Shihezi 832011, P.R.China

4 National Key Laboratory of Crop Genetic Improvement/College of Plant Sciences & Technology, Huazhong Agricultural University, Wuhan 430070, P.R.China

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木质素代谢在植物对病原菌的防御中起着关键作用,并且在抵御病原菌侵染的过程中总是起到正向作用。因此,解析植物木质素响应病原菌代谢相关抗性基因的遗传机理具有重要意义。本研究以8个陆地棉品系为材料,构建了一个多亲本高世代杂交(MAGIC)群体(n=280),该群体表现出控制优良性状的等位基因的聚合特征。为了研究木质素对黄萎病的响应(LRVW),本研究在4种环境下分别建立了人工病圃(ADN)和轮作苗圃(RN)。通过采集和测定棉秆的木质素含量,并将不同环境下ADN/RN木素比值作为LRVW值,结果表明,群体LRVW值表现出较丰富的变异。利用63K芯片获得了9323个高质量单核苷酸多态(SNP)标记,用于MAGIC群体的基因分型,结果显示,SNPs分布于全基因组,平均密度为4.78SNP/Mb,在染色体间的分布范围为1.14 SNP/Mb (ChrA06)~10.08 SNP/Mb (ChrD08)。利用混合线性模型(MLM)对LRVW进行全基因组关联分析,并在两个以上的环境中共同检测到3个稳定的QTL,即qLRVW-A04qLRVW-A10qLRVW-D05。结合分析候选基因编码序列变异、诱导表达模式和功能注释,最终在QTL区间选择了两个关键候选基因Ghi_D05G01046Ghi_D05G01221。这两个基因在编码区都出现了非同义突变,并且都受黄萎病菌强烈诱导。Ghi_D05G01046编码一个富含亮氨酸的延伸素(LRx)蛋白,与拟南芥细胞壁的生物合成和结构有关。Ghi_D05G01221编码Jaz的转录抑制因子,它在茉莉酸(JA)信号通路中发挥作用。综上所述,本研究不仅为陆地棉抗黄萎病育种和QTL定位创造了宝贵的遗传资源,也为解析陆地棉抗黄萎病的遗传基础开辟了新的视角。


Lignin metabolism plays a pivotal role in plant defense against pathogens and is always positively correlated as a response to pathogen infection.  Thus, understanding resistance genes against pathogens in plants depends on a genetic analysis of lignin response.  In the study, eight upland cotton lines were used to construct a multi-parent advanced generation intercross (MAGIC) population (n=280), which exhibited peculiar characteristics from the convergence of various alleles coding for advantageous traits.  To measure the lignin response to Verticillium wilt (LRVW), artificial disease nursery (ADN) and rotation nursery (RN) were prepared for MAGIC population planting in four environments.  The stem lignin contents were collected, and the LRVW was measured with the lignin value of ADN/RN in each environment, which showed great variation.  A total of 9323 high-quality single-nucleotide polymorphism (SNP) markers obtained from the Cotton-SNP63K array were employed for genotyping the MAGIC population.  The SNPs were distributed through the whole genome with 4.78 SNP/Mb density, ranging from 1.14 (ChrA06) to 10.08 (ChrD08).  A genome-wide association study was performed using a mixed linear model (MLM) for LRVW, and three stable quantitative trait loci (QTLs), qLRVW-A04, qLRVW-A10 and qLRVW-D05, were identified in more than two environments.  Two key candidate genes, Ghi_D05G01046 and Ghi_D05G01221, were selected within the QTLs through the combination of variations in the coding sequence, induced expression patterns, and function annotations, both of which presented nonsynonymous mutations in coding regions and were strongly induced by Verticillium dahliae. Ghi_D05G01046 encodes a leucine-rich extensin (LRx) protein, which is involved in Arabidopsis cell wall biosynthesis and organization.  Ghi_D05G01221 encodes a transcriptional co-repressor novel interactor of jaz (NINJA), which functions in the jasmonic acid (JA) signaling pathway.  In summary, the study creates valuable genetic resources for breeding and QTL mapping and opens up a new perspective to uncover the genetic basis of VW resistance in upland cotton.

Keywords:  genome-wide association study       lignin response       MAGIC population       upland cotton       Verticillium wilt  
Received: 14 March 2022   Accepted: 10 May 2022
Fund: This work was financed by the National Natural Science Foundation of China (31760402 and 31771844) and the Innovation Leadership Program in Sciences and Technologies for Young and Middle-aged Scientists of Xinjiang Production and Construction Corps, China (2019CB027).

About author:  TIAN Xiao-min, E-mail:; HAN Peng, E-mail:; #Correspondence ZHU Long-fu, Tel: +86-27-87283955, E-mail:; PAN Zhen-yuan, Tel: +86-993-2058970, E-mail:; NIE Xin-hui, Tel: +86-993-2058970, E-mail: * These authors contributed equally to this study.

Cite this article: 

TIAN Xiao-min, HAN Peng, WANG Jing, SHAO Pan-xia, AN Qiu-shuang, Nurimanguli AINI, YANG Qing-yong, YOU Chun-yuan, LIN Hai-rong, ZHU Long-fu, PAN Zhen-yuan, NIE Xin-hui. 2023. Association mapping of lignin response to Verticillium wilt through an eight-way MAGIC population in Upland cotton. Journal of Integrative Agriculture, 22(5): 1324-1337.

Abdelraheem A, Elassbli H, Zhu Y, Kuraparthy V, Hinze L, Stelly D, Wedegaertner T, Zhang J. 2020. A genome-wide association study uncovers consistent quantitative trait loci for resistance to Verticillium wilt and Fusarium wilt race 4 in the US Upland cotton. Theoretical and Applied Genetics, 133, 563–577.
Abdelraheem A, Liu F, Song M, Zhang J F. 2017. A meta-analysis of quantitative trait loci for abiotic and biotic stress resistance in tetraploid cotton. Molecular Genetics and Genomics, 292, 1221–1235.
Dell’Acqua M, Gatti D M, Pea G, Cattonaro F, Coppens F, Magris G, Hlaing A L, Aung H H, Nelissen H, Baute J, Frascaroli E, Churchill G A, Inzé D, Morgante M, Pè M E. 2015. Genetic properties of the MAGIC maize population: A new platform for high definition QTL mapping in Zea mays. Genome Biology, 16, 167.
Alexander D H, Novembre J, Lange K. 2009. Fast model-based estimation of ancestry in unrelated individuals. Genome Research, 19, 1655–1664.
Ball R D. 2013. Statistical analysis of genomic data. Methods in Molecular Biology, 1019, 171–192.
Bandillo N, Raghavan C, Muyco P A, Sevilla M A L, Lobina I T, Dilla-Ermita C J, Tung C W, McCouch S, Thomson M, Mauleon R, Singh R K, 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 (New York, NY), 6, 11.
Barah P, Winge P, Kusnierczyk A, Tran D H, Bones A M. 2013. Molecular signatures in Arabidopsis thaliana in response to insect attack and bacterial infection. PLoS ONE, 8, e58987.
Bardak A, Çelik S, Erdogan O, Ekinci R, Dumlupinar Z. 2021. Association mapping of verticillium wilt disease in a worldwide collection of cotton (Gossypium hirsutum L.). Plants, 10, 306.
Baumberger N, Ringli C, Keller B. 2001. The chimeric leucine-rich repeat/extensin cell wall protein LRX1 is required for root hair morphogenesis in Arabidopsis thaliana. Genes Development, 15, 1128–1139.
Bubna G A, Lima R B, Zanardo D Y L, dos Santos W D, Ferrarese M D L L, Ferrarese-Filho O. 2011. Exogenous caffeic acid inhibits the growth and enhances the lignification of the roots of soybean (Glycine max). Journal of Plant Physiology, 168, 1627–1633.
Cavanagh C, Morell M, Mackay I, Powell W. 2008. From mutations to MAGIC: Resources for gene discovery, validation and delivery in crop plants. Current Opinion in Plant Biology, 11, 215–221.
Chezem W R, Clay N K. 2016. Regulation of plant secondary metabolism and associated specialized cell development by MYBs and bHLHs. Phytochemistry, 131, 26–43.
Cingolani P, Platts A, Wang L L, Coon M, Nguyen T, Wang L, Land S J, Lu X, Ruden D M. 2012. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly, 6, 80–92.
Crous P W, Liebenberg M M, Braun U, Groenewald J Z. 2006. Re-evaluating the taxonomic status of Phaeoisariopsis griseola, the causal agent of angular leaf spot of bean. Studies in Mycology, 55, 163–173.
Crous P W, Wingfield M J, Cheewangkoon R, Carnegie A J, Burgess T I, Summerell B A, Edwards J, Taylor P W J, Groenewald J Z. 2019. Foliar pathogens of eucalypts. Studies in Mycology, 94, 125–298.
Cui Y, Ge Q, Zhao P, Chen W, Sang X, Zhao Y, Chen Q, Wang H. 2021. Rapid mining of candidate genes for Verticillium wilt resistance in cotton based on BSA-Seq analysis. Frontiers in Plant Science, 12, 703011.
Denness L, McKenna J F, Segonzac C, Wormit A, Madhou P, Bennett M, Mansfield J, Zipfel C, Hamann T. 2011. Cell wall damage-induced lignin biosynthesis is regulated by a reactive oxygen species- and jasmonic acid-dependent process in Arabidopsis. Plant Physiology, 156, 1364–1374.
Diaz S, Ariza-Suarez D, Izquierdo P, Lobaton J D, de la Hoz J F, Acevedo F, Duitama J, Guerrero A F, Cajiao C, Mayor V, Beebe S E, Raatz B. 2020. Genetic mapping for agronomic traits in a MAGIC population of common bean (Phaseolus vulgaris L.) under drought conditions. BMC Genomics, 21, 799–819.
Dong H, Zhang X, Choen Y, Zhou Y, Li W, Li Z. 2006. Dry mycelium of Penicillium chrysogenum protects cotton plants against wilt diseases and increases yield under field conditions. Crop Protection, 25, 324–330.
Draeger C, Ndinyanka Fabrice T, Gineau E, Mouille G, Kuhn B M, Moller I, Abdou M T, Frey B, Pauly M, Bacic A, Ringli C. 2015. Arabidopsis leucine-rich repeat extensin (LRX) proteins modify cell wall composition and influence plant growth. BMC Plant Biology, 15, 155–166.
Fang H, Zhou H, Sanogo S, Flynn R, Percy R G, Hughs S E, Ulloa M, Jones D C, Zhang J. 2013. Quantitative trait locus mapping for Verticillium wilt resistance in a backcross inbred line population of cotton (Gossypium hirsutum×Gossypium barbadense) based on RGA-AFLP analysis. Euphytica, 194, 79–91.
Fang H, Zhou H, Sanogo S, Lipka A E, Fang D D, Percy R G, Hughs S E, Jones D C, Gore M A, Zhang J. 2014. Quantitative trait locus analysis of Verticillium wilt resistance in an introgressed recombinant inbred population of Upland cotton. Molecular Breeding, 33, 709–720.
Feng L, Chi B J, Dong H Z. 2022. Cotton cultivation technology with Chinese characteristics has driven the 70-year development of cotton production in China. Journal of Integrative Agriculture, 21, 597–609.
Fu L P, Xiao Y G, Yan J, Liu J D, Wen W E, Zhang Y, Xia X C, He Z H. 2019. Characterization of TaCOMT genes associated with stem lignin content in common wheat and development of a gene-specific marker. Journal of Integrative Agriculture, 18, 939–947.
Guo X H, Cai C P, Yuan D D, Zhang R S, Xi J I, Guo W Z. 2016. Development and identification of Verticillium wilt-resistant upland cotton accessions by pyramiding QTL related to resistance. Journal of Integrative Agriculture, 15, 512–520.
Hardy O J, Vekemans X. 2002. spagedi: A versatile computer program to analyse spatial genetic structure at the individual or population levels. Molecular Ecology Notes, 2, 618–620.
Hu Q, Xiao S, Guan Q, Tu L, Sheng F, Du X, Zhang X. 2020. The laccase gene GhLac1 modulates fiber initiation and elongation by coordinating jasmonic acid and flavonoid metabolism. The Crop Journal, 8, 522–533.
Huang B E, George A W, Forrest K L, Kilian A, Hayden M J, Morell M K, Cavanagh C R. 2012. A multiparent advanced generation inter-cross population for genetic analysis in wheat. Plant Biotechnology Journal, 10, 826–839.
Huang B E, Verbyla K L, Verbyla A P, Raghavan C, Singh V K, Gaur P, Leung H, Varshney R K, Cavanagh C R. 2015. MAGIC populations in crops: Current status and future prospects. Theoretical and Applied Genetics, 128, 999–1017.
Huang C, Shen C, Wen T, Gao B, Zhu D, Li X, Ahmed M M, Li D, Lin Z. 2018. SSR-based association mapping of fiber quality in upland cotton using an eight-way MAGIC population. Molecular Genetics and Genomics, 293, 793–805.
Hückelhoven R. 2007. Cell wall-associated mechanisms of disease resistance and susceptibility. Annual Reviews of Phytopathology, 45, 101–127.
Hulse-Kemp A M, Lemm J, Plieske J, Ashrafi H, Buyyarapu R, Fang D D, Frelichowski J, Giband M, Hague S, Hinze L L, Kochan K J, Riggs P K, Scheffler J A, Udall J A, Ulloa M, Wang S S, Zhu Q H, Bag S K, Bhardwaj A, Burke J J, et al. 2015. Development of a 63K SNP array for cotton and high-density mapping of intraspecific and interspecific populations of Gossypium spp. G3 - Genes Genomes Genetics (Bethesda), 5, 1187–1209.
Jiang F, Zhao J, Zhou L, Guo W, Zhang T. 2009. Molecular mapping of Verticillium wilt resistance QTL clustered on chromosomes D7 and D9 in upland cotton. Science in China (Series C: Life Sciences), 52, 872–884.
Karasov T L, Chae E, Herman J J, Bergelson J. 2017. Mechanisms to mitigate the trade-off between growth and defense. The Plant Cell, 29, 666–680.
Klosterman S J, Atallah Z K, Vallad G E, Subbarao K V. 2009. Diversity, pathogenicity, and management of Verticillium species. Annual Review of Phytopathology, 47, 39–62.
Li B, Gao F, Ren B Z, Dong S T, Liu P, Zhao B, Zhang J W. 2021. Lignin metabolism regulates lodging resistance of maize hybrids under varying planting density. Journal of Integrative Agriculture, 20, 2077–2089.
Li H, Durbin R. 2010. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics (Oxford, England), 26, 589–595.
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Genome Project Data Processing S. 2009. The sequence alignment/map format and SAMtools. Bioinformatics (Oxford, England), 25, 2078–2079.
Li T, Ma X, Li N, Zhou L, Liu Z, Han H, Gui Y, Bao Y, Chen J, Dai X. 2017. Genome-wide association study discovered candidate genes of Verticillium wilt resistance in upland cotton (Gossypium hirsutum L.). Plant Biotechnology Journal, 15, 1520–1532.
Li Z K, Chen B, Li X X, Wang J P, Zhang Y, Wang X F, Yan Y Y, Ke H F, Yang J, Wu J H, Wang G N, Zhang G Y, Wu L Q, Wang X Y, Ma Z Y. 2019. A newly identified cluster of glutathione S-transferase genes provides Verticillium wilt resistance in cotton. The Plant Journal, 98, 213–227.
Lipka A E, Tian F, Wang Q, Peiffer J, Li M, Bradbury P J, Gore M A, Buckler E S, Zhang Z. 2012. GAPIT: Genome association and prediction integrated tool. Bioinformatics (Oxford, England), 28, 2397–2399.
Liu K, Muse S. 2005. PowerMaker: An integrated analysis environment for genetic maker analysis. Bioinformatics (Oxford, England), 21, 2128–2129.
Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2–∆∆CT method. Methods, 25, 402–408.
Lopisso D T, Kühlmann V, Siebold M. 2017. Potential of soil-derived fungal biocontrol agents applied as a soil amendment and a seed coating to control Verticillium wilt of sugar beet. Biocontrol Science and Technology, 27, 1019–1037.
Luo J, Ma C, Li Z, Zhu B Q, Zhang J, Lei C I, Jin S X, Hull J J, Chen L Z. 2018. Assessment of suitable reference genes for qRT-PCR analysis in Adelphocoris suturalis. Journal of Integrative Agriculture, 17, 2745–2757.
Martinez G, Abdelraheem A, Darapuneni M, Jenkins J N, McCarty J C, Zhang J. 2018. Evaluation of a multi-parent advanced generation inter-cross (MAGIC) introgressed line population for Verticillium wilt resistance in Upland cotton. Euphytica, 214, 197.
Nishida H, Suzaki T. 2018. Nitrate-mediated control of root nodule symbiosis. Current Opinion in Plant Biology, 44, 129–136.
Novakazi F, Krusell L, Jensen J D, Orabi J, Jahoor A, Bengtsson T, on behalf of the PPP Barley Consortium. 2020. You had me at “MAGIC”!: four barley MAGIC populations reveal novel resistance QTL for powdery mildew. Genes, 11, 1512–1533.
Oh E, Seo P J, Kim J. 2018. Signaling peptides and receptors coordinating plant root development. Trends in Plant Science, 23, 337–351.
Okamoto S, Tabata R, Matsubayashi Y. 2016. Long-distance peptide signaling essential for nutrient homeostasis in plants. Current Opinion in Plant Biology, 34, 35–40.
Ongom P O, Ejeta G. 2018. Mating design and genetic structure of a multi-parent advanced generation intercross (MAGIC) population of sorghum (Sorghum bicolor (L.) moench). G3 - Genes Genomes Genetics (Bethesda), 8, 331–341.
Palanga K K, Jamshed M, Rashid M H O, Gong J, Li J, Iqbal M S, Liu A, Shang H, Shi Y, Chen T, Ge Q, Zhang Z, Dilnur T, Li W, Li P, Gong W, Yuan Y. 2017. Quantitative trait locus mapping for Verticillium wilt resistance in an upland cotton recombinant inbred line using SNP-based high density genetic map. Frontiers in Plant Science, 8, 382.
Piepho H P. 1994. Best linear unbiased prediction (BLUP) for regional yield trials: A comparison to additive main effects and multiplicative interaction (AMMI) analysis. Theoretical and Applied Genetics, 89, 647–654.
Price A L, Patterson N J, Plenge R M, Weinblatt M E, Shadick N A, Reich D. 2006. Principal components analysis corrects for stratification in genome-wide association studies. Nature Genetics, 38, 904–909.
Rashid M H O, Li P T, Chen T T, Palanga K K, Gong W K, Ge Q, Gong J W, Liu A Y, Lu Q W, Diouf L, Sarfraz Z, Jamshed M, Shi Y Z, Yuan Y L. 2021. Genome-wide quantitative trait loci mapping on Verticillium wilt resistance in 300 chromosome segment substitution lines from Gossypium hirsutum×Gossypium barbadense. G3 - Genes Genomes Genetics (Bethesda), 11, doi: 10.1093/g3journal/jkab027.
Sannemann W, Huang B E, Mathew B, Léon J. 2015. Multi-parent advanced generation inter-cross in barley: High-resolution quantitative trait locus mapping for flowering time as a proof of concept. Molecular Breeding, 35, 86–102.
Shitan N, Sugiyama A, Yazaki K. 2013. Functional analysis of jasmonic acid-responsive secondary metabolite transporters. In: Goossens A, Pauwels L, eds., Jasmonate Signaling: Methods and Protocols. Humana Press, Totowa, NJ. pp. 241–250.
Sobczak J, Bonine C, Viana J, Dornelas M, Mazzafera P. 2010. Abiotic and biotic stresses and changes in the lignin content and composition in plants. Journal of Integrative Plant Biology, 52, 360–376.
Su J, Wang C, Ma Q, Zhang A, Shi C, Liu J, Zhang X, Yang D, Ma X. 2020. An RTM-GWAS procedure reveals the QTL alleles and candidate genes for three yield-related traits in upland cotton. BMC Plant Biology, 20, 416.
Takahashi F, Shinozaki K. 2019. Long-distance signaling in plant stress response. Current Opinion in Plant Biology, 47, 106–111.
Tang Y, Zhang Z, Lei Y, Hu G, Liu J, Hao M, Chen A, Peng Q, Wu J. 2019. Cotton WATs modulate SA biosynthesis and local lignin deposition participating in plant resistance against Verticillium dahliae. Frontiers in Plant Science, 10, 526.
Tian L, Huang C D, Zhang D D, Li R, Chen J Y, Sun W X, Qiu N W, Dai X F. 2021. Extracellular superoxide dismutase VdSOD5 is required for virulence in Verticillium dahliae. Journal of Integrative Agriculture, 20, 1858–1870.
Toyota M, Spencer D, Sawai-Toyota S, Jiaqi W, Zhang T, Koo A, Howe G, Gilroy S. 2018. Glutamate triggers long-distance, calcium-based plant defense signaling. Science, 361, 1112–1115.
Wang L, Feng H, Gong M, Zhou L. 2011. Effect of various tillage measures on cotton Verticillium wilt in drip irrigation cotton field under film. Transactions of the Chinese Society of Agricultural Engineering, 27, 31–36. (in Chinese)
Wang Z Y, Bao Y F, Pei T, Wu T R, Du X, He M X, Wang Y, Liu Q F, Yang H H, Jiang J B, Zhang H, Li J F, Zhao T T, Xu XY. 2020. Silencing the SLB3 transcription factor gene decreases drought stress tolerance in tomato. Journal of Integrative Agriculture, 19, 2699–2708.
Wildermuth G B. 1971. Varietal resistance to Verticillium wilt of cotton in Queensland. Australian Journal of Experimental Agriculture, 11, 365–368.
Wu Y, Zhang L, Zhou J, Zhang X, Feng Z, Wei F, Zhao L, Zhang Y, Feng H, Zhu H. 2021. Calcium-dependent protein kinase GhCDPK28 was dentified and involved in Verticillium wilt resistance in cotton. Frontiers in Plant Science, 12, 772649.
Xiong X P, Sun S C, Zhu Q H, Zhang X Y, Li Y J, Liu F, Xue F, Sun J. 2021. The cotton lignin biosynthetic gene Gh4CL30 regulates lignification and phenolic content and contributes to Verticillium wilt resistance. Molecular Plant-Microbe Interactions, 34, 240–254.
Xu L, Zhu L, Tu L, Liu L, Yuan D, Jin L, Long L, Zhang X. 2011. Lignin metabolism has a central role in the resistance of cotton to the wilt fungus Verticillium dahliae as revealed by RNA-Seq-dependent transcriptional analysis and histochemistry. Journal of Experimental Botany, 62, 5607–5621.
Yang J, Zhang Y, Wang X, Wang W, Li Z, Wu J, Wang G, Wu L, Zhang G, Ma Z. 2018. HyPRP1 performs a role in negatively regulating cotton resistance to V. dahliae via the thickening of cell walls and ROS accumulation. BMC Plant Biology, 18, 339–357.
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 (Oxford, England), 35, 1786–1788.
Zhang J, Abdelraheem A, Thyssen G N, Fang D D, Jenkins J N, McCarty J C, Wedegaertner T. 2019. Evaluation and genome-wide association study of Verticillium wilt resistance in a MAGIC population derived from intermating of eleven Upland cotton (Gossypium hirsutum) parents. Euphytica, 216, 9.
Zhang J, Fang H, Zhou H, Sanogo S, Ma Z. 2014. Genetics, breeding, and marker-assisted selection for Verticillium wilt resistance in cotton. Crop Science, 54, 1289–1303.
Zhang J, Sanogo S, Ma Z, Qu Y. 2015a. Breeding, genetics, and quantitative trait locus mapping for Fusarium wilt resistance in cotton. Crop Science, 55, 2435–2452.
Zhang J, Yu J, Pei W, Li X, Said J, Song M, Sanogo S. 2015b. Genetic analysis of Verticillium wilt resistance in a backcross inbred line population and a meta-analysis of quantitative trait loci for disease resistance in cotton. BMC Genomics, 16, 577.
Zhang Q, Gao X, Ren Y, Ding X, Qiu J, Li N, Zeng F, Chu Z. 2018. Improvement of Verticillium wilt resistance by applying arbuscular mycorrhizal fungi to a cotton variety with high symbiotic efficiency under field conditions. International Journal of Molecular Sciences, 19, 241.
Zhang T, Hu Y, Jiang W, Fang L, Guan X, Chen J, Zhang J, Saski C A, Scheffler B E, Stelly D M, Hulse-Kemp A M, Wan Q, Liu B, Liu C, Wang S, Pan M, Wang Y, Wang D, Ye W, Chang L, et al. 2015. Sequencing of allotetraploid cotton (Gossypium hirsutum L. acc. TM-1) provides a resource for fiber improvement. Nature Biotechnology, 33, 531–537.
Zhang Y, Chen B, Sun Z, Liu Z, Cui Y, Ke H, Wang Z, Wu L, Zhang G, Wang G, Li Z, Yang J, Wu J, Shi R, Liu S, Wang X, Ma Z. 2021. A large-scale genomic association analysis identifies a fragment in Dt11 chromosome conferring cotton Verticillium wilt resistance. Plant Biotechnology Journal, 19, 2126–2138.
Zhao P, Zhao Y L, Jin Y, Zhang T, Guo H S. 2014. Colonization process of Arabidopsis thaliana roots by a green fluorescent protein-tagged isolate of Verticillium dahliae. Protein & Cell, 5, 94–98.
Zhao Y, Chen W, Cui Y, Sang X, Lu J, Jing H, Wang W, Zhao P, Wang H. 2021. Detection of candidate genes and development of KASP markers for Verticillium wilt resistance by combining genome-wide association study, QTL-seq and transcriptome sequencing in cotton. Theoretical and Applied Genetics, 134, 1063–1081.
Zhao Y, Wang H, Chen W, Li Y. 2014. Genetic structure, linkage disequilibrium and association mapping of Verticillium wilt resistance in elite cotton (Gossypium hirsutum L.) germplasm population. PLoS ONE, 9, e86308.
Zheng M, Peng C, Liu H, Tang M, Yang H, Li X, Liu J, Sun X, Wang X, Xu J, Hua W, Wang H. 2017. Genome-wide association study reveals candidate genes for control of plant height, branch initiation height and branch number in rapeseed (Brassica napus L.). Frontiers in Plant Science, 8, 1246.
Zhu J K. 2016. Abiotic stress signaling and responses in plants. Cell, 167, 313–324.

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