全基因组关联分析挖掘陆地棉苗期根系形态相关性状优异位点和候选基因

doi:10.1016/j.jia.2024.03.037

Journal of Integrative Agriculture ›› 2024, Vol. 23 ›› Issue (10): 3406-3418.DOI: 10.1016/j.jia.2024.03.037

全基因组关联分析挖掘陆地棉苗期根系形态相关性状优异位点和候选基因

收稿日期:2023-10-17 接受日期:2024-02-01 出版日期:2024-10-20 发布日期:2024-09-11

Mining elite loci and candidate genes for root morphology-related traits at the seedling stage by genome-wide association studies in upland cotton (Gossypium hirsutum L.)

Huaxiang Wu^*, Xiaohui Song^*, Muhammad Waqas-Amjid, Chuan Chen, Dayong Zhang^#, Wangzhen Guo^#

State Key Laboratory of Crop Genetics & Germplasm Enhancement and Utilization/Engineering Research Center of Cotton Germplasm Enhancement and Application, Ministry of Education/Nanjing Agricultural University, Nanjing 210095, China

Received:2023-10-17 Accepted:2024-02-01 Online:2024-10-20 Published:2024-09-11
About author:Huaxiang Wu, E-mail: wuhx@mail.nankai.edu.cn; Xiaohui Song, E-mail: 2018101045@njau.edu.cn; #Correspondence Wangzhen Guo, E-mail: moelab@njau.edu.cn; Dayong Zhang, Tel: +86-25-84396523, E-mail: dyzhang@njau.edu.cn * These authors contributed equally to this study.
Supported by:
This work was supported by the Jiangsu Natural Science Foundation, China (BK20231468), the Fundamental Research Funds for the Central Universities, China (ZJ24195012) the National Natural Science Foundation in China (31871668), the Jiangsu Key R&D Program, China (BE2022384), the Xinjiang Uygur Autonomous Region Science and Technology Support Program, China (2021E02003), and the Jiangsu Collaborative Innovation Center for Modern Crop Production Project, China (No. 10).

摘要/Abstract

摘要：

根系结构在植物获取水分和养分方面发挥着至关重要的作用，同时在植物适应各种环境胁迫方面扮演关键的角色。本研究利用242份陆地棉材料，研究了棉花幼苗期的6个根系形态特征，包括主根长（MRL）、根系鲜重（RFW）、总根长（TRL）、根表面积（RSA）、根体积（RV）和根平均直径（AvgD）。相关性分析表明，TRL与RSA、RV与RSA和AvgD呈正相关，而TRL与AvgD呈显著负相关。利用实验室前期鉴定的该套材料含56，010个单核苷酸多态性（SNPs）位点的基因型数据，结合根表型数据进行了全基因组关联分析（GWAS）。共鉴定出41个数量性状位点（QTLs），其中与MRL相关的QTL 9个、RFW 6个、TRL 9个、RSA 12个、RV 12个、AvgD 2个。有8个QTLs在两个或多个性状上被重复检测到。结合转录组数据分析，在这些QTLs区间筛选到17个在根组织中高表达（TPM值≥ 30）的候选基因。进一步对一个编码包含WPP结构域、具有调节根系发育功能的候选基因GH_D05G2106进行了功能验证，病毒诱导基因沉默（VIGS）试验表明，降低GH_D05G2106的表达显著抑制棉花根系发育，表明其在根系形态建成中具有正调节作用。研究结果为棉花根系发育生物学和根系相关育种研究提供了理论依据和候选基因。

Abstract:

Root system architecture plays an essential role in water and nutrient acquisition in plants, and it is significantly involved in plant adaptations to various environmental stresses. In this study, a panel of 242 cotton accessions was collected to investigate six root morphological traits at the seedling stage, including main root length (MRL), root fresh weight (RFW), total root length (TRL), root surface area (RSA), root volume (RV), and root average diameter (AvgD). The correlation analysis of the six root morphological traits revealed strong positive correlations of TRL with RSA, as well as RV with RSA and AvgD, whereas a significant negative correlation was found between TRL and AvgD. Subsequently, a genome-wide association study (GWAS) was performed using the root phenotypic and genotypic data reported previously for the 242 accessions using 56,010 single nucleotide polymorphisms (SNPs) from the CottonSNP80K array. A total of 41 quantitative trait loci (QTLs) were identified, including nine for MRL, six for RFW, nine for TRL, 12 for RSA, 12 for RV and two for AvgD. Among them, eight QTLs were repeatedly detected in two or more traits. Integrating these results with a transcriptome analysis, we identified 17 candidate genes with high transcript values of transcripts per million (TPM)≥30 in the roots. Furthermore, we functionally verified the candidate gene GH_D05G2106, which encodes a WPP domain protein 2 in root development. A virus-induced gene silencing (VIGS) assay showed that knocking down GH_D05G2106 significantly inhibited root development in cotton, indicating its positive role in root system architecture formation. Collectively, these results provide a theoretical basis and candidate genes for future studies on cotton root developmental biology and root-related cotton breeding.

Key words: cotton , root-morphology traits , quantitative trait loci , candidate genes , GWAS

Huaxiang Wu, Xiaohui Song, Muhammad Waqas-Amjid, Chuan Chen, Dayong Zhang, Wangzhen Guo. 全基因组关联分析挖掘陆地棉苗期根系形态相关性状优异位点和候选基因[J]. Journal of Integrative Agriculture, 2024, 23(10): 3406-3418.

Huaxiang Wu, Xiaohui Song, Muhammad Waqas-Amjid, Chuan Chen, Dayong Zhang, Wangzhen Guo. Mining elite loci and candidate genes for root morphology-related traits at the seedling stage by genome-wide association studies in upland cotton (Gossypium hirsutum L.) [J]. Journal of Integrative Agriculture, 2024, 23(10): 3406-3418.

参考文献

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, Thyssen G N, Fang D D, Jenkins J N, McCarty J C, Wedegaertner T, Zhang J. 2021. GWAS reveals consistent QTL for drought and salt tolerance in a MAGIC population of 550 lines derived from intermating of 11 upland cotton (Gossypium hirsutum) parents. Molecular Genetics and Genomics, 296, 119–129.

Atkinson J A, Wingen L U, Griffiths M, Pound M P, Gaju O, Foulkes M J, Le Gouis J, Griffiths S, Bennett M J, King J, Wells D M. 2015. Phenotyping pipeline reveals major seedling root growth QTL in hexaploid wheat. Journal of Experimental Botany, 66, 2283–2292.

Awlia M, Alshareef N, Saber N, Korte A, Oakey H, Panzarová K, Trtílek M, Negrão S, Tester M, Julkowska M M. 2021. Genetic mapping of the early responses to salt stress in Arabidopsis thaliana. The Plant Journal, 107, 544–563.

Bac-Molenaar J A, Granier C, Keurentjes J J, Vreugdenhil D. 2016. Genome-wide association mapping of time-dependent growth responses to moderate drought stress in Arabidopsis. Plant, Cell and Environment, 39, 88–102.

Bouain N, Korte A, Satbhai S B, Nam H I, Rhee S Y, Busch W, Rouached H. 2019. Systems genomics approaches provide new insights into Arabidopsis thaliana root growth regulation under combinatorial mineral nutrient limitation. PLoS Genetics, 15, e1008392.

Bruce W, Desbons P, Crasta O, Folkerts O. 2001. Gene expression profiling of two related maize inbred lines with contrasting root-lodging traits. Journal of Experimental Botany, 52, 459–468.

Cai C, Wang X, Zhang B, Guo W. 2019. Tobacco rattle virus-induced gene silencing in cotton. Methods in Molecular Biology, 1902, 105–119.

Cai C, Zhu G, Zhang T, Guo W. 2017. High-density 80K SNP array is a powerful tool for genotyping G. hirsutum accessions and genome analysis. BMC Genomics, 18, 654.

Chen J, Liu L, Wang Z, Sun H, Zhang Y, Lu Z, Li C. 2018. Determining the effects of nitrogen rate on cotton root growth and distribution with soil cores and minirhizotrons. PLoS ONE, 13, e0197284.

Chen Y, Liu Z H, Feng L, Zheng Y, Li D D, Li X B. 2013. Genome-wide functional analysis of cotton (Gossypium hirsutum) in response to drought. PLoS ONE, 8, e80879.

Comas L H, Becker S R, Cruz V M, Byrne P F, Dierig D A. 2013. Root traits contributing to plant productivity under drought. Frontiers in Plant Science, 4, 442.

Comas L H, Mueller K E, Taylor L L, Midford P E, Callahan H S, Beerling D J 2012. Evolutionary patterns and biogeochemical significance of angiosperm root traits. International Journal of Plant Sciences, 173, 584–595.

Cui Z, Liu S, Ge C, Shen Q, Zhang S, Ma H, Liu R, Zhao X, Liu R, Li P, Wang H, Wu Q, Pang C, Chen J. 2022. Genome-wide association study reveals that GhTRL1 and GhPIN8 affect cotton root development. Theoretical and Applied Genetics, 135, 3161–3176.

El-Soda M, Kruijer W, Malosetti M, Koornneef M, Aarts M G. 2015. Quantitative trait loci and candidate genes underlying genotype by environment interaction in the response of Arabidopsis thaliana to drought. Plant, Cell and Environment, 38, 585–599.

Eroglu S, Aksoy E. 2017. Genome-wide analysis of gene expression profiling revealed that COP9 signalosome is essential for correct expression of Fe homeostasis genes in Arabidopsis. Biometals, 30, 685–698.

Falik O, Mordoch Y, Ben-Natan D, Vanunu M, Goldstein O, Novoplansky A. 2012. Plant responsiveness to root–root communication of stress cues. Annals of Botany, 110, 271–280.

Feng L, Xu W, Tang G, Gu M, Geng Z. 2021. Biochar induced improvement in root system architecture enhances nutrient assimilation by cotton plant seedlings. BMC Plant Biology, 21, 269.

Goyal P, Devi R, Verma B, Hussain S, Arora P, Tabassum R, Gupta S. 2023. WRKY transcription factors: Evolution, regulation, and functional diversity in plants. Protoplasma, 260, 331–348.

Hernández E I, Vilagrosa A, Pausas J G, Bellot J. 2010. Morphological traits and water use strategies in seedlings of Mediterranean coexisting species. Plant Ecology, 207, 233–244.

Hirel B, Le Gouis J, Ney B, Gallais A. 2007. The challenge of improving nitrogen use efficiency in crop plants: Towards a more central role for genetic variability and quantitative genetics within integrated approaches. Journal of Experimental Botany, 58, 2369–2387.

Hu D, He S, Jia Y, Nazir M F, Sun G, Geng X, Pan Z, Wang L, Chen B, Li H, Ge Y, Pang B, Du X. 2022. Genome-wide association study for seedling biomass-related traits in Gossypium arboreum L. BMC Plant Biology, 22, 54.

Hu Y, Chen J, Fang L, Zhang Z, Ma W, Niu Y, Ju L, Deng J, Zhao T, Lian J, Baruch K, Fang D, Liu X, Ruan Y L, Rahman M U, Han J, Wang K, Wang Q, Wu H, Mei G, et al. 2019. Gossypium barbadense and Gossypium hirsutum genomes provide insights into the origin and evolution of allotetraploid cotton. Nature Genetics, 51, 739–748.

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. Genes Genomes Genetics, 5, 1187–1209.

Irizarry I, White J F. 2017. Application of bacteria from non-cultivated plants to promote growth, alter root architecture and alleviate salt stress of cotton. Journal of Applied Microbiology, 122, 1110–1120.

Jha P, Ochatt S J, Kumar V. 2020. WUSCHEL: A master regulator in plant growth signaling. Plant Cell Reports, 39, 431–444.

Kabir M R, Liu G, Guan P, Wang F, Khan A A, Ni Z, Yao Y, Hu Z, Xin M, Peng H, Sun Q. 2015. Mapping QTLs associated with root traits using two different populations in wheat (Triticum aestivum L.). Euphytica, 206, 175–190.

Kobayashi Y, Sadhukhan A, Tazib T, Nakano Y, Kusunoki K, Kamara M, Chaffai R, Iuchi S, Sahoo L, Kobayashi M, Hoekenga O A, Koyama H. 2016. Joint genetic and network analyses identify loci associated with root growth under NaCl stress in Arabidopsis thaliana. Plant, Cell and Environment, 39, 918–934.

Li B, Chen L, Sun W, Wu D, Wang M, Yu Y, Chen G, Yang W, Lin Z, Zhang X, Duan L, Yang X. 2020. Phenomics-based GWAS analysis reveals the genetic architecture for drought resistance in cotton. Plant Biotechnology Journal, 18, 2533–2544.

Li W, Lan P. 2015. Genome-wide analysis of overlapping genes regulated by iron deficiency and phosphate starvation reveals new interactions in Arabidopsis roots. BMC Research Notes, 8, 555.

Liang Q, Li P, Hu C, Hua H, Li Z, Rong Y, Wang K, Hua J. 2014. Dynamic QTL and epistasis analysis on seedling root traits in upland cotton. Journal of Genetics, 93, 63–78.

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.

Luo Z, Kong X, Zhang Y, Li W, Zhang D, Dai J, Fang S, Chu J, Dong H. 2019a. Leaf-derived jasmonate mediates water uptake from hydrated cotton roots under partial root-zone irrigation. Plant Physiology, 180, 1660–1676.

Luo Z, Xin C S, Li W J, Zhang D M, Dong H Z. 2019b. Effects of partial root-zone irrigation and rational close planting on yield and water productivity of cotton in arid area. The Journal of Applied Ecology, 30, 3137–3144.

Ma J, Zhao D, Tang X, Yuan M, Zhang D, Xu M, Duan Y, Ren H, Zeng Q, Wu J, Han D, Li T, Jiang L. 2022. Genome-wide association study on root system architecture and identification of candidate genes in wheat (Triticum aestivum L.). International Journal of Molecular Sciences, 23, 1843.

Mai W, Xue X, Feng G, Tian C. 2018. Simultaneously maximizing root/mycorrhizal growth and phosphorus uptake by cotton plants by optimizing water and phosphorus management. BMC Plant Biology, 18, 334.

Mandozai A, Moussa A A, Zhang Q, Qu J, Du Y, Anwari G, Al Amin N, Wang P. 2021. Genome-wide association study of root and shoot related traits in spring soybean (Glycine max L.) at seedling stages using SLAF-Seq. Frontiers in Plant Science, 12, 568995.

Meister R, Rajani M S, Ruzicka D, Schachtman D P. 2014. Challenges of modifying root traits in crops for agriculture. Trends in Plant Science, 19, 779–788.

Moussa A A, Mandozai A, Jin Y, Qu J, Zhang Q, Zhao H, Anwari G, Khalifa M A S, Lamboro A, Noman M, Bakasso Y, Zhang M, Guan S, Wang P. 2021. Genome-wide association screening and verification of potential genes associated with root architectural traits in maize (Zea mays L.) at multiple seedling stages. BMC Genomics, 22, 558.

Neto J B D A, Hurtado-Perez M C, Wimmer M A, Frei M. 2017. Genetic factors underlying boron toxicity tolerance in rice: Genome-wide association study and transcriptomic analysis. Journal of Experimental Botany, 68, 687–700.

Nicotra A, Babicka N, Westoby M. 2002. Seedling root anatomy and morphology: An examination of ecological differentiation with rainfall using phylogenetically independent contrasts. Oecologia, 130, 136–145.

Pace J, Gardner C, Romay C, Ganapathysubramanian B, Lübberstedt T. 2015. Genome-wide association analysis of seedling root development in maize (Zea mays L.). BMC Genomics, 16, 47.

Park C, Lim C W, Baek W, Kim J H, Lim S, Kim S H, Kim K N, Lee S C. 2017. The pepper WPP domain protein, CaWDP1, acts as a novel negative regulator of drought stress via ABA signaling. Plant and Cell Physiology, 58, 779–788.

Patel S, Rose A, Meulia T, Dixit R, Cyr R J, Meier I. 2004. Arabidopsis WPP-domain proteins are developmentally associated with the nuclear envelope and promote cell division. The Plant Cell, 16, 3260–3273.

Petrarulo M, Marone D, Ferragonio P, Cattivelli L, Rubiales D, De Vita P, Mastrangelo A M. 2015. Genetic analysis of root morphological traits in wheat. Molecular Genetics and Genomics, 290, 785–806.

Qian H, Lu H, Ding H, Lavoie M, Li Y, Liu W, Fu Z. 2015. Analyzing Arabidopsis thaliana root proteome provides insights into the molecular bases of enantioselective imazethapyr toxicity. Scientific Reports, 5, 11975.

Ren W L, Wen Y J, Dunwell J M, Zhang Y M. 2018. pKWmEB: Integration of Kruskal-Wallis test with empirical Bayes under polygenic background control for multi-locus genome-wide association study. Heredity, 120, 208–218.

Ristova D, Busch W. 2017. Genome-wide association mapping of root traits in the context of plant hormone research. Methods in Molecular Biology, 1497, 47–55.

Rose A, Meier I. 2001. A domain unique to plant RanGAP is responsible for its targeting to the plant nuclear rim. Proceedings of the National Academy of Sciences of the United States of America, 98, 15377–15382.

Santisree P, Nongmaithem S, Sreelakshmi Y, Ivanchenko M, Sharma R. 2012. The root as a drill: An ethylene–auxin interaction facilitates root penetration in soil. Plant Signal Behavior, 7, 151–156.

Satbhai S B, Göschl C, Busch W. 2017. Automated high-throughput root phenotyping of Arabidopsis thaliana under nutrient deficiency conditions. Methods in Molecular Biology, 1610, 135–153.

Seck W, Torkamaneh D, Belzile F. 2020. Comprehensive genome-wide association analysis reveals the genetic basis of root system architecture in soybean. Frontiers in Plant Science, 11, 590740.

Sertse D, You F M, Ravichandran S, Cloutier S. 2019. The complex genetic architecture of early root and shoot traits in flax revealed by genome-wide association analyses. Frontiers in Plant Science, 10, 1483.

Sharma R, Singh G, Bhattacharya S, Singh A. 2018. Comparative transcriptome meta-analysis of Arabidopsis thaliana under drought and cold stress. PLoS ONE, 13, e0203266.

Snapp S, Koide R, Lynch J. 1995. Exploitation of localized phosphorus patches by common bean roots. Plant and Soil, 177, 211–218.

Song X, Zhu G, Hou S, Ren Y, Amjid M W, Li W, Guo W. 2021. Genome-wide association analysis reveals loci and candidate genes involved in fiber quality traits under multiple field environments in cotton (Gossypium hirsutum). Frontiers in Plant Science, 12, 695503.

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.

Sun S, Han B, Chen L, Sun W, Zhang X, Yang X. 2022. Root system architecture analysis and genome-wide association study of root system architecture related traits in cotton. Acta Agronomica Sinica, 48, 1081–1090. (in Chinese)

Sun Z, Wang X, Liu Z, Gu Q, Zhang Y, Li Z, Ke H, Yang J, Wu J, Wu L, Zhang G, Zhang C, Ma Z. 2018. A genome-wide association study uncovers novel genomic regions and candidate genes of yield-related traits in upland cotton. Theoretical and Applied Genetics, 131, 2413–2425.

Sureshkumar V, Dutta B, Kumar V, Prakash G, Mishra D C, Chaturvedi K K, Rai A, Sevanthi A M, Solanke A U. 2019. RiceMetaSysB: A database of blast and bacterial blight responsive genes in rice and its utilization in identifying key blast-resistant WRKY genes. Database (Oxford), 2019, baz015.

Szick-Miranda K, Zanial A S, Zanial A S, Abidayo S, Slater K L C. 2010. Analysis of RPS15aE, an isoform of a plant-specific evolutionarily distinct ribosomal protein in Arabidopsis thaliana, reveals its potential role as a growth regulator. Plant Molecular Biology Reporter, 28, 239–252.

Tamba C L, Ni Y L, Zhang Y M. 2017. Iterative sure independence screening EM-Bayesian LASSO algorithm for multi-locus genome-wide association studies. PLoS Computational Biology, 13, e1005357.

Uga Y, Sugimoto K, Ogawa S, Rane J, Ishitani M, Hara N, Kitomi Y, Inukai Y, Ono K, Kanno N, Inoue H, Takehisa H, Motoyama R, Nagamura Y, Wu J, Matsumoto T, Takai T, Okuno K, Yano M. 2013. Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nature Genetics, 45, 1097–1102.

Waidmann S, Ruiz Rosquete M, Schöller M, Sarkel E, Lindner H, LaRue T, Petřík I, Dünser K, Martopawiro S, Sasidharan R, Novak O, Wabnik K, Dinneny J R, Kleine-Vehn J. 2019. Cytokinin functions as an asymmetric and anti-gravitropic signal in lateral roots. Nature Communications, 10, 3540.

Wang C, Lu W, He X, Wang F, Zhou Y, Guo X, Guo X. 2016. The cotton mitogen-activated protein kinase Kinase 3 functions in drought tolerance by regulating stomatal responses and root growth. Plant and Cell Physiology, 57, 1629–1642.

Wang F, Longkumer T, Catausan S C, Calumpang C L F, Tarun J A, Cattin-Ortola J, Ishizaki T, Pariasca Tanaka J, Rose T, Wissuwa M, Kretzschmar T. 2018. Genome-wide association and gene validation studies for early root vigour to improve direct seeding of rice. Plant, Cell and Environment, 41, 2731–2743.

Wang S B, Feng J Y, Ren W L, Huang B, Zhou L, Wen Y J, Zhang J, Dunwell J M, Xu S, Zhang Y M. 2016. Improving power and accuracy of genome-wide association studies via a multi-locus mixed linear model methodology. Scientific Reports, 6, 19444.

Wang X, Zhang Y, Wang L, Pan Z, He S, Gao Q, Chen B, Gong W, Du X. 2020. Casparian strip membrane domain proteins in Gossypium arboreum: Genome-wide identification and negative regulation of lateral root growth. BMC Genomics, 21, 340.

Wasson A P, Richards R A, Chatrath R, Misra S C, Prasad S V, Rebetzke G J, Kirkegaard J A, Christopher J, Watt M. 2012. Traits and selection strategies to improve root systems and water uptake in water-limited wheat crops. Journal of Experimental Botany, 63, 3485–3498.

Wen Y J, Zhang H, Ni Y L, Huang B, Zhang J, Feng J Y, Wang S B, Dunwell J M, Zhang Y M, Wu R. 2018. Methodological implementation of mixed linear models in multi-locus genome-wide association studies. Briefings in Bioinformatics, 19, 700–712.

Wintermans P C, Bakker P A, Pieterse C M. 2016. Natural genetic variation in Arabidopsis for responsiveness to plant growth-promoting rhizobacteria. Plant Molecular Biology, 90, 623–634.

Xiao Y, Chen Y, Ding Y, Wu J, Wang P, Yu Y, Wei X, Wang Y, Zhang C, Li F, Ge X. 2018. Effects of GhWUS from upland cotton (Gossypium hirsutum L.) on somatic embryogenesis and shoot regeneration. Plant Science, 270, 157–165.

Xu P, Guo Q, Meng S, Zhang X, Xu Z, Guo W, Shen X. 2021. Genome-wide association analysis reveals genetic variations and candidate genes associated with salt tolerance related traits in Gossypium hirsutum. BMC Genomics, 22, 26.

Zaidi P H, Seetharam K, Krishna G, Krishnamurthy L, Gajanan S, Babu R, Zerka M, Vinayan M T, Vivek B S. 2016. Genomic regions associated with root traits under drought stress in tropical maize (Zea mays L.). PLoS ONE, 11, e0164340.

Zhang H, San M L, Jang S G, Lee J H, Kim N E, Lee A R, Park S Y, Cao F Y, Chin J H, Kwon S W. 2020. Genome-wide association study of root system development at seedling stage in rice. Genes, 11, 1395.

Zhang J, Feng J Y, Ni Y L, Wen Y J, Niu Y, Tamba C L, Yue C, Song Q, Zhang Y M. 2017. pLARmEB: Integration of least angle regression with empirical Bayes for multilocus genome-wide association studies. Heredity, 118, 517–524.

Zhang Y W, Tamba C L, Wen Y J, Li P, Ren W L, Ni Y L, Gao J, Zhang Y M. 2020. mrMLM v4.0.2: An R platform for multi-locus genome-wide association studies. Genomics, Proteomics and Bioinformatics, 18, 481–487.

Zhao P, Qin T, Chen W, Sang X, Zhao Y, Wang H. 2021. Genome-wide study of NOT2_3_5 protein subfamily in cotton and their necessity in resistance to Verticillium wilt. International Journal of Molecular Sciences, 22, 5634.

Zhao Z, Hu D, Azhar M T, Li H, Ma C, He S, Wang X, Sun G, Mahmood T, Dev W, Du X. 2021. Genome-wide association and transcriptome analysis of root color-related genes in Gossypium arboreum L. Planta, 253, 95.

Zheng J, Zhang Z, Gong Z, Liang Y, Sang Z, Xu Y, Li X, Wang J. 2021. Genome-wide association analysis of salt-tolerant traits in terrestrial cotton at seedling stage. Plants, 11, 97.

Zhu G, Hou S, Song X, Wang X, Wang W, Chen Q, Guo W. 2021. Genome-wide association analysis reveals quantitative trait loci and candidate genes involved in yield components under multiple field environments in cotton (Gossypium hirsutum). BMC Plant Biology, 21, 250.

全基因组关联分析挖掘陆地棉苗期根系形态相关性状优异位点和候选基因

Mining elite loci and candidate genes for root morphology-related traits at the seedling stage by genome-wide association studies in upland cotton (Gossypium hirsutum L.)

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