Abstract
Nulliplex branch is a key architectural trait in sea-island cotton (Gossypium barbadense L.), but its genetic basis is not well understood. Here we investigated the genetic basis of the nulliplex-branch trait in cotton by combining newly created bulked segregant analysis (BSA)-seq data, published RNA-seq data, and published whole-genome resequencing (WGR) data. We delimited the nulliplex-branch locus (qD07-NB) to D07, region 14.8–17.1 Mb, using various BSA methods and markers. We integrated our BSA data with WGR data of sea-island cotton varieties and detected a missense single-nucleotide polymorphism in the candidate gene (Gbar_D07G011870) of qD07-NB. This gene was under positive selection during sea-island cotton breeding in the **njiang Uygur Autonomous Region, China. Notably, the nulliplex-branch varieties possessed a better fiber quality than the long-branch varieties, and a set of high-quality molecular markers was identified for molecular breeding of the nulliplex-branch trait in cotton. We combined BSA-seq and RNA-seq data to compare gene expression profiles between two elite sea-island cotton varieties during three developmental stages. We identified eleven relevant candidate genes, five downregulated and six upregulated, in the qD07-NB locus. This research will expand our understanding of the genetic basis of the nulliplex-branch trait and provide guidance for architecture-focused breeding in cotton.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11032-021-01229-w/MediaObjects/11032_2021_1229_Fig1_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11032-021-01229-w/MediaObjects/11032_2021_1229_Fig2_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11032-021-01229-w/MediaObjects/11032_2021_1229_Fig3_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11032-021-01229-w/MediaObjects/11032_2021_1229_Fig4_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11032-021-01229-w/MediaObjects/11032_2021_1229_Fig5_HTML.png)
Similar content being viewed by others
Data availability
All relevant data can be found within the manuscript and its supporting materials.
References
Abe A, Kosugi S, Yoshida K, Natsume S, Takagi H, Kanzaki H, Matsumura H, Yoshida K, Mitsuoka C, Tamiru M, Innan H, Cano L, Kamoun S, Terauchi R (2012) Genome sequencing reveals agronomically important loci in rice using MutMap. Nat Biotechnol 30(2):174–178
Alonge M, Wang X, Benoit M, Soyk S, Pereira L, Zhang L, Suresh H, Ramakrishnan S, Maumus F, Ciren D, Levy Y, Harel TH, Shalev-Schlosser G, Amsellem Z, Razifard H, Caicedo AL, Tieman DM, Klee H, Kirsche M, Aganezov S, Ranallo-Benavidez TR, Lemmon ZH, Kim J, Robitaille G, Kramer M, Goodwin S, McCombie WR, Hutton S, Van Eck J, Gillis J, Eshed Y, Sedlazeck FJ, van der Knaap E, Schatz MC, Lippman ZB (2020) Major impacts of widespread structural variation on gene expression and crop improvement in tomato. Cell 182(1):145–161
Anders S, Pyl PT, Huber W (2015) HTSeq-a Python framework to work with high-throughput sequencing data. Bioinformatics 31(2):166–169
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30(15):2114–2120
Browning SR, Browning BL (2007) Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. Am J Hum Genet 81(5):1084–1097
Chen W, Yao J, Chu L, Yuan Z, Li Y, Zhang Y (2015) Genetic map** of the nulliplex-branch gene (gb_nb1) in cotton using next-generation sequencing. Theor Appl Genet 128(3):539–547
Chen F, Jia H, Zhang X, Qiao L, Li X, Zheng J, Guo H, Powers C, Yan L, Chang Z (2019a) Positional cloning of PmCH1357 reveals the origin and allelic variation of the Pm2 gene for powdery mildew resistance in wheat. Crop J 7(6):771–783
Chen W, Yao J, Li Y, Zhao L, Liu J, Guo Y, Wang J, Yuan L, Liu Z, Lu Y, Zhang Y (2019b) Nulliplex-branch, a TERMINAL FLOWER 1 ortholog, controls plant growth habit in cotton. Theor Appl Genet 132:97–112
Cingolani P, Platts A, Wang L, Coon M, Nguyen T, Wang L, Land SJ, Lu X, Ruden DM (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(2):80–92
Constable GA, Bange MP (2015) The yield potential of cotton (Gossypium hirsutum L.). Field Crops Res 182:98–106
Dai J, Dong H (2014) Intensive cotton farming technologies in China: achievements, challenges and countermeasures. Field Crops Res 155:99–110
Dai J, Kong X, Zhang D, Li W, Dong H (2017) Technologies and theoretical basis of light and simplified cotton cultivation in China. Field Crops Res 214:142–148
Dai X, He C, Zhou L, Liang M, Fu X, Qin P, Yang Y, Chen L (2018) Identification of a specific molecular marker for the rice blast-resistant gene Pigm and molecular breeding of thermo-sensitive genic male sterile leaf-color marker lines. Mol Breeding 38(6):72
Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, Handsaker RE, Lunter G, Marth GT, Sherry ST, McVean G, Durbin R, 100 Genomes Project Analysis Group (2011) The variant call format and VCFtools. Bioinformatics 27(15):2156–2158
Di J, Chen X, Zhao L (2014) Genetic research and breeding evaluation on short branch trait of Gossypium hirsutum L. China Cotton 41(11):5–7
Doebley J, Stec A, Hubbard L (1997) The evolution of apical dominance. Nature 386(3):485–488
Du X (1996) Unification of fruit branch type division of cotton. China Cotton 23(4):19
Geng H, Zhang Y, He Z, Zhang L, Appels R, Qu Y, **a X (2011) Molecular markers for tracking variation in lipoxygenase activity in wheat breeding. Mol Breeding 28(1):117–126
Guo W, Chen L, Herrera-Estrella L, Cao D, Tran LP (2020) Altering plant architecture to improve performance and resistance. Trends Plant Sci 25(11):1154–1170
Hu M, Lv S, Wu W, Fu Y, Zhu Z (2018) The domestication of plant architecture in African rice. Plant J 94:661–669
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 YL, Rahman MU, Han J, Wang K, Wang Q, Wu H, Mei G, Zang Y, Han Z, Xu C, Shen W, Yang D, Si Z, Dai F, Zou L, Huang F, Bai Y, Zhang Y, Brodt A, Ben-Hamo H, Zhu X, Zhou B, Guan X, Zhu S, Chen X, Zhang T (2019) Gossypium barbadense and Gossypium hirsutum genomes provide insights into the origin and evolution of allotetraploid cotton. Nat Genet 51(4):739–748
Huang L, Tang W, Bu S, Wu W (2020) BRM: a statistical method for QTL map** based on bulked segregant analysis by deep sequencing. Bioinformatics 36(7):2150–2156
Kaggwa-Asiimwea R, Andrade-Sanchez P, Wang G (2013) Plant architecture influences growth and yield response of upland cotton to population density. Field Crops Res 145:52–59
Kulwal PL (2018) Trait map** approaches through linkage map** in plants. In: Varshney RK, Pandey MK, Chitikineni A (eds) Plant genetics and molecular biology. Springer International Publishing, Cham, pp 53–82
Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25(14):1754–1760
Li H, Li J, Song J, Zhao B, Guo C, Wang B, Zhang Q, Wang J, King GJ, Liu K (2019) An auxin signaling gene BnaA3.IAA7 contributes to improved plant architecture and yield heterosis in rapeseed. New Phytol 222:837–851
Liu M, Shi Z, Zhang X, Wang M, Zhang L, Zheng K, Liu J, Hu X, Di C, Qian Q, He Z, Yang DL (2019) Inducible overexpression of Ideal Plant Architecture1 improves both yield and disease resistance in rice. Nat Plants 5(4):389–400
McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo MA (2010) The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20(9):1297–1303
Michelmore RW, Paran I, Kesseli RV (1991) Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc Natl Acad Sci USA 88:9828–9832
Moraes TS, Dornelas MC, Martinelli AP (2019) FT/TFL1: calibrating plant architecture. Front Plant Sci 10:97
Nie X, Wen T, Shao P, Tang B, Nuriman-Guli A, Yu Y, Du X, You C, Lin Z (2020) High-density genetic variation maps reveal the correlation between asymmetric interspecific introgressions and improvement of agronomic traits in Upland and Pima cotton varieties developed in **njiang, China. Plant J 103(2):677–689
Pickrell JK, Marioni JC, Pai AA, Degner JF, Engelhardt BE, Nkadori E, Veyrieras JB, Stephens M, Gilad Y, Pritchard JK (2010) Understanding mechanisms underlying human gene expression variation with RNA sequencing. Nature 464(7289):768–772
Reinhardt D, Kuhlemeier C (2002) Plant architecture. EMBO Rep 3(9):846–851
Ren X, Zhang L, Du M, Evers JB, van der Werf W, Tian XL, Li ZH (2013) Managing mepiquat chloride and plant density for optimal yield and quality of cotton. Field Crop Res 149(2):1–10
Schlötterer C, Tobler R, Kofler R, Nolte V (2014) Sequencing pools of individuals - mining genome-wide polymorphism data without big funding. Nat Rev Genet 15(11):749–763
Si Z, Liu H, Zhu J, Chen J, Wang Q, Fang L, Gao F, Tian Y, Chen Y, Chang L, Liu B, Han Z, Zhou B, Hu Y, Huang X, Zhang T (2018) Mutation of SELF-PRUNING homologs in cotton promotes short-branching plant architecture. J Exp Bot 69(10):2543–2553
Song X, Zhang T (2009) Quantitative trait loci controlling plant architectural traits in cotton. Plant Sci 177(4):317–323
Soyk S, Lemmon ZH, Oved M, Fisher J, Liberatore KL, Park SJ, Goren A, Jiang K, Ramos A, van der Knaap E, Van Eck J, Zamir D, Eshed Y, Lippman ZB (2017) Bypassing negative epistasis on yield in tomato imposed by a domestication gene. Cell 169(6):1142–1155
Su JJ, Li LB, Zhang C, Wang CX, Gu LJ, Wang HT, Wei HL, Liu QB, Huang L, Yu SX (2018) Genome-wide association study identified genetic variations and candidate genes for plant architecture component traits in Chinese upland cotton. Theor Appl Genet 131:1299–1314
Sun Q, Du X, ChaoweiCai LL, Zhang S, Qiao P, Wang W, Zhou K, Wang G, Liu X, Zhang H, Geng S, Yang C, Gao W, Mo J, Miao C, Song C, Cai Y (2016) To be a flower or fruiting branch insights revealed by mRNA and small RNA transcriptomes from different cotton developmental stages. Sci Rep 6:23212
Sun Z, Su C, Yun J, Jiang Q, Wang L, Wang Y, Cao D, Zhao F, Zhao Q, Zhang M, Zhou B, Zhang L, Kong F, Liu B, Tong Y, Li X (2019) Genetic improvement of the shoot architecture and yield in soybean plants via the manipulation of GmmiR156b. Plant Biotechnol J 17:50–62
Takagi H, Abe A, Yoshida K, Kosugi S, Natsume S, Mitsuoka C, Uemura A, Utsushi H, Tamiru M, Takuno S, Innan H, Cano LM, Kamoun S, Terauchi R (2013) QTL-seq: rapid map** of quantitative trait loci in rice by whole genome resequencing of DNA from two bulked populations. Plant J 74(1):174–183
Tian J, Wang C, **a J, Wu L, Xu G, Wu W, Li D, Qin W, Han X, Chen Q, ** W, Tian F (2019) Teosinte ligule allele narrows plant architecture and enhances high-density maize yields. Science 365:658–664
Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25(9):1105–1111
Wang M, Wang P, Tu L, Zhu S, Zhang L, Li Z, Zhang Q, Yuan D, Zhang X (2016) Multi-omics maps of cotton fibre reveal epigenetic basis for staged single-cell differentiation. Nucleic Acids Res 44(9):4067–4079
Wang B, Smith SM, Li J (2018a) Genetic regulation of shoot architecture. Annu Rev Plant Biol 69:437–468
Wang P, Zhang J, Sun L, Ma Y, Xu J, Liang S, Deng J, Tan J, Zhang Q, Tu L, Daniell H, ** S, Zhang X (2018b) High efficient multisites genome editing in allotetraploid cotton (Gossypium hirsutum) using CRISPR/Cas9 system. Plant Biotechnol J 16:137–150
Wang C, Tang S, Zhan Q, Hou Q, Zhao Y, Zhao Q, Feng Q, Zhou C, Lyu D, Cui L, Li Y, Miao J, Zhu C, Lu Y, Wang Y, Wang Z, Zhu J, Shangguan Y, Gong J, Yang S, Wang W, Zhang J, ** informs a rice-improvement strategy. Nat Commun 10(1):2982
Wang M, Tu L, Yuan D, Zhu D, Shen C, Li J, Liu F, Pei L, Wang P, Zhao G, Ye Z, Huang H, Yan F, Ma Y, Zhang L, Liu M, You J, Yang Y, Liu Z, Huang F, Li B, Qiu P, Zhang Q, Zhu L, ** S, Yang X, Min L, Li G, Chen L-L, Zheng H, Lindsey K, Lin Z, Udall JA, Zhang X (2019b) Reference genome sequences of two cultivated allotetraploid cottons, Gossypium hirsutum and Gossypium barbadense. Nat Genet 51:224–229
Wen T, Wu M, Shen C, Gao B, Zhu D, Zhang X, You C, Lin Z (2018) Linkage and association map** reveals the genetic basis of brown fibre (Gossypium hirsutum). Plant Biotechnol J 16:1654–1666
Wen T, Dai B, Wang T, Liu X, You C, Lin Z (2019) Genetic variations in plant architecture traits in cotton (Gossypium hirsutum) revealed by a genome-wide association study. Crop J 7:209–216
Wen T, Yao T, You C, Lin Z (2020) A case study of a micro-inversion event in dark brown fibre cotton (Gossypium hirsutum). Crop J 8(4):577–585
Wray GA (2007) The evolutionary significance of cis-regulatory mutations. Nat Rev Genet 8(3):206–216
Xu Y, Li ZK, Thomson MJ (2012) Molecular breeding in plants: moving into the mainstream. Mol Breeding 29(4):831–832
Xu Y, Li P, Yang Z, Xu C (2017) Genetic map** of quantitative trait loci in crops. Crop J 5(2):175–184
Yan W, Du M, Zhao W, Li F, Wang X, Eneji AE, Yang F, Huang J, Meng L, Qi H, Xue G, Xu D, Tian X, Li Z (2019) Relationships between plant architecture traits and cotton yield within the plant height range of 80–120 cm desired for mechanical harvesting in the Yellow River Valley of China. Agronomy 9:587
Ye S, Tian C, Liu F, Lu X, Han W, Qi M, Zhang Y, Qiu P, Wu D (2018) Study on the value of early fruiting cotton with limited fruit branches in Changjiang River Basin. China Cotton 45(8):20–23
Zhang X, Wang W, Guo N, Zhang Y, Bu Y, Zhao J, ** to fine map a wild soybean allele characteristic of greater plant height. BMC Genomics 19(1):226
Zhang H, Wang X, Pan Q, Li P, Liu Y, Lu X, Zhong W, Li M, Han L, Li J, Wang P, Li D, Liu Y, Li Q, Yang F, Zhang YM, Wang G, Li L (2019) QTG-seq accelerates QTL fine map** through QTL partitioning and whole-genome sequencing of bulked segregant samples. Mol Plant 12(3):426–437
Zhu J, Chen J, Gao F, Xu C, Wu H, Chen K, Si Z, Yan H, Zhang T (2017) Rapid map** and cloning of the virescent-1 gene in cotton by bulked segregant analysis-next generation sequencing and virus-induced gene silencing strategies. J Exp Bot 68(15):4125–4135
Acknowledgements
We would like to acknowledge Prof. Zhongxu Lin in Huazhong Agricultural University for providing a platform to analyze the BSA-seq data.
Funding
This work was supported by the National Natural Science Foundation of China (Grant no. 31460362) and Science and Technology Research Project of the Education Department of Jiangxi Province, China (Grant no. GJJ200440).
Author information
Authors and Affiliations
Contributions
Liangrong He designed this program and performed the experiment. Feiyu Tang and Mengxing Wang revised the manuscript. Tianwang Wen analyzed the data and drafted the manuscript. Chunyan Liu and Tianyou Wang conducted the field investigation. All the authors read and approved the final version of the manuscript.
Corresponding authors
Ethics declarations
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.
Tianwang Wen and Chunyan Liu are co-first authors.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Wen, T., Liu, C., Wang, T. et al. Genomic map** and identification of candidate genes encoding nulliplex-branch trait in sea-island cotton (Gossypium barbadense L.) by multi-omics analysis. Mol Breeding 41, 34 (2021). https://doi.org/10.1007/s11032-021-01229-w
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11032-021-01229-w