Abstract
Key message
GhAP genes were identified as the candidates involved in cotton fiber length under the scope of fine mapping a stable fiber length QTL, qFLD05. Moreover, the transcription factor GhWRKY40 positively regulated GhAP3 to decrease fiber length.
Abstract
Fiber length (FL) is an economically important fiber quality trait. Although several genes controlling cotton fiber development have been identified, our understanding of this process remains limited. In this study, an FL QTL (qFLD05) was fine-mapped to a 216.9-kb interval using a secondary F2:3 population derived from the upland hybrid cultivar Ji1518. This mapped genomic segment included 15 coding genes, four of which were annotated as aspartyl proteases (GhAP1-GhAP4). GhAPs were identified as candidates for qFLD05 as the sequence variations in GhAPs were associated with FL deviations in the mapping population, and functional validation of GhAP3 and GhAP4 indicated a longer FL following decreases in their expression levels through virus-induced gene silencing (VIGS). Subsequently, the potential involvement of GhWRKY40 in the regulatory network was revealed: GhWRKY40 positively regulated GhAP3’s expression according to transcriptional profiling, VIGS, yeast one-hybrid assays and dual-luciferase experiments. Furthermore, alterations in the expression of the eight previously reported cotton FL-responsive genes from the above three VIGS lines (GhAP3, GhAP4 and GhWRKY40) implied that MYB5_A12 was involved in the GhWRKY40-GhAP network. In short, we unveiled the unprecedented FL regulation roles of GhAPs in cotton, which was possibly further regulated by GhWRKY40. These findings will reveal the genetic basis of FL development associated with qFLD05 and be beneficial for the marker-assisted selection of long-staple cotton.
Similar content being viewed by others
Data availability
The BSA-seq data can be found at NCBI under the accession PRJNA1019498 (https://www.ncbi.nlm.nih.gov/bioproject/PRJNA1019498/).
References
Abe A, Kosugi S, Yoshida K, Natsume S, Takagi H, Kanzaki H et al (2012) Genome sequencing reveals agronomically important loci in rice using MutMap. Nat Biotechnol 30(2):174–178. https://doi.org/10.1038/nbt.2095
Cao Z, Zhu X, Chen H, Zhang T (2015) Fine mapping of clustered quantitative trait loci for fiber quality on chromosome 7 using a Gossypium barbadense introgressed line. Mol Breed 35:1–13. https://doi.org/10.1007/s11032-015-0393-3
Cao S, Guo M, Cheng J, Cheng H, Liu X, Ji H et al (2022) Aspartic proteases modulate programmed cell death and secondary cell wall synthesis during wood formation in poplar. J Exp Bot 73(19):6876–6890. https://doi.org/10.1093/jxb/erac347
Chen H, Huang Y, Huang G, Huang S, Chow T, Lin Y (2015) Sweet potato SPAP1 is a typical aspartic protease and participates in ethephon-mediated leaf senescence. J Plant Physiol 180:1–17. https://doi.org/10.1016/j.jplph.2015.03.009
Chen H, Han Z, Ma Q, Dong C, Ning X, Li J et al (2022) Identification of elite fiber quality loci in upland cotton based on the genotyping-by-target-sequencing technology. Front Plant Sci 13:1027806. https://doi.org/10.3389/fpls.2022.1027806
Contour-Ansel D, Torres-Franklin M, Zuily-Fodil Y, Cruz de Carvalho M (2010) An aspartic acid protease from common bean is expressed ‘on call’ during water stress and early recovery. J Plant Physiol 167(18):1606–1612. https://doi.org/10.1016/j.jplph.2010.06.018
Dunn BM (2002) Structure and mechanism of the pepsin-like family of aspartic peptidases. Chem Rev 102(12):4431–4458. https://doi.org/10.1021/cr010167q
Fang L, Zhao T, Hu Y, Si Z, Zhu X, Han Z et al (2021) Divergent improvement of two cultivated allotetraploid cotton species. Plant Biotechnol J 19(7):1325–1336. https://doi.org/10.1111/pbi.13547
Feng L, Zhou C, Su Q, Xu M, Yue H, Zhang S et al (2020) Fine-mapping and candidate gene analysis of qFS-Chr D02, a QTL for fibre strength introgressed from a semi-wild cotton into Gossypium hirsutum. Plant Sci 297:110524. https://doi.org/10.1016/j.plantsci.2020.110524
He S, Sun G, Geng X, Gong W, Dai P, Jia Y et al (2021) The genomic basis of geographic differentiation and fiber improvement in cultivated cotton. Nat Genet 53(6):916–924. https://doi.org/10.1038/s41588-021-00844-9
Huang Y, Wang J, Zhang L, Zuo K (2013) A cotton annexin protein AnxGb6 regulates fiber elongation through its interaction with actin 1. PLoS ONE 8(6):e66160. https://doi.org/10.1371/journal.pone.0066160
Irshad M, Canut H, Borderies G, Pont-Lezica R, Jamet E (2008) A new picture of cell wall protein dynamics in elongating cells of Arabidopsis thaliana: confirmed actors and newcomers. BMC Plant Biol 8:94. https://doi.org/10.1186/1471-2229-8-94
Jan M, Liu Z, Guo C, Sun X (2022) Molecular regulation of cotton fiber development: a review. Int J Mol Sci 23(9):5004. https://doi.org/10.3390/ijms23095004
Lacape J, Jacobs J, Arioli T, Derijcker R, Forestier-Chiron N, Llewellyn D et al (2009) A new interspecific, Gossypium hirsutum × G. barbadense, RIL population: towards a unified consensus linkage map of tetraploid cotton. Theor Appl Genet 119(2):281–292. https://doi.org/10.1007/s00122-009-1037-y
Li X, Fan X, Wang X, Cai L, Yang W (2005) The cotton ACTIN1 gene is functionally expressed in fibers and participates in fiber elongation. Plant Cell 17(3):859–875. https://doi.org/10.1105/tpc.104.029629
Li S, Wang J, Zhang L (2015) Inclusive composite interval mapping of QTL by environment interactions in biparental populations. PLoS ONE 10(7):e0132414. https://doi.org/10.1371/journal.pone.0132414
Li S, Liu A, Kong L, Gong J, Li J, Gong W et al (2019) QTL mapping and genetic effect of chromosome segment substitution lines with excellent fiber quality from Gossypium hirsutum × Gossypium barbadense. Mol Genet Genomics 294(5):1123–1136. https://doi.org/10.3390/plants10122805
Li S, Kong L, Xiao X, Li P, Liu A, Li J et al (2022) Genome-wide artificial introgressions of Gossypium barbadense into G. hirsutum reveal superior loci for simultaneous improvement of cotton fiber quality and yield traits. J Adv Res. https://doi.org/10.1016/j.jare.2022.11.009
Liu Y, Yi Q, Hou X, Zhang X, Zhang J, Liu H et al (2016) Comparative quantitative trait locus mapping of maize flowering-related traits in an F2:3 and recombinant inbred line population. Genet Mol Res 30:15. https://doi.org/10.4238/gmr.15028465
Milisavljevic M, Timotijevic G, Radovic S, Konstantinovic M, Maksimovic V (2008) Two types of aspartic proteinases from buckwheat seed - genes structure and expression analysis. J Plant Physiol 165(9):983–990. https://doi.org/10.1016/j.jplph.2007.03.016
Nie X, Wen T, Shao P, Tang B, Nuriman-guli A, Yu Y et al (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 Xinjiang. Plant J 103(2):677–689. https://doi.org/10.1111/tpj.14760
Park Y, Alabady M, Ulloa M, Sickler B, Wilkins T, Yu J et al (2005) Genetic mapping of new cotton fiber loci using EST-derived microsatellites in an interspecific recombinant inbred line cotton population. Mol Gen Genomics 274(4):428–441. https://doi.org/10.1007/s00438-005-0037-0
Raimbault AK, Zuily-Fodil Y, Soler A, Cruz de Carvalho MH (2013) A novel aspartic acid protease gene from pineapple fruit (Ananas comosus): Cloning, characterization and relation to postharvest chilling stress resistance. J Plant Physiol 170(17):1536–1540. https://doi.org/10.1016/j.jplph.2013.06.007
Sebastián D, Fernando F, Raúl D, Gabriela G (2020) Overexpression of Arabidopsis aspartic protease APA1 gene confers drought tolerance. Plant Sci 292:110406. https://doi.org/10.1016/j.plantsci.2020.110406
Si Z, Chen H, Zhu X, Cao Z, Zhang T (2017) Genetic dissection of lint yield and fiber quality traits of G. hirsutum in G. barbadense background. Mol Breed 37:9. https://doi.org/10.1007/s11032-016-0607-3
Simões I, Faro C (2004) Structure and function of plant aspartic proteinases. Eur J Biochem 271(11):2067–2075. https://doi.org/10.1111/j.1432-1033.2004.04136.x
Song X, Zhu G, Hou S, Ren Y, Amjid M, Li W et al (2021) Genome-wide association analysis reveals loci and candidate genes involved in fiber quality traits under multiple field environments in cotton (Gossypium hirsutum). Front Plant Sci 12:695503. https://doi.org/10.3389/fpls.2021.695503
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93(1):77–78. https://doi.org/10.1093/jhered/93.1.77
Wang H, Wang J, Gao P, Jiao G, Zhao P, Li Y et al (2009) Down-regulation of GhADF1 gene expression affects cotton fibre properties. Plant Biotechnol J 7(1):13–23. https://doi.org/10.1111/j.1467-7652.2008.00367.x
Wang F, Zhang J, Chen Y, Zhang C, Gong J, Song Z et al (2020) Identification of candidate genes for key fibre-related QTLs and derivation of favourable alleles in Gossypium hirsutum recombinant inbred lines with G. barbadense introgressions. Plant Biotechnol J 18(3):707–720. https://doi.org/10.1111/pbi.13237
Wang N, Li Y, Chen Y, Lu R, Zhou L, Wang Y et al (2021a) Phosphorylation of WRKY16 by MPK3-1 is essential for its transcriptional activity during fiber initiation and elongation in cotton (Gossypium hirsutum). Plant Cell 10(6):1235. https://doi.org/10.1093/plcell/koab153
Wang N, Ma Q, Wu M, Pei W, Song J, Jia B et al (2021b) Genetic variation in MYB5_A12 is associated with fibre initiation and elongation in tetraploid cotton. Plant Biotechnol J 19(10):1892–1894. https://doi.org/10.1111/pbi.13662
Wang M, Qi Z, Thyssen G, Naoumkina M, Jenkins J, McCarty J et al (2022) Genomic interrogation of a MAGIC population highlights genetic factors controlling fiber quality traits in cotton. Commun Biol 5(1):60. https://doi.org/10.1038/s42003-022-03022-7
Wu H, Fan L, Guo M, Liu L, Liu L, Hou L et al (2023) GhPRE1A promotes cotton fibre elongation by activating the DNA-binding bHLH factor GhPAS1. Plant Biotechnol J 21(5):896–898. https://doi.org/10.1111/pbi.14005
Xin W, Liu H, Yang L, Ma T, Wang J, Zheng H et al (2022) BSA-seq and fine linkage mapping for the identification of a novel Locus (qPH9) for mature plant height in rice (Oryza sativa). Rice (n Y) 15(1):26. https://doi.org/10.1186/s12284-022-00576-2
Yang D, Liu Y, Cheng H, Wang Q, Lv L, Zhang Y et al (2021) Identification of the group III WRKY subfamily and the functional analysis of GhWRKY53 in Gossypium hirsutum L. Plants (basel) 10(6):1235. https://doi.org/10.3390/plants10061235
Yu J, Jung S, Cheng C, Lee T, Zheng P, Buble K et al (2021) CottonGen: The community database for cotton genomics, genetics, and breeding research. Plants 10(12):2805. https://doi.org/10.3390/plants10122805
Zhang X, Wang G, Chen B, Du H, Geng S (2018) Candidate genes for first flower node identified in pepper using combined SLAF-seq and BSA. PLoS ONE 13(3):e0194071. https://doi.org/10.1371/journal.pone.0194071
Zhang K, Kuraparthy V, Fang H, Zhu L, Sood S, Jones D (2019) High-density linkage map construction and QTL analyses for fiber quality, yield and morphological traits using CottonSNP63K array in upland cotton (Gossypium hirsutum L.). BMC Genomics 20(1):889. https://doi.org/10.1186/s12864-019-6214-z
Zhang S, Zhou X, Tang L, Li X, Wang H, Liu C et al (2020a) QTL mapping and genetic analysis of fiber quality traits in hybrid cotton ‘Ji1518.’ Mole Plant Breed 11(15):1–11. https://doi.org/10.5376/MPB.2020.11.0015
Zhang Z, Li J, Jamshed M, Shi Y, Liu A, Gong J et al (2020b) Genome-wide quantitative trait loci reveal the genetic basis of cotton fibre quality and yield-related traits in a Gossypium hirsutum recombinant inbred line population. Plant Biotechnol J 18(1):239–253. https://doi.org/10.1111/pbi.13191
Zhang J, Jia X, Guo X, Wei H, Zhang M, Wu A et al (2021) QTL and candidate gene identification of the node of the first fruiting branch (NFFB) by QTL-seq in upland cotton (Gossypium hirsutum L.). BMC Genomics 22(1):1–14. https://doi.org/10.1186/s12864-021-08164-2
Zhang R, Shen C, Zhu D, Le Y, Wang N, Li Y et al (2022a) Fine-mapping and candidate gene analysis of qFL-c10–1 controlling fiber length in upland cotton (Gossypium hirsutum L.). Theor Appl Genet 135(12):4483–4494. https://doi.org/10.1007/s00122-022-04233-6
Zhang S, Chen J, Jiang T, Cai X, Wang H, Liu C et al (2022b) Genetic mapping, transcriptomic sequencing and metabolic profiling indicated a glutathione S-transferase is responsible for the red-spot-petals in Gossypium arboreum. Theor Appl Genet 135(10):3443–3454. https://doi.org/10.1007/s00122-022-04191-z
Zhao B, Cao J, Hu G, Chen Z, Wang L, Shangguan X et al (2018) Core cis-element variation confers subgenome-biased expression of a transcription factor that functions in cotton fiber elongation. New Phytol 218(3):1061–1075. https://doi.org/10.1111/nph.15063
Zheng J, Oluoch G, Riaz Khan M, Wang X, Cai X, Zhou Z et al (2016) Mapping QTLs for drought tolerance in an F2:3 population from an inter-specific cross between Gossypium tomentosum and Gossypium hirsutum. Genet Mol Res. https://doi.org/10.4238/gmr.15038477
Zou X, Liu A, Zhang Z, Ge Q, Fan S, Gong W et al (2019) Co-expression network analysis and hub gene selection for high-quality fiber in upland cotton (Gossypium hirsutum) using RNA sequencing analysis. Genes (basel) 10(2):119. https://doi.org/10.3390/genes10020119
Acknowledgements
Thanks to Prof. Chen Jie, Prof. Yuan Youlu, Prof. Dai Maohua and Dr. Li Shaoqi for their long-term guidance and assistance in this project, as well as Yuanbao Biotech (Nanjing, China) for their aid in the dual-luciferase assay.
Funding
This work was supported by Basic Research Funds of Hebei Academy of Agriculture and Forestry Sciences (HAAFS) (2021070204), the Youth Fund of Hebei Natural Science Foundation (C2021301039), and the HAAFS Science and Technology Innovation Special Project (2022KJCXZX-MHS-1). The funders had no role in the design of the study, data collection, analysis and interpretation, decision to publish, or preparation of the manuscript.
Author information
Authors and Affiliations
Contributions
JZ, XZ and SZ conceived and designed the experiments. SZ, HW, XL, LT, XC and CL performed the experiments. SZ analyzed the data and wrote the paper. All the authors have read and approved the final version of the paper.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Additional information
Communicated by David D. Fang.
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.
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.
About this article
Cite this article
Zhang, S., Wang, H., Li, X. et al. Aspartyl proteases identified as candidate genes of a fiber length QTL, qFLD05, that regulates fiber length in cotton (Gossypium hirsutum L.). Theor Appl Genet 137, 59 (2024). https://doi.org/10.1007/s00122-024-04559-3
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00122-024-04559-3