Abstract
Ligon lintless-1 (Li1) is a Gossypium hirsutum mutant that is controlled by a dominant gene that arrests the development of cotton fiber after anthesis. Two F2 mapping populations were developed from mutant (Li1 × H7124) F1 plants in 2012 and 2013; each was composed of 142 and 1024 plants, respectively. Using these populations, Li1 was mapped to a 0.3-cM region in which nine single-strand conformation polymorphism markers co-segregated with the Li1 locus. In the published G. raimondii genome, these markers were mapped to a region of about 1.2 Mb (the Li1 region) and were separated by markers that flanked the Li1 locus in the genetic map, dividing the Li1 region into three segments. Thirty-six genes were annotated by the gene prediction software FGENESH (Softberry) in the Li1 region. Twelve genes were candidates of Li1, while the remaining 24 genes were identified as transposable elements, DNA/RNA polymerase superfamily or unknown function genes. Among the 12 candidate genes, those encoding ribosomal protein s10, actin protein, ATP synthase, and beta-tubulin 5 were the most-promising candidates of the Li1 mutant because the function of these genes is closely related to fiber development. High-throughput RNA sequencing and quantitative PCR revealed that these candidate genes had obvious differential gene expression between mutant and wild-type plants at the fiber elongation stage, strengthening the inference that they could be the most likely candidate gene of the Li1 mutant phenotype.
Similar content being viewed by others
References
Arpat AB, Waugh M, Sullivan JP, Gonzales M, Frisch D, Main D, Wood T, Leslie A, Wing RA, Wilkins TA (2004) Functional genomics of cell elongation in developing cotton fibers. Plant Mol Biol 54:911–929
Bibikova TN, Blancaflor EB, Gilroy S (1999) Microtubules regulate tip growth and orientation in root hairs of Arabidopsis thaliana. Plant J 17:657–665
Bolton JJ, Soliman KM, Wilkins TA, Jenkins JN (2009) Aberrant expression of critical genes during secondary cell wall biogenesis in a cotton mutant, Ligon lintless-1 (Li-1). Comp Funct Genomics. doi:10.1155/2009/659301
Cai C, Tong X, Liu F, Lv F, Wang H, Zhang T, Guo W (2013) Discovery and identification of a novel Ligon lintless-like mutant (Lix) similar to the Ligon lintless (Li1) in allotetraploid cotton. Theor Appl Genet 126:963–970
Ding M, Jiang Y, Cao Y, Lin L, He S, Zhou W, Rong J (2014) Gene expression profile analysis of Ligon lintless-1 (Li1) mutant reveals important genes and pathways in cotton leaf and fiber development. Gene 535:273–285
Gilbert MK, Turley RB, Kim HJ, Li P, Thyssen G, Tang Y, Delhom CD, Naoumkina M, Fang DD (2013) Transcript profiling by microarray and marker analysis of the short cotton (Gossypium hirsutum L.) fiber mutant Ligon lintless-1 (Li1). BMC Genom 14:403
Gilbert MK, Kim HJ, Tang Y, Naoumkina M, Fang DD (2014) Comparative transcriptome analysis of short fiber mutants Ligon-lintless 1 and 2 reveals common mechanisms pertinent to fiber elongation in cotton (Gossypium hirsutum L.). PLoS ONE 9:e95554
Griffee F, Ligon LL (1929) Occurrence of lintless cotton plants and the inheritance of the character lintless. Agron J 21:711–717
Guan X, Lee JJ, Pang M, Shi X, Stelly DM, Chen ZJ (2011) Activation of Arabidopsis seed hair development by cotton fiber-related genes. PLoS One 6:e21301
He XC, Qin YM, Xu Y, Hu CY, Zhu YX (2008) Molecular cloning, expression profiling, and yeast complementation of 19 β-tubulin cDNAs from developing cotton ovules. J Exp Bot 59:2687–2695
He S, Zheng Y, Chen A, Ding M, Lin L, Cao Y, Zhou W, Rong J, Jenkins J (2013) Converting restriction fragment length polymorphism to single-strand conformation polymorphism markers and its application in the fine mapping of a trichome gene in cotton. Plant Breed 132:337–343
Janda M, Matoušková J, Burketová L, Valentová O (2014) Interconnection between action cytoskeleton and plant defense signaling. Plant Signal Behav 9:e976486
Jiang J, Zhang T (2003) Extraction of total RNA in cotton tissues with CTAB-acidic phenolic method. Cotton Sci 15:166–167
Karaca M, Saha S, Jenkins JN, Zipf A, Kohel R, Stelly DM (2002) Simple sequence repeat (SSR) markers linked to the Ligon lintless (Li1) mutant in cotton. J Hered 93:221–224
Kohel RJ (1972) Linkage tests in upland cotton, Gossypium hirsutum L. Crop Sci 12:66–69
Kohel RJ, Narbuth EV, Benedict CR (1992) Fiber development of Ligon lintless-2 mutant of cotton. Crop Sci 32:733–735
Kohel RJ, Benedict CR, Jividen GM (1993) Incorporation of [14C] glucose into crystalline cellulose in aberrant fibers of a cotton mutant. Crop Sci 33:1036–1040
Kohel RJ, Stelly DM, Yu J (2002) Tests of six cotton (Gossypium hirsutum L.) mutants for association with aneuploids. J Hered 93:130–132
Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg L (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181
Lee JJ, Hassan OS, Gao W, Wei NE, Kohel RJ, Chen XY, Payton P, Sze SH, Stelly DM, Chen ZJ (2006) Developmental and gene expression analyses of a cotton naked seed mutant. Planta 223:418–432
Lee JJ, Woodward AW, Chen ZJ (2007) Gene expression changes and early events in cotton fibre development. Ann Bot 100:1391–1401
Li XB, Fan XP, Wang XL, Cai L, Yang WC (2005) The cotton ACTIN1 gene is functionally expressed in fibers and participates in fiber elongation. Plant Cell 17:859–875
Li L, Wang XL, Huang GQ, Li XB (2007) Molecular characterization of cotton GhTUA9 gene specifically expressed in fibre and involved in cell elongation. J Exp Bot 58:3227–3238
Liew KM, Xiang P, Zhang LW (2015) Mechanical properties and characteristics of microtubules: a review. Compos Struct 124:98–108
Liu K, Sun J, Yao L, Yuan Y (2012) Transcriptome analysis reveals critical genes and key pathways for early cotton fiber elongation in Ligon lintless-1 mutant. Genomics 100:42–50
Majewski P, Wołoszyńska M, Jańska H (2009) Developmentally early and late onset of Rps10 silencing in Arabidopsis thaliana: genetic and environmental regulation. J Exp Bot 60:1163–1178
Mathur J, Chua NH (2000) Microtubule stabilization leads to growth reorientation in Arabidopsis trichomes. Plant Cell 12:465–477
Naoumkina M, Thyssen GN, Fang DD (2015) RNA-seq analysis of short fiber mutants Ligon-lintless-1 (Li 1) and -2 (Li 2) revealed important role of aquaporins in cotton (Gossypium hirsutum L.) fiber elongation. BMC Plant Biol 15(1):65
Narbuth EV, Kohel RJ (1990) Inheritance and linkage analysis of a new fiber mutant in cotton. J Hered 81:131–133
Pang Y, Wang H, Song WQ, Zhu YX (2010) The cotton ATP synthase δ1 subunit is required to maintain a higher ATP/ADP ratio that facilitates rapid fibre cell elongation. Plant Biol 12:903–909
Paterson AH, Wendel JF, Gundlach H, Guo H, Jenkins J, Jin D, Llewellyn D, Showmaker KC, Shu S, Udall J, Yoo MJ, Byers R, Chen W, Doron-Faigenboim A, Duke MV, Gong L, Grimwood J, Grover C, Grupp K, Hu G, Lee TH, Li J, Lin L, Liu T, Marler BS, Page JT, Roberts AW, Romanel E, Sanders WS, Szadkowski E, Tan X, Tang H, Xu C, Wang J, Wang Z, Zhang D, Zhang L, Ashrafi H, Bedon F, Bowers JE, Brubaker CL, Chee PW, Das S, Gingle AR, Haigler CH, Harker D, Hoffmann LV, Hovav R, Jones DC, Lemke C, Mansoor S, ur Rahman M, Rainville LN, Rambani A, Reddy UK, Rong JK, Saranga Y, Scheffler BE, Scheffler JA, Stelly DM, Triplett BA, Van Deynze A, Vaslin MF, Waghmare VN, Walford SA, Wright RJ, Zaki EA, Zhang T, Dennis ES, Mayer KF, Peterson DG, Rokhsar DS, Wang X, Schmutz J (2012) Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres. Nature 492:423–427
Qin YM, Zhu YX (2011) How cotton fibers elongate: a tale of linear cell-growth mode. Curr Opin Plant Biol 14:106–111
Rong JK, Abbey C, Bowers JE, Brubaker CL, Chang C, Chee PW, Delmonte TA, Ding XL, Garza JJ, Marler BS, Park CH, Pierce GJ, Rainey KM, Rastogi VK, Schulze SR, Trolinder NL, Wendel JF, Wilkins TA, Williams-Coplin TD, Wing RA, Wright RJ, Zhao XP, Zhu LH, Paterson AH (2004) A 3347-locus genetic recombination map of sequence-tagged sites reveals features of genome organization, transmission and evolution of cotton (Gossypium). Genetics 166:389–417
Rong J, Pierce GJ, Waghmare VN, Rogers CJ, Desai A, Chee PW, May OL, Gannaway JR, Wendel JF, Wilkins TA, Patersn AH (2005) Genetic mapping and comparative analysis of seven mutants related to seed fiber development in cotton. Theor Appl Genet 111:1137–1146
Schippers JHM, Mueller-Roeber B (2010) Ribosomal composition and control of leaf development. Plant Sci 179:307–315
Shangguan X, Yu N, Wang L, Chen X (2010) Recent advances in molecular biology research on cotton fiber development cotton. Springer, Berlin, pp 161–175
Stock D, Leslie AG, Walker JE (1999) Molecular architecture of the rotary motor in ATP synthase. Science 286:1700–1705
Sun YL, Jia YH, He SP, Zhou ZL, Sun JL, Pang BY, Du XM (2012) Genetic analysis of fuzzless in cotton germplasm. Hereditas (Beijing) 34:1073–1078
Turley RB, Kloth RH (2002) Identification of a third fuzzless seed locus in upland cotton (Gossypium hirsutum L.). J Hered 93:359–364
Turley RB, Kloth RH (2008) The inheritance model for the fiberless trait in upland cotton (Gossypium hirsutum L.) line SL1-7-1: variation on a theme. Euphytica 164:123–132
Turley R, Vaughn K, Scheffler J (2007) Lint development and properties of fifteen fuzzless seed lines of Upland cotton (Gossypium hirsutum L.). Euphytica 156:57–65
Zhao PM, Wang LL, Han LB, Wang J, Yao Y, Wang HY, Du XM, Luo YM, Xia GX (2010) Proteomic identification of differentially expressed proteins in the Ligon lintless mutant of upland cotton (Gossypium hirsutum L.). J Proteome Res 9:1076–1087
Zhou W, Huang C, Gong Y, Feng Q, Gao F (2010) Molecular cloning and expression analysis of an ANS gene encoding anthocyanidin synthase from purple-fleshed sweet potato [Ipomoea batatas (L.) Lam]. Plant Mol Biol Rep 28:112–121
Acknowledgments
Dr. Xiongming Du of the Cotton Research Institute, Chinese Academy of Agricultural Sciences (CRI-CAAS) at Anyang, China, kindly provided all cotton materials including the Li1 mutant. We sincerely express our thanks to an anonymous reviewer for his/her helpful comments, suggestions, and corrections.
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Funding
This study was funded jointly by the National High Technology Research and Development Program of China (863 Program, Grant No. 2011AA100202), the National Natural Science Foundation of China (Grant Nos. 31200909 and 31301372), and the State Key Laboratory of Cotton Biology Open Fund (CB2014A06) to Yurong Jiang.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by J. Zhang
Y. Jiang and M. Ding have contributed equally to this work.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Jiang, Y., Ding, M., Cao, Y. et al. Genetic fine mapping and candidate gene analysis of the Gossypium hirsutum Ligon lintless-1 (Li1) mutant on chromosome 22(D). Mol Genet Genomics 290, 2199–2211 (2015). https://doi.org/10.1007/s00438-015-1070-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-015-1070-2