Abstract
Comparative proteomic analyses were performed to detail the evolutionary consequences of strong directional selection for enhanced fiber traits in modern upland cotton (Gossypium hirsutum L.). Using two complementary proteomic approaches, 2-DE and iTRAQ LC–MS/MS, fiber proteomes were examined for four representative stages of fiber development. Approximately 1,000 protein features were characterized using each strategy, collectively resulting in the identification and functional categorization of 1,223 proteins. Unequal contributions of homoeologous proteins were detected for over a third of the fiber proteome, but overall expression was balanced with respect to the genome-of-origin in the allopolyploid G. hirsutum. About 30 % of the proteins were differentially expressed during fiber development within wild and domesticated cotton. Notably, domestication was accompanied by a doubling of protein developmental dynamics for the period between 10 and 20 days following pollination. Expression levels of 240 iTRAQ proteins and 293 2-DE spots were altered by domestication, collectively representing multiple cellular and metabolic processes, including metabolism, energy, protein synthesis and destination, defense and stress response. Analyses of homoeolog-specific expression indicate that duplicated gene products in cotton fibers can be differently regulated in response to selection. These results demonstrate the power of proteomics for the analysis of crop domestication and phenotypic evolution.





Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.Abbreviations
- 2-DE:
-
Two-dimensional gel electrophoresis
- iTRAQ:
-
Isobaric tag for relative and absolute quantification
- LC:
-
Liquid chromatography
- MS:
-
Mass spectrometry
References
Aggarwal K, Choe LH, Lee KH (2006) Shotgun proteomics using the iTRAQ isobaric tags. Brief Funct Genomic Proteomic 5:112–120
Al-Ghazi Y, Bourot S, Arioli T, Dennis ES, Llewellyn DJ (2009) Transcript profiling during fiber development identifies pathways in secondary metabolism and cell wall structure that may contribute to cotton fiber quality. Plant Cell Physiol 50:1364–1381
Amor Y, Haigler CH, Johnson S, Wainscott M, Delmer DP (1995) A membrane-associated form of sucrose synthase and its potential role in synthesis of cellulose and callose in plants. Proc Natl Acad Sci USA 92:9353–9357
Applequist WL, Cronn R, Wendel JF (2001) Comparative development of fiber in wild and cultivated cotton. Evol Dev 3:3–17
Bao Y, Hu G, Flagel LE, Salmon A, Bezanilla M, Paterson AH, Wang Z, Wendel JF (2011) Parallel up-regulation of the profilin gene family following independent domestication of diploid and allopolyploid cotton (Gossypium). Proc Natl Acad Sci USA 108:21152–21157
Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29:1165–1188
Bevan M, Bancroft I, Bent E, Love K, Goodman H, Dean C, Bergkamp R, Dirkse W et al (1998) Analysis of 1.9 Mb of contiguous sequence from chromosome 4 of Arabidopsis thaliana. Nature 391:485–488
Brubaker CL, Wendel JF (1994) Reevaluating the origin of domesticated cotton (Gossypium hirsutum; Malvaceae) using nuclear restriction fragment length polymorphisms (RFLPs). Am J Bot 81:1309–1326
Burger JC, Chapman MA, Burke JM (2008) Molecular insights into the evolution of crop plants. Am J Bot 95:113–122
Burke JM, Burger JC, Chapman MA (2007) Crop evolution: from genetics to genomics. Curr Opin Genet Dev 17:525–532
Chaudhary B, Hovav R, Rapp R, Verma N, Udall JA, Wendel JF (2008) Global analysis of gene expression in cotton fibers from wild and domesticated Gossypium barbadense. Evol Dev 10:567–582
Chaudhary B, Hovav R, Flagel L, Mittler R, Wendel JF (2009) Parallel expression evolution of oxidative stress-related genes in fiber from wild and domesticated diploid and polyploid cotton (Gossypium). BMC Genom 10:378
Chen S, Harmon AC (2006) Advances in plant proteomics. Proteomics 6:5504–5516
Chen A, He S, Li F, Li Z, Ding M, Liu Q, Rong J (2012) Analyses of the sucrose synthase gene family in cotton: structure, phylogeny and expression patterns. BMC Plant Biol 12:85
Chong PK, Gan CS, Pham TK, Wright PC (2006) Isobaric tags for relative and absolute quantitation (iTRAQ) reproducibility: implication of multiple injections. J Proteome Res 5:1232–1240
Darwin C (1859) On the origin of the species by means of natural selection: or, the preservation of favoured races in the struggle for life. John Murray, London
Diz AP, Martinez-Fernandez M, Rolan-Alvarez E (2012) Proteomics in evolutionary ecology: linking the genotype with the phenotype. Mol Ecol 21:1060–1080
Doebley JF, Gaut BS, Smith BD (2006) The molecular genetics of crop domestication. Cell 127:1309–1321
Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38:W64–W70
Fan L, Shi WJ, Hu WR, Hao XY, Wang DM, Yuan H, Yan HY (2009) Molecular and biochemical evidence for phenylpropanoid synthesis and presence of wall-linked phenolics in cotton fibers. J Integr Plant Biol 51:626–637
Fenselau C (2007) A review of quantitative methods for proteomic studies. J Chromatogr B Analyt Technol Biomed Life Sci 855:14–20
Fisher RA (1948) Questions and answers #14. Am Stat 2:30–31
Gross BL, Olsen KM (2010) Genetic perspectives on crop domestication. Trends Plant Sci 15:529–537
Haigler CH, Betancur L, Stiff MR, Tuttle JR (2012) Cotton fiber: a powerful single-cell model for cell wall and cellulose research. Front Plant Sci 3:104
Hanin M, Brini F, Ebel C, Toda Y, Takeda S, Masmoudi K (2011) Plant dehydrins and stress tolerance: versatile proteins for complex mechanisms. Plant Signal Behav 6:1503–1509
Hovav R, Udall JA, Chaudhary B, Hovav E, Flagel L, Hu G, Wendel JF (2008) The evolution of spinnable cotton fiber entailed prolonged development and a novel metabolism. PLoS Genet 4:e25
Hu G, Houston NL, Pathak D, Schmidt L, Thelen JJ, Wendel JF (2011) Genomically biased accumulation of seed storage proteins in allopolyploid cotton. Genetics 189:1103–1115
Hu G, Koh J, Yoo MJ, Grupp K, Chen S, Wendel JF (2013) Proteomic profiling of developing cotton fibers from wild and domesticated Gossypium barbadense. New Phytol 200:570–582
Koh J, Chen S, Zhu N, Yu F, Soltis PS, Soltis DE (2012) Comparative proteomics of the recently and recurrently formed natural allopolyploid Tragopogon mirus (Asteraceae) and its parents. New Phytol 196:292–305
Lemkin PF, Thornwall GC, Evans J (2005) Comparing 2-D electrophoretic gels across internet databases. In: Walker J (ed) The proteomics protocols handbook. Humana Press, Totowa, pp 279–306
Li HB, Qin YM, Pang Y, Song WQ, Mei WQ, Zhu YX (2007) A cotton ascorbate peroxidase is involved in hydrogen peroxide homeostasis during fibre cell development. New Phytol 175:462–471
Liu D, Tu L, Wang L, Li Y, Zhu L, Zhang X (2008) Characterization and expression of plasma and tonoplast membrane aquaporins in elongating cotton fibers. Plant Cell Rep 27:1385–1394
Liu K, Han M, Zhang C, Yao L, Sun J, Zhang T (2012) Comparative proteomic analysis reveals the mechanisms governing cotton fiber differentiation and initiation. J Proteomics 75:845–856
Mi H, Dong Q, Muruganujan A, Gaudet P, Lewis S, Thomas PD (2010) PANTHER version 7: improved phylogenetic trees, orthologs and collaboration with the Gene Ontology Consortium. Nucleic Acids Res 38:D204–D210
Olsen KM, Wendel JF (2013a) A bountiful harvest: genomic insights into crop domestication phenotypes. Annu Rev Plant Biol 64:47–70
Olsen KM, Wendel JF (2013b) Crop plants as models for understanding plant adaptation and diversification. Front Plant Sci 4:1–16
Pang CY, Wang H, Pang Y, Xu C, Jiao Y, Qin YM, Western TL, Yu SX, Zhu YX (2010) Comparative proteomics indicates that biosynthesis of pectic precursors is important for cotton fiber and Arabidopsis root hair elongation. Mol Cell Proteomics 9:2019–2033
Paterson AH (2005) Polyploidy, evolutionary opportunity, and crop adaptation. Genetics of adaptation. Genetica 123:191–196
Rapp RA, Haigler CH, Flagel L, Hovav RH, Udall JA, Wendel JF (2010) Gene expression in developing fibres of Upland cotton (Gossypium hirsutum L.) was massively altered by domestication. BMC Biol 8:139
Rose JK, Bashir S, Giovannoni JJ, Jahn MM, Saravanan RS (2004) Tackling the plant proteome: practical approaches, hurdles and experimental tools. Plant J 39:715–733
Ruan YL, Llewellyn DJ, Furbank RT, Chourey PS (2005) The delayed initiation and slow elongation of fuzz-like short fibre cells in relation to altered patterns of sucrose synthase expression and plasmodesmata gating in a lintless mutant of cotton. J Exp Bot 56:977–984
Salnikov VV, Grimson MJ, Seagull RW, Haigler CH (2003) Localization of sucrose synthase and callose in freeze-substituted secondary-wall-stage cotton fibers. Protoplasma 221:175–184
Shilov IV, Seymour SL, Patel AA, Loboda A, Tang WH, Keating SP, Hunter CL, Nuwaysir LM, Schaeffer DA (2007) The Paragon Algorithm, a next generation search engine that uses sequence temperature values and feature probabilities to identify peptides from tandem mass spectra. Mol Cell Proteomics 6:1638–1655
Stiff RM, Haigler HC (2012) Recent advances in cotton fiber development. In: Oosterhuis DM, Cothren JT (eds) Flowering and fruiting in cotton. The Cotton Foundation, Tennessee, pp 163–192
Suzuki R, Shimodaira H (2006) Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 22:1540–1542
Tan J, Tu L, Deng F, Hu H, Nie Y, Zhang X (2013) A genetic and metabolic analysis revealed that cotton fiber cell development was retarded by flavonoid naringenin. Plant Physiol 162:86–95
Tang WH, Shilov IV, Seymour SL (2008) Nonlinear fitting method for determining local false discovery rates from decoy database searches. J Proteome Res 7:3661–3667
Thelen JJ, Peck SC (2007) Quantitative proteomics in plants: choices in abundance. Plant Cell 19:3339–3346
Udall JA, Wendel JF (2006) Polyploidy and crop improvement. Crop Sci 46:S-3–S-14
Vercauteren FG, Arckens L, Quirion R (2007) Applications and current challenges of proteomic approaches, focusing on two-dimensional electrophoresis. Amino Acids 33:405–414
Wang L, Li X-R, Lian H, Ni D-A, He Y-k, Chen X-Y, Ruan Y-L (2010) Evidence that high activity of vacuolar invertase Is required for cotton fiber and arabidopsis root elongation through osmotic dependent and independent pathways, respectively. Plant Physiol 154:744–756
Wendel JF (1989) New World tetraploid cottons contain Old World cytoplasm. Proc Natl Acad Sci USA 86:4132–4136
Wendel JF, Brubaker CL, Percival AE (1992) Genetic diversity in Gossypium hirsutum and the origin of upland cotton. Am J Bot 79:1291–1310
Wendel JF, Brubaker CL, Seelanan T (2010) The origin and evolution of Gossypium. In: Stewart JM, Oosterhuis DM, Heitholt JJ, Mauney JR (eds) Physiology of cotton. Springer, The Netherlands, pp 1–18
Wendel JF, Flagel LE, Adams KL (2012) Jeans, genes, and genomes: cotton as a model for studying polyploidy. In: Soltis PS, Soltis DE (eds) Polyploidy and genome evolution. Springer, Berlin, Heidelberg, pp 181–207
Wu WW, Wang G, Baek SJ, Shen RF (2006) Comparative study of three proteomic quantitative methods, DIGE, cICAT, and iTRAQ, using 2D gel- or LC-MALDI TOF/TOF. J Proteome Res 5:651–658
Yang YW, Bian SM, Yao Y, Liu JY (2008) Comparative proteomic analysis provides new insights into the fiber elongating process in cotton. J Proteome Res 7:4623–4637
Yao Y, Yang YW, Liu JY (2006) An efficient protein preparation for proteomic analysis of developing cotton fibers by 2-DE. Electrophoresis 27:4559–4569
Yoo MJ, Wendel JF (2014) Comparative evolutionary and developmental dynamics of the cotton (Gossypium hirsutum) fiber transcriptome. PLoS Genet 10:e1004073
Zhang B, Yang YW, Zhang Y, Liu JY (2013) A high-confidence reference dataset of differentially expressed proteins in elongating cotton fiber cells. Proteomics 13:1159–1163
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 M, Sun G, Sun Z, Tang Y, Wu Y (2014) Cotton proteomics for deciphering the mechanism of environment stress response and fiber development. J Proteomics 105:74–84
Acknowledgments
We thank Kara Grupp and Anna Tuchin for help in tissue collection. We acknowledge the Protein and Proteomics Facility of the Iowa State University for technical assistance in 2-DE analysis. We acknowledge the Proteomics and Mass Spectrometry Facility of the University of Florida’s Interdisciplinary Center for Biotechnology Research for assistance in LC–MS/MS analysis. DP was supported by a training grant from Punjab Agricultural University, Ludhiana, India. The LC–MS/MS system was funded by National Institute of Health grant 1S10RR025418-01 to SC. This work was funded by Cotton Incorporated grant 09-558 and by the NSF Plant Genome Research Program, both to JFW.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Hu, G., Koh, J., Yoo, MJ. et al. Proteomics profiling of fiber development and domestication in upland cotton (Gossypium hirsutum L.). Planta 240, 1237–1251 (2014). https://doi.org/10.1007/s00425-014-2146-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-014-2146-7
Keywords
Profiles
- Guanjing Hu View author profile