Skip to main content
Log in

Quantitative proteomic analysis of upland cotton stem terminal buds reveals phytohormone-related pathways associated with dwarfism

  • Original Paper
  • Published:
Biologia Plantarum

Abstract

Identifying important regulative elements and pathways related to dwarfism in cotton is a major challenge in cotton breeding. Isobaric tags for relative and absolute quantitation-based proteomics of stem terminal buds from upland cotton (Gossypium hirsutum L.) dwarf line LA-1 and high near-isogenic line LH-1 was performed. Moreover, transcriptional expression of differentially-expressed proteins (DEPs) belonging to phytohormone signal transduction, hormone biosynthesis, and ubiquitin system were analysed using quantitative real-time polymerase chain reaction. A total of 4 849 proteins were identified from LA-1 and LH-1, 697 of which showed differential accumulations. Most of the DEPs have catalytic, binding, and transporter activity and are involved in metabolism- and protein processing-related pathways. In particular, seven DEPs, including two gibberellin (GA) receptors, three cytokinin (CK) receptors, CKoxidase, and CK-N-glucosyltransferase were up-regulated in LA-1, and GA20-oxidase was down-regulated in LH-1. Our results suggest that the DELLA-independent GAsignalling pathway is the primary cause of dwarfism in LA-1 and indicate that CKresponse element 1-2, GA-insensitive dwarf, CKoxidase, and GA3-β-dioxygenase are potential indicators of dwarf cotton. The profiling of DEPs may offer a valuable resource for cotton breeding.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

ABA:

abscisic acid

ACN:

acetonitrile

CK:

cytokinin

CKX:

cytokinin oxidase

DEPs:

differentially-expressed proteins

GA:

gibberellin

iTRAQ:

isobaric tags for relative and absolute quantitation

MS/MS:

tandem mass spectrometry

NIL:

near-isogenic line

RT-qPCR:

reverse transcription quantitative PCR

References

  • Achard, P., Cheng, H., De, G.L., Decat, J., Schoutteten, H., Moritz, T., Van, D.S.D., Peng, J., Harberd, N.P.: Integration of plant responses to environmentally activated phytohormonal signals. - Science 311: 91–94, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Ashikari, M., Sakakibara, H., Lin, S., Yamamoto, T., Takashi, T., Nishimura, A., Angeles, E.R., Qian, Q., Kitano, H., Matsuoka, M.: Cytokinin oxidase regulates rice grain production. - Science 309: 741–745, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Bachmair, A., Novatchkova, M., Potuschak, T., Eisenhaber, F.: Ubiquitylation in plants: a postgenomic look at a posttranslational modification. - Trends. Plant. Sci. 6: 463–470, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Borlaug, N.E.: Contributions of conventional plant breeding to food production. - Science 219: 689–693, 1983.

    Article  CAS  PubMed  Google Scholar 

  • Bradford, M.M.: A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. - Anal. Biochem. 72: 248–254, 1976.

    Article  CAS  PubMed  Google Scholar 

  • Chen, S., Yuan, H.M., Liu, G.F., Li, H.Y., Jiang, J.: A label-free differential quantitative proteomics analysis of a TaLEAintroduced transgenic Populus simonii × Populus nigra dwarf mutant. - Mol. biol. Rep. 39: 7657–7664, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Chen, Y., Hou, M.M., Liu, L.J., Wu, S., Shen, Y., Ishiyama, K., Kobayashi, M., McCarty, D.R., Tan, B.C.: The maize DWARF1 encodes a gibberellin 3-oxidase and is dual localized to the nucleus and cytosol. - Plant. Physiol. 166: 2028–2039, 2014.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cheng, Z.J., Wang, L., Sun, W., Zhang, Y., Zhou, C., Su, Y.H., Li, W., Sun, T.T., Zhao, X.Y., Li, X.G., Cheng, Y., Zhao, Y., Xie, Q., Zhang, X.S.: Pattern of auxin and cytokinin responses for shoot meristem induction results from the regulation of cytokinin biosynthesis by auxin response factor3. - Plant. Physiol. 161: 240–251, 2014.

    Article  Google Scholar 

  • Eastmond, P.J., Astley, H.M., Parsley, K., Aubry, S., Williams, B.P., Menard, G.N., Craddock, C.P., Nunes-Nesi, A., Fernie, A.R., Hibberd, J.M.: Arabidopsis uses two gluconeogenic gateways for organic acids to fuel seedling establishment. - Nat. Commun. 6: 6659, 2015.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ge, X., Zhang, C., Wang, Q., Yang, Z., Wang, Y., Zhang, X., Wu, Z., Hou, Y., Wu, J., Li, F.: iTRAQ protein profile differential analysis between somatic globular and cotyledonary embryos reveals stress, hormone, and respiration involved in increasing plantlet regeneration of Gossypium hirsutum L. - J. Proteome. Res. 14: 268–278, 2015.

    Article  CAS  PubMed  Google Scholar 

  • Han, Y.J., Cho, K.C., Hwang, O.J., Choi, Y.S., Shin, A.Y., Hwang, I., Kim, J.I.: Overexpreßsion of an Arabidopsis ß-glucosidase gene enhances drought resistance with dwarf phenotype in creeping bentgrass. - Plant. Cell Rep. 31:1677–1686, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Hepworth, J., Lenhard, M.: Regulation of plant lateral-organ growth by modulating cell number and size. - Curr. Opin. Plant. Biol. 17: 36–42, 2014.

    Article  PubMed  Google Scholar 

  • Huang, J.G., Yang, M., Liu, P., Yang, G.D., Wu, C.A., Zheng, C.C.: GhDREB1 enhances abiotic stress tolerance, delays GA-mediated development and represses cytokinin signalling in transgenic Arabidopsis. - Plant Cell Environ. 32: 1132–1145, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Jonsson, T.H.: Terminal bud failure of black cottonwood (Populus trichocarpa) exposed to salt-laden winter storms. - Tree. Physiol. 26: 905–914, 2006.

    Article  PubMed  Google Scholar 

  • Kato, H., Saito, T., Ito, H., Komeda, Y., Kato, A.: Overexpression of the TIR-X gene results in a dwarf phenotype and activation of defense-related gene expression in Arabidopsis thaliana. - J. Plant. Physiol. 171: 382–388, 2014.

    Article  CAS  PubMed  Google Scholar 

  • Khush, G.S.: Green revolution: preparing for the 21st century. - Genome 42: 646–655, 1999.

    Article  CAS  PubMed  Google Scholar 

  • Khush, G.S.: Green revolution: the way forward. - Nat. Rev. Genet. 2: 815–822, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Li, B., Xu, W., Xu, Y., Zhang, Y., Wang, T., Bai, Y., Han, C., Zhang, A., Xu, Z., Chong, K.: Integrative study on proteomics, molecular physiology, and genetics reveals an accumulation of cyclophilin-like protein, TaCYP20-2, leading to an increase of Rht protein and dwarf in a novel GA-insensitive mutant (gaid) in wheat. - J. Proteome Res. 9: 4242–4253, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Li, H.P., Wang, Y., Li, X.C., Gao, Y., Wang, Z.J., Zhao, Y., Wang, M.L.: A GA-insensitive dwarf mutant of Brassica napus L. correlated with mutation in pyrimidine box in the promoter of GID1. - Mol. Biol. Rep. 38: 191–197, 2011a.

    Article  CAS  PubMed  Google Scholar 

  • Li, Y.H., Yang, L.M., Pathak, M., Li, D.W., He, X.M., Weng, Y.Q.: Fine genetic mapping of cp: a recessive gene for compact (dwarf) plant architecture in cucumber, Cucumis sativus L. - Theor. appl. Genet. 123: 973–983, 2011b.

    Article  PubMed  Google Scholar 

  • Li, Y.J., Zhang, X.Y., Wang, F.X., Yang, C.L., Liu, F., Xia, G.X., Sun, J.: A comparative proteomic analysis provides insights into pigment biosynthesis in brown color fiber. - J. Proteomics 14: 374–388, 2013.

    Article  Google Scholar 

  • Liao, W.B., Xu, N.F., Peng, M.: Transgenic Arabidopsis plants over-expressing cotton DELLA or DELLA domain deletion: insights into DELLA gene function. - Biol. Plant. 57: 627–634, 2013.

    Article  CAS  Google Scholar 

  • Liu, J., Pang, C., Wei, H., Song, M., Meng, Y., Ma, J., Fan, S., Yu, S.: iTRAQ-facilitated proteomic profiling of anthers from a photosensitive male sterile mutant and wild-type cotton (Gossypium hirsutum L.). - J. Proteomics 126: 68–81, 2015.

    Article  CAS  PubMed  Google Scholar 

  • Livak, K.J., Schmittgen, T.D.: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) Method. - Methods 25: 402–408, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Maymon, I., Greenboim, W.Y., Sagiv, S., Kieber, J.J., Moshelion, M., Olszewski, N., Weiss, D.: Cytosolic activity of SPINDLY implies the existence of a DELLAindependent gibberellin-response pathway. - Plant. J. 58: 979–988, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Ning, D.L., Liu, C.C., Liu, J.W., Shen, Z., Chen, S., Liu, F., Wang, B.C., Yang, C.P.: Label-free quantitative proteomics analysis of dormant terminal buds of poplar. - Mol. Biol. Rep. 40: 4529–4542, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Reid, J.B., Davidson, S.E., Ross, J.J.: Auxin acts independently of DELLA proteins in regulating gibberellin levels. - Plant. Signal. Behav. 6: 406–408, 2014.

    Article  Google Scholar 

  • Ren, X.F., Sun, D.F., Guan, W.W., Sun, G.L., Li, C.D.: Inheritance and identification of molecular markers associated with a novel dwarfing gene in barley. - BMC. Genet. 11: 89, 2010.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sheoran, I.S., Ross, A.R., Olson, D.J., Sawhney, V.K.: Compatibility of plant protein extraction methods with mass spectrometry for proteome analysis. - Plant. Sci. 176: 99–104, 2009.

    Article  CAS  Google Scholar 

  • Shi, Y.S., Yu, Y.T., Song, Y.C., Liu, Z.Z., Li, Y., Wang, T.Y.: Identification of a QTL for plant height in a new dwarf germplasm of maize. - Acta agron. sinica. 36: 256–260, 2010.

    Article  CAS  Google Scholar 

  • Soh, M.S.: Isolation and characterization of a novel mutation that confers gibberellin-sensitive dwarfism in Arabidopsis thaliana. - J. Plant. Biol. 49: 160–166, 2006.

    Article  CAS  Google Scholar 

  • Stone, S.L., Callis, J.: Ubiquitin ligases mediate growth and development by promoting protein death. - Curr. Opin. Plant. Biol. 10: 624–632, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Tang, X.D., Fu, X.L., Hao, B.F., Zhu, F., Xiao, S.Y., Xu, L., Shen, Z.Y.: Identification of sumoylated proteins in the silkworm Bombyx mori. - Int. J. mol. Sci. 15: 22011–22027, 2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomas, S., Mooney, P.J., Burrell, M.M., Fell, D.A.: Metabolic control analysis of glycolysis in tuber tissue of potato (Solanum tuberosum): explanation for the low control coefficient of phosphofructokinase over respiratory flux. - Biochem. J. 322: 119–127, 1997.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ueguchi, T.M., Ashikari, M., Nakajima, M., Itoh, H., Katoh, E., Kobayashi, M., Chow, T.Y., Hsing, Y.I., Kitano, H., Yamaguchi, I., Matsuoka, M.: GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. - Nature 437: 693–698. 2005.

    Article  Google Scholar 

  • Wang, X.C., Li, Q., Jin, X., Xiao, G.H., Liu, G.J., Liu, N.J., Qin, Y.M.: Quantitative proteomics and transcriptomics reveal key metabolic processes associated with cotton fiber initiation. - J. Proteomics 114: 16–27, 2015.

    Article  CAS  PubMed  Google Scholar 

  • Wang, Y., Li, J.: Branching in rice. - Curr. Opin. Plant. Biol. 14: 94–99, 2014.

    Article  CAS  Google Scholar 

  • Wu, C., Zhou, B., Zhang, T.: Isolation and characterization of a sterile-dwarf mutant in Asian cotton (Gossypium arboreum L.). - J. Genet. Genomics 36: 343–353, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Xu, H., Liu, Q., Yao, T., Fu, X.D.: Shedding light on integrative GAsignaling. - Curr. Opin. Plant. Biol. 21: 89–95, 2014.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, C.L., Sun, J.L., Jia, Y.H., Wang, J., Xu, Z.J., Du, X.M.: Morphological characters, inheritance and response to exogenous hormones of a cotton super-dwarf mutant of Gossypium hirsutum - Plant. Breed. 130: 67–72, 2011.

    Article  CAS  Google Scholar 

  • Zhang, J., Liu, X.Q., Li, S.Y., Cheng, Z.K., Li, C.Y.: The rice semi-dwarf mutant sd37, caused by a mutation in CYP96B4, plays an important role in the fine-tuning of plant growth. - PLoS One. 9: e88068, 2014.

    Article  Google Scholar 

  • Zhang, Y.J., Hao, X.Y., Liang, Z.S., Ke, W.D., Guo, H.B.: Efficient isolation of high-quality RNA from lotus Nelumbo nucifera ssp. nucifera tissues. - Genet. mol. Res. 12: 223–229, 2013

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Q. Wang or A. Liu.

Additional information

Acknowledgements: This work was supported by grants from the National Natural Science Foundation of China (31571593 and 31301081), the specialized research fund for the doctoral program of higher education (20124320110001), and the youth scientific fund of the Hunan Agricultural University (14QN02). The first two authors contributed equally to this work.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tu, X., Li, J., Wang, Q. et al. Quantitative proteomic analysis of upland cotton stem terminal buds reveals phytohormone-related pathways associated with dwarfism. Biol Plant 61, 106–114 (2017). https://doi.org/10.1007/s10535-016-0644-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10535-016-0644-0

Additional key words

Navigation