Abstract
Cotton, as a natural fiber crop, plays a pivotal role in advancing global textile industry. Comparative transcriptome analyses of single-cell ‘fiber’ from wild and domesticated plant revealed the evolutionary selection of cell wall-associated profilin gene family during cotton domestication. However, the evolutionary significance of elevated transcript abundance of profilins (GhPRFs) in floral and fiber tissues, and their practical application in the field for improving crop yield remain poorly understood. In this study, the domestication-driven 402 bp long GhPRF1 gene (Pro35Sde:GhPRF1-pA) was constitutively overexpressed in cotton (Gossypium hirsutum L. cv. Coker 310FR) through Agrobacterium-mediated genetic transformation of 1513 cotyledonary explants undergoing somatic embryogenesis. Out of the 32 putative GhPRF1 transgenic overexpression (Ox) lines produced, 26 lines were successfully confirmed with independent transgene integrations. Compared with those of the untransformed wild type (WT), the cumulative abundance of GhPRF1 transcripts in the leaf tissues of GhPRF1 overexpressing lines Pf-CaOx7, Pf-CaOx14, and Pf-CaOx19 substantially increased (> 12-fold). These transgenic lines exhibited increased numbers of secondary branches, flower buds per branch, and trichome density on the abaxial surface of leaves compared to the WT plants. Despite comparable fiber lengths between the overexpression lines and the WT, the enhanced fiber yields in the overexpression lines were attributed to increased flower number and boll production per branch. Remarkably, GhPRF1 overexpression also manifested transcriptional biases specific to profilin homologs in vegetative, floral, and fiber tissues. This is primarily attributed to increased actin polymerization and the formation of dense F-actin bundles, which are especially evident in the vascular regions of overexpression lines compared to those of the WT. This study revealed novel phenotypic and genetic foundations influencing floral and fiber architecture in cotton and offers promising avenues for manipulating agronomic traits.
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References
Bajwa KS, Shahid AA, Rao AQ, Bashir A, Aftab A, Husnain T (2015) Stable transformation and expression of GhEXPA8 fiber expansin gene to improve fiber length and micronaire value in cotton. Front Plant Sci 6:838. https://doi.org/10.3389/fpls.2015.00838
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 U S A 108:21152–21157. https://doi.org/10.1073/pnas.1115926109
Beck M, Komis G, Ziemann A, Menzel D, Šamaj J (2011) Mitogen-activated protein kinase 4 is involved in the regulation of mitotic and cytokinetic microtubule transitions in Arabidopsis thaliana. New Phytol 189:1069–1083. https://doi.org/10.1111/j.1469-8137.2010.03565.x
Benfey PN, Chua NH (1990) The cauliflower mosaic virus 35S promoter: combinatorial regulation of transcription in plants. Science 250:959–966
Chaudhary B, Kumar S, Prasad KVSK, Oinam GS, Burma PK, Pental D (2003) Slow desiccation leads to high-frequency shoot recovery from transformed somatic embryos of cotton (Gossypium hirsutum L. cv. Coker 310 FR). Plant Cell Rep 21:955–960. https://doi.org/10.1007/s00299-003-0613-x
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. https://doi.org/10.1111/j.1525-142X.2008.00272.x
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 Genomics 10:378. https://doi.org/10.1186/1471-2164-10-378
Deng T, Yao H, Wang J, Wang J, Xue H, Zuo K (2016) GhLTPG1, a cotton GPI-anchored lipid transfer protein, regulates the transport of phosphatidylinositol monophosphates and cotton fiber elongation. Sci Rep 6:1–12. https://doi.org/10.1038/srep26829
Dillehay TD, Rossen J, Andres TC, Williams DE (2007) Preceramic adoption of peanut, squash, and cotton in Northern Peru. Science 316:1890–1893. https://doi.org/10.1126/science.1141395
Dominguez R, Holmes KC (2011) Actin structure and function. Annu Rev Biophys 40:169–186. https://doi.org/10.1146/annurev-biophys-042910-155359
Firoozabady E, DeBoer DL, Merlo DJ, Halk EL, Amerson LN, Rashka KE, Murray EE (1987) Transformation of cotton (Gossypium hirsutum L.) by Agrobacterium tumefaciens and regeneration of transgenic plants. Plant Mol Biol 10:105–116. https://doi.org/10.1007/BF00016148
Gallagher JP, Grover CE, Hu G, Jareczek JJ, Wendel JF (2020) Conservation and divergence in duplicated fiber coexpression networks accompanying domestication of the polyploid Gossypium hirsutum L. G3 Genes Genomes Genet 10:2879–2892. https://doi.org/10.1534/g3.120.401362
Gelvin SB (2003) Agrobacterium-mediated plant transformation: the biology behind the “Gene-Jockeying” tool. Microbiol Mol Biol Rev 67:16–37. https://doi.org/10.1128/mmbr.67.1.16-37.2003
Guan X, Li Q, Shan C, Wang S, Mao Y, Wang L, Chen X (2008) The HD-Zip IV gene GaHOX1 from cotton is a functional homologue of the Arabidopsis GLABRA2. Physiol Plant 134:174–182. https://doi.org/10.1111/j.1399-3054.2008.01115.x
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 3:1–7. https://doi.org/10.3389/fpls.2012.00104
Han LB, Li YB, Wang HY, Wu XM, Li CL, Luo M, Wu SJ, Kong ZS, Pei Y, Jiao GL, Xia GX (2013) The dual functions of WLIM1a in cell elongation and secondary wall formation in developing cotton fibers. Plant Cell 25:4421–4438. https://doi.org/10.1105/tpc.113.116970
Hao J, Tu L, Hu H, Tan J, Deng F, Tang W, Nie Y, Zhang X (2012) GbTCP, a cotton TCP transcription factor, confers fibre elongation and root hair development by a complex regulating system. J Exp Bot 63:6267–6281. https://doi.org/10.1093/jxb/ers278
He Q, Jones DC, Li W, Xie F, Ma J, Sun R, Wang Q, Zhu S, Zhang B (2016) Genome-wide identification of R2R3-MYB genes and expression analyses during abiotic stress in Gossypium raimondii. Sci Rep 6:1–14. https://doi.org/10.1038/srep22980
Higaki T, Kutsuna N, Sano T, Kondo N, Hasezawa S (2010) Quantification and cluster analysis of actin cytoskeletal structures in plant cells: role of actin bundling in stomatal movement during diurnal cycles in Arabidopsis guard cells. Plant J 61:156–165. https://doi.org/10.1111/j.1365-313X.2009.04032.x
Huang GQ, Gong SY, Xu WL, Li W, Li P, Zhang CJ, Di LD, Zheng Y, Li FG, Li XB (2013a) A fasciclin-like arabinogalactan protein, GhFLA1, is involved in fiber initiation and elongation of cotton. Plant Physiol 161:1278–1290. https://doi.org/10.1104/PP.112.203760
Huang Y, Wang J, Zhang L, Zuo K (2013b) A cotton annexin protein AnxGb6 regulates fiber elongation through its interaction with actin 1. PLoS ONE 8:1–14. https://doi.org/10.1371/journal.pone.0066160
Humphries JA, Walker AR, Timmis JN, Orford SJ (2005) Two WD-repeat genes from cotton are functional homologues of the Arabidopsis thaliana TRANSPARENT TESTA GLABRA1 (TTG1) gene. Plant Mol Biol 57:67–81. https://doi.org/10.1007/s11103-004-6768-1
Jiang Y, Guo W, Zhu H, Ruan YL, Zhang T (2012) Overexpression of GhSusA1 increases plant biomass and improves cotton fiber yield and quality. Plant Biotechnol J 10:301–312. https://doi.org/10.1111/j.1467-7652.2011.00662.x
Kumar S, Sharma P, Pental D (1998) A genetic approach to in vitro regeneration of non-regenerating cotton (Gossypium hirsutum L.) cultivars. Plant Cell Rep 18:59–63. https://doi.org/10.1007/s002990050532
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. https://doi.org/10.1105/tpc.104.029629
Li B, Yang Y, Hu W, Li X, Cao J, Fan L (2015) Over-expression of GhUGP1 in upland cotton improves fibre quality and reduces fibre sugar content. Plant Breed 134:197–202. https://doi.org/10.1111/pbr.12247
Li Y, Tu L, Pettolino FA, Ji S, Hao J, Yuan D, Deng F, Tan J, Hu H, Wang Q, Llewellyn DJ, Zhang X (2016) GbEXPATR, a species-specific expansin, enhances cotton fibre elongation through cell wall restructuring. Plant Biotechnol J 14:951–963. https://doi.org/10.1111/pbi.12450
Liu B, Zhu Y, Zhang T (2015) The R3-MYB gene GhCPC negatively regulates cotton fiber elongation. PLoS ONE 10:1–17. https://doi.org/10.1371/journal.pone.0116272
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Luo M, Xiao Y, Li X, Lu X, Deng W, Li D, Hou L, Hu M, Li Y, Pei Y (2007) GhDET2, a steroid 5α-reductase, plays an important role in cotton fiber cell initiation and elongation. Plant J 51:419–430. https://doi.org/10.1111/j.1365-313X.2007.03144.x
Lv F, Wang H, Wang X, Han L, Ma Y, Wang S, Feng Z, Niu X, Cai C, Kong Z, Zhang T, Guo W (2015) GhCFE1A, a dynamic linker between the ER network and actin cytoskeleton, plays an important role in cotton fibre cell initiation and elongation. J Exp Bot 66:1877–1889. https://doi.org/10.1093/jxb/eru530
Lv F, Li P, Zhang R, Li N, Guo W (2016) Functional divergence of GhCFE5 homoeologs revealed in cotton fiber and Arabidopsis root cell development. Plant Cell Rep 35:867–881. https://doi.org/10.1007/s00299-015-1928-0
Machado A, Wu Y, Yang Y, Llewellyn DJ, Dennis ES (2009) The MYB transcription factor GhMYB25 regulates early fibre and trichome development. Plant J 59:52–62. https://doi.org/10.1111/j.1365-313X.2009.03847.x
Pandey DK, Chaudhary B (2014) Oxidative stress responsive SERK1 gene directs the progression of somatic embryogenesis in cotton (Gossypium hirsutum L. cv. Coker 310). Am J Plant Sci 05:80–102. https://doi.org/10.4236/ajps.2014.51012
Pandey DK, Chaudhary B (2016) Domestication-driven Gossypium profilin 1 (GhPRF1) gene transduces early flowering phenotype in tobacco by spatial alteration of apical/floral-meristem related gene expression. BMC Plant Biol 16:201310. https://doi.org/10.1186/s12870-016-0798-0
Pandey DK, Chaudhary B (2017) Evolutionary expansion and structural functionalism of the ancient family of profilin proteins. Gene 626:70–86. https://doi.org/10.1016/j.gene.2017.05.024
Pandey DK, Chaudhary B (2019) Synchronous transcription of cytoskeleton-associated genes is critical to cotton fiber elongation. J Plant Growth Regul 38:1037–1061. https://doi.org/10.1007/s00344-019-09913-0
Pandey DK, Chaudhary B (2021) Transcriptional loss of domestication-driven cytoskeletal GhPRF1 gene causes defective floral and fiber development in cotton (Gossypium). Plant Mol Biol 107:519–532. https://doi.org/10.1007/S11103-021-01200-5
Prelich G (2012) Gene overexpression: uses, mechanisms, and interpretation. Genetics 190:841–854
Pu L, Li Q, Fan X, Yang W, Xue Y (2008) The R2R3 MYB transcription factor GhMYB109 is required for cotton fiber development. Genetics 180:811–820. https://doi.org/10.1534/genetics.108.093070
Ramachandran S, Christensen HEM, Ishimaru Y, Dong CH, Chao-Ming W, Cleary AL, Chua NH (2000) Profilin plays a role in cell elongation, cell shape maintenance, and flowering in Arabidopsis. Plant Physiol 124:1637–1647. https://doi.org/10.1104/pp.124.4.1637
Rao AQ, Irfan M, Saleem Z, Nasir IA, Riazuddin S, Husnain T (2011) Overexpression of the phytochrome B gene from Arabidopsis thaliana increases plant growth and yield of cotton (Gossypium hirsutum). J Zhejiang Univ Sci B 12:326–334. https://doi.org/10.1631/jzus.B1000168
Shan C-M, Shangguan X-X, Zhao B, Zhang X-F, Chao L, Yang C-Q, Wang L-J, Zhu H-Y, Zeng Y-D, Guo W-Z, Zhou B-L, Hu G-J, Guan X-Y, Chen ZJ, Wendel JF, Zhang T-Z, Chen X-Y (2014) Control of cotton fibre elongation by a homeodomain transcription factor GhHOX3. Nat Commun 5:5519. https://doi.org/10.1038/ncomms6519
Stewart JM (1975) Fiber initiation on the cotton ovule (Gossypium hirsutum). Am J Bot 62:723–730. https://doi.org/10.1002/j.1537-2197.1975.tb14105.x
Taliercio EW, Boykin D (2007) Analysis of gene expression in cotton fiber initials. BMC Plant Biol. https://doi.org/10.1186/1471-2229-7-22
Veitia RA, Bottani S, Birchler JA (2008) Cellular reactions to gene dosage imbalance: genomic, transcriptomic and proteomic effects. Trends Genet 24:390–397
Walford S-A, Wu Y, Llewellyn DJ, Dennis ES (2012) Epidermal cell differentiation in cotton mediated by the homeodomain leucine zipper gene, GhHD-1. Plant J. https://doi.org/10.1111/j.1365-313X.2012.05003.x
Wan CY, Wilkins TA (1994) A modified hot borate method significantly enhances the yield of high-quality RNA from cotton (Gossypium hirsutum L.). Anal Biochem 223:7–12. https://doi.org/10.1006/abio.1994.1538
Wang S, Wang J-W, Yu N, Li C-H, Luo B, Gou J-Y, Wang L-J, Chen X-Y (2004) Control of plant trichome development by a cotton fiber MYB gene. Plant Cell 16:2323–2334. https://doi.org/10.1105/tpc.104.024844
Wang HY, Wang J, Gao P, Jiao GL, Zhao PM, Li Y, Wang GL, Xia GX (2009) Down-regulation of GhADF1 gene expression affects cotton fibre properties. Plant Biotechnol J 7:13–23. https://doi.org/10.1111/j.1467-7652.2008.00367.x
Wang J, Wang HY, Zhao PM, Han LB, Jiao GL, Zheng YY, Huang SJ, Xia GX (2010) Overexpression of a profilin (GhPFN2) promotes the progression of developmental phases in cotton fibers. Plant Cell Physiol 51:1276–1290. https://doi.org/10.1093/pcp/pcq086
Wang L, Cook A, Patrick JW, Chen XY, Ruan YL (2014) Silencing the vacuolar invertase gene GhVIN1 blocks cotton fiber initiation from the ovule epidermis, probably by suppressing a cohort of regulatory genes via sugar signaling. Plant J 78:686–696. https://doi.org/10.1111/tpj.12512
Xu WL, Zhang DJ, Wu YF, Qin LX, Huang GQ, Li J, Li L, Li XB (2013) Cotton PRP5 gene encoding a proline-rich protein is involved in fiber development. Plant Mol Biol 82:353–365. https://doi.org/10.1007/s11103-013-0066-8
Zhang M, Zheng X, Song S, Zeng Q, Hou L, Li D, Zhao J, Wei Y, Li X, Luo M, Xiao Y, Luo X, Zhang J, Xiang C, Pei Y (2011) Spatiotemporal manipulation of auxin biosynthesis in cotton ovule epidermal cells enhances fiber yield and quality. Nat Biotechnol 29:453–458. https://doi.org/10.1038/nbt.1843
Zhang F, Jin X, Wang L, Li S, Wu S, Cheng C, Zhang T, Guo W (2016) A cotton annexin affects fiber elongation and secondary cell wall biosynthesis associated with Ca2+ influx, ROS homeostasis, and actin filament reorganization. Plant Physiol 171:1750–1770. https://doi.org/10.1104/PP.16.00597
Zhang M, Han LB, Wang WY, Wu SJ, Jiao GL, Su L, Xia GX, Wang HY (2017) Overexpression of GhFIM2 propels cotton fiber development by enhancing actin bundle formation. J Integr Plant Biol 59:531–534
Acknowledgements
The authors are thankful to the Department of Biotechnology (DBT), Government of India for providing financial support to carry out this research work. The authors also thank Prof. Deepak Pental, University of Delhi South Campus, New Delhi, India for providing the cotton seeds, pPRT100 cloning vector, pPZP200 binary vector and Agrobacterium tumefaciens strain GV3101.
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The current research is funded by the Department of Biotechnology (DBT), Government of India.
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Both authors contributed to conceptualizing the present study. The experiments were conducted by DKP, and BC helped with the data collection. Both DKP and BC wrote and approved the final manuscript.
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Pandey, D.K., Chaudhary, B. Ectopic Overexpression of Domestication-Driven Cytoskeletal Profilin (GhPRF1) Gene Improves Flowering and Trichome Development in Cotton (Gossypium hirsutum L.). J Plant Growth Regul (2024). https://doi.org/10.1007/s00344-024-11329-4
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DOI: https://doi.org/10.1007/s00344-024-11329-4