Skip to main content
SpringerLink
Log in

Functional divergence of GhCFE5 homoeologs revealed in cotton fiber and Arabidopsis root cell development

  • Original Article
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

In GhCFE5 homoeologs, GhCFE5D interacted with more actin homologs and stronger interaction activity than GhCFE5A. GhCFE5D - but not GhCFE5A -overexpression severely disrupted actin cytoskeleton organization and significantly suppressed cell elongation.

Abstract

Homoeologous genes are common in polyploid plants; however, their functional divergence is poorly elucidated. Allotetraploid Upland cotton (Gossypium hirsutum, AADD) is the most widely cultivated cotton; accounting for more than 90 % of the world’s cotton production. Here, we characterized GhCFE5A and GhCFE5D homoeologs from G. hirsutum acc TM-1. GhCFE5 homoeologs are expressed preferentially in fiber cells; and a significantly greater accumulation of GhCFE5A mRNA than GhCFE5D mRNA was found in all tested tissues. Overexpression of GhCFE5D but not GhCFE5A seriously inhibits the Arabidopsis hypocotyl and root cell elongation. Yeast two-hybrid assay and bimolecular fluorescence complementation (BiFC) analysis showed that compared with GhCFE5A, GhCFE5D interacts with more actin homologs and has a stronger interaction activity both from Arabidopsis and Upland cotton. Interestingly, subcellular localization showed that GhCFE5 resides on the cortical endoplasmic reticulum (ER) network and is colocalized with actin cables. The interaction activities between GhCFE5 homoeologs and actin differ in their effects on F-actin structure in transgenic Arabidopsis root cells. The F-actin changed direction from vertical to lateral, and the actin cytoskeleton organization was severely disrupted in GhCFE5D-overexpressing root cells. These data support the functional divergence of GhCFE5 homoeologs in the actin cytoskeleton structure and cell elongation, implying an important role for GhCFE5 in the evolution and selection of cotton fiber.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

CaMV:

Caulifower mosaic virus

DAG:

Day after germination

DPA:

Day post anthesis

DUF:

Domain of unknown function

SNPs:

Single-nucleotide polymorphisms

NPT-II:

Neomycin phosphotransferase II

ER:

Endoplasmic reticulum

GFP:

Green fluorescent protein

RFP:

Red fluorescent protein

References

  • Abbott R, Albach D, Ansell S, Arntzen JW, Baird SJ, Bierne N, Boughman J, Brelsford A, Buerkle CA, Buggs R, Butlin RK, Dieckmann U, Eroukhmanoff F, Grill A, Cahan SH, Hermansen JS, Hewitt G, Hudson AG, Jiggins C, Jones J, Keller B, Marczewski T, Mallet J, Martinez-Rodriguez P, Most M, Mullen S, Nichols R, Nolte AW, Parisod C, Pfennig K, Rice AM, Ritchie MG, Seifert B, Smadja CM, Stelkens R, Szymura JM, Vainola R, Wolf JB, Zinner D (2013) Hybridization and speciation. J Evol Biol 26:229–246

    Article  CAS  PubMed  Google Scholar 

  • Adams KL, Cronn R, Percifield R, Wendel JF (2003) Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing. Proc Natl Acad Sci USA 100:4649–4654

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Applequist WL, Cronn R, Wendel JF (2001) Comparative development of fiber in wild and cultivated cotton. Evol Dev 3:3–17

    Article  CAS  PubMed  Google Scholar 

  • Bateman A, Coggill P, Finn RD (2010) DUFs: families in search of function. Acta Crystallogr Sect F Struct Biol Cryst Commun 66:1148–1152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen ZJ (2010) Molecular mechanisms of polyploidy and hybrid vigor. Trends Plant Sci 15:57–71

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen CY, Cheung AY, Wu HM (2003) Actin-depolymerizing factor mediates Rac/Rop GTPase-regulated pollen tube growth. Plant Cell 15:237–249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen M, Ha M, Lackey E, Wang J, Chen ZJ (2008) RNAi of met1 reduces DNA methylation and induces genome-specific changes in gene expression and centromeric small RNA accumulation in Arabidopsis allopolyploids. Genetics 178:1845–1858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Doyle JJ, Flagel LE, Paterson AH, Rapp RA, Soltis DE, Soltis PS, Wendel JF (2008) Evolutionary genetics of genome merger and doubling in plants. Annu Rev Genet 42:443–461

    Article  CAS  PubMed  Google Scholar 

  • Endrizzi JE, Turcotte EL, Kohel RJ (1985) Genetics, cytology and evolution of Gossypium. Adv Genet 23:271–375

    Article  Google Scholar 

  • Finn RD, Mistry J, Schuster-Bockler B, Griffiths-Jones S, Hollich V, Lassmann T, Moxon S, Marshall M, Khanna A, Durbin R, Eddy SR, Sonnhammer EL, Bateman A (2006) Pfam: clans, web tools and services. Nucleic Acids Res 34:D247–D251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39:W29–W37

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gilliland LU, Kandasamy MK, Pawloski LC, Meagher RB (2002) Both vegetative and reproductive actin isovariants complement the stunted root hair phenotype of the Arabidopsis act2-1 mutation. Plant Physiol 130:2199–2209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gilliland LU, Pawloski LC, Kandasamy MK, Meagher RB (2003) Arabidopsis actin gene ACT7 plays an essential role in germination and root growth. Plant J 33:319–328

    Article  CAS  PubMed  Google Scholar 

  • Guan X, Pang M, Nah G, Shi X, Ye W, Stelly DM, Chen ZJ (2014) miR828 and miR858 regulate homoeologous MYB2 gene functions in Arabidopsis trichome and cotton fibre development. Nat Commun 5:3050

    Article  PubMed  Google Scholar 

  • Guo W, Cai C, Wang C, Han Z, Song X, Wang K, Niu X, Wang C, Lu K, Shi B, Zhang T (2007) A microsatellite-based, gene-rich linkage map reveals genome structure, function and evolution in Gossypium. Genetics 176:527–541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo W, Cai C, Wang C, Zhao L, Wang L, Zhang T (2008) A preliminary analysis of genome structure and composition in Gossypium hirsutum. BMC Genom 9:314

    Article  Google Scholar 

  • Ha M, Lu J, Tian L, Ramachandran V, Kasschau KD, Chapman EJ, Carrington JC, Chen X, Wang XJ, Chen ZJ (2009) Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids. Proc Natl Acad Sci USA 106:17835–17840

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ha M, Ng DW, Li WH, Chen ZJ (2011) Coordinated histone modifications are associated with gene expression variation within and between species. Genome Res 21:590–598

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu Z, Song N, Xing J, Chen Y, Han Z, Yao Y, Peng H, Ni Z, Sun Q (2013) Overexpression of three TaEXPA1 homoeologous genes with distinct expression divergence in hexaploid wheat exhibit functional retention in Arabidopsis. PLoS One 8:e63667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hutchinson JB (1951) Intra-specific differentiation in Gossypium hirsutum. Heredity 5:161–193

    Article  Google Scholar 

  • Jiang JX, Zhang TZ (2003) Extraction of total RNA in cotton tissues with CTAB-acidic phenolic method. Cotton Sci 15:166–167

    Google Scholar 

  • Jiang C, Wright RJ, El-Zik KM, Paterson AH (1998) Polyploid formation created unique avenues for response to selection in Gossypium (cotton). Proc Natl Acad Sci USA 95:4419–4424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kandasamy MK, McKinney EC, Meagher RB (2009) A single vegetative actin isovariant overexpressed under the control of multiple regulatory sequences is sufficient for normal Arabidopsis development. Plant Cell 21:701–718

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kenan-Eichler M, Leshkowitz D, Tal L, Noor E, Melamed-Bessudo C, Feldman M, Levy AA (2011) Wheat hybridization and polyploidization results in deregulation of small RNAs. Genetics 188:263–272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lashermes P, Combes MC, Hueber Y, Severac D, Dereeper A (2014) Genome rearrangements derived from homoeologous recombination following allopolyploidy speciation in coffee. Plant J 78:674–685

    Article  CAS  PubMed  Google Scholar 

  • Lee JJ, Woodward AW, Chen ZJ (2007) Gene expression changes and early events in cotton fibre development. Ann Bot 100:1391–1401

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leitch AR, Leitch IJ (2008) Genomic plasticity and the diversity of polyploid plants. Science 320:481–483

    Article  CAS  PubMed  Google Scholar 

  • Li S, Blanchoin L, Yang Z, Lord EM (2003) The putative Arabidopsis arp2/3 complex controls leaf cell morphogenesis. Plant Physiol 132:2034–2044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Jiang J, Li L, Wang XL, Wang NN, Li DD, Li XB (2013) A cotton LIM domain-containing protein (GhWLIM5) is involved in bundling actin filaments. Plant Physiol Biochem 66:34–40

    Article  CAS  PubMed  Google Scholar 

  • Li F, Fan G, Wang K, Sun F, Yuan Y, Song G, Li Q, Ma Z, Lu C, Zou C, Chen W, Liang X, Shang H, Liu W, Shi C, Xiao G, Gou C, Ye W, Xu X, Zhang X, Wei H, Li Z, Zhang G, Wang J, Liu K, Kohel RJ, Percy RG, Yu JZ, Zhu YX, Wang J, Yu S (2014) Genome sequence of the cultivated cotton Gossypium arboreum. Nat Genet 46:567–572

    Article  CAS  PubMed  Google Scholar 

  • Li L, Li Y, Wang NN, Li Y, Lu R, Li XB (2015) Cotton LIM domain-containing protein GhPLIM1 is specifically expressed in anthers and participates in modulating F-actin. Plant Biol (Stuttg) 17:528–534

    Article  CAS  Google Scholar 

  • Liu T, Tian J, Wang G, Yu Y, Wang C, Ma Y, Zhang X, Xia G, Liu B, Kong Z (2014) Augmin triggers microtubule-dependent microtubule nucleation in interphase plant cells. Curr Biol 24:2708–2713

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Mathur J, Hulskamp M (2002) Microtubules and microfilaments in cell morphogenesis in higher plants. Curr Biol 12:R669–R676

    Article  CAS  PubMed  Google Scholar 

  • Miller DD, De Ruijter NCA, Bisseling T, Emons AMC (1999) The role of actin in root hair morphogenesis: studies with lipochito-oligosaccharides as a growth stimulator and cytochalasin as an actin perturbing drug. Plant J 17:141–154

    Article  CAS  Google Scholar 

  • Ng DW, Lu J, Chen ZJ (2012) Big roles for small RNAs in polyploidy, hybrid vigor, and hybrid incompatibility. Curr Opin Plant Biol 15:154–161

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Ruan YL (2007) Goldacre paper: rapid cell expansion and cellulose synthesis regulated by plasmodesmata and sugar: insights from the single-celled cotton fibre. Funct Plant Biol 34:1–10

    Article  CAS  Google Scholar 

  • Ruan YL, Llewellyn DJ, Furbank RT (2001) The control of single-celled cotton fiber elongation by developmentally reversible gating of plasmodesmata and coordinated expression of sucrose and K+ transporters and expansin. Plant Cell 13:47–60

    CAS  PubMed  PubMed Central  Google Scholar 

  • Smart LB, Vojdani F, Maeshima M, Wilkins TA (1998) Genes involved in osmoregulation during turgor-driven cell expansion of developing cotton fibers are differentially regulated. Plant Physiol 116:1539–1549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Ooijen JW, Voorrips RE (2001) JoinMap® Version 3.0, software for the calculation of genetic linkage maps. Plant Research International, Wageningen

    Google Scholar 

  • Waadt R, Kudla J (2008) In planta visualization of protein interactions using bimolecular fluorescence complementation (BiFC). CSH Protoc 3:t4995

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Wang H, Guo Y, Lv F, Zhu H, Wu S, Jiang Y, Li F, Zhou B, Guo W, Zhang T (2010a) The essential role of GhPEL gene, encoding a pectate lyase, in cell wall loosening by depolymerization of the de-esterified pectin during fiber elongation in cotton. Plant Mol Biol 72:397–406

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Wang HY, Zhao PM, Han LB, Jiao GL, Zheng YY, Huang SJ, Xia GX (2010b) Overexpression of a profilin (GhPFN2) promotes the progression of developmental phases in cotton fibers. Plant Cell Physiol 51:1276–1290

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Zhang J, Yuan M, Ehrhardt DW, Wang Z, Mao T (2012) Arabidopsis microtubule destabilizing protein40 is involved in brassinosteroid regulation of hypocotyl elongation. Plant Cell 24:4012–4025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wendel JF (1989) New World tetraploid cottons contain Old World cytoplasm. In Proc Natl Acad Sci USA 86:4132–4136

    Article  CAS  Google Scholar 

  • Wendel JF, Cronn RC (2003) Polyploidy and the evolutionary history of cotton. Adv Agron 78:139–186

    Article  Google Scholar 

  • Yamamoto E, Baird WV (1998) Three cotton fiber-expressed cDNAs (Accession Nos. AF072404, AF072405, and AF072406) (PGR 98–144). Plant Physiol 117:1525–1527

    Article  Google Scholar 

  • Yoo MJ, Wendel JF (2014) Comparative evolutionary and developmental dynamics of the cotton (Gossypium hirsutum) fiber transcriptome. PLoS Genet 10:e1004073

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang T, Hu Y, Jiang W, Fang L, Guan X, Chen J, Zhang J, Saski CA, Scheffler BE, Stelly DM, Hulse-Kemp AM, Wan Q, Liu B, Liu C, Wang S, Pan M, Wang Y, Wang D, Ye W, Chang L, Zhang W, Song Q, Kirkbride RC, Chen X, Dennis E, Llewellyn DJ, Peterson DG, Thaxton P, Jones DC, Wang Q, Xu X, Zhang H, Wu H, Zhou L, Mei G, Chen S, Tian Y, Xiang D, Li X, Ding J, Zuo Q, Tao L, Liu Y, Li J, Lin Y, Hui Y, Cao Z, Cai C, Zhu X, Jiang Z, Zhou B, Guo W, Li R, Chen ZJ (2015) Sequencing of allotetraploid cotton (Gossypium hirsutum acc. TM-1) provides a resource for fiber improvement. Nat Biotechnol 33:531–537

    Article  CAS  PubMed  Google Scholar 

  • Zhou R, Moshgabadi N, Adams KL (2011) Extensive changes to alternative splicing patterns following allopolyploidy in natural and resynthesized polyploids. Proc Natl Acad Sci USA 108:16122–16127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This program was financially supported in part by National Natural Science Foundation of China (31471539), a project funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions (010-809001), and Jiangsu Collaborative Innovation Center for Modern Crop Production (No. 10).

Author information

Authors and Affiliations

  1. State Key Laboratory of Crop Genetics and Germplasm Enhancement, Hybrid Cotton R&D Engineering Research Center, MOE, Nanjing Agricultural University, Nanjing, 210095, Jiangsu, People’s Republic of China

    Fenni Lv, Peng Li, Rui Zhang, Nina Li & Wangzhen Guo

Authors
  1. Fenni Lv
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peng Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rui Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nina Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Wangzhen Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Wangzhen Guo.

Ethics declarations

Conflict of interest

The authors have declared that no competing interests exist.

Additional information

Communicated by D.-B. Zhang.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lv, F., Li, P., Zhang, R. et al. Functional divergence of GhCFE5 homoeologs revealed in cotton fiber and Arabidopsis root cell development. Plant Cell Rep 35, 867–881 (2016). https://doi.org/10.1007/s00299-015-1928-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-015-1928-0

Keywords

Search

Navigation