Skip to main content
SpringerLink
Log in

Overexpression of Arabidopsis cyclin D2;1 in cotton results in leaf curling and other plant architectural modifications

  • Original Paper
  • Published:
Plant Cell, Tissue and Organ Culture (PCTOC) Aims and scope Submit manuscript

Abstract

The D-class cyclin genes play key roles in controlling the cell cycle in plant development. To evaluate the effects of D-type cyclins on plant architecture, ectopic expression of the Arabidopsis cyclinD2;1 (Arath;CYCD2;1) gene driven by the CaMV35S promoter was investigated in cotton via Agrobacterium-mediated transformation. Northern blot showed the cyclinD2;1 gene was highly expressed in transgenic cotton plants. Phenotype investigation showed that overexpression of Arath;CYCD2;1 led to obvious leaf architecture change: the leaf epidermis of transgenic plants consist of more small cells compared to the wild-type. Mesophyll cells in the inner layers of Arath;CYCD2;1 plants were organized more loosely than those in the inner layers of wild-type plants. Moreover, transgenic plants had darker leaves, more chlorophyll, and a higher rate of photosynthesis than wild-type plants in the field. Tissue cultures indicated that the overexpression of Arath;CYCD2;1 promoted callus formation in the absence of exogenous auxin, but inhibited cell differentiation. The qRT-PCR revealed that several cell cycle–associated genes, particularly the transcript levels of GhRBR and GhCYCD3;1 were regulated by the Arath;CYCD2;1 insertion. The results implied that the cotton plant architecture or cell culture characters could be regulated by ectopic expression of the Arabidopsis cyclinD2;1 gene.

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
Fig. 8

Similar content being viewed by others

Abbreviations

CaMV:

Cauliflower mosaic virus

CDK:

Cyclin-dependent kinase

ICK:

Inhibitor of cyclin-dependent kinase

RBR:

Retinoblastoma-related protein

NPA:

N-1-naphthylphthalamic acid

MCM:

Minichromosomal maintenance

References

  • Arnon DI (1949) Cooper enzymes isolated chloroplasts polyphenol oxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  PubMed  CAS  Google Scholar 

  • Beemster GTS, Mironov V, Inze D (2005) Tuning the cell-cycle engine for improved plant performance. Curr Opin Biotechnol 16:142–146

    Article  PubMed  CAS  Google Scholar 

  • Borghi L, Gutzat R, Futterer J, Laizet YH, Hennig L, Gruissem W (2010) Arabidopsis RETINOBLASTOMA-RELATED is required for stem cell maintenance, cell differentiation, and lateral organ production. Plant Cell 22:1792–1811

    Article  PubMed  CAS  Google Scholar 

  • Brendel V, Kleffe J, Carle Urioste JC, Walbot V (1998) Prediction of splice sites in plant pre-mRNA from sequence properties. J Mol Biol 276:85–104

    Article  PubMed  CAS  Google Scholar 

  • Cockcroft CE, den Boer BGW, Healy JM, Murray JAH (2000) Cyclin D control of growth rate in plants. Nature 405:575–579

    Article  PubMed  CAS  Google Scholar 

  • De Veylder L, Beeckman T, Inze D (2007) The ins and outs of the plant cell cycle. Nat Rev Mol Cell Biol 8:655–665

    Article  PubMed  Google Scholar 

  • Desvoyes B, Ramirez Parra E, Xie Q, Chua NH, Gutierrez C (2006) Cell type-specific role of the retinoblastoma/E2F pathway during Arabidopsis leaf development. Plant Physiol 140:67–80

    Article  PubMed  CAS  Google Scholar 

  • Dewitte W, Riou Khamlichi C, Scofield S, Healy JM, Jacqmard A, Kilby NJ, Murray JAH (2003) Altered cell cycle distribution, hyperplasia, and inhibited differentiation in Arabidopsis caused by the D-type cyclin CYCD3. Plant Cell 15:79–92

    Article  PubMed  CAS  Google Scholar 

  • Ebel C, Mariconti L, Gruissem W (2004) Plant retinoblastoma homologues control nuclear proliferation in the female gametophyte. Nature 429:776–780

    Article  PubMed  CAS  Google Scholar 

  • Falster DS, Westoby M (2003) Leaf size and angle vary widely across species: what consequences for light interception? New Phytol 158:509–525

    Article  Google Scholar 

  • Francis D (2007) The plant cell cycle—15 years on. New Phytol 174:261–278

    Article  PubMed  CAS  Google Scholar 

  • Hu YX, Bao F, Li JY (2000) Promotive effect of brassinosteroids on cell division involves a distinct CycD3-induction pathway in Arabidopsis. Plant J 24:693–701

    Article  PubMed  CAS  Google Scholar 

  • Huntley R, Healy S, Freeman D, Lavender P, de Jager S, Greenwood J, Makker J, Walker E, Jackman M, Xie Q, Bannister AJ, Kouzarides T, Gutiérrez C, Doonan JH, Murray JAH (1998) The maize retinoblastoma protein homologue ZmRb-1 is regulated during leaf development and displays conserved interactions with G1/S regulators and plant cyclin D (CycD) proteins. Plant Mol Biol 37:155–169

    Article  PubMed  CAS  Google Scholar 

  • Inze D, De Veylder L (2006) Cell cycle regulation in plant development. Annu Rev Genet 40:77–105

    Article  PubMed  CAS  Google Scholar 

  • Jin SX, Zhang XL, Liang SG, Nie YC, Guo XP, Huang C (2005) Factors affecting transformation efficiency of embryogenic callus of upland cotton (Gossypium hirsutum) with Agrobacterium tumefaciens. Plant Cell, Tissue Organ Cult 81:229–237

    Article  CAS  Google Scholar 

  • Jin SX, Zhang XL, Nie YC, Guo XP, Liang SG, Zhu HG (2006) Identification of a novel elite genotype for in vitro culture and genetic transformation of cotton. Biol Plantarum 50:519–524

    Article  CAS  Google Scholar 

  • Meijer M, Murray JAH (2001) Cell cycle controls and the development of plant form. Curr Opin Plant Biol 4:44–49

    Article  PubMed  CAS  Google Scholar 

  • Menges M, Samland AK, Planchais S, Murray JAH (2006) The D-type cyclin CYCD3;1 is limiting for the G1-to-S-phase transition in Arabidopsis. Plant Cell 18:893–906

    Article  PubMed  CAS  Google Scholar 

  • Menges M, Pavesi G, Morandini P, Bogre L, Murray JAH (2007) Genomic organization and evolutionary conservation of plant D-type cyclins. Plant Physiol 145:1558–1576

    Article  PubMed  CAS  Google Scholar 

  • Montero-Cortés M, Rodríguez-Paredes F, Burgeff C, Pérez-Nuñez T, Córdova I, Oropeza C, Verdeil JL, Sáenz L (2010) Characterisation of a cyclin-dependent kinase (CDKA) gene expressed during somatic embryogenesis of coconut palm. Plant Cell, Tissue Organ Cult 102:251–258

    Article  Google Scholar 

  • Montero-Cortés M, Cordova I, Verdeil J-L, Hocher V, Pech y Ake A, Sandoval A, Oropeza C, Saenz L (2011) GA3 induces expression of E2F-like genes and CDKA during in vitro germination of zygotic embryos of Cocos nucifera (L). Plant Cell, Tissue Organ Cult 107:461–470

    Article  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plantarum 15:473–497

    Article  CAS  Google Scholar 

  • Nakagami H, Kawamura K, Sugisaka K, Sekine M, Shinmyo A (2002) Phosphorylation of retinoblastoma-related protein by the cyclin D/cyclin-dependent kinase complex is activated at the G1/S-phase transition in tobacco. Plant Cell 14:1847–1857

    Article  PubMed  CAS  Google Scholar 

  • Oakenfull EA, Riou Khamlichi C, Murray JAH (2002) Plant D-type cyclins and the control of G1 progression. Philos T Roy Soc B 357:749–760

    Article  CAS  Google Scholar 

  • Oh SJ, Kim SJ, Kim Y, Park SH, Ha SH, Kim JK (2008) Arabidopsis cyclin D2 expressed in rice forms a functional cyclin-dependent kinase complex that enhances seedling growth. Plant Biotechnol Rep 2:227–231

    Article  Google Scholar 

  • Park JA, Ahn JW, Kim YK, Kim SJ, Kim JK, Kim WT, Pai HS (2005) Retinoblastoma protein regulates cell proliferation, differentiation, and endoreduplication in plants. Plant J 42:153–163

    Article  PubMed  CAS  Google Scholar 

  • Paul S, Dam A, Bhattacharyya A, Bandyopadhyay T (2011) An efficient regeneration system via direct and indirect somatic embryogenesis for the medicinal tree Murraya koenigii. Plant Cell, Tissue Organ Cult 105:271–283

    Article  Google Scholar 

  • Qi R, John PCL (2007) Expression of genomic AtCYCD2;1 in Arabidopsis induces cell division at smaller cell sizes: Implications for the control of plant growth. Plant Physiol 144:1587–1597

    Article  PubMed  CAS  Google Scholar 

  • Riou-Khamlichi C, Huntley R, Jacqmard A, Murray JAH (1999) Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science 283:1541–1544

    Article  PubMed  CAS  Google Scholar 

  • Riou-Khamlichi C, Menges M, Healy JM, Murray JAH (2000) Sugar control of the plant cell cycle: differential regulation of Arabidopsis D-type cyclin gene expression. Mol Cell Biol 20:4513–4521

    Article  PubMed  CAS  Google Scholar 

  • Sanz L, Dewitte W, Forzani C, Patell F, Nieuwland J, Wen B, Quelhas P, De Jager S, Titmus C, Campilho A, Ren H, Estelle M, Wang H, Murray JAH (2011) The Arabidopsis D-type cyclin CYCD2;1 and the inhibitor ICK2/KRP2 modulate auxin-induced lateral root formation. Plant Cell 23:641–666

    Article  PubMed  CAS  Google Scholar 

  • Shen LL, Chen Y, Su XH, Zhang SG, Pan HX, Huang MR (2012) Two FT orthologs from Populus simonii Carrière induce early flowering in Arabidopsis and poplar trees. Plant Cell, Tissue Organ Cult 108:371–379

    Article  CAS  Google Scholar 

  • Soni R, Carmichael JP, Shah ZH, Murray JAH (1995) A family of cyclin D homologs from plants differentially controlled by growth regulators and containing the conserved retinoblastoma protein interaction motif. Plant Cell 7:85–103

    PubMed  CAS  Google Scholar 

  • Tsukaya H (2006) Mechanism of leaf-shape determination. Annu Rev Plant Biol 57:477–496

    Article  PubMed  CAS  Google Scholar 

  • Wang F, Huo SN, Guo J, Zhang XS (2006) Wheat D-type cyclin Triae;CYCD2;1 regulate development of transgenic Arabidopsis plants. Planta 224:1129–1140

    Article  PubMed  CAS  Google Scholar 

  • Wyrzykowska J, Schorderet M, Pien S, Gruissem W, Fleming AJ (2006) Induction of differentiation in the shoot apical meristem by transient overexpression of a retinoblastoma-related protein. Plant Physiol 141:1338–1348

    Article  PubMed  CAS  Google Scholar 

  • Zeng FC, Zhang XL, Zhu LF, Tu LL, Guo XP, Nie YC (2006) Isolation and characterization of genes associated to cotton somatic embryogenesis by suppression subtractive hybridization and macroarray. Plant Mol Biol 60:167–183

    Article  PubMed  CAS  Google Scholar 

  • Zhang GH, Xu Q, Zhu XD, Qian Q, Xue HW (2009) SHALLOT-LIKE1 is a KANADI transcription factor that modulates rice leaf rolling by regulating leaf abaxial cell development. Plant Cell 21:719–735

    Article  PubMed  Google Scholar 

  • Zhou YM, Fowke LC, Wang H (2002) Plant CDK inhibitors: studies of interactions with cell cycle regulators in the yeast two-hybrid system and functional comparisons in transgenic Arabidopsis plants. Plant Cell Rep 20:967–975

    Article  CAS  Google Scholar 

  • Zhou YM, Wang H, Gilmer S, Whitwill S, Fowke LC (2003) Effects of co-expressing the plant CDK inhibitor ICK1 and D-type cyclin genes on plant growth, cell size and ploidy in Arabidopsis thaliana. Planta 216:604–613

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Dr. Y. M. Zhou for his generosity in providing the CycD2 cDNA vector and Dr. J. L. Yao for her help with histological observation. This work was supported by the National Natural Science Foundation of China (No. 30810103911).

Author information

Authors and Affiliations

  1. National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, 430070, Hubei, People’s Republic of China

    Guanze Liu, Shuangxia Jin, Xuyan Liu, Jiafu Tan, Xiyan Yang & Xianlong Zhang

Authors
  1. Guanze Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shuangxia Jin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xuyan Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jiafu Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xiyan Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xianlong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xianlong Zhang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liu, G., Jin, S., Liu, X. et al. Overexpression of Arabidopsis cyclin D2;1 in cotton results in leaf curling and other plant architectural modifications. Plant Cell Tiss Organ Cult 110, 261–273 (2012). https://doi.org/10.1007/s11240-012-0148-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-012-0148-3

Keywords

Search

Navigation