Abstract
In higher plants, one of the major components of developmental processes is cell division. The cell division cycle in plants is controlled by cyclins and cyclin-dependend kinases. Nutrient and hormonal signals can influence the roles that D-type cyclins play in the G1-to-S phase transition. Auxins and cytokinins are long known to be important plant hormones controlling plant growth. Additionally, as sucrose is the major transported carbon source in higher plants, it is possible that it plays a major role in cell division. To access the molecular aspects of the effect of auxin, cytokinin and sucrose on the regulation of cell cycle machinery and plant development, we cloned a Passiflora morifolia putative homolog to a D-type cyclin, PmCYCD1, which showed high sequence similarity to other known plant D-type cyclins. We examined the expression patterns of PmCYCD1 during callus induction and growth in in vitro conditions. We observed incremented expression levels of PmCYCD1 correlated to increasing concentrations of sucrose, α-naphthalene acetic acid and 6-benzyladenine in the culture medium. Additionally, the results of in situ hybridization experiments indicated a dynamic spatial expression pattern for PmCYCD1 during callus growth.
Similar content being viewed by others
References
Ach RA, Durfee T, Muller AB, Taranto P, Hanley-Bowdoin L, Zambryski PC, Gruissem W (1997) RRB1 and RRB2 encode maize retinoblastoma-related proteins that interact with a plant D-type cyclin and geminivirus replication protein. Mol Cell Biol 17:5077–5086
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Barroco RM, DeVeylder L, Magyar Z, Engler G, Inzé D, Mironov V (2003) Novel complexes of cyclin-dependent kinases and a cyclin-like protein from Arabidopsis thaliana with a function unrelated to cell division. Cell Mol Life Sci 60:401–412
Berckmans B, De Veylder L (2009) Transcriptional control of the cell cycle. Curr Opin Plant Biol 12:599–605
Bernier G, Havelange A, Houssa C, Petitjean A, Lejeune P (1993) Physiological signals that induce flowering. Plant Cell 5:1147–1155
Boniotti MB, Gutierrez C (2001) A cell-cycle-regulated kinase activity phosphorylates plant retinoblastoma protein and contains, in Arabidopsis, a CDKA/cyclin D complex. Plant J 28:341–350
Cho JW, Park SC, Shin EA, Kim CK, Han W, Sohn SI, Song PS, Wang MH (2004) Cyclin D1 and p22ack1 play opposite roles in plant growth and development. Biochem Biophys Res Commun 324:52–57
Cutri L, Dornelas MC (2012) PASSIOMA: exploring expressed sequence tags during flower development in Passiflora spp. Comp Func Genomics. doi:10.1155/2012/510549
Dahl M, Meskiene I, Bogre L, Ha DTC, Swoboda I, Hubmann R, Hirt H, Heberle-Bors E (1995) The D-type alfalfa cyclin gene cycMs4 complements G(I) cyclin-deficient yeast and is induced in the G(1) phase of the cell cycle. Plant Cell 7:1847–1857
Dangl JL, Preuss D, Schroeder JI (1985) Talking through walls: signaling in plant development. Cell 83:1071–1077
De Almeida-Engler J, Deveylder L, De Groodt R, Rombauts S, Boudolf V, De Meyer B, Hemerly A, Ferreira P, Beeckman T, Karimi M, Hilson P, Inzé D, Engler G (2009) Systematic analysis of cell-cycle gene expression during Arabidopsis development. Plant J 59:645–660
De Veylder L, De Almeida-Engler J, Burssens S, Manevski A, Lescure B, Van Montagu M, Engler G, Inzé D (1999) A new D-type cyclin of Arabidopsis thaliana expressed during lateral root primordia formation. Planta 208:453–462
Dewitte W, Murray JA (2003) The plant cell cycle. Annu Rev Plant Biol 54:235–264
Dewitte W, Scofield A, Alcasabas A, Maughan SC, Menges M, Braun N, Collins C, Nieuwland J, Prinsen E, Sundaresan V, Murray JAH (2007) Arabidopsis CYCD3 D-type cyclins link cell proliferation and endocycles and are rate-limiting for cytokinin responses. Proc Natl Acad Sci USA 104:14537–14542
Diehl JA, Sherr CJ (1997) A dominant-negative cyclin D1 mutant prevents nuclear import of cyclin-dependent kinase 4 (CDK4) and its phosphorylation by CDK-activating kinase. Mol Cell Biol 17:7362–7374
Diehl JA, Zindy F, Sherr CJ (1997) Inhibition of cyclin D1 phosphorylation on threonine-286 prevents its rapid degradation via the ubiquintinproteasome pathway. Genes Dev 11:957–972
Diehl JA, Cheng MG, Roussel MF, Sherr CJ (1998) Glycogen synthase kinase 3 beta regulates cyclin D1 proteolysis and subcellular localization. Genes Dev 12:3499–3511
Dong Q, Zhao Y, Jiang H, He H, Zhu S, Cheng B, Xiang Y (2011) Genome-wide identification and characterization of the cyclin gene family in Populus trichocarpa. Plant Cell Tiss Organ Cult 107:55–67
Dornelas MC, Vieira MLC (1994) Tissue culture on species of Passiflora. Plant Cell Tiss Organ Cult 36:211–217
Dornelas MC, Van Lammeren AA, Kreis M (2000) Arabidopsis thaliana SHAGGY-related protein kinases (AtSK11 and 12) function in perianth and gynoecium development. Plant J 21:419–429
Dornelas MC, Fonseca TC, Rodriguez APM (2006) Brazilian passionflowers and novel passionate tropical flowering gems. In: Silva JAT (ed) Floriculture, ornamental and plant biotechnology, vol 4. Global Science Books, London, pp 629–639
Ewen ME, Sluss HK, Sherr CJ, Matsushime H, Kato J, Livingston DM (1993) Functional interactions of the retinoblastoma protein with mammalian D-type cyclins. Cell 73:487–497
Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunasekaran P, Ceric G, Forslund K, Holm L, Sonnhammer LE, Eddy SR, Bateman A (2010) The Pfam protein families database. Nucleic Acids Res 38(Database issue):D211–D222
Gaudin V, Lunness PA, Fobert PR, Tower M, Riou-Khamlichi C, Murray JAH, Coen E, Doonan JH (2000) The expression of D-cyclin genes defines distinct developmental zones in snap-dragon apical meristems and is locally regulated by the Cycloidea gene. Plant Physiol 122:1137–1148
Gonzalez N, Beemster GT, Inzé D (2009) David and Goliath: what can the tiny weed Arabidopsis teach us to improve biomass production in crops? Curr Opin Plant Biol 12:157–164
Halford NG, Paul MJ (2003) Carbon metabolite sensing and signaling. Plant Biotechnol J 1:381–398
Harashima H, Schnittger A (2010) The integration of cell division, growth and differentiation. Curr Opin Plant Biol 13:66–74
Harashima H, Kato K, Shinmyo A, Sekine M (2007) Auxin is required for the assembly of A-type cyclin-dependent kinase complexes in tobacco cell suspension culture. J Plant Physiol 164:1103–1112
Hartig K, Beck E (2005) Crosstalk between auxin, cytokinins, and sugars in the plant cell cycle. Plant Biol 8:389–396
Huang X, Madan A (1999) CAP3: a DNA sequence assembly program. Genome Res 9:868–877
Huntley R, Healy JMS, Freeman D, Lavender P, De Jager SM, Greenwood J, Makker J, Walker E, Jackman M, Xie Q, Bannister AJ, Kouzarides T, Gutiérrez C, Doonan JH, Murray JA (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
Jeffrey PD, Russo AA, Polyak K, Gibbs E, Hurwitz J, Massagué J, Pavletich NP (1995) Mechanism of CDK activation revealed by the structure of a cyclin A-CDK2 complex. Nature 376:313–320
Kawamura K, Murray JAH, Shinmyo A, Sekine M (2006) Cell cycle regulated D3-type cyclins form active complexes with plant-specific B-type cyclin-dependent kinase in vitro. Plant Mol Biol 61:311–327
Kono A, Umeda-Hara C, Adachi S, Nagata N, Konomi M, Nakagawa T, Ushimiya H, Umeda M (2007) The Arabidopsis D-type cyclin CYCD4 controls cell division in the stomatal lineage of the hypocotyl epidermis. Plant Cell 19:1265–1277
Koroleva OA, Tomlinson M, Parinyapong P, Sakvarelidze L, Leader D, Shaw P, Doonan JH (2004) CYCD1, a putative G1 cyclin from Antirrhinum majus, accelerates the cell cycle in cultured tobacco BY-2 cells by enhancing both G1/S entry and progression through S and G2 phases. Plant Cell 16:2364–2379
Kwon HK, Wang MH (2011) The D-type cyclin gene (Nicta;CycD3;4) controls cell cycle progression in response to sugar availability in tobacco. J Plant Physiol 168:133–139
Liu G, Jin S, Liu X, Tan J, Yang X, Zhang X (2012) 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
Marcel M, Murray JAH (2001) Cell cycle controls and the development of plant form. Curr Opin Plant Biol 4:44–49
Menges M, Murray JAH (2007) Plant D-type cyclins: structure, roles and functions. In: Bryant J, Francis D (eds) Eukaryotic cell cycle, society for experimental biology seminar series, vol 59. Taylor and Francis, Abingdon, pp 1–28
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
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
Montero-Cortés M, Rodríguez-Paredes F, Burgeff C, Pérez-Nuñes T, Cordova I, Oropeza C, Verdeil J-L, Saénz L (2010) Characterisation of a cyclin-dependent kinase (CDKA) gene expressed during somatic embryogenesis of coconut palm. Plant Cell Tiss Organ Cult 102:251–258
Montero-Cortés M, Cordova I, Verdeil J-L, Hocher V, Ake AP, Sandoval A, Oropeza C, Saénz L (2011) GA3 induces expression of E2F-like genes and CDKA during in vitro germination of zygotic embryos of Cocos nucifera (L.). Plant Cell Tiss Organ Cult 107:461–470
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497
Nakagami H, Kawamura K, Sugisaka K, Sekine M, Shinmyo A (2002) Phosphorilation 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
Nieuwland J, Maughan S, Dewitte W, Scofield S, Sanz L, Murray JAH (2009) The D-type cyclin CYCD4;1 modulates lateral root densisty in Arabidopsis by affecting the basal meristem region. Proc Natl Acad Sci USA 106:22528–22533
Oakenfull EA, Riou-Khamlichi C, Murray JAH (2002) Plant D-type cyclins and the control of G1 progression. Philos Trans R Soc Lond B Biol Sci 357:749–760
Page RDM (1996) Treeview: an application to display phylogenetic trees on personal computers. Comp Appl Biosci 12:357–358
Planchais S, Samland AK, Murray JAH (2004) Differential stability of Arabidopsis D-type cyclins: CYCD3;1 is a highly unstable protein degraded by a proteasome-dependent mechanism. Plant J 38:616–625
Potuschak T, Doerner P (2001) Cell cycle controls: genome-wide analysis in Arabidopsis. Curr Opin Plant Biol 4:501–506
Rechsteiner M, Rogers SW (1996) PEST sequences and regulation by Proteolysis. Trends Biochem Sci 21:267–271
Renaudin JP, Doonan JH, Freeman D, Hashimoto J, Hirt H, Inzé D, Jacobs T, Kouchi H, Rouzé P, Sauter M, Savouré A, Sorrel DA, Sundaresan V, Murray JA (1996) Plant cyclins: a unified nomenclature for plant A-, B- and D-type cyclins based on sequence organization. Plant Mol Biol 33:1003–1018
Riou-Khamlichi C, Menges M, Healy JMS, 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
Rosa YBCJ, Dornelas MC (2012) In vitro plant regeneration and de novo differentiation of secretory trichomes in Passiflora foetida L. (Passifloraceae). Plan Cell Tiss Organ Cult 108:91–99
Saitou M, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Singh RK, Dasgupta S, Bhattacharya N, Chunder N, Mondal R, Roy A, Mandal S, Roychowdhury S, Panda CK (2005) Deletion in chromosome 11 and Bcl-1/Cyclin-D1 alterations are independently associated with the development of uterine cervical carcinoma. J Cancer Res Clin Oncol 131:395–406
Soni R, Carmichael JP, Shah ZH, Murray JA (1995) A family of cyclinD homologs from plants differentially controlled by growth regulators and containing the conserved retinoblastoma protein interaction motif. Plant Cell 7:85–103
Sorrell DA, Combettes B, Chaubet-Gigot N, Gigot C, Murray JAH (1999) Distinct cyclin D genes show mitotic accumulation or constant levels of transcripts in tobacco bright yellow-2 cells. Plant Physiol 119:343–351
Steeves TA, Sussex IM (1989) Patterns in plant development. Cambridge University Press, Cambridge
Su’udi M, Cha JY, Ahn I-P, Kwak Y-S, Woo Y-M, Son D (2012) Functional characterization of a B-type cell cycle switch in rice (OsCCS52B). Plant Cell Tiss Organ Cult 111:101–111
Thomas BR, Rodriguez RL (1994) Metabolite signals regulate gene expression and source/sink relations in cereal seedlings. Plant Physiol 106:1235–1239
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Vandepoele K, Raes J, De Veylder L, Rouze P, Rombauts S, Inzé D (2002) Genome-wide analysis of core cell cycle genes in Arabidopsis. Plant Cell 14:903–916
Wang G, Kong H, Sun Y, Zhang X, Zhang W, Altman N, De Pamphilis CW, Ma H (2004) Genome-wide analysis of the cyclin family in Arabidopsis and comparative phylogenetic analysis of plant cyclin-like proteins. Plant Physiol 135:1084–1099
Wang F, Huo SN, Guo J, Zhang XS (2006) Wheat D-type cyclin Triae;CYCD2;1 regulates development of transgenic Arabidopsis plants. Planta 224:1129–1140
Acknowledgments
To Prof EW Kitajima and Prof F Tanaka for maintaining the electron microscope facility at NAP/MEPA-ESALQ/USP. To Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Brazil), Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, São Paulo, Brazil) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil) for funding.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Rosa, Y.B.C.J., Aizza, L.C.B., Armanhi, J.S.L. et al. A Passiflora homolog of a D-type cyclin gene is differentially expressed in response to sucrose, auxin, and cytokinin. Plant Cell Tiss Organ Cult 115, 233–242 (2013). https://doi.org/10.1007/s11240-013-0355-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11240-013-0355-6