Abstract
This paper includes the characterization of an activation-tagged mutant named rippled leaf that displays distinctive rippled-leaf morphology. Gene expression and microscopic analysis were done to characterize the rippled leaf mutant, and transgenic overexpression lines were generated and characterized using these methods. The rippled leaf mutant was found to have an activated CYCLIN D1 (CYCD1;2), and overexpression of the gene using the 35S CaMV promoter resulted in plants with a highly similar leaf morphology. Microscopic analysis of the midvein of the rippled leaf mutant revealed that the mutant possessed significantly smaller and more numerous cortical parenchyma cells in its midvein compared with wild type. As well, in rippled leaf, the vascular tissue represented a larger proportion of the midvein. In transgenic lines, there was a similar change in cortical cell size, and an even larger proportion of the midvein was vascular tissue. In conclusion, a mutant with a leaf alteration phenotype was characterized. The CYCD1;2 gene was found to be responsible for this phenotype, and the phenotype was recapitulated using overexpression of transgenic lines. Further studies with mutants such as rippled leaf are necessary for a better understanding of cell division and its relationship to plant growth and development.
Similar content being viewed by others
References
Arias RS, Filichkin SA, Strauss SH (2006) Divide and conquer: development and cell cycle genes in plant transformation. Trends Biotechnol 24:267–273
Buendía-Monreal M, Rentería-Canett I, Guerrero-Andrade O, Bravo-Alberto CE, Martínez-Castilla LP, García E, Vázquez-Ramos JM (2011) The family of maize D-type cyclins: genomic organization, phylogeny and expression patterns. Physiol Plant 143:297–308
Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Report 11:113–116
Cho JW, Park SC, Shin EA, Kim CK, Han W, Sohn S, Song PS, Wang MH (2004) Cyclin D1 and p22 ack1 play opposite roles in plant growth and development. Biochem Biophys Res Commun 324:52–57
Cockcroft CE, den Boer BGW, Healy JMS, Murray JAH (2000) Cyclin D control of growth rate in plants. Nature 405:575–579
Cui L, Li J, Zhang T, Guo Q, Xu J, Lou Q, Chen J (2014) Identification and expression analysis of D-type cyclin genes in early developing fruit of cucumber (Cucumis sativus L.). Plant Mol Biol Report 32:209–218
De Veylder L, Beeckman T, Beemster GTS, de Almeida EJ, Ormenese S, Maes S, Naudts M, Van Der Schueren E, Jacqmard A, Engler G et al (2002) Control of proliferation, endoreduplication and differentiation by the Arabidopsis E2Fa/DPa transcription factor. EMBO J 21:1360–1368
De Veylder L, Beeckman T, Inzé D (2007) The ins and outs of plant cell cycle. Nat Rev Mol Cell Biol 8:655–665
Dewitte W, Riou-Khamlichi C, Scofield S, Healy JMS, 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
Dewitte W, Scofield S, Alcasabas AA, Maughan SC, Menges M, Braun N, Collins C, Nieuwland J, Prinsen E, Sundaresan V et al (2007) Arabidopsis CYCD3 D-type cyclins link cell proliferation and endocycles and are rate-limiting for cytokinin responses. Proc Natl Acad Sci 104:14537–14542
Donnelly PM, Bonetta D, Tsukaya H, Dengler RE, Dengler NG (1999) Cell cycling and cell enlargement in developing leaves of Arabidopsis. Dev Biol 215:407–419
Erickson RO, Michelini FJ (1957) The plastochron index. Am J Bot 44:297–304
Gaudin V, Lunness PA, Fobert PR, Towers M, Riou-Khamlichi C, Murray JAH, Coen E, Doonan JH (2000) The expression of D-cyclin genes defines distinct developmental zones in snapdragon apical meristems and is locally regulated by the Cycloidea gene. Plant Physiol 122:1137–1148
Gleave AP (1992) A versatile binary vector system with a T-DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome. Plant Mol Biol 20:1203–1207
Gonzalez N, Vanhaeren H, Inzé D (2012) Leaf size control: complex coordination of cell division and expansion. Trends Plant Sci 17:332–340
Groover A, Robischon M (2006) Developmental mechanisms regulating secondary growth in woody plants. Curr Opin Plant Biol 9:55–58
Guivarc’h A, Carneiro M, Vilaine F, Pautot V, Chriqui D (1996) Tissue-specific expression of the ROLA gene mediates morphological changes in transgenic tobacco. Plant Mol Biol 30:125–134
Guo Y, Harwalkar J, Stacey DW, Hitomi M (2005) Destabilization of cyclin D1 message plays a critical role in cell cycle exit upon mitogen withdrawal. Oncogene 24:1032–1042
Gutierrez C (2005) Coupling cell proliferation and development in plants. Nat Cell Biol 7:535–541
Gutierrez C (2009) The Arabidopsis cell division cycle. Arabidopsis Book 7:e0120. doi:10.1199/tab.0120
Harrison EJ, Bush M, Plett JM, McPhee DP, Vitez R, O’Malley B, Sharma V, Bosnich W, Séguin A, MacKay J et al (2007) Diverse developmental mutants revealed in an activation-tagged population of poplar. Can J Bot 85:1071–1081
Hartmann T, Mult S, Suter M, Rennenberg H, Herschbach C (2000) Leaf age-dependent differences in sulphur assimilation and allocation in poplar (Populus tremula x P. alba) leaves. J Exp Bot 51:1077–1088
Ito M, Iwase M, Kodama H, Lavisse P, Komamine A, Nishihama R, Machida Y, Watanabe A (1998) A novel cis-acting element in promoters of plant B-type cyclin genes activates M phase-specific transcription. Plant Cell 10:331–341
Jasinski S, Riou-Khamlichi C, Roche O, Perennes C, Bergounioux C, Glab N (2002) The CDK inhibitor NtKIS1a is involved in plant development, endoreduplication and restores normal development of cyclin D3;1-overexpressing plants. J Cell Sci 115:973–982
Kee JJ, Jun SE, Baek SA, Lee TS, Cho MR, Hwang HS, Lee SC, Kim J, Kim GT, Im KH (2009) Overexpression of the DOWNWARD LEAF CURLING (DLC) gene from melon changes leaf morphology by controlling cell size and shape in Arabidopsis leaves. Mol Cells 28:93–98
Klynstra FB, Lycklama JC, Siebers AM, Burggraaf PD (1964) On the anatomy of the woody stem of the twisted hazel, Corylus anellana L. “Contorta”. Acta Bot Neerl 13:198–208
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
Larson PR, Isebrands JG (1971) The plastochron index as applied to developmental studies of cottonwood. Can J For Res 1:1–11
Lin J, Gunter LE, Harding SA, Kopp RF, McCord RP, Tsai C, Tuskan GA, Smart LB (2007) Development of AFLP and RAPD markers linked to a locus associated with twisted growth in corkscrew willow (Salix matsudana “Tortuosa”). Tree Physiol 27:1575–1583
Magyar Z, Mészáros T, Miskolczi P, Deák M, Fehér A, Brown S, Kondorosi E, Athanasiadis A, Pongor S, Bilgin M et al (1997) Cell cycle phase specificity of putative cyclin-dependant kinase variants in synchronized alfalfa cell. Plant Cell 9:223–235
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, Bögre L, Murray JAH (2007) Genomic organization and evolutionary conservation of plant D-type cyclins. Plant Physiol 145:1558–1576
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
Perikles S (2003) Q-Gene: processing quantitative real-time RT-PCR data. Bioinformatics 19:1439–1440
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
Renaudin JP, Doonan JH, Freeman D, Hashimoto J, Hirt H, Inzé D, Jacobs T, Kouchi H, Rouzé P, Sauter M et al (1996) Plant cyclins: a unified nomenclature for plant A-, B- and D-type cyclins based on sequence organization. Plant Mol Biol 32:1003–1018
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
Smith DC, Mechlenbacher SA (1996) Inheritance and contorted growth in hazelnut. Euphytica 89:211–213
Smolarkiewicz M, Dhonukshe P (2013) Formative cell divisions: principal determinants of plant morphogenesis. Plant Cell Physiol 54:333–342
Tsukaya H (2014) Comparative leaf development in angiosperms. Curr Opin Plant Biol 17:103–109
Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604
Uemukai K, Iwakawa H, Kosugi S, de Uemukai S, Kato K, Kondorosi E, Murray JAH, Ito M, Shinmyo A, Sekine M (2005) Transcriptional activation of tobacco E2F is repressed by co-transfection with the retinoblastoma-related proteins: cyclin D expression overcomes this repressor activity. Plant Mol Biol 57:83–100
Van’t Hof J (1966) Experimental control of DNA synthesizing and dividing cells in excised root tips of Pisum. Am J Bot 53:970–976
Wang G, Kong H, Sun Y, Zhang X, Zhang W, Altman N, dePamphilis 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
Acknowledgments
We would like to thank Laurie Yeates, the manager of the CFS greenhouse, and Terry Hay, Peter Tucker, and Kevin Mann for their advice and care of the mutants. We also thank Ying Chen for technical assistance in creation of the transgenic lines, Dr. Hans-Cees Speel for his willingness to share the photograph of corkscrew willow from bomengids.nl, Dr. Steven Strauss for permission to use a photo taken at his field trial of the activation-tagged lines in Corvallis, Oregon, Liz Clarke for her help in preparing the pictures for the figures and Caroline Simpson for editing the manuscript. This research was funded by the Natural Sciences and Engineering Research Council (SR) and Natural Resources Canada, Canadian Forestry Service A-base funds (TB). The activation-tagged lines were created with Genome Canada funding to SR.
Compliance with ethical standards
ᅟ
Conflict of interest
The authors declare that they have no conflict of interest.
Data archiving statement
PtaCYCD1;2 cDNA sequence has been submitted to GenBank (accession number KP902591).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by A. Brunner
This article is part of the Topical Collection on Gene Expression
Rights and permissions
About this article
Cite this article
Williams, M., Lowndes, L., Regan, S. et al. Overexpression of CYCD1;2 in activation-tagged Populus tremula x Populus alba results in decreased cell size and altered leaf morphology. Tree Genetics & Genomes 11, 66 (2015). https://doi.org/10.1007/s11295-015-0895-5
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11295-015-0895-5