Abstract
An autopolyploid that contains more than two sets of the same chromosomes causes apparent alterations in morphology, development, physiology and gene expression compared to diploid. However, the mechanisms for these changes remain largely unknown. In the present study, cytological observations of mature embryos and growing cotyledons demonstrated that enlarged organ size of an autotetraploid Arabidopsis was caused by cell size and not by cell number. Quantitative real time PCR (qRT-PCR) analysis of 34 core cell cycle genes revealed a subtle but stable increase in the expression of ICK1, ICK2 and ICK5 in autotetraploid seedlings. Autotetraploid Arabidopsis plants were found to be more sensitive to glucose treatment than diploid with decreased number of rosette leaves and suppressed root elongation. Cytological observations demonstrated that both cell proliferation and cell expansion of autotetraploid were dramatically suppressed under glucose treatment. Expression levels of ICK1, ICK5 together with Cyclin D and Cyclin B was increased under glucose treatment in both diploid and autotetraploid plants. These results suggest that ICK1 and ICK5 may be involved in developmental delay and that the suppressed growth under glucose treatment probably resulted from disturbed mitotic and endoreduplication cycle in autotetraploid Arabidopsis.
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Abbreviations
- WT:
-
Wild type
- DAS:
-
Days after sowing
- DAP:
-
Days after pollination
- DAT:
-
Days after treating
References
Abràmoff MD, Magalhes PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics Int 11:36–42
Albertin W, Brabant P, Catrice O, Eber F, Jenczewski E, Chèvre AM, Thiellement H (2005) Autopolyploidy in cabbage (Brassica oleracea L.) does not alter significantly the proteomes of green tissues. Proteomics 5:2131–2139
Allario T, Brumos J, Colmenero-Flores JM, Tadeo F, Froelicher Y, Talon M, Navarro L, Ollitrault P, Morillon R (2011) Large changes in anatomy and physiology between diploid Rangpur lime (Citrus limonia) and its autotetraploid are not associated with large changes in leaf gene expression. J Exp Bot 62:2507–2519
Anderson LE (1954) Hoyer’s solution as a rapid permanent mounting medium for bryophytes. Bryologist 57:242–244
Anssour S, Krugel T, Sharbel TF, Saluz HP, Bonaventure G, Baldwin IT (2009) Phenotypic, genetic and genomic consequences of natural and synthetic polyploidization of Nicotiana attenuata and Nicotiana obtusifolia. Ann Bot Lond 103:1207–1217
Bolouri-Moghaddam MR, Le Roy K, Xiang L, Rolland F, Van den Ende W (2010) Sugar signalling and antioxidant network connections in plant cells. FEBS J 277:2022–2037
Boudolf V, Vlieghe K, Beemster GTS, Magyar Z, Acosta JAT, Maes S, Van Der Schueren E, Inzé D, De Veylder L (2004) The plant-specific cyclin-dependent kinase CDKB1;1 and transcription factor E2Fa-DPa control the balance of mitotically dividing and endoreduplicating cells in Arabidopsis. Plant Cell 16:2683–2692
Bouharmont J, Mace F (1972) Valeur competitive des plantes autotetraploides d’Arabidopsis thaliana. Can J Genet Cytol 14:257–263
Bowman JL, Smyth DR, Meyerowitz EM (1991) Genetic interactions among floral homeotic genes of Arabidopsis. Development 112:1–20
Chen ZJ (2007) Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annu Rev Plant Biol 58:377–406
Chen ZJ, Ni Z (2006) Mechanisms of genomic rearrangements and gene expression changes in plant polyploids. BioEssays 28:240–252
Comai L (2005) The advantages and disadvantages of being polyploid. Nat Rev Genet 6:836–846
Couée I, Sulmon C, Gouesbet G, El Amrani A (2006) Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. J Exp Bot 57:449–459
Datar SA, Jacobs HW, de la Cruz AFA, Lehner CF, Edgar BA (2000) The Drosophila cyclin D–Cdk4 complex promotes cellular growth. EMBO J 19:4543–4554
Deng B, Du W, Liu C, Sun W, Tian S, Dong H (2012) Antioxidant response to drought, cold and nutrient stress in two ploidy levels of tobacco plants: low resource requirement confers polytolerance in polyploids? Plant Growth Regul 66:37–47
Dewitte W, Murray JAH (2003) The plant cell cycle. Annu Rev Plant Biol 54:235–264
Dong S, Adams KL (2011) Differential contributions to the transcriptome of duplicated genes in response to abiotic stresses in natural and synthetic polyploids. New Phytol 190:1045–1057
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
Ferreira T, Rasband W (2010) The ImageJ User Guide-Version 1.43. US National Institutes of Health, Bethesda. Available at http://rsb.info.nih.gov/ij
Freeling M, Thomas BC (2006) Gene-balanced duplications, like tetraploidy, provide predictable drive to increase morphological complexity. Genome Res 16:805–814
Fujikura U, Horiguchi G, Tsukaya H (2007) Dissection of enhanced cell expansion processes in leaves triggered by a defect in cell proliferation, with reference to roles of endoreduplication. Plant Cell Physiol 48:278–286
Galbraith DW, Harkins KR, Knapp S (1991) Systemic endopolyploidy in Arabidopsis thaliana. Plant Physiol 96:985–989
Inzé D, De Veylder L (2006) Cell cycle regulation in plant development. Annu Rev Genet 40:77–105
Kasajima I, Yoshizumi T, Ichikawa T, Matsui M, Fujiwara T (2010) Possible involvement of ploidy in tolerance to boron deficiency in Arabidopsis thaliana. Plant Biotechnol 27:435–445
Kurata T, Ishida T, Kawabata-Awai C, Noguchi M, Hattori S, Sano R, Nagasaka R, Tominaga R, Koshino-Kimura Y, Kato T (2005) Cell-to-cell movement of the CAPRICE protein in Arabidopsis root epidermal cell differentiation. Development 132:5387–5398
León P, Sheen J (2003) Sugar and hormone connections. Trends Plant Sci 8:110–116
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 −ΔΔ CT method. Methods 25:402–408
MacAuley A, Cross JC, Werb Z (1998) Reprogramming the cell cycle for endoreduplication in rodent trophoblast cells. Mol Biol Cell 9:795–807
Mallet J (2007) Hybrid speciation. Nature 446:279–283
Meng H, Jiang S, Hua S, Lin X, Li Y, Guo W, Jiang L (2011) Comparison between a tetraploid turnip and its diploid progenitor (Brassica rapa L.): the adaptation to salinity stress. Agr Sci China 10:363–375
Mhadhbi H, Jebara M, Zitoun A, Limam F, Aouani ME (2008) Symbiotic effectiveness and response to mannitol-mediated osmotic stress of various chickpea-rhizobia associations. World J Microb Biot 24:1027–1035
Moore B, Zhou L, Rolland F, Hall Q, Cheng WH, Liu YX, Hwang I, Jones T, Sheen J (2003) Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science 300:332–336
Mouhaya W, Allario T, Brumos J, Andrés F, Froelicher Y, Luro F, Talon M, Ollitrault P, Morillon R (2010) Sensitivity to high salinity in tetraploid citrus seedlings increases with water availability and correlates with expression of candidate genes. Funct Plant Biol 37:674–685
Osborn TC, Chris Pires J, Birchler JA, Auger DL, Chen ZJ, Lee HS, Comai L, Madlung A, Doerge R, Colot V (2003) Understanding mechanisms of novel gene expression in polyploids. Trends Genet 19:141–147
Pignatta D, Dilkes BP, Yoo SY, Henry IM, Madlung A, Doerge RW, Chen ZJ, Comai L (2010) Differential sensitivity of the Arabidopsis thaliana transcriptome and enhancers to the effects of genome doubling. New Phytol 186:194–206
Ramon M, Rolland F, Sheen J (2008) Sugar sensing and signaling. Arabidopsis Book 6:e0117. doi:10.1199/tab.0117
Riddle NC, Jiang HM, An LL, Doerge RW, Birchler JA (2010) Gene expression analysis at the intersection of ploidy and hybridity in maize. Theor Appl Genet 120:341–353
Riou-Khamlichi C, Menges M, Healy J, 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
Saleh B, Allario T, Dambier D, Ollitrault P, Morillon R (2008) Tetraploid citrus rootstocks are more tolerant to salt stress than diploid. CR Biol 331:703–710
Schnittger A, Schöbinger U, Bouyer D, Weinl C, Stierhof YD, Hülskamp M (2002a) Ectopic D-type cyclin expression induces not only DNA replication but also cell division in Arabidopsis trichomes. Proc Natl Acad Sci USA 99:6410–6415
Schnittger A, Schbinger U, Stierhof YD, Hülskamp M (2002b) Ectopic B-type cyclin expression induces mitotic cycles in endoreduplicating Arabidopsis trichomes. Curr Biol 12:415–420
Sheen J (2010) Discover and connect cellular signaling. Plant Physiol 154:562–566
Sherr CJ (1995) D-type cyclins. Trends Biochem Sci 20:187–190
Soltis PS, Soltis DE (2009) The role of hybridization in plant speciation. Annu Rev Plant Biol 60:561–588
Soltis DE, Soltis PS, Tate JA (2004) Advances in the study of polyploidy since plant speciation. New Phytol 161:173–191
Stupar RM, Bhaskar PB, Yandell BS, Rensink WA, Hart AL, Ouyang S, Veilleux RE, Busse JS, Erhardt RJ, Buell CR, Jiang JM (2007) Phenotypic and transcriptomic changes associated with potato autopolyploidization. Genetics 176:2055–2067
Sugiyama S (2005) Polyploidy and cellular mechanisms changing leaf size: comparison of diploid and autotetraploid populations in two species of Lolium. Ann Bot Lond 96:931–938
Vandepoele K, Raes J, De Veylder L, Rouzé P, Rombauts S, Inzé D (2002) Genome-wide analysis of core cell cycle genes in Arabidopsis. Plant Cell 14:903–916
Wang H, Qi Q, Schorr P, Cutler AJ, Crosby WL, Fowke LC (1998) ICK1, a cyclin-dependent protein kinase inhibitor from Arabidopsis thaliana interacts with both Cdc2a and CycD3, and its expression is induced by abscisic acid. Plant J 15:501–510
Wang H, Zhou Y, Fowke LC (2006) The emerging importance of cyclin-dependent kinase inhibitors in the regulation of the plant cell cycle and related processes. Can J Bot 84:640–650
Wolf G, Schroeder R, Ziyadeh F, Thaiss F, Zahner G, Stahl R (1997) High glucose stimulates expression of p27Kip1 in cultured mouse mesangial cells: relationship to hypertrophy. Am J Physiol Renal 273:348–356
Wolf G, Schroeder R, Zahner G, Stahl RAK, Shankland SJ (2001) High glucose-induced hypertrophy of mesangial cells requires p27Kip1, an inhibitor of cyclin-dependent kinases. Am J Pathol 158:1091–1100
Yanagisawa S, Yoo SD, Sheen J (2003) Differential regulation of EIN3 stability by glucose and ethylene signalling in plants. Nature 425:521–525
Yang M, Yang Q, Fu T, Zhou Y (2011) Overexpression of the Brassica napus BnLAS gene in Arabidopsis affects plant development and increases drought tolerance. Plant Cell Rep 30:373–388
Yao H, Kato A, Mooney B, Birchler JA (2011) Phenotypic and gene expression analyses of a ploidy series of maize inbred Oh43. Plant Mol Biol 75:237–251
Yu Z, Haage K, Streit VE, Gierl A, Ruiz RAT (2009) A large number of tetraploid Arabidopsis thaliana lines, generated by a rapid strategy, reveal high stability of neo-tetraploids during consecutive generations. Theor Appl Genet 118:1107–1119
Yu Z, Haberer G, Matthes M, Rattei T, Mayer KF, Gierl A, Torres-Ruiz RA (2010) Impact of natural genetic variation on the transcriptome of autotetraploid Arabidopsis thaliana. Proc Natl Acad Sci USA 107:17809–17814
Zhang XY, Hu CG, Yao JL (2010) Tetraploidization of diploid Dioscorea results in activation of the antioxidant defense system and increased heat tolerance. J Plant Physiol 167:88–94
Zhou Y, Fowke L, Wang H (2002a) 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
Zhou YM, Wang H, Gilmer S, Whitwill S, Keller W, Fowke LC (2002b) Control of petal and pollen development by the plant cyclin-dependent kinase inhibitor ICK1 in transgenic Brassica plants. Planta 215:248–257
Zhu G, Ye N, Zhang J (2009) Glucose-induced delay of seed germination in rice is mediated by the suppression of ABA catabolism rather than an enhancement of ABA biosynthesis. Plant Cell Physiol 50:644–651
Acknowledgments
We thank Professor Luca Comai (University of California, Davis, USA) for providing the autotetraploid Arabidopsis 4COL seeds. This research was financially supported by a NSFC project (30471097) and the National Basic Research Program (2006CB101604) from Ministry of Science and Technology of China, and a PCSIRT fund (IRT0442) from Ministry of Education of China.
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425_2012_1629_MOESM8_ESM.tif
Supplementary Fig. S7 Flow cytometric analysis (FCM) of autotetraploid and diploid under glucose and mannitol treatment (TIFF 769 kb)
425_2012_1629_MOESM9_ESM.tif
Supplementary Fig. S8 Relative expression level of cell cycle genes in WT, BS and 4COL plants under glucose treatment (TIFF 481 kb)
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Li, X., Yu, E., Fan, C. et al. Developmental, cytological and transcriptional analysis of autotetraploid Arabidopsis . Planta 236, 579–596 (2012). https://doi.org/10.1007/s00425-012-1629-7
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DOI: https://doi.org/10.1007/s00425-012-1629-7