Abstract
Low temperature restrains plant growth by inhibiting the cell cycle, and phytohormones play important roles in this case; however, the molecular mechanisms whereby phytohormones affect growth at low temperature are largely unknown. When grown at 23, 16, 10, and 4°C, we found that Arabidopsis thaliana could develop with normal morphology, but needed a prolonged period of cultivation. By screening mutants, we could implicate cytokinin and salicylic acid. At 4°C, both amp1 plants, which have an increased level of cytokinin, and wild-type plants treated with exogenous cytokinin, displayed relative growth rates greater than control by increasing total cell number. Additionally, transgenic NahG plants, which have lower salicylic acid content, grew faster than wild-type accompanied by larger cells. Expression of C-repeat binding transcription factors (CBFs), that mediate cold acclimation by stimulation of the expression of cold-inducible genes, was similar in all tested genotypes. Thus CBF expression did not correlate with the observed enhanced growth in mutants. The improved growth coincided with elevated expression of CYCD3;1, especially in NahG plants. At 4°C, enhanced endoreduplication took responsibility for larger cells in NahG plants, while enhanced cell division was observed in amp1 plants.
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References
Barnouin K, Dubuisson ML, Child ES, Fernandez de Mattos S, Glassford J, Medema RH, Mann DJ, Lam EW (2002) H2O2 induces a transient multi-phase cell cycle arrest in mouse fibroblasts through modulating cyclin D and p21Cip1 expression. J Biol Chem 277:13761–13770. doi:10.1074/jbc.M111123200
Chaudhury AM, Letham S, Craig S, Dennis ES (1993) amp1: a mutant with high cytokinin levels and altered embryonic pattern, faster vegetative growth, constitutive photomorphogenesis and precocious flowering. Plant J 4:907–916. doi:10.1046/j.1365-313X.1993.04060907.x
Chin-Atkins AN, Craig S, Hocart CH, Dennis ES, Chaudhury AM (1996) Increased endogenous cytokinin in the Arabidopsis amp1 mutant corresponds with de-etiolation responses. Planta 198:549–556. doi:10.1007/BF00262641
Cook D, Fowler S, Fiehn O, Thomashow M (2004) A prominent role for the CBF cold response pathway in configuring the low-temperature metabolome of Arabidopsis. Proc Natl Acad Sci USA 101:15243–15248. doi:10.1073/pnas.0406069101
Dewitte W, Riou-Khamlichi C, Scofield S, Healy JM, Jacqmard A, Kilby NJ, Murray JA (2003) Altered cell cycle distribution, hyperplasia, and inhibited differentiation in Arabidopsis caused by the D-type cyclin CYCD3. Plant Cell 15:79–92. doi:10.1105/tpc.004838
Dewitte W, Scofield S, Alcasabas AA, Maughan SC, Menges M, Braun N, Collins C, Nieuwland J, Prinsen E, Sundaresan V, Murray AH (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. doi:10.1073/pnas.0704166104
Francis D, Barlow PW (1988) Temperature and cell cycle. Symp Soc Exp Biol 42:181–201
Galbraith DW, Harkins KR, Knapp S (1991) Systemic endopolypolidy in Arabidopsis thaliana. Plant Physiol 96:985–989
Gendreau E, Traas J, Desnos T, Grandjean O, Caboche M, Höfte H (1997) Cellular basis of hypocotyl growth in Arabidopsis thaliana. Plant Physiol 114:295–305. doi:10.1104/pp.114.1.295
Gendreau E, Orbovic V, Höfte H, Traas J (1999) Gibberelin and ethylene control endoreduplication levels in the Arabidopsis thaliana hypocotyl. Planta 209:513–516
Gilmour SJ, Artus NN, Thomashow MF (1992) cDNA sequence analysis and expression of two cold-regulated genes of Arabidopsis thaliana. Plant Mol Biol 18:13–21. doi:10.1007/BF00018452
Gilmour SJ, Zarka DG, Stockinger EJ, Salazar MP, Houghton JM, Thomashow MF (1998) Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant J 16:433–442. doi:10.1046/j.1365-313x.1998.00310.x
Giménez-Abián MI, Rozalén AE, Carballo JA, Botella LM, Pincheira J, López-Sáez JF, de la Torrel C (2004) HSP90 and checkpoint-dependent lengthening of the G2 phase observed in plant cells under hypoxia and cold. Protoplasma 223:191–196. doi:10.1007/s00709-003-0022-6
Hartwell LH, Weinert TA (1989) Checkpoints: controls that ensure the order of cell cycle events. Science 246:629–634. doi:10.1126/science.2683079
Helliwell CA, Chin-Atkins AN, Wilson IW, Chapple R, Dennis ES, Chaudhury A (2001) The Arabidopsis AMP1 gene encodes a putative glutamate carboxypeptidase. Plant Cell 13:2115–2125
Hu Y, Bao F, Li J (2000) Promotive effect of brassinosteroids on cell division involves a distinct CYCD3-induction pathway in Arabidopsis. Plant J 24:693–701. doi:10.1046/j.1365-313x.2000.00915.x
Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280:104–106. doi:10.1126/science.280.5360.104
Kieber JJ, Rothenberg M, Roman G, Feldmann KA, Ecker JR (1993) CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a number of the raf family of protein kinases. Cell 72:427–441. doi:10.1016/0092-8674(93)90119-B
Kondorosi E, Roudier F, Gendreau E (2000) Plant cell-size control: growing by ploidy? Curr Opin Plant Biol 3:488–492. doi:10.1016/S1369-5266(00)00118-7
Kurkela S, Borg-Frank M (1992) Structure and expression of kin2, one of two cold- and ABA-induced genes of Arabidopsis thaliana. Plant Mol Biol 19:689–692. doi:10.1007/BF00026794
Levitt J (1980) Responses of plants to environmental stress: chilling, freezing, and high temperature stress. Academic Press, New York, pp 166–248
Lyons JM (1973) Chilling injury in plants. Annu Rev Plant Physiol 24:445–466. doi:10.1146/annurev.pp.24.060173.002305
Melaragno JK, Mehrotra B, Coleman AW (1993) Relationship between endopolyploidy and cell size in epidermal tissue of Arabidopsis. Plant Cell 5:1661–1668
Menges M, Samland AK, Planchais S, Murray AH (2006) The D-type cyclin CYCD3;1 is limiting for the G1-to-S-phase transition in Arabidopsis. Plant Cell 18:893–906. doi:10.1105/tpc.105.039636
Nogué F, Hocart C, Letham DS, Dennis ES, Chaudhury AM (2000) Cytokinin synthesis is higher in the Arabidopsis amp1 mutant. Plant Growth Regul 32:267–273. doi:10.1023/A:1010720420637
Nordin K, Vahala T, Palva ET (1993) Differential expression of two related low-temperature-induced genes in Arabidopsis thaliana (L.) Heynh. Plant Mol Biol 21:641–653. doi:10.1007/BF00014547
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. doi:10.1098/rstb.2002.1085
Pearce RS (1999) Molecular analysis of acclimation to cold. Plant Growth Regul 29:47–76. doi:10.1023/A:1006291330661
Riou-Khamlichi C, Huntley R, Jacqmard A, Murray AH (1999) Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science 283:1541–1544. doi:10.1126/science.283.5407.1541
Riou-Khamlichi C, Menges M, Sandra Healy JM, Murray AH (2000) Sugar control of plant cell cycle: differential regulation of Arabidopsis D-type cyclin gene expression. Mol Cell Biol 20:4513–4521. doi:10.1128/MCB.20.13.4513-4521.2000
Rymen B, Fiorani F, Kartl F, Vandepoele K, Inzé D, Beemaster GTS (2007) Cold nights impair leaf growth and cell cycle progression in maize through transcriptional changes of cell cycle genes. Plant Physiol 143:1429–1438. doi:10.1104/pp.106.093948
Schneider JC, Nielsen E, Somerville C (1995) A chilling-sensitive mutant of Arabidopsis is deficient in chloroplast protein accumulation at low temperature. Plant Cell Environ 18:23–31. doi:10.1111/j.1365-3040.1995.tb00540.x
Scott IM, Clarke SM, Wood JE, Mur LA (2004) Salicylate accumulation inhibits growth at chilling temperature in Arabidopsis. Plant Physiol 135:1040–1049. doi:10.1104/pp.104.041293
Sozzani R, Maggio C, Varotto S, Canova S, Bergounioux C, Albani D, Cella R (2006) Interplay between Arabidopsis activating factors E2Fb and E2Fa in cell cycle progression and development. Plant Physiol 140:1355–1366. doi:10.1104/pp.106.077990
Sugimoto-Shirasu K, Roberts K (2003) “Big it up”: endoreduplication and cell size control in plants. Curr Opin Plant Biol 6:544–553. doi:10.1016/j.pbi.2003.09.009
Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol 50:571–599. doi:10.1146/annurev.arplant.50.1.571
Thomashow MF (2001) So what’s new in the filed of plant cold acclimation? Lots! Plant Physiol 125:89–93. doi:10.1104/pp.125.1.89
Vanacker H, Lu H, Rate DN, Greenberg JT (2001) A role for salicylic acid and NPR1 in regulating cell growth in Arabidopsis. Plant J 28:209–216. doi:10.1046/j.1365-313X.2001.01158.x
Veselova SV, Farhutdinov RG, Veselov SY, Kudoyarova GR, Veselov DS, Hartung W (2005) The effect of root cooling on hormone content, leaf conductance and root hydraulic conductivity of durum wheat seedlings (Triticum durum L.). J Plant Physiol 162:21–26. doi:10.1016/j.jplph.2004.06.001
Xiong L, Ishitani M, Lee H, Zhu JK (2001) The Arabidopsis LOS5/ABA3 locus encodes a molybdenum cofactor sulfurase and modulates cold stress- and osmotic stress-responsive gene expression. Plant Cell 13:2063–2083
Yamaguchi-Shinozaki K, Shinozaki K (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low temperature, or high-salt stress. Plant Cell 6:251–264
Zhu J, Dong CH, Zhu JK (2007) Interplay between cold-responsive gene regulation, metabolism and RNA processing during plant cold acclimation. Curr Opin Plant Biol 10:290–295. doi:10.1016/j.pbi.2007.04.010
Acknowledgments
This work was supported by NSF of China (Grant No. 30328003), STM of China (Grant No. 2007CB948201) and PHR (IHLB) of Beijing Municipal Commission of Education to He. We are very grateful to Tobias I. Baskin (University of Massachusetts Amherst) for critical revision and comments on the manuscript and Ren Zhang (University of Wollongong, Australia) for invaluable discussions.
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Xia, J., Zhao, H., Liu, W. et al. Role of cytokinin and salicylic acid in plant growth at low temperatures. Plant Growth Regul 57, 211–221 (2009). https://doi.org/10.1007/s10725-008-9338-8
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DOI: https://doi.org/10.1007/s10725-008-9338-8