Plant Growth Regulation

, 57:211 | Cite as

Role of cytokinin and salicylic acid in plant growth at low temperatures

  • Jinchan Xia
  • Huan Zhao
  • Weizhong Liu
  • Legong LiEmail author
  • Yikun HeEmail author
Original Paper


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.


Arabidopsis thaliana Cell cycle Low temperature amp1 NahG 



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.


  1. 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 PubMedCrossRefGoogle Scholar
  2. 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 CrossRefGoogle Scholar
  3. 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 CrossRefGoogle Scholar
  4. 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 PubMedCrossRefGoogle Scholar
  5. 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 PubMedCrossRefGoogle Scholar
  6. 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 PubMedCrossRefGoogle Scholar
  7. Francis D, Barlow PW (1988) Temperature and cell cycle. Symp Soc Exp Biol 42:181–201PubMedGoogle Scholar
  8. Galbraith DW, Harkins KR, Knapp S (1991) Systemic endopolypolidy in Arabidopsis thaliana. Plant Physiol 96:985–989PubMedCrossRefGoogle Scholar
  9. 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 PubMedCrossRefGoogle Scholar
  10. Gendreau E, Orbovic V, Höfte H, Traas J (1999) Gibberelin and ethylene control endoreduplication levels in the Arabidopsis thaliana hypocotyl. Planta 209:513–516PubMedGoogle Scholar
  11. 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 PubMedCrossRefGoogle Scholar
  12. 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 PubMedCrossRefGoogle Scholar
  13. 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 PubMedCrossRefGoogle Scholar
  14. Hartwell LH, Weinert TA (1989) Checkpoints: controls that ensure the order of cell cycle events. Science 246:629–634. doi: 10.1126/science.2683079 PubMedCrossRefGoogle Scholar
  15. 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 13:2115–2125PubMedCrossRefGoogle Scholar
  16. 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 PubMedCrossRefGoogle Scholar
  17. 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 PubMedCrossRefGoogle Scholar
  18. 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 PubMedCrossRefGoogle Scholar
  19. 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 PubMedCrossRefGoogle Scholar
  20. 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 PubMedCrossRefGoogle Scholar
  21. Levitt J (1980) Responses of plants to environmental stress: chilling, freezing, and high temperature stress. Academic Press, New York, pp 166–248Google Scholar
  22. Lyons JM (1973) Chilling injury in plants. Annu Rev Plant Physiol 24:445–466. doi: 10.1146/annurev.pp.24.060173.002305 CrossRefGoogle Scholar
  23. Melaragno JK, Mehrotra B, Coleman AW (1993) Relationship between endopolyploidy and cell size in epidermal tissue of Arabidopsis. Plant Cell 5:1661–1668PubMedCrossRefGoogle Scholar
  24. 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 PubMedCrossRefGoogle Scholar
  25. 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 CrossRefGoogle Scholar
  26. 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 PubMedCrossRefGoogle Scholar
  27. 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 PubMedCrossRefGoogle Scholar
  28. Pearce RS (1999) Molecular analysis of acclimation to cold. Plant Growth Regul 29:47–76. doi: 10.1023/A:1006291330661 CrossRefGoogle Scholar
  29. 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 PubMedCrossRefGoogle Scholar
  30. 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 PubMedCrossRefGoogle Scholar
  31. 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 PubMedCrossRefGoogle Scholar
  32. 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 CrossRefGoogle Scholar
  33. 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 PubMedCrossRefGoogle Scholar
  34. 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 PubMedCrossRefGoogle Scholar
  35. 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 PubMedCrossRefGoogle Scholar
  36. 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 CrossRefGoogle Scholar
  37. 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 PubMedCrossRefGoogle Scholar
  38. 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 PubMedCrossRefGoogle Scholar
  39. 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 PubMedCrossRefGoogle Scholar
  40. 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 13:2063–2083PubMedCrossRefGoogle Scholar
  41. 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 6:251–264PubMedCrossRefGoogle Scholar
  42. 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 PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  1. 1.College of Life ScienceCapital Normal UniversityBeijingChina
  2. 2.College of Life ScienceShanxi Normal UniversityLinfenChina

Personalised recommendations