Cytokinin response factor 6 negatively regulates leaf senescence and is induced in response to cytokinin and numerous abiotic stresses

Plant and Cell Physiology

Volumn 54, Issue 6, 2013, Pages 971-981

  Zwack, Paul J ^a   Robinson, Bruce R ^a   Risley, Monica G ^a   Rashotte, Aaron M ^a  

^a AUBURN UNIVERSITY   (United States)

Author keywords

Abiotic stress; Arabidopsis; Cytokinin; Cytokinin response factor; Senescence; Transcription factor

Indexed keywords

ARABIDOPSIS PROTEIN; CRF6 PROTEIN, ARABIDOPSIS; CYTOKININ; MESSENGER RNA; TRANSCRIPTION FACTOR;

ABIOTIC STRESS; ARABIDOPSIS; ARTICLE; BIOLOGICAL MODEL; CYTOKININ RESPONSE FACTOR; DARKNESS; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT DEVELOPMENT; PLANT LEAF; SENESCENCE; VASCULAR BUNDLE (PLANT);

ABIOTIC STRESS; ARABIDOPSIS; CYTOKININ; CYTOKININ RESPONSE FACTOR; SENESCENCE; TRANSCRIPTION FACTOR;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CYTOKININS; DARKNESS; GENE EXPRESSION REGULATION, PLANT; MODELS, BIOLOGICAL; MUTATION; PLANT DEVELOPMENT; PLANT LEAVES; PLANT VASCULAR BUNDLE; RNA, MESSENGER; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS;

ARABIDOPSIS;

EID: 84878869431     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pct049     Document Type: Article

References (52)

1. Abeles, F.B., Dunn, L.J., Morgens, P., Callahan, A., Dinterman, R.E. and Schmidt, J. (1988) Induction of 33-Kd and 60-Kd peroxidases during ethylene-induced senescence of cucumber cotyledons. Plant Physiol. 87: 609-615.
2. Ambler, J.R., Morgan, P.W. and Jordan, W.R. (1992) Amounts of zeatin and zeatin riboside in xylem sap of senescent and nonsenescent sorghum. Crop Sci. 32: 411-419.
3. Balazadeh, S., Parlitz, S., Mueller-Roeber, B. and Meyer, R.C. (2008) Natural developmental variations in leaf and plant senescence in Arabidopsis thaliana. Plant Biol. 10: 136-147.
4. Bano, A., Hansen, H., Dorffling, K. and Hahn, H. (1994) Changes in the contents of free and conjugated abscisic-acid, phaseic acid and cytokinins in xylem sap of drought-stressed sunflower plants. Phytochemistry 37: 345-347.
5. Besseau, S.B., Li, J. and Palva, E.T. (2012) WRKY54 and WRKY70 cooperate as negative regulators of leaf senescence in Arabidopsis thaliana. J. Exp. Bot. 63: 2667-2679.
6. Breeze, E., Harrison, E., McHattie, S., Hughes, L., Hickman, R., Hill, C. et al. (2011) High-resolution temporal profiling of transcripts during Arabidopsis leaf senescence reveals a distinct chronology of processes and regulation. Plant Cell 23: 873-894.
7. Buchanan-Wollaston, V., Earl, S., Harrison, E., Mathas, E., Navabpour, S., Page, T. et al. (2003) The molecular analysis of leaf senescence-a genomics approach. Plant Biotechnol. J. 1: 3-22.
8. Buchanan-Wollaston, V., Page, T., Harrison, E., Breeze, E., Lim, P.O., Nam, H.G. et al. (2005) Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant J. 42: 567-585.
9. Chen, W.Q., Provart, N.J., Glazebrook, J., Katagiri, F., Chang, H.S., Eulgem, T. et al. (2002) Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell 14: 559-574.
10. Clough, S.J. and Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735-743.
11. Cutcliffe, J.W., Hellmann, E., Heyl, A. and Rashotte, A.M. (2011) CRFs form protein-protein interactions with each other and with members of the cytokinin signalling pathway in Arabidopsis via the CRF domain. J. Exp. Bot. 62: 4995-5002.
12. Gan, S.S. and Amasino, R.M. (1996) Cytokinins in plant senescence: from spray and pray to clone and play. Bioessays 18: 557-565.
13. Gepstein, S. and Thimann, K.V. (1980) Changes in the abscisic-acid content of oat leaves during senescence. Proc. Natl Acad. Sci. USA 77: 2050-2053.
14. Ghanem, M.E., Albacete, A., Martinez-Andujar, C., Acosta, M., Romero-Aranda, R., Dodd, I.C. et al. (2008) Hormonal changes during salinity-induced leaf senescence in tomato (Solanum lycopersicum L.). J. Exp. Bot. 59: 3039-3050.
15. He, Y.H., Fukushige, H., Hildebrand, D.F. and Gan, S.S. (2002) Evidence supporting a role of jasmonic acid in Arabidopsis leaf senescence. Plant Physiol. 128: 876-884.
16. Himelblau, E. and Amasino, R.M. (2001) Nutrients mobilized from leaves of Arabidopsis thaliana during leaf senescence. J. Plant Physiol. 158: 1317-1323.
17. Hortensteiner, S. and Feller, U. (2002) Nitrogen metabolism and remobilization during senescence. J. Exp. Bot. 53: 927-937.
18. Inze, A., Vanderauwera, S., Hoeberichts, F.A., Vandorpe, M., Van Gaever, T. and Van Breusegem, F. (2012) A subcellular localization compendium of hydrogen peroxide-induced proteins. Plant Cell Environ. 35: 308-320.
19. Jing, H.C., Schippers, J.H.M., Hille, J. and Dijkwei, P.P. (2005) Ethyleneinduced leaf senescence depends on age-related changes and OLD genes in Arabidopsis. J. Exp. Bot. 56: 2915-2923.
20. Kim, H.J., Ryu, H., Hong, S.H., Woo, H.R., Lim, P.O., Lee, I.C. et al. (2006) Cytokinin-mediated control of leaf longevity by AHK3 through phosphorylation of ARR2 in Arabidopsis. Proc. Natl Acad. Sci. USA 103: 814-819.
21. Kleine, T., Kindgren, P., Benedict, C., Hendrickson, L. and Strand, A. (2007) Genome-wide gene expression analysis reveals a critical role for CRYPTOCHROME1 in the response of arabidopsis to high irradiance. Plant Physiol. 144: 1391-1406.
22. Kong, Z., Li, M., Yang, W., Xu, W. and Xue, Y. (2006) A novel nuclearlocalized CCCH-type zinc finger protein, OsDOS, is involved in delaying leaf senescence in rice. Plant Physiol. 141: 1376-1388.
23. Levey, S. and Wingler, A. (2005) Natural variation in the regulation of leaf senescence and relation to other traits in Arabidopsis. Plant Cell Environ. 28: 223-231.
24. Lim, P.O., Kim, H.J. and Nam, H.G. (2007) Leaf senescence. Annu. Rev. Plant Biol. 58: 115-136.
25. Mizoguchi, M., Umezawa, T., Nakashima, K., Kidokoro, S., Takasaki, H., Fujita, Y. et al. (2010) Two closely related subclass II SnRK2 protein kinases cooperatively regulate drought-inducible gene expression. Plant and Cell Physiology 51: 842-847.
26. Morris, K., Mackerness, S.A.H., Page, T., John, C.F., Murphy, A.M., Carr, J.P. et al. (2000) Salicylic acid has a role in regulating gene expression during leaf senescence. Plant J. 23: 677-685.
27. Nishiyama, R., Watanabe, Y., Fujita, Y., Le, D.T., Kojima, M., Werner, T. et al. (2011) Analysis of cytokinin mutants and regulation of cytokinin metabolic genes reveals important regulatory roles of cytokinins in drought, salt and abscisic acid responses, and abscisic acid biosynthesis. Plant Cell 23: 2169-2183.
28. Noodâen, L.D. and Leopold, A.C. (1988) Senescence and Aging in Plants. Academic Press, San Diego.
29. Ono, K., Nishi, Y., Watanabe, A. and Terashima, I. (2001) Possible mechanisms of adaptive leaf senescence. Plant Biol. 3: 234-243.
30. Park, J.H., Oh, S.A., Kim, Y.H., Woo, H.R. and Nam, H.G. (1998) Differential expression of senescence-associated mRNAs during leaf senescence induced by different senescence-inducing factors in Arabidopsis. Plant Mol. Biol. 37: 445-454.
31. Pecinka, A., Dinh, H.Q., Baubec, T., Rosa, M., Lettner, N. and Scheid, O.M. (2010) Epigenetic regulation of repetitive elements is attenuated by prolonged heat stress in Arabidopsis. Plant Cell 22: 3118-3129.
32. Peleg, Z. and Blumwald, E. (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr. Opin. Plant Biol. 14: 290-295.
33. Quirino, B.F., Noh, Y.S., Himelblau, E. and Amasino, R.M. (2000) Molecular aspects of leaf senescence. Trends Plant Sci. 5: 278-282.
34. Rao, M.V., Lee, H. and Davis, K.R. (2002) Ozone-induced ethylene production is dependent on salicylic acid, and both salicylic acid and ethylene act in concert to regulate ozone-induced cell death. Plant J. 32: 447-456.
35. Rashotte, A.M., Mason, M.G., Hutchison, C., Ferreira, F.J., Schaller, G.E. and Kieber, J.J. (2006) A subset of Arabidopsis AP2 transcription factors mediates cytokinin responses in concert with a two-component pathway. Proc. Natl Acad. Sci. USA 103: 11081-11085.
36. Richmond, A.E. and Lang, A. (1957) Effect of kinetin on protein content and survival of detached xanthium leaves. Science 125: 650-651.
37. Ritchie, R. (2006) Consistent sets of spectrophotometric chlorophyll equations for acetone, methanol and ethanol solvents. Photosynth. Res. 89: 27-41.
38. Shashidhar, V.R., Prasad, T.G. and Sudharshan, L. (1996) Hormone signals from roots to shoots of sunflower (Helianthus annuus L). Moderate soil drying increases delivery of abscisic acid and depresses delivery of cytokinins in xylem sap. Ann. Bot. 78: 151-155.
39. Singh, S., Letham, D.S. and Palni, L.M.S. (1992) Cytokinin biochemistry in relation to leaf senescence. 7. Endogenous cytokinin levels and exogenous applications of cytokinins in relation to sequential leaf senescence of tobacco. Physiol. Plant. 86: 388-397.
40. Thomas, H. and Stoddart, J.L. (1980) Leaf senescence. Annu. Rev. Plant Physiol. Plant Mol. Biol. 31: 83-111.
41. Ueda, J. and Kato, J. (1980) Isolation and identification of a senescencepromoting substance from wormwood (Artemisia-Absinthium L). Plant Physiol. 66: 246-249.
42. Ueguchi, C., Koizumi, H., Suzuki, T. and Mizuno, T. (2001) Novel family of sensor histidine kinase genes in Arabidopsis thaliana. Plant Cell Physiol. 42: 231-235.
43. Usadel, B., Blasing, O.E., Gibon, Y., Retzlaff, K., Hoehne, M., Gunther, M. et al. (2008) Global transcript levels respond to small changes of the carbon status during progressive exhaustion of carbohydrates in Arabidopsis rosettes. Plant Physiol. 146: 1834-1861.
44. van der Graaff, E., Schwacke, R., Schneider, A., Desimone, M., Fluegge, U.-I. and Kunze, R. (2006) Transcription analysis of arabidopsis membrane transporters and hormone pathways during developmental and induced leaf senescence. Plant Physiol. 141: 776-792.
45. Weaver, L.M., Gan, S.S., Quirino, B. and Amasino, R.M. (1998) A comparison of the expression patterns of several senescence-associated genes in response to stress and hormone treatment. Plant Mol. Biol. 37: 455-469.
46. Weigel, D. and Glazebrook, J. (2002) Arabidopsis: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
47. Wilkinson, S., Kudoyarova, G.R., Veselov, D.S., Arkhipova, T.N. and Davies, W.J. (2012) Plant hormone interactions: innovative targets for crop breeding and management. J. Exp. Bot. 63: 3499-3509.
48. Wingler, A. and Roitsch, T. (2008) Metabolic regulation of leaf senescence: interactions of sugar signalling with biotic and abiotic stress responses. Plant Biol. 10: 50-62.
49. Winter, D., Vinegar, B., Nahal, H., Ammar, R., Wilson, G.V. and Provart, N.J. (2007) An 'Electronic Fluorescent Pictograph' browser for exploring and analyzing large-scale biological data sets. PLoS One 2: e718.
50. Zeevaart, J.A.D. and Creelman, R.A. (1988) Metabolism and physiology of abscisic-acid. Annu. Rev. Plant Physiol. Plant Mol. Biol. 39: 439-473.
51. Zimmermann, P. and Zentgraf, U. (2005) The correlation between oxidative stress and leaf senescence during plant development. Cell. Mol. Biol. Lett. 10: 515-534.
52. Zwack, P.J., Shi, X., Robinson, B.R., Gupta, S., Gerken, D.M., Compton, M.A. et al. (2012) Vascular expression and C-terminal sequence divergence of cytokinin response factors in flowering plants. Plant Cell Physiol. 53: 1683-1695.