Gene Network Analysis and Functional Studies of Senescence-associated Genes Reveal Novel Regulators of Arabidopsis Leaf Senescence

Journal of Integrative Plant Biology

Volumn 54, Issue 8, 2012, Pages 526-539

  Li, Zhonghai ^a   Peng, Jinying ^a   Wen, Xing ^a   Guo, Hongwei ^a  

^a Tsinghua University   (China)

Author keywords

Arabidopsis; Leaf senescence; Phytohormone; SAG; Systems biology

Indexed keywords

ARABIDOPSIS PROTEIN; AZF PROTEIN, ARABIDOPSIS; DNA BINDING PROTEIN; MKP2 PROTEIN, ARABIDOPSIS; PROTEIN TYROSINE PHOSPHATASE; TRANSCRIPTION FACTOR; WRKY75 PROTEIN, ARABIDOPSIS;

GENETIC ANALYSIS; HORMONE; LEAF; MOLECULAR ANALYSIS; NETWORK ANALYSIS; PLANT; PROTEIN; SENESCENCE;

ARABIDOPSIS; ARTICLE; DARKNESS; GENE REGULATORY NETWORK; GENETICS; PHYSIOLOGY; PLANT GENE; PLANT LEAF;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; DARKNESS; DNA-BINDING PROTEINS; GENE REGULATORY NETWORKS; GENES, PLANT; PLANT LEAVES; PROTEIN TYROSINE PHOSPHATASES; TRANSCRIPTION FACTORS;

EID: 84865445002     PISSN: 16729072     EISSN: 17447909     Source Type: Journal    
DOI: 10.1111/j.1744-7909.2012.01136.x     Document Type: Article

References (59)

1. Aharoni N, Lieberman M (1979) Ethylene as a regulator of senescence in tobacco leaf discs. Plant Physiol. 64, 801-804.
2. Back A, Richmond A (1969) An interaction between the effects of kinetin and gibberellin in retarding leaf senescence. Physiol. Plant 22, 1207-1216.
3. Besseau S, Li J, Palva ET (2012) WRKY54 and WRKY70 co-operate as negative regulators of leaf senescence in Arabidopsis thaliana. J. Exp. Bot. 63, 2667-2679.
4. Breeze E, Harrison E, McHattie S, Hughes L, Hickman R, Hill C, Kiddle S, Kim YS, Penfold CA, Jenkins D, Zhang C, Morris K, Jenner C, Jackson S, Thomas B, Tabrett A, Legaie R, Moore JD, Wild DL, Ott S, Rand D, Beynon J, Denby K, Mead A, Buchanan-Wollaston V (2011) High-resolution temporal profiling of transcripts during Arabidopsis leaf senescence reveals a distinct chronology of processes and regulation. Plant Cell 23, 873-894.
5. Buchanan-Wollaston V, Ainsworth, C (1997) Leaf senescence in Brassica napus: Cloning of senescence related genes by subtractive hybridisation. Plant Mol. Biol. 33, 821-834.
6. Buchanan-Wollaston V, Earl S, Harrison E, Mathas E, Navabpour S, Page T, Pink D (2003) The molecular analysis of leaf senescence-a genomics approach. Plant Biotechnol. J. 1, 3-22.
7. Buchanan-Wollaston V, Page T, Harrison E, Breeze E, Lim PO, Nam HG, Lin JF, Wu SH, Swidzinski J, Ishizaki K, Leaver CJ (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.
8. Burg SP (1968) Ethylene, plant senescence and abscission. Plant Physiol. 43, 1503-1511.
9. Chao Q, Rothenberg M, Solano R, Roman G, Terzaghi W, Ecker JR (1997) Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins. Cell 89, 1133-1144.
10. Chou CM, Kao CH (1992) Methyl jasmonate, calcium, and leaf senescence in rice. Plant Physiol. 99, 1693-1694.
11. Devaiah BN, Karthikeyan AS, Raghothama KG (2007) WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiol. 143, 1789-1801.
12. Drechsel G, Raab S, Hoth S (2010) Arabidopsis zinc-finger protein 2 is a negative regulator of ABA signaling during seed germination. J. Plant Physiol. 167, 1418-1421.
13. Ellis CM, Nagpal P, Young JC, Hagen G, Guilfoyle TJ, Reed JW (2005) AUXIN RESPONSE FACTOR1 and AUXIN RESPONSE FACTOR2 regulate senescence and floral organ abscission in Arabidopsis thaliana. Development 132, 4563-4574.
14. Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci. 5, 199-206.
15. Gan S, Amasino RM (1995) Inhibition of leaf senescence by autoregulated production of cytokinin. Science 270, 1986-1988.
16. Gan S, Amasino RM (1997) Making sense of senescence (molecular genetic regulation and manipulation of leaf senescence). Plant Physiol. 113, 313-319.
17. Guo FQ, Crawford NM (2005) Arabidopsis nitric oxide synthase1 is targeted to mitochondria and protects against oxidative damage and dark-induced senescence. Plant Cell 17, 3436-3450.
18. Guo Y, Gan S (2005) Leaf senescence: Signals, execution, and regulation. Curr. Top Dev. Biol. 71, 83-112.
19. Guo Y, Gan SS (2012) Convergence and divergence in gene expression profiles induced by leaf senescence and 27 senescence-promoting hormonal, pathological and environmental stress treatments. Plant Cell Environ. 35, 644-655.
20. He Y, Fukushige H, Hildebrand DF, Gan S (2002) Evidence supporting a role of jasmonic acid in Arabidopsis leaf senescence. Plant Physiol. 128, 876-884.
21. Jing HC, Dijkwel PP (2008) CPR5: A Jack of all trades in plants. Plant Signal Behav. 3, 562-563.
22. Jing HC, Sturre MJ, Hille J, Dijkwel PP (2002) Arabidopsis onset of leaf death mutants identify a regulatory pathway controlling leaf senescence. Plant J. 32, 51-63.
23. Jing HC, Anderson L, Sturre MJ, Hille J, Dijkwel PP (2007) Arabidopsis CPR5 is a senescence-regulatory gene with pleiotropic functions as predicted by the evolutionary theory of senescence. J. Exp. Bot. 58, 3885-3894.
24. Jing HC, Hebeler R, Oeljeklaus S, Sitek B, Stuhler K, Meyer HE, Sturre MJ, Hille J, Warscheid B, Dijkwel PP (2008) Early leaf senescence is associated with an altered cellular redox balance in Arabidopsis cpr5/old1 mutants. Plant Biol. (Stuttg) 10 Suppl 1, 85-98.
25. John I, Hackett R, Cooper W, Drake R, Farrell A, Grierson D (1997) Cloning and characterization of tomato leaf senescence-related cDNAs. Plant Mol. Biol. 33, 641-651.
26. Kim HJ, Ryu H, Hong SH, Woo HR, Lim PO, Lee IC, Sheen J, Nam HG, Hwang I (2006) Cytokinin-mediated control of leaf longevity by AHK3 through phosphorylation of ARR2 in Arabidopsis. Proc. Natl. Acad. Sci. USA 103, 814-819.
27. Kim JH, Woo HR, Kim J, Lim PO, Lee IC, Choi SH, Hwang D, Nam HG (2009) Trifurcate feed-forward regulation of age-dependent cell death involving miR164 in Arabidopsis. Science 323, 1053-1057.
28. Kodaira KS, Qin F, Tran LS, Maruyama K, Kidokoro S, Fujita Y, Shinozaki K, Yamaguchi-Shinozaki K (2011) Arabidopsis Cys2/His2 zinc-finger proteins AZF1 and AZF2 negatively regulate abscisic acid-repressive and auxin-inducible genes under abiotic stress conditions. Plant Physiol. 157, 742-756.
29. Lai Z, Vinod K, Zheng Z, Fan B, Chen Z (2008) Roles of Arabidopsis WRKY3 and WRKY4 transcription factors in plant responses to pathogens. BMC Plant Biol. 8, 68.
30. Lee JS, Ellis BE (2007) Arabidopsis MAPK phosphatase 2 (MKP2) positively regulates oxidative stress tolerance and inactivates the MPK3 and MPK6 MAPKs. J. Biol. Chem. 282, 25020-25029.
31. Li HW, Lin FY, Wang G, Jing RL, Zheng Q, Li B, Li ZS (2012) Quantitative trait loci mapping of dark-induced senescence in winter wheat (Triticum aestivum). J. Integr. Plant Biol. 54, 33-44.
32. Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu. Rev. Plant. Biol. 58, 115-136.
33. Lim PO, Lee IC, Kim J, Kim HJ, Ryu JS, Woo HR, Nam HG (2010) Auxin response factor 2 (ARF2) plays a major role in regulating auxin-mediated leaf longevity. J. Exp. Bot. 61, 1419-1430.
34. Liu H, Wang Y, Xu J, Su T, Liu G, Ren D (2008) Ethylene signaling is required for the acceleration of cell death induced by the activation of AtMEK5 in Arabidopsis. Cell Res. 18, 422-432.
35. Liu X, Li Z, Jiang Z, Zhao Y, Peng J, Jin J, Guo H, Luo J (2011) LSD: A leaf senescence database. Nucleic Acids Res. 39, D1103-1107.
36. 2+-conducting Arabidopsis cyclic nucleotide gated channel2 acts through nitric oxide to repress senescence programming. Plant Physiol. 154, 733-743.
37. Miao Y, Zentgraf U (2007) The antagonist function of Arabidopsis WRKY53 and ESR/ESP in leaf senescence is modulated by the jasmonic and salicylic acid equilibrium. Plant Cell 19, 819-830.
38. Mishina TE, Lamb C, Zeier J (2007) Expression of a nitric oxide degrading enzyme induces a senescence programme in Arabidopsis. Plant Cell Environ. 30, 39-52.
39. Nam HG (1997) The molecular genetic analysis of leaf senescence. Curr. Opin. Biotechnol. 8, 200-207.
40. Narusaka Y, Narusaka M, Seki M, Umezawa T, Ishida J, Nakajima M, Enju A, Shinozaki K (2004) Crosstalk in the responses to abiotic and biotic stresses in Arabidopsis: analysis of gene expression in cytochrome P450 gene superfamily by cDNA microarray. Plant Mol. Biol. 55, 327-342.
41. Oh SA, Park JH, Lee GI, Paek KH, Park SK, Nam HG (1997) Identification of three genetic loci controlling leaf senescence in Arabidopsis thaliana. Plant J. 12, 527-535.
42. Osborne DJ (1959) Control of leaf senescence by auxins. Nature 183, 1459-1460.
43. Pontier D, Gan S, Amasino RM, Roby D, Lam E (1999) Markers for hypersensitive response and senescence show distinct patterns of expression. Plant Mol. Biol. 39, 1243-1255.
44. Poovaiah BW, Leopold AC (1973) Deferral of leaf senescence with calcium. Plant Physiol. 52, 236-239.
45. Ren GD, Zhou Q, Wu SX, Zhang YF, Zhang LG, Huang JR, Sun ZF, Kuai BK (2010) Reverse Genetic Identification of CRN1 and its Distinctive Role in Chlorophyll Degradation in Arabidopsis. J. Integr. Plant Biol. 52, 496-504.
46. Robatzek S, Somssich IE (2002) Targets of AtWRKY6 regulation during plant senescence and pathogen defense. Genes Dev. 16, 1139-1149.
47. Sakamoto H, Araki T, Meshi T, Iwabuchi M (2000) Expression of a subset of the Arabidopsis Cys(2)/His(2)-type zinc-finger protein gene family under water stress. Gene 248, 23-32.
48. Schommer C, Palatnik JF, Aggarwal P, Chetelat A, Cubas P, Farmer EE, Nath U, Weigel D (2008) Control of jasmonate biosynthesis and senescence by miR319 targets. PLoS Biol. 6, e230.
49. Srivalli S, Khanna-Chopra R (2009) Delayed wheat flag leaf senescence due to removal of spikelets is associated with increased activities of leaf antioxidant enzymes, reduced glutathione/oxidized glutathione ratio and oxidative damage to mitochondrial proteins. Plant Physiol. Biochem. 47, 663-670.
50. To JP, Haberer G, Ferreira FJ, Deruere J, Mason MG, Schaller GE, Alonso JM, Ecker JR, Kieber JJ (2004) Type-A Arabidopsis response regulators are partially redundant negative regulators of cytokinin signaling. Plant Cell 16, 658-671.
51. Ulker B, Shahid Mukhtar M, Somssich IE (2007) The WRKY70 transcription factor of Arabidopsis influences both the plant senescence and defense signaling pathways. Planta 226, 125-137.
52. Woo HR, Chung KM, Park JH, Oh SA, Ahn T, Hong SH, Jang SK, Nam HG (2001) ORE9, an F-box protein that regulates leaf senescence in Arabidopsis. Plant Cell 13, 1779-1790.
53. Xu F, Meng T, Li P, Yu Y, Cui Y, Wang Y, Gong Q, Wang NN (2011) A soybean dual-specificity kinase, GmSARK, and its Arabidopsis homolog, AtSARK, regulate leaf senescence through synergistic actions of auxin and ethylene. Plant Physiol. 157, 2131-2153.
54. Yoshida S (2003) Molecular regulation of leaf senescence. Curr. Opin. Plant Biol. 6, 79-84.
55. Yoshida S, Ito M, Nishida I, Watanabe A (2002) Identification of a novel gene HYS1/CPR5 that has a repressive role in the induction of leaf senescence and pathogen-defence responses in Arabidopsis thaliana. Plant J. 29, 427-437.
56. Zentgraf U, Laun T, Miao Y (2010) The complex regulation of WRKY53 during leaf senescence of Arabidopsis thaliana. Eur. J. Cell Biol. 89, 133-137.
57. Zhang P, Wang WQ, Zhang GL, Kaminek M, Dobrev P, Xu J, Gruissem W (2010) Senescence-Inducible Expression of Isopentenyl Transferase Extends Leaf Life, Increases Drought Stress Resistance and Alters Cytokinin Metabolism in Cassava. J. Integr. Plant Biol. 52, 653-669.
58. Zhou C, Cai Z, Guo Y, Gan S (2009) An arabidopsis mitogen-activated protein kinase cascade, MKK9-MPK6, plays a role in leaf senescence. Plant Physiol. 150, 167-177.
59. Zhou X, Jiang Y, Yu D (2011) WRKY22 transcription factor mediates dark-induced leaf senescence in Arabidopsis. Mol. Cells 31, 303-313.