EIN3 and ORE1 Accelerate Degreening during Ethylene-Mediated Leaf Senescence by Directly Activating Chlorophyll Catabolic Genes in Arabidopsis

PLoS Genetics

Volumn 11, Issue 7, 2015, Pages

  Qiu, Kai ^a   Li, Zhongpeng ^a   Yang, Zhen ^a   Chen, Junyi ^a   Wu, Shouxin ^a   Zhu, Xiaoyu ^a   Gao, Shan ^a   Gao, Jiong ^a   Ren, Guodong ^a   Kuai, Benke ^a   Zhou, Xin ^a  

^a FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CHLOROPHYLL; ARABIDOPSIS PROTEIN; DNA BINDING PROTEIN; EIN3 PROTEIN, ARABIDOPSIS; ETHYLENE; ETHYLENE DERIVATIVE; MEMBRANE PROTEIN; NAC2 PROTEIN, ARABIDOPSIS; NON-YELLOW COLORING 1 PROTEIN, ARABIDOPSIS; NUCLEAR PROTEIN; ORE1 PROTEIN, ARABIDOPSIS; OXIDOREDUCTASE; OXYGENASE; PHEIDE A OXYGENASE; PROTEIN BINDING; REPRESSOR PROTEIN; TRANSCRIPTION FACTOR;

ACS2 GENE; ARABIDOPSIS; ARTICLE; BIODEGRADATION; CHLOROPHYLL CATABOLIC GENE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; EIN3 GENE; GEL MOBILITY SHIFT ASSAY; GENE ACTIVITY; GENE EXPRESSION REGULATION; GENE REPRESSION; GENE SYNTHESIS; GENE TARGETING; GENETIC TRANSCRIPTION; LEAF AGE; LUCIFERASE ASSAY; NONHUMAN; NYC1 GENE; NYE1 GENE; ORE1 GENE; PAO GENE; PLANT GENE; POSITIVE FEEDBACK; PROMOTER REGION; PROTEIN PROTEIN INTERACTION; PROTOPLAST; SENESCENCE; SIGNAL TRANSDUCTION; AGING; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY; PLANT LEAF;

ARABIDOPSIS;

AGING; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHLOROPHYLL; CHROMATIN IMMUNOPRECIPITATION; DNA-BINDING PROTEINS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ETHYLENES; GENE EXPRESSION REGULATION, PLANT; MEMBRANE PROTEINS; NUCLEAR PROTEINS; OXIDOREDUCTASES; OXYGENASES; PLANT LEAVES; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84938790849     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005399     Document Type: Article

References (49)

1. Gan S, Amasino RM, Making Sense of Senescence (Molecular Genetic Regulation and Manipulation of Leaf Senescence). Plant Physiology. 1997;113: 313–319. 12223609
2. Lim PO, Kim HJ, Nam HG, Leaf senescence. Annu Rev Plant Biol. 2007;58: 115–136. 17177638
3. Guo Y, Gan SS, Convergence and divergence in gene expression profiles induced by leaf senescence and 27 senescence-promoting hormonal, pathological and environmental stress treatments. Plant Cell Environ. 2012;35: 644–655. doi: 10.1111/j.1365-3040.2011.02442.x 21988545
4. Sakuraba Y, Jeong J, Kang MY, Kim J, Paek NC, Choi G, Phytochrome-interacting transcription factors PIF4 and PIF5 induce leaf senescence in Arabidopsis. Nat Commun. 2014;5: 4636. doi: 10.1038/ncomms5636 25119965
5. Sato Y, Morita R, Katsuma S, Nishimura M, Tanaka A, Kusaba M, Two short-chain dehydrogenase/reductases, NON-YELLOW COLORING 1 and NYC1-LIKE, are required for chlorophyll b and light-harvesting complex II degradation during senescence in rice. Plant J. 2009;57: 120–131. doi: 10.1111/j.1365-313X.2008.03670.x 18778405
6. Horie Y, Ito H, Kusaba M, Tanaka R, Tanaka A, Participation of chlorophyll b reductase in the initial step of the degradation of light-harvesting chlorophyll a/b-protein complexes in Arabidopsis. J Biol Chem. 2009;284: 17449–17456. doi: 10.1074/jbc.M109.008912 19403948
7. Meguro M, Ito H, Takabayashi A, Tanaka R, Tanaka A, Identification of the 7-hydroxymethyl chlorophyll a reductase of the chlorophyll cycle in Arabidopsis. Plant Cell. 2011;23: 3442–3453. doi: 10.1105/tpc.111.089714 21934147
8. Schelbert S, Aubry S, Burla B, Agne B, Kessler F, Krupinska K, et al. Pheophytin pheophorbide hydrolase (pheophytinase) is involved in chlorophyll breakdown during leaf senescence in Arabidopsis. Plant Cell. 2009;21: 767–785. doi: 10.1105/tpc.108.064089 19304936
9. Ren G, Zhou Q, Wu S, Zhang Y, Zhang L, Huang J, et al. Reverse genetic identification of CRN1 and its distinctive role in chlorophyll degradation in Arabidopsis. J Integr Plant Biol. 2010;52: 496–504. doi: 10.1111/j.1744-7909.2010.00945.x 20537045
10. Pruzinska A, Tanner G, Anders I, Roca M, Hortensteiner S, Chlorophyll breakdown: pheophorbide a oxygenase is a Rieske-type iron-sulfur protein, encoded by the accelerated cell death 1 gene. Proc Natl Acad Sci U S A. 2003;100: 15259–15264. 14657372
11. Sakuraba Y, Schelbert S, Park SY, Han SH, Lee BD, Andres CB, et al. STAY-GREEN and chlorophyll catabolic enzymes interact at light-harvesting complex II for chlorophyll detoxification during leaf senescence in Arabidopsis. Plant Cell. 2012;24: 507–518. doi: 10.1105/tpc.111.089474 22366162
12. Ren G, An K, Liao Y, Zhou X, Cao Y, Zhao H, et al. Identification of a novel chloroplast protein AtNYE1 regulating chlorophyll degradation during leaf senescence in Arabidopsis. Plant Physiology. 2007;144: 1429–1441. 17468209
13. Kusaba M, Tanaka A, Tanaka R, Stay-green plants: what do they tell us about the molecular mechanism of leaf senescence. Photosynth Res. 2013;117: 221–234. doi: 10.1007/s11120-013-9862-x 23771643
14. Jibran R, Hunter DA, Dijkwel PP, Hormonal regulation of leaf senescence through integration of developmental and stress signals. Plant Mol Biol. 2013;82: 547–561. doi: 10.1007/s11103-013-0043-2 23504405
15. van der Graaff E, Schwacke R, Schneider A, Desimone M, Flugge UI, Kunze R, Transcription analysis of arabidopsis membrane transporters and hormone pathways during developmental and induced leaf senescence. Plant Physiology. 2006;141: 776–792. 16603661
16. Jing HC, Schippers JH, Hille J, Dijkwel PP, Ethylene-induced leaf senescence depends on age-related changes and OLD genes in Arabidopsis. J Exp Bot. 2005;56: 2915–2923. 16172137
17. Tsuchisaka A, Yu G, Jin H, Alonso JM, Ecker JR, Zhang X, et al. A combinatorial interplay among the 1-aminocyclopropane-1-carboxylate isoforms regulates ethylene biosynthesis in Arabidopsis thaliana. Genetics. 2009;183: 979–1003. doi: 10.1534/genetics.109.107102 19752216
18. Hua J, Meyerowitz EM, Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell. 1998;94: 261–271. 9695954
19. Kieber JJ, Rothenberg M, Roman G, Feldmann KA, Ecker JR, CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases. Cell. 1993;72: 427–441. 8431946
20. Alonso JM, Hirayama T, Roman G, Nourizadeh S, Ecker JR, EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science. 1999;284: 2148–2152. 10381874
21. Bisson MM, Bleckmann A, Allekotte S, Groth G, EIN2, the central regulator of ethylene signalling, is localized at the ER membrane where it interacts with the ethylene receptor ETR1. Biochem J. 2009;424: 1–6. doi: 10.1042/BJ20091102 19769567
22. Ju C, Yoon GM, Shemansky JM, Lin DY, Ying ZI, Chang J, et al. CTR1 phosphorylates the central regulator EIN2 to control ethylene hormone signaling from the ER membrane to the nucleus in Arabidopsis. Proc Natl Acad Sci U S A. 2012;109: 19486–19491. doi: 10.1073/pnas.1214848109 23132950
23. Wen X, Zhang C, Ji Y, Zhao Q, He W, An F, et al. Activation of ethylene signaling is mediated by nuclear translocation of the cleaved EIN2 carboxyl terminus. Cell Res. 2012;22: 1613–1616. doi: 10.1038/cr.2012.145 23070300
24. Qiao H, Shen Z, Huang SS, Schmitz RJ, Urich MA, Briggs SP, et al. Processing and subcellular trafficking of ER-tethered EIN2 control response to ethylene gas. Science. 2012;338: 390–393. doi: 10.1126/science.1225974 22936567
25. Grbic V, Bleecker AB, Ethylene regulates the timing of leaf senescence in Arabidopsis. Plant J. 1995;8: 595–602.
26. Oh SA, Park JH, Lee GI, Paek KH, Park SK, Nam HG, Identification of three genetic loci controlling leaf senescence in Arabidopsis thaliana. Plant J. 1997;12: 527–535. 9351240
27. Li Z, Peng J, Wen X, Guo H, Ethylene-insensitive3 is a senescence-associated gene that accelerates age-dependent leaf senescence by directly repressing miR164 transcription in Arabidopsis. Plant Cell. 2013;25: 3311–3328. doi: 10.1105/tpc.113.113340 24064769
28. Kim JH, Woo HR, Kim J, Lim PO, Lee IC, Choi SH, et al. Trifurcate feed-forward regulation of age-dependent cell death involving miR164 in Arabidopsis. Science. 2009;323: 1053–1057. doi: 10.1126/science.1166386 19229035
29. Matallana-Ramirez LP, Rauf M, Farage-Barhom S, Dortay H, Xue GP, Droge-Laser W, et al. NAC Transcription Factor ORE1 and Senescence-Induced BIFUNCTIONAL NUCLEASE1 (BFN1) Constitute a Regulatory Cascade in Arabidopsis. Mol Plant. 2013;6: 1432–1452.
30. Farage-Barhom S, Burd S, Sonego L, Mett A, Belausov E, Gidoni D, et al. Localization of the Arabidopsis senescence- and cell death-associated BFN1 nuclease: from the ER to fragmented nuclei. Mol Plant. 2011;4: 1062–1073. doi: 10.1093/mp/ssr045 21665915
31. Kim HJ, Hong SH, Kim YW, Lee IH, Jun JH, Phee BK, et al. Gene regulatory cascade of senescence-associated NAC transcription factors activated by ETHYLENE-INSENSITIVE2-mediated leaf senescence signalling in Arabidopsis. J Exp Bot. 2014;65: 4023–4036. doi: 10.1093/jxb/eru112 24659488
32. Zhong S, Zhao M, Shi T, Shi H, An F, Zhao Q, et al. EIN3/EIL1 cooperate with PIF1 to prevent photo-oxidation and to promote greening of Arabidopsis seedlings. Proc Natl Acad Sci U S A. 2009;106: 21431–21436. doi: 10.1073/pnas.0907670106 19948955
33. Konishi M, Yanagisawa S, Ethylene signaling in Arabidopsis involves feedback regulation via the elaborate control of EBF2 expression by EIN3. Plant J. 2008;55: 821–831. doi: 10.1111/j.1365-313X.2008.03551.x 18466304
34. Kosugi S, Ohashi Y, Cloning and DNA-binding properties of a tobacco Ethylene-Insensitive3 (EIN3) homolog. Nucleic Acids Res. 2000;28: 960–967. 10648789
35. Yamasaki K, Kigawa T, Inoue M, Yamasaki T, Yabuki T, Aoki M, et al. Solution structure of the major DNA-binding domain of Arabidopsis thaliana ethylene-insensitive3-like3. J Mol Biol. 2005;348: 253–264. 15811366
36. Hellens RP, Allan AC, Friel EN, Bolitho K, Grafton K, Templeton MD, et al. Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant Methods. 2005;1: 13. 16359558
37. Olsen AN, Ernst HA, Leggio LL, Skriver K, DNA-binding specificity and molecular functions of NAC transcription factors. Plant Science. 2005;169: 785–797.
38. Balazadeh S, Siddiqui H, Allu AD, Matallana-Ramirez LP, Caldana C, Mehrnia M, et al. A gene regulatory network controlled by the NAC transcription factor ANAC092/AtNAC2/ORE1 during salt-promoted senescence. Plant J. 2010;62: 250–264. doi: 10.1111/j.1365-313X.2010.04151.x 20113437
39. Delmas F, Sankaranarayanan S, Deb S, Widdup E, Bournonville C, Bollier N, et al. ABI3 controls embryo degreening through Mendel's I locus. Proc Natl Acad Sci U S A. 2013;110: E3888–3894. doi: 10.1073/pnas.1308114110 24043799
40. Song Y, Yang C, Gao S, Zhang W, Li L, Kuai B, Age-Triggered and Dark-Induced Leaf Senescence Require the bHLH Transcription Factors PIF3, 4, and 5. Mol Plant. 2014;7: 1776–1787. doi: 10.1093/mp/ssu109 25296857
41. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, et al. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science. 2003;301: 653–657. 12893945
42. Chen H, Xue L, Chintamanani S, Germain H, Lin H, Cui H, et al. ETHYLENE INSENSITIVE3 and ETHYLENE INSENSITIVE3-LIKE1 repress SALICYLIC ACID INDUCTION DEFICIENT2 expression to negatively regulate plant innate immunity in Arabidopsis. Plant Cell. 2009;21: 2527–2540. doi: 10.1105/tpc.108.065193 19717619
43. Aoyama T, Chua NH, A glucocorticoid-mediated transcriptional induction system in transgenic plants. Plant J. 1997;11: 605–612. 9107046
44. Clough SJ, Bent AF, Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1998;16: 735–743. 10069079
45. Li J, Chen X, Luo LQ, Yu J, Ming F, Functions of ANAC092 involved in regulation of anther development in Arabidopsis thaliana]. Yi Chuan. 2013;35: 913–922. 23853363
46. Zhang W, Wen CK, Preparation of ethylene gas and comparison of ethylene responses induced by ethylene, ACC, and ethephon. Plant Physiol Biochem. 2010;48: 45–53. doi: 10.1016/j.plaphy.2009.10.002 19836254
47. Zheng XY, Spivey NW, Zeng W, Liu PP, Fu ZQ, Klessig DF, et al. Coronatine promotes Pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation. Cell Host Microbe. 2012;11: 587–596. doi: 10.1016/j.chom.2012.04.014 22704619
48. Earley KW, Haag JR, Pontes O, Opper K, Juehne T, Song K, et al. Gateway-compatible vectors for plant functional genomics and proteomics. Plant J. 2006;45: 616–629. 16441352
49. Yoo SD, Cho YH, Sheen J, Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc. 2007;2: 1565–1572. 17585298