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Plant Molecular Biology

, Volume 82, Issue 6, pp 519–528 | Cite as

Towards systems biological understanding of leaf senescence

  • Yongfeng Guo
Article

Abstract

The application of systems biology approaches has greatly facilitated the process of deciphering the molecular mechanisms underlying leaf senescence. Analyses of the leaf senescence transcriptome have identified some of the major biochemical events during senescence including protein degradation and nutrient remobilization. Proteomic studies have confirmed these findings and have suggested up-regulated energy metabolism during leaf senescence which might be important for cell viability maintenance. As a critical part of systems biology, studies involving transcription regulation networking and senescence-inducing signaling have deepened our understanding on the molecular regulation of leaf senescence. The important next steps towards a systems biological understanding of leaf senescence will be discussed.

Keywords

Transcriptome Proteome Protein degradation Nutrient remobilization Networking 

Notes

Acknowledgments

I thank Dr. Susheng Gan at Cornell University for discussion and Dr. Jessica Westbrook at Sandia National Laboratories for critical reading of the manuscript. Research in our lab is supported by a startup fund from the Tobacco Research Institute of Chinese Academy of Agricultural Sciences.

References

  1. Andersson A, Keskitalo J, Sjodin A, Bhalerao R, Sterky F, Wissel K, Tandre K, Aspeborg H, Moyle R, Ohmiya Y, Brunner A, Gustafsson P, Karlsson J, Lundeberg J, Nilsson O, Sandberg G, Strauss S, Sundberg B, Uhlen M, Jansson S, Nilsson P (2004) A transcriptional timetable of autumn senescence. Genome Biol 5:R24PubMedCrossRefGoogle Scholar
  2. Balazadeh S, Riano-Pachon DM, Mueller-Roeber B (2008) Transcription factors regulating leaf senescence in Arabidopsis thaliana. Plant Biol (Stuttg) 10(Suppl 1):63–75CrossRefGoogle Scholar
  3. Balazadeh S, Kwasniewski M, Caldana C, Mehrnia M, Zanor MI, Xue GP, Mueller-Roeber B (2011) ORS1, an H(2)O(2)-responsive NAC transcription factor, controls senescence in Arabidopsis thaliana. Mol Plant 4(2):346–360PubMedCrossRefGoogle Scholar
  4. 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(7):2667–2679PubMedCrossRefGoogle Scholar
  5. Bhalerao R, Keskitalo J, Sterky F, Erlandsson R, Bjorkbacka H, Birve SJ, Karlsson J, Gardestrom P, Gustafsson P, Lundeberg J, Jansson S (2003) Gene expression in autumn leaves. Plant Physiol 131(2):430–442PubMedCrossRefGoogle Scholar
  6. 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(3):873–894PubMedCrossRefGoogle Scholar
  7. BuchananWollaston V (1997) The molecular biology of leaf senescence. J Exp Bot 48(307):181–199CrossRefGoogle Scholar
  8. Buchanan-Wollaston V (1994) Isolation of cDNA clones for genes that are expressed during leaf senescence in Brassica napus. Identification of a gene encoding a senescence-specific metallothionein-like protein. Plant Physiol 105(3):839–846PubMedCrossRefGoogle Scholar
  9. 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(1):3–22PubMedCrossRefGoogle Scholar
  10. Buchanan-Wollaston V, Page T, Harrison E, Breeze E, Lim PO, Nam HG, Lin J-F, Wu S-H, 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(4):567–585PubMedCrossRefGoogle Scholar
  11. Cantu D, Pearce SP, Distelfeld A, Christiansen MW, Uauy C, Akhunov E, Fahima T, Dubcovsky J (2011) Effect of the down-regulation of the high grain protein content (GPC) genes on the wheat transcriptome during monocarpic senescence. BMC Genomics 12:492PubMedCrossRefGoogle Scholar
  12. Carp MJ, Gepstein S (2007) Genomics and proteomics of leaf senescence. In: Gan S (ed) Senescence processes in plants. Blackwell Publishing Oxford, UK, pp 202–230CrossRefGoogle Scholar
  13. Chen WQ, Provart NJ, Glazebrook J, Katagiri F, Chang HS, Eulgem T, Mauch F, Luan S, Zou GZ, Whitham SA, Budworth PR, Tao Y, Xie ZY, Chen X, Lam S, Kreps JA, Harper JF, Si-Ammour A, Mauch-Mani B, Heinlein M, Kobayashi K, Hohn T, Dangl JL, Wang X, Zhu T (2002) Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell 14(3):559–574PubMedCrossRefGoogle Scholar
  14. Chen Y, Qiu K, Kuai B, Ding Y (2011) Identification of an NAP-like transcription factor BeNAC1 regulating leaf senescence in bamboo (Bambusa emeiensis ‘Viridiflavus’). Physiol Plant 142(4):361–371PubMedCrossRefGoogle Scholar
  15. Desclos M, Etienne P, Coquet L, Jouenne T, Bonnefoy J, Segura R, Reze S, Ourry A, Avice JC (2009) A combined 15 N tracing/proteomics study in Brassica napus reveals the chronology of proteomics events associated with N remobilisation during leaf senescence induced by nitrate limitation or starvation. Proteomics 9(13):3580–3608PubMedCrossRefGoogle Scholar
  16. 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(20):4563–4574PubMedCrossRefGoogle Scholar
  17. Ewing RM, Kahla AB, Poirot O, Lopez F, Audic S, Claverie J-M (1999) Large-scale statistical analyses of rice ESTs reveal correlated patterns of gene expression. Genome Res 9(10):950–959PubMedCrossRefGoogle Scholar
  18. Feild TS, Lee DW, Holbrook NM (2001) Why leaves turn red in autumn. The role of anthocyanins in senescing leaves of red-osier dogwood. Plant Physiol 127(2):566–574PubMedCrossRefGoogle Scholar
  19. Fortes AM, Agudelo-Romero P, Silva MS, Ali K, Sousa L, Maltese F, Choi YH, Grimplet J, Martinez-Zapater JM, Verpoorte R, Pais MS (2011) Transcript and metabolite analysis in Trincadeira cultivar reveals novel information regarding the dynamics of grape ripening. BMC Plant Biol 11:149PubMedCrossRefGoogle Scholar
  20. Gan S (2003) Mitotic and postmitotic senescence in plants. Sci Aging Knowledge Environ 2003(38):RE7PubMedCrossRefGoogle Scholar
  21. Gan S (2005) Hormonal regulation of senescence. In: Davies PJ (ed) Plant hormones: biosynthesis, signal transduction, action. Kluwer, The Netherlands, pp 561–581Google Scholar
  22. Gepstein S (2004) Leaf senescence—not just a ‘wear and tear’ phenomenon. Genome Biol 5(3):212PubMedCrossRefGoogle Scholar
  23. Gepstein S, Sabehi G, Carp MJ, Hajouj T, Nesher MFO, Yariv I, Dor C, Bassani M (2003) Large-scale identification of leaf senescence-associated genes. Plant J 36(5):629–642PubMedCrossRefGoogle Scholar
  24. Gregersen PL, Holm PB (2007) Transcriptome analysis of senescence in the flag leaf of wheat (Triticum aestivum L.). Plant Biotechnol J 5(1):192–206PubMedCrossRefGoogle Scholar
  25. Guiboileau A, Sormani R, Meyer C, Masclaux-Daubresse C (2010) Senescence and death of plant organs: nutrient recycling and developmental regulation. C R Biol 333(4):382–391PubMedCrossRefGoogle Scholar
  26. Guo YF, Gan SS (2005) Leaf senescence: signals, execution, and regulation. Curr Top Dev Biol 71:83–112PubMedCrossRefGoogle Scholar
  27. Guo Y, Gan S (2006) AtNAP, a NAC family transcription factor, has an important role in leaf senescence. Plant J 46(4):601–612PubMedCrossRefGoogle Scholar
  28. 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(3):644–655CrossRefGoogle Scholar
  29. Guo Y, Cai Z, Gan S (2004) Transcriptome of Arabidopsis leaf senescence. Plant, Cell Environ 27(5):521–549CrossRefGoogle Scholar
  30. He YH, Tang WN, Swain JD, Green AL, Jack TP, Gan SS (2001) Networking senescence-regulating pathways by using Arabidopsis enhancer trap lines. Plant Physiol 126(2):707–716PubMedCrossRefGoogle Scholar
  31. Hebeler R, Oeljeklaus S, Reidegeld KA, Eisenacher M, Stephan C, Sitek B, Stuhler K, Meyer HE, Sturre MJ, Dijkwel PP, Warscheid B (2008) Study of early leaf senescence in Arabidopsis thaliana by quantitative proteomics using reciprocal 14 N/15 N labeling and difference gel electrophoresis. Mol Cell Proteomics MCP 7(1):108–120CrossRefGoogle Scholar
  32. Hinderhofer K, Zentgraf U (2001) Identification of a transcription factor specifically expressed at the onset of leaf senescence. Planta 213(3):469–473PubMedCrossRefGoogle Scholar
  33. Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, Oertle L, Widmayer P, Gruissem W, Zimmermann P (2008) Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes. Adv Bioinf 2008:420747Google Scholar
  34. 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(1):51–63PubMedCrossRefGoogle Scholar
  35. Jordan KW, Nordenstam J, Lauwers GY, Rothenberger DA, Alavi K, Garwood M, Cheng LL (2009) Metabolomic characterization of human rectal adenocarcinoma with intact tissue magnetic resonance spectroscopy. Dis Colon Rectum 52(3):520–525PubMedCrossRefGoogle Scholar
  36. 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(3):814–819PubMedCrossRefGoogle Scholar
  37. 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(5917):1053–1057PubMedCrossRefGoogle Scholar
  38. Kirschner MW (2005) The meaning of systems biology. Cell 121(4):503–504PubMedCrossRefGoogle Scholar
  39. KleberJanke T, Krupinska K (1997) Isolation of cDNA clones for genes showing enhanced expression in barley leaves during dark-induced senescence as well as during senescence under field conditions. Planta 203(3):332–340CrossRefGoogle Scholar
  40. Kontunen-Soppela S, Riikonen J, Ruhanen H, Brosche M, Somervuo P, Peltonen P, Kangasjarvi J, Auvinen P, Paulin L, Keinanen M, Oksanen E, Vapaavuori E (2010) Differential gene expression in senescing leaves of two silver birch genotypes in response to elevated CO2 and tropospheric ozone. Plant, Cell Environ 33(6):1016–1028CrossRefGoogle Scholar
  41. Lee S, Seo PJ, Lee HJ, Park CM (2012) A NAC transcription factor NTL4 promotes reactive oxygen species production during drought-induced leaf senescence in Arabidopsis. Plant J. doi: 10.1111/j.1365-313X.2012.04932.x
  42. Lim PO, Woo HR, Nam HG (2003) Molecular genetics of leaf senescence in Arabidopsis. Trends Plant Sci 8(6):272–278PubMedCrossRefGoogle Scholar
  43. Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136PubMedCrossRefGoogle Scholar
  44. 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(5):1419–1430PubMedCrossRefGoogle Scholar
  45. Lin JF, Wu SH (2004) Molecular events in senescing Arabidopsis leaves. Plant J 39(4):612–628PubMedCrossRefGoogle Scholar
  46. 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 (Database issue):D1103–D1107Google Scholar
  47. Lohman KN, Gan SS, John MC, Amasino RM (1994) Molecular analysis of natural leaf senescence in Arabidopsis thaliana. Physiol Plant 92(2):322–328CrossRefGoogle Scholar
  48. 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(3):819–830PubMedCrossRefGoogle Scholar
  49. Miao Y, Zentgraf U (2010) A HECT E3 ubiquitin ligase negatively regulates Arabidopsis leaf senescence through degradation of the transcription factor WRKY53. Plant J 63(2):179–188PubMedCrossRefGoogle Scholar
  50. Miao Y, Laun T, Zimmermann P, Zentgraf U (2004) Targets of the WRKY53 transcription factor and its role during leaf senescence in Arabidopsis. Plant Mol Biol 55(6):853–867PubMedGoogle Scholar
  51. Miao Y, Laun TM, Smykowski A, Zentgraf U (2007) Arabidopsis MEKK1 can take a short cut: it can directly interact with senescence-related WRKY53 transcription factor on the protein level and can bind to its promoter. Plant Mol Biol 65(1–2):63–76PubMedCrossRefGoogle Scholar
  52. Miao Y, Smykowski A, Zentgraf U (2008) A novel upstream regulator of WRKY53 transcription during leaf senescence in Arabidopsis thaliana. Plant Biol (Stuttg) 10(Suppl 1):110–120CrossRefGoogle Scholar
  53. Nagaraj SH, Gasser RB, Ranganathan S (2007) A hitchhiker’s guide to expressed sequence tag (EST) analysis. Brief Bioinf 8(1):6–21CrossRefGoogle Scholar
  54. 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(3):527–535PubMedCrossRefGoogle Scholar
  55. Osorio S, Alba R, Damasceno CM, Lopez-Casado G, Lohse M, Zanor MI, Tohge T, Usadel B, Rose JK, Fei Z, Giovannoni JJ, Fernie AR (2011) Systems biology of tomato fruit development: combined transcript, protein, and metabolite analysis of tomato transcription factor (nor, rin) and ethylene receptor (Nr) mutants reveals novel regulatory interactions. Plant Physiol 157(1):405–425PubMedCrossRefGoogle Scholar
  56. Quirino BF, Normanly J, Amasino RM (1999) Diverse range of gene activity during Arabidopsis thaliana leaf senescence includes pathogen-independent induction of defense-related genes. Plant Mol Biol 40(2):267–278PubMedCrossRefGoogle Scholar
  57. Quirino BF, Noh YS, Himelblau E, Amasino RM (2000) Molecular aspects of leaf senescence. Trends Plant Sci 5(7):278–282PubMedCrossRefGoogle Scholar
  58. Robatzek S, Somssich IE (2001) A new member of the Arabidopsis WRKY transcription factor family, AtWRKY6, is associated with both senescence- and defence-related processes. Plant J 28(2):123–133PubMedCrossRefGoogle Scholar
  59. Robatzek S, Somssich IE (2002) Targets of AtWRKY6 regulation during plant senescence and pathogen defense. Genes Dev 16(9):1139–1149PubMedCrossRefGoogle Scholar
  60. Rogers S, Girolami M, Kolch W, Waters KM, Liu T, Thrall B, Wiley HS (2008) Investigating the correspondence between transcriptomic and proteomic expression profiles using coupled cluster models. Bioinformatics 24(24):2894–2900PubMedCrossRefGoogle Scholar
  61. Schiltz S, Gallardo K, Huart M, Negroni L, Sommerer N, Burstin J (2004) Proteome reference maps of vegetative tissues in pea. An investigation of nitrogen mobilization from leaves during seed filling. Plant Physiol 135(4):2241–2260PubMedCrossRefGoogle Scholar
  62. Schmitt AO, Specht T, Beckmann G, Dahl E, Pilarsky CP, Hinzmann B, Rosenthal A (1999) Exhaustive mining of EST libraries for genes differentially expressed in normal and tumour tissues. Nucleic Acids Res 27(21):4251–4260PubMedCrossRefGoogle Scholar
  63. Sharabi-Schwager M, Samach A, Porat R (2010) Overexpression of the CBF2 transcriptional activator in Arabidopsis counteracts hormone activation of leaf senescence. Plant Signal Behav 5(3):296–299PubMedCrossRefGoogle Scholar
  64. Smart CM (1994) Gene-expression during leaf senescence. New Phytol 126(3):419–448CrossRefGoogle Scholar
  65. Smykowski A, Zimmermann P, Zentgraf U (2010) G-Box binding factor1 reduces CATALASE2 expression and regulates the onset of leaf senescence in Arabidopsis. Plant Physiol 153(3):1321–1331PubMedCrossRefGoogle Scholar
  66. Solomos T (1988) Respiration in senescing plant organs: its nature, regulation, and physiological significance. In: Nooden LD, Leopold AC (eds) Senescence and aging in plants. Academic Press, San Diego, pp 111–145Google Scholar
  67. Sun Q, Zybailov B, Majeran W, Friso G, Olinares PD, van Wijk KJ (2009) PPDB, the plant proteomics database at Cornell. Nucleic Acids Res 37 (Database issue):D969–D974Google Scholar
  68. Tallis MJ, Lin Y, Rogers A, Zhang J, Street NR, Miglietta F, Karnosky DF, De Angelis P, Calfapietra C, Taylor G (2010) The transcriptome of Populus in elevated CO reveals increased anthocyanin biosynthesis during delayed autumnal senescence. New Phytol 186(2):415–428PubMedCrossRefGoogle Scholar
  69. Uauy C, Distelfeld A, Fahima T, Blechl A, Dubcovsky J (2006) A NAC gene regulating senescence improves grain protein, zinc, and iron content in wheat. Science 314(5803):1298–1301PubMedCrossRefGoogle Scholar
  70. van der Graaff E, Schwacke R, Schneider A, Desimone M, Flugge U-I, Kunze R (2006) Transcription analysis of Arabidopsis membrane transporters and hormone pathways during developmental and induced leaf senescence. Plant Physiol 141:776–792PubMedCrossRefGoogle Scholar
  71. Wilson KA, McManus MT, Gordon ME, Jordan TW (2002) The proteomics of senescence in leaves of white clover, Trifolium repens (L.). Proteomics 2(9):1114–1122PubMedCrossRefGoogle Scholar
  72. 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(8):1779–1790PubMedGoogle Scholar
  73. Woo HR, Kim JH, Kim J, Lee U, Song IJ, Lee HY, Nam HG, Lim PO (2010) The RAV1 transcription factor positively regulates leaf senescence in Arabidopsis. J Exp Bot 61(14):3947–3957PubMedCrossRefGoogle Scholar
  74. Wu A, Allu AD, Garapati P, Siddiqui H, Dortay H, Zanor MI, Asensi-Fabado MA, Munne-Bosch S, Antonio C, Tohge T, Fernie AR, Kaufmann K, Xue GP, Mueller-Roeber B, Balazadeh S (2012) JUNGBRUNNEN1, a reactive oxygen species-responsive NAC transcription factor, regulates longevity in Arabidopsis. Plant Cell 24(2):482–506PubMedCrossRefGoogle Scholar
  75. Xu H, Wang X, Chen J (2010) Overexpression of the Rap2.4f transcriptional factor in Arabidopsis promotes leaf senescence. Sci China Life Sci 53(10):1221–1226PubMedCrossRefGoogle Scholar
  76. Yang SD, Seo PJ, Yoon HK, Park CM (2011) The Arabidopsis NAC transcription factor VNI2 integrates abscisic acid signals into leaf senescence via the COR/RD genes. Plant Cell 23(6):2155–2168PubMedCrossRefGoogle Scholar
  77. Yuan JS, Galbraith DW, Dai SY, Griffin P, Stewart CN Jr (2008) Plant systems biology comes of age. Trends Plant Sci 13(4):165–171PubMedCrossRefGoogle Scholar
  78. Zhang K, Gan SS (2012) An abscisic acid-AtNAP transcription factor-SAG113 protein phosphatase 2C regulatory chain for controlling dehydration in senescing Arabidopsis leaves. Plant Physiol 158(2):961–969PubMedCrossRefGoogle Scholar
  79. Zhang A, Lu Q, Yin Y, Ding S, Wen X, Lu C (2010) Comparative proteomic analysis provides new insights into the regulation of carbon metabolism during leaf senescence of rice grown under field conditions. J Plant Physiol 167(16):1380–1389PubMedCrossRefGoogle Scholar
  80. Zhang J, Wang X, Yu O, Tang J, Gu X, Wan X, Fang C (2011a) Metabolic profiling of strawberry (Fragaria x ananassa Duch.) during fruit development and maturation. J Exp Bot 62(3):1103–1118PubMedCrossRefGoogle Scholar
  81. Zhang X, Ju HW, Chung MS, Huang P, Ahn SJ, Kim CS (2011b) The R–R-type MYB-like transcription factor, AtMYBL, is involved in promoting leaf senescence and modulates an abiotic stress response in Arabidopsis. Plant Cell Physiol 52(1):138–148PubMedCrossRefGoogle Scholar
  82. Zhang K, Xia X, Zhang Y, Gan SS (2012) An ABA-regulated and golgi-localized protein phosphatase controls water loss during leaf senescence in Arabidopsis. Plant J 69(4):667–678PubMedCrossRefGoogle Scholar
  83. Zhou X, Jiang Y, Yu D (2011) WRKY22 transcription factor mediates dark-induced leaf senescence in Arabidopsis. Mol Cells 31(4):303–313PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media Dordrecht 2012

Authors and Affiliations

  1. 1.Tobacco Research InstituteChinese Academy of Agricultural SciencesQingdaoChina
  2. 2.Key Laboratory of Tobacco Biology and ProcessingMinistry of AgricultureQingdaoChina

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