Abstract
Leaf senescence is a sequence of biochemical and physiological events comprising the final stage in leaf development. It encompasses the period from a fully expanded mature state up to the death, thereby limiting longevity. The changes occurring during leaf senescence are very complex but highly regulated, and are genetically programmed with actions coordinated at the cellular, tissue, organ, and organism levels. A major breakthrough in our molecular understanding of this phenomenon has been achieved through the characterization of various mutants and senescence-associated genes, including regulatory genes. In particular, a genetic screening and assay system for leaf senescence has been well established inArabidopsis, which led leaf senescence into the realm of genetic subject along with the rich genetic and genomic resources in this model plant. These advances have not only revealed the existence of a complex regulatory network of senescence-associated signaling pathways, but have also allowed us to postulate the molecular mechanisms for signal perception, execution, and regulation. The key regulatory genes identified to date encode a variety of proteins, including transcription regulators and signal-transduction proteins, regulators of protein degradation, proteins associated with phytohormone pathways, and regulators of metabolism. Elucidation of their roles in leaf senescence and analyses of senescence regulatory pathways, including systems-level approaches, will increase our knowledge of the networks involved in senescence activity.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Abbreviations
- HR:
-
hypersensitive reaction
- PCD:
-
programmed cell death
- SAG:
-
senescence-associated gene
Literature cited
Andersson A, Keskitalo J, Sjodin A, Bhalerao R, Sterky F, Wissel K, Tandre K, Aspeborg H, Moyle R, Ohmiya Y, Bhalerao R, Brunner A, Gustafsson P, Karlsson J, Lundeberg J, Nilsson O, Sandber G, Strauss S, Sundberg B, Uhlen M, Jansson S, Nilsson P (2004) A transcriptional timetable of autumn senescence. Genome Biol5: R24
Bate NJ, Rothstein SJ, Thompson JE (1990) Expression of nuclear and chloroplast photosynthesis-specific genes during leaf senescence. J Exp Bot239: 801–811
Bleecker AB, Patterson SE (1997) Last exit: Senescence, abscission, and meristem arrest inArabidopsis. Plant Cell9: 1169–1179
Buchanan-Wollaston V (1997) The molecular biology of leaf senescence. J Exp Bot48: 181–199
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 J1: 3–22
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 inArabidopsis. Plant J42: 567–585
Cao J, Jiang F, Sodmergen, Cui K (2003) Time-course of programmed cell death during leaf senescence inEucommia ulmoides. J Plant Res162: 7–12
Chen W, Provart NJ, Glazebrook J, Katagiri F, Chang HS, Eulgem T, Mauch F, Luan S, Zou G, Whitham SA, Budworth PR, Tao Y, Xie Z, 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 ofArabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell14: 559–574
Cherry, JR, Hershey HP, Vierstra RD (1991) Characterization of tobacco expressing functional oat phytochrome. Plant Physiol96: 775–785
Dai N, Schaffer A, Petreikov M, Shahak Y, Ciller Y, Ratner K, Levine A, Granot D (1999) Overexpressionof Arabidopsis hexokinase in tomato plants inhibits growth, reduces photosynthesis, and induces rapid senescence. Plant Cell11: 1253–1266
Diaz C, Purdy S, Christ A, Morot-Gaudry JF, Wingler A, Masclaux-Daubresse C (2005) Characterization of markers to determine the extent and variability of leaf senescence inArabidopsis: A metabolic profiling approach. Plant Physiol138: 898–908
Doelling JH, Walker JM, Friedman EM, Thompson AR, Vierstra RD (2002) The APG8/12 activating enzyme APC7 is required for proper nutrient recycling and senescence inArabidopsis thaliana. J Biol Chem277: 33105–33114
Ellis CM, Nagpal R Young JC, Hagen G, Guilfoyle TJ, Reed JW (2005) AUXIN RESPONSE FACTOR1 and AUXIN RESPONSE FACTOR2 regulate senescence and floral organ abscission inArabidopsis thaliana. Development132: 4563–4574
Ewbank JJ, Barnes TM, Lakowski B, Lussier M, Bussey H, Hekimi S (1997) Structural and functional conservation of the Cae-norhabditis elegans timing gene clk-1. Science275: 980–983
Gan S (2003) Mitotic and postmitotic senescence in plants. Sci Aging Knowl Environ38: 7
Gan S, Amasino RM (1995) Inhibition of leaf senescence by auto-regulated production of cytokinin. Science270: 1986–1988
Gan S, Amasino RM (1999) Developmental targeting of gene expression by the use of a senescence-specific promoter.In P Reynolds, ed, Inducible Gene Expression in Plants. CAB International, New York, pp 169–186
Gepstein S, Sabehi G, Carp MJ, Hajouj T, Nesher MF, Yariv I, Dor C, Bassani M (2003) Large-scale identification of leaf senescence-associated genes. Plant J36: 629–642
Gepstein S, Thimann KV (1980) Changes in the abscisic acid content of oat leaves during senescence. Proc Natl Acad Sci USA77: 2050–2053
Gonzalez N, Botella JR (2003) Characterization of three ACC synthase gene family members during post-harvest-induced senescence in broccoli(Brassica oleracea L. var. italica). J Plant Biol46: 223–230
Grbic V, Bleecker AB (1995) Ethylene regulates the timing of leaf senescence inArabidopsis. Plant J8: 595–602
Gregersen PL, Holm PB (2007) Transcriptome analysis of senescence in the flag leaf of wheat(Triticum aestivum L). Plant Biotechnol J5: 192–206
Guarente L (1997) Aging: What makes us tick? Science275: 943–944
Guo Y, Cai Z, Gan S (2004) Transcriptome ofArabidopsis leaf senescence. Plant Cell Environ27: 521–549
Guo Y, Gan S (2006) AtNAP, a NAC family transcription factor, has an important role in leaf senescence. Plant J46: 601–612
Guterman A, Hajouj T, Gepstein S (2003) Senescence-associated mRNAs that may participate in signal transduction and protein trafficking. Physiol Plant118: 439–446
Hanaoka H, Noda T, Shirano Y, Kato T, Hayashi H, Shibata D, Tabata S, Ohsumi Y (2002) Leaf senescence and starvation-induced chlorosis are accelerated by the disruption of anArabidopsis autophagy gene. Plant Physiol129: 1181–1193
He Y, Can S (2002) A gene encoding an acyl hydrolase is involved in leaf senescence inArabidopsis. Plant Cell14: 805–815
He Y, Fukushige H, Hildebrand DF, Can S (2002) Evidence supporting a role of jasmonic acid inArabidopsis leaf senescence. Plant Physiol128: 876–884
He Y, Tang W, Swain JD, Green AL, Jack TP, Gan S (2001) Networking senescence-regulating pathways by usingArabidopsis enhancer trap lines. Plant Physiol126: 707–716
Hensel L, Crbic V, Baumgarten DA, Bleecker AB (1993) Developmental and age-related processes that influence the longevity and senescence of photosynthetic tissues inArabidopsis. Plant Cell5: 553–564
Hinderhofer K, Zentgraf U (2001) Identification of a transcription factor specifically expressed at the onset of leaf senescence. Planta213: 469–473
Hörtensteiner S, Feller U (2002) Nitrogen metabolism and remobilization during senescence. J Exp Bot53: 927–937
Jang JC, Leon P, Zhou L, Sheen J (1997) Hexokinase as a sugar sensor in higher plants. Plant Cell9: 5–19
Jing HC, Sturre MJC, Hille J, Dijkwel PP (2002)Arabidopsis onset of leaf death mutants identify a regulatory pathway controlling leaf senescence. Plant J32: 51–63
John I, Hackett R, Cooper W, Drake R, Farrell A, Crierson D (1997) Cloning and characterization of tomato leaf senescence-related cDNAs. Plant Mol Biol33: 641–651
Jones AM, Dangl JL (1996) Logjam at the Styx: Programmed cell death in plants. Trends Plant Sci1: 114–119
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 inArabidopsis. Proc Natl Acad Sci USA103: 814–819
Kimura KD, Tissenbaum HA, Liu Y, Ruvkun G (1997)daf-2, an insulin receptor-like gene that regulates longevity and diapause inCaenorhabditis elegans. Science277: 942–946
Li XP, Gan R, Li PL, Ma YY, Zhang LW, Zhang R, Wang Y, Wang NN (2006) Identification and functional characterization of a leucine-rich repeat receptor-like kinase gene that is involved in regulation of soybean senescence. Plant Mol Biol61: 829–844
Lim PO, Nam HG (2005) The molecular and genetic control of leaf senescence and longevity inArabidopsis. Curr Top Dev Biol67: 49–83
Lim PO, Woo HR, Nam HG (2003) Molecular genetics of leaf senescence inArabidopsis. Trends Plant Sci8: 272–278
Lin JF, Wu SH (2004) Molecular events in senescingArabidopsis leaves. Plant J39: 612–628
Masclaux C, Valadier M, Brugière N, Morot-Gaudry J, Hirel B (2000) Characterization of the sink/source transition in tobacco(Nicotiana tabacum L.) shoots in relation to nitrogen management and leaf senescence. Planta211: 510–518
McCabe MS, Garratt LC, Schepers F, Jordi WJRM, Stoopen GM, Davelaar E, van Rhijk JHA, Power B, Davey MR (2001) Effects of PSAG12-IPT gene expression on development and senescence in transgenic lettuce. Plant Physiol127: 505–516
McKenzie MJ, Mett V, Reynolds PHS, Jameson PE (1998) Controlled cytokinin production in transgenic tobacco using a copper-inducible promoter. Plant Physiol116: 969–977
Miao Y, Laun T, Zimmermann P, Zentgraf U (2004) Targets of the WRKY53 transcription factor and its role during leaf senescence inArabidopsis. Plant Mol Biol55: 853–867
Moore B, Zhou L, Rolland F, Hall Q, Cheng WH, Liu YX, Hwang I, Jones T, Sheen J (2003) Role of theArabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science300: 332–336
Morris KAH, Mackerness S, Page T, John CF, Murphy AM, Carr JF, Buchanan-Wollaston V (2000) Salicylic acid has a role in regulating gene expression during leaf senescence. Plant J23: 677–685
Nam HG (1997) Molecular genetic analysis of leaf senescence. Curr Opin Biotech8: 200–207
Noodén LD (1988) The phenomena of senescence and aging,In LD Noodén, AC Leopold, eds, Senescence and Aging In Plants. Academic Press, San Diego, pp 1–50
Oh MH, Kim JH, Zulfugarow IS, Moon YH, Rhew TH, Lee CH (2005) Effects of benzyladenine and abscisic acid on the disassembly process of photosystems in anArabidopsis delayed-senescence mutant,ore9. J Plant Biol48: 170–177
Oh SA, Park JH, Lee Gl, Paek KH, Park SK, Nam HG (1997) Identification of three genetic loci controlling leaf senescence inArabidopsis thaliana. Plant J12: 527–535
Okushima Y, Mitina I, Quach HL, Theologis A (2005) AUXIN RESPONSE FACTOR 2 (ARF2): A pleiotropic developmental regulator. Plant J43: 29–46
Otegui MS, Noh YS, Martinez DE, Vila Petroff MG, Staehelin LA, Amasino RM, Guiamet JJ (2005) Senescence-associated vacuoles with intense proteolytic activity develop in leavesof Arabidopsis and soybean. Plant J41: 831–844
Park JH, Oh SA, Kim YH, Woo HR, Nam HG (1998) Differential expression of senescence associated mRNAs during leaf senescence induced by different senescence-inducing factors inArabidopsis. Plant Mol Biol37: 445–454
Patton EE, Willems AR, Tyers M (1998) Combinational control in ubiquitin-dependent proteolysis: Don’t Skp the F-box hypothesis. Trends Genet14: 236–243
Quirino BF, Noh YS, Himelblau E, Amasino RM (2000) Molecular aspects of leaf senescence. Trends Plant Sci5: 278–282
Quirino BF, Normanly J, Amasino RM (1999) Diverse range of gene activity duringArabidopsis thaliana leaf senescence includes pathogen-independent induction of defense-related genes. Plant Mol Biol40: 267–278
Robatzek S, Somssich IE (2002) Targets of AtWRKY6 regulation during plant senescence and pathogen defense. Genes Dev16: 1139–1149
Rolland F, Moore B, Sheen J (2002) Sugar sensing and signaling in plants. Plant Cell Suppl14: S185–205
Simeonova E, Sikira S, Charzynska M, Mostowska A (2000) Aspects of programmed cell death during leaf senescence of mono- and dicotyledonous plants. Protoplasma214: 93–101
Swidzinski JA, Sweetlove LJ, Leaver CJ (2002) A custom microarray analysis of gene expression during programmed cell death inArabidopsis thaliana. Plant J30: 431–446
Taylor CB, Bariola PA, delCardayre SB, Raines RT, Green PJ (1993) RNS2: A senescence associated RNase ofArabidopsis that diverged from the S-RNase before speciation. Proc Natl Acad Sci USA90: 5118–5122
Thiele A, Herold M, Lenk I, Quail PH, Gatz C (1999) Heterologous expression ofArabidopsis phytochrome B in transgenic potato influences photosynthetic performance and tuber development. Plant Physiol120: 73–81
Thompson J, Taylor C, Wang TW (2000) Altered membrane lipase expression delays leaf senescence. Biochem Soc Trans28: 775–777
Thompson JE, Froese CD, Madey E, Smith MD, Hong Y (1998) Lipid metabolism during plant senescence. Prog Lipid Res37: 119–141
Uauy C, Fahima T, Blechl A, Dubcovsky J (2006) A NAC gene regulating senescence improves grain protein, zinc, and iron content in wheat. Science314: 1298–1301
van der GraaffE, Schwacke R, Schneider A, Desimone M, Flugge Ul, Kunze R (2006) Transcription analysis ofArabidopsis membrane transporters and hormone pathways during developmental and induced leaf senescence. Plant Physiol141: 776–792
van Doom WC, Woltering EJ (2004) Senescence and programmed cell death: Substance or semantics? J Exp Bot55: 2147–153
Weaver LM, Gan S, Quirino B, Amasino RM (1998) A comparison of the expression patterns of several senescence-associated genes in response to stress and hormone treatment. Plant Mol Biol37: 455–469
Wingler A, Lea PJ, Quick WP, Leegood RC (2000) Photorespiration: Metabolic pathways and their role in stress protection. Philos Trans R Soc Lond B Biol Sci355: 1517–1529
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 inArabidopsis. Plant Cell13: 1779–1790
Woo HR, Goh CH, Park JH, Teyssendier B, Kim JH, Park Yl, Nam HG (2002) Extended leaf longevity in theore4-l mutant ofArabidopsis with a reduced expression of a plastid ribosomal protein gene. Plant J31: 331–340
Xiao S, Dai L, Liu F, Wang Z, Peng W, Xie D (2004) COS1: AnArabidopsis coronatine insensitivel suppressor essential for regulation of jasmonate-mediated plant defense and senescence. Plant Cell16: 1132–1142
Xiong Y, Contento AL, Bassham DC (2005) AtATG18a is required for the formation of autophagosomes during nutrient stress and senescence inArabidopsis thaliana. Plant J42: 535–546
Yen CH, Yang CH (1998) Evidence for programmed cell death during leaf senescence in plants. Plant Cell Physiol39: 922–927
Yoshida S, Ito M, Callis J, Nishida I, Watanabe A (2002a) A delayed leaf senescence mutant is defective in arginyl-tRNA:protein arginyltransferase, a component of the N-end rule pathway inArabidopsis. Plant J32: 129–137
Yoshida S, Ito M, Nishida I, Watanabe A (2002b) Identification of a novel gene HYS1/CPR5 that has a repressive role in the induction of leaf senescence and pathogen-defence responses inArabidopsis thaliana. Plant J29: 427–437
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Lim, P.O., Nam, H.G. Aging and senescence of the leaf organ. J. Plant Biol. 50, 291–300 (2007). https://doi.org/10.1007/BF03030657
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF03030657