Leaf Senescence Pyung Ok Lim (2007)

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Leaf SenescencePyung Ok Lim,1 Hyo Jung Kim,2

and Hong Gil Nam2

1Department of Science Education, Cheju National University, Jeju,Jeju, 690-756, Korea2Division of Molecular Life Sciences and National Core Research Centerfor Systems Bio-Dynamics, POSTECH, Pohang, Kyungbuk, 790-784, Korea;email: [email protected]

Annu. Rev. Plant Biol. 2007. 58:115–36

The Annual Review of Plant Biology is online atplant.annualreviews.org

This article’s doi:10.1146/annurev.arplant.57.032905.105316

Copyright c© 2007 by Annual Reviews.All rights reserved

First published online as a Review in Advance onDecember 19, 2006

1543-5008/07/0602-0115$20.00

Key Words

longevity, developmental aging, programmed cell death, nutrientremobilization, environmental factors

AbstractLeaf senescence constitutes the final stage of leaf development andis critical for plants’ fitness as nutrient relocation from leaves to re-producing seeds is achieved through this process. Leaf senescenceinvolves a coordinated action at the cellular, tissue, organ, and organ-ism levels under the control of a highly regulated genetic program.Major breakthroughs in the molecular understanding of leaf senes-cence were achieved through characterization of various senescencemutants and senescence-associated genes, which revealed the natureof regulatory factors and a highly complex molecular regulatory net-work underlying leaf senescence. The genetically identified regula-tory factors include transcription regulators, receptors and signalingcomponents for hormones and stress responses, and regulators ofmetabolism. Key issues still need to be elucidated, including cellular-level analysis of senescence-associated cell death, the mechanismof coordination among cellular-, organ-, and organism-level senes-cence, the integration mechanism of various senescence-affectingsignals, and the nature and control of leaf age.

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Contents

INTRODUCTION. . . . . . . . . . . . . . . . . 116LEAF SENESCENCE-

ASSOCIATED CELL DEATHAS A PROGRAMMED CELLDEATH . . . . . . . . . . . . . . . . . . . . . . . . . 117Structural and Biochemical

Changes in LeafSenescence-Associated CellDeath. . . . . . . . . . . . . . . . . . . . . . . . . 118

Molecular Comparison of LeafSenescence-Associated CellDeath with Other ProgrammedCell Deaths . . . . . . . . . . . . . . . . . . . 119

MOLECULAR AND GENETICAPPROACHES FORANALYZING LEAFSENESCENCE . . . . . . . . . . . . . . . . . 120Assay of Leaf Senescence . . . . . . . . . 120Genetic Analysis of Leaf

Senescence . . . . . . . . . . . . . . . . . . . . 121Molecular Approaches to

Understanding LeafSenescence . . . . . . . . . . . . . . . . . . . . 121

MOLECULAR GENETICREGULATION OF LEAFSENESCENCE . . . . . . . . . . . . . . . . . 122Onset of Leaf Senescence . . . . . . . . . 123Environmental Factors and Leaf

Senescence . . . . . . . . . . . . . . . . . . . . 123Involvement of Phytohormone

Pathways in Leaf Senescence . . . 124Other Regulatory Genes

of Senescence . . . . . . . . . . . . . . . . . 128CONCLUSIONS AND FUTURE

CHALLENGES . . . . . . . . . . . . . . . . . 130

INTRODUCTION

Senescence is the age-dependent deteriora-tion process at the cellular, tissue, organ, ororganismal level, leading to death or the end ofthe life span (48). Leaf senescence is an organ-level senescence but is often intimately associ-ated with cellular or organismal death. Annual

plants undergo leaf senescence along with theorganismal-level senescence when they reachthe end of their temporal niche, as we observeat the grain-filling and maturation stage of thecrop fields of soybean, corn, or rice. For treesand other perennial plants, leaf senescence isillustrated by the splendid autumn scenery ofcolor changes in leaves.

Leaf senescence is not a passive andunregulated degeneration process. Duringsenescence, leaf cells undergo rather orderlychanges in cell structure, metabolism, andgene expression. The earliest and most signif-icant change in cell structure is the breakdownof the chloroplast, the organelle that containsup to 70% of the leaf protein. Metabolically,carbon assimilation is replaced by catabolismof chlorophyll and macromolecules such asproteins, membrane lipids, and RNA. In-creased catabolic activity is responsible forconverting the cellular materials accumulatedduring the growth phase of leaf into ex-portable nutrients that are supplied to devel-oping seeds or to other growing organs. Thus,although leaf senescence is a deleterious pro-cess for the sake of the leaf organ, it can beseen as an altruistic process: It critically con-tributes to the fitness of whole plants by ensur-ing optimal production of offspring and bet-ter survival of plants in their given temporaland spatial niches. Leaf senescence is thus anevolutionarily selected developmental processand comprises an important phase in the plantlife cycle (7, 40, 46, 48). In agricultural aspects,however, leaf senescence may limit yield incrop plants by limiting the growth phase andmay also cause postharvest spoilage such asleaf yellowing and nutrient loss in vegetablecrops. Thus, studying leaf senescence will notonly enhance our understanding of a funda-mental biological process, but also may pro-vide means to control leaf senescence to im-prove agricultural traits of crop plants.

Leaf senescence is basically governed bythe developmental age. However, leaf senes-cence is also influenced by various internaland environmental signals that are integratedinto the age information: Leaf senescence is

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an integrated response of leaf cells to ageinformation and other internal and environ-mental signals. This integrated senescence re-sponse provides plants with optimal fitness byincorporating the environmental and endoge-nous status of plants in a given ecological set-ting by fine-tuning the initiation timing, pro-gression rate, and nature of leaf senescence.The environmental factors that influence leafsenescence include abiotic and biotic factors.The abiotic factors include drought, nutrientlimitation, extreme temperature, and oxida-tive stress by UV-B irradiation and ozone, etc.The biotic factors include pathogen infectionand shading by other plants. Leaf senescencecan occur prematurely under these unfavor-able environmental conditions (39).

In naturally senescing leaves, senescenceoccurs in a coordinated manner at the whole-leaf level, usually starting from the tips or themargins of a leaf toward the base of a leaf.However, when the uneven environmentalstress is targeted locally on a leaf, the stressedleaf region undergoes earlier senescence thando the other parts. Thus, leaf cells show somedegree of locality in a senescence program.

Leaf senescence can occur without an ob-vious correlation with senescence of other or-gans in some plants, such as many tree species,although it is often developmentally coor-dinated with senescence of other organs orwhole plants, especially monocarpic plants. Insome monocarpic plants, the reproductive de-velopment often governs senescence of leaves.This so-called correlative control is dramati-cally observed in pea and soybean, where re-moval of the reproductive organ can actuallyreverse the fate of senescing leaves to juve-nile leaves. However, in some plants such asArabidopsis, leaf senescence does not appearto be under correlative control, but the leafsenescence at the whole-plant level is some-what correlated with the life span of the wholeplant.

Arabidopsis thaliana is a favorite model forthe molecular genetic study of leaf senescence(5, 7, 39). As a monocarpic plant, it has ashort life cycle. Its leaves undergo readily dis-

Monocarpic plant:a plant thatreproduces once andthen dies at the endof its reproductivephase

Leaf longevity:reflects the period ofa whole life span of aleaf from itsemergence as a leafprimordium to death

tinguishable developmental stages and showa well-defined and reproducible senescenceprogram (Figure 1), which makes geneticanalysis of leaf senescence feasible. Extensivegenomic resources available for Arabidopsis al-low rapid identification and functional analy-sis of senescence regulatory genes.

In this review, we discuss recent progresstoward molecular and genetic understand-ing of leaf senescence and longevity thathas been achieved mostly from Arabidopsis.It is cautioned that Arabidopsis leaves have asenescence character different from that ofsome other monocarpic plants in that the leaflongevity in Arabidopsis is not controlled bythe developing reproductive structures. Thus,the findings in Arabidopsis might not revealsome of the mechanisms involved in leafsenescence of other plants. Thus, whereverappropriate we also discuss the discoveriesachieved from other plants.

LEAF SENESCENCE-ASSOCIATED CELL DEATH AS APROGRAMMED CELL DEATH

Leaf senescence involves cell death that iscontrolled by age under the influence ofother endogenous and environmental fac-tors. Programmed cell death (PCD) is aself-destructing cellular process triggered byexternal or internal factors and mediatedthrough an active genetic program. Cell deathin leaf senescence is controlled by many ac-tive genetic programs (10). The cell death oc-curring in leaf senescence is thus a type ofPCD. Leaf organs are composed of variouscell types. Cell death in leaf senescence startsfrom mesophyll cells and then proceeds toother cell types. It also appears that cell deathdoes not occur coherently but starts with localpatches of early-dying cells and then propa-gates into the whole-leaf area.

PCD plays crucial roles in various devel-opmental and defense responses in plants.Typical examples of PCD in plants are ob-served in the formation of tracheary elements,germination-related degeneration of aleuron

www.annualreviews.org • Leaf Senescence 117

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Figure 1Characteristics of whole-plant senescence and leaf senescence in Arabidopsis. (a) Stages in the life cycle ofwhole plants. Plants are pictured at 15, 25, 30, 40, 50, and 60 days after germination. (b) Anage-dependent senescence phenotype in the third rosette leaf. Leaves are pictured at 12, 16, 20, 24, 28,and 32 days after emergence. (c) As leaves senesce, nutrients such as nitrogen, phosphorus, and metals arerelocated to other parts of the plants such as developing seeds and leaves.

layer cells, and pathogen-induced hypersen-sitive response (HR) (34, 70). PCD in leafsenescence has some features distinctive fromother PCDs (71). First, leaf senescence in-volves an organ-level cell death that eventuallyencompasses the entire leaf, whereas otherPCDs involve rather localized cell death oroccur in limited tissues and cell types. Sec-ond, cell death rate during leaf senescence isslower than that in the other PCDs. Third,in terms of the biological function, PCD inleaf senescence is mostly for remobilizationof nutrients from the leaf to other organs in-cluding developing seeds. The leaf organ isthe major photosynthetic organ. Thus, opti-mal utilization of nutrients accumulated dur-ing the photosynthetic period is critical for

plants’ fitness and is critically affected by finecontrol of senescence process. In this regard,the slow degeneration of cells during leafsenescence is in part to ensure effective re-mobilization of nutrients that are generatedby macromolecular hydrolysis during senes-cence. Many molecular events during leafsenescence can be readily understood fromthe viewpoint of this altruistic remobilizationactivity.

Structural and Biochemical Changesin Leaf Senescence-Associated CellDeath

Leaf cells at the senescence stage showsome distinctive structural and biochemical


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changes. A notable feature of cellular struc-tural change during leaf senescence is theorder of disintegration of intracellular or-ganelles (48, 68). The earliest structuralchanges occur in the chloroplast, i.e., changesin the grana structure and content and forma-tion of lipid droplet called plastoglobuli. Incontrast, the nucleus and mitochondria thatare essential for gene expression and energyproduction, respectively, remain intact untilthe last stages of senescence. This reflects thatthe leaf cells need to remain functional forprogression of senescence until a late stage ofsenescence, possibly for effective mobilizationof the cellular materials. In the last stage of leafsenescence, typical symptoms of PCD such ascontrolled vacuolar collapse, chromatin con-densation, and DNA laddering are detectedin naturally senescing leaves from a variety ofplants including Arabidopsis, tobacco, and fivetrees (10, 62, 78). These observations implythat leaf senescence involves cellular eventsthat ultimately lead to PCD. Eventually, visi-ble disintegration of the plasma and vacuolarmembranes appears. The loss of integrity ofthe plasma membrane then leads to disrup-tion of cellular homeostasis, ending the life ofa cell in senescing leaves.

The cellular biochemical changes insenescing leaves are first accompanied by re-duced anabolism (4, 5, 76). The overall cel-lular content of polysomes and ribosomesdecreases fairly early, reflecting a decreasein protein synthesis. This occurs concomi-tantly with reduced synthesis of rRNAs andtRNAs. Further cellular biochemical changesare most easily understood from the view-point of nutrient salvage, e.g., hydrolysis ofmacromolecules and subsequent remobiliza-tion, which requires operating a complex arrayof metabolic pathways. Chloroplast degener-ation is accompanied by chlorophyll degra-dation and the progressive loss of proteinsin the chloroplast, such as ribulose biphos-phate carboxylase (Rubisco) and chlorophylla/b binding protein (CAB). Hydrolysis of pro-teins to free amino acids depends on the ac-tions of several endo- and exopeptidases (6,

28, 52). Senescence-associated cystein pro-teases, which are accumulated in the vacuole,also play a role in protein degradation. Lipid-degrading enzymes, such as phospholipase D,phosphatidic acid phosphatase, lytic acyl hy-drolase, and lipoxygenase appear to be in-volved in hydrolysis and metabolism of themembrane lipid in senescing leaves (66, 67).Most of the fatty acids are either oxidized toprovide energy for the senescence process orconverted to α-ketoglutarate via the glyoxy-late cycle. The α-ketoglutarate can be con-verted into phloem-mobile sugars throughgluconeogenesis or used to mobilize aminoacids released during leaf protein degradation(28, 66). A massive decrease in nucleic acidsoccurs during leaf senescence (65). Total RNAlevels are rapidly reduced along with progres-sion of senescence. The initial decrease in theRNA levels is distinctively observed for thechloroplast rRNAs and cytoplasmic rRNAs.The amount of various rRNA species is likelyregulated coordinately, although this aspecthas not been analyzed. The decrease of theamount of rRNAs is followed by that of thecytoplasmic mRNA and tRNA. The decreasein the RNA levels is accompanied by increasedactivity of several RNases.

Molecular Comparison of LeafSenescence-Associated Cell Deathwith Other Programmed Cell Deaths

One obvious question regarding leafsenescence-associated cell death is how thecell death pathways during leaf senescenceare distinct from those of other types ofPCDs at the molecular level. Cell death inpathogen-induced HR is best-characterizedamong plant PCDs. Pathogenesis-related(PR) proteins are associated with PCD in HR.A few earlier works showed that many PRgenes are induced during leaf senescence inseveral plant species (55, 56). A comparativestudy of leaf senescence and HR showedthat HIN1, an HR cell death marker, is alsoexpressed at late stages of leaf senescence(63). Furthermore, defense-related genes


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Photochemicalefficiency: deducedfrom thecharacteristics ofchlorophyllfluorescence of PSII.The ratio ofmaximum variablefluorescence (Fv) tomaximum yield offluorescence (Fm),which correspondsto the potentialquantum yield of thephotochemicalreactions of PSII, isused as the measureof the photochemicalefficiency of PSII

including the Arabidopsis ELI3 gene showed asenescence-associated induction as well (56).The LSC54 gene encoding a metallothionineis also highly induced during both senescenceand pathogen-related cell death (9). Theseobservations indicate that, at the molecularlevel, some common steps or crosstalksexist between senescence-associated andpathogen-induced cell death.

In contrast, a few molecular markers thatare specific for each of the senescence-associated and HR-associated PCDs were alsoidentified. For example, HSR203J is upregu-lated during HR but not during leaf senes-cence (54). Similarly, the Arabidopsis SAG12gene expression is associated with leaf senes-cence but is not detected in the HR PCD intobacco. Thus, these two genes may be a spe-cific part of signaling steps for HR PCD andsenescence-associated cell death, respectively,indicating that there are specific branches ofmolecular pathways leading to these two typesof PCD.

A comparison of changes in global geneexpression patterns during natural leaf senes-cence with those during starvation-induceddeath of suspension culture cells has shownsimilarities as well as considerable differencesbetween these two PCDs (8). Of the 827senescence-enhanced genes, 326 showed atleast threefold upregulation in the starvation-induced PCD of suspension culture. In con-trast, the rest of the senescence-upregulatedgenes were not significantly upregulated instarvation-induced PCD of suspension cul-ture. The result implies that distinctivepathways for the two PCD processes arepresent.

MOLECULAR AND GENETICAPPROACHES FOR ANALYZINGLEAF SENESCENCE

As with any other biological phenomena, itwas critical to develop an accurate and properassay for leaf senescence. Two main pointsmust be seriously considered in analyzing leafsenescence. First, leaf senescence should be

measured on a single leaf base along with itsage information. Measuring senescence pa-rameters with a mixture of several leaves ata given age of a plant is not a valid analy-sis for leaf senescence because the individualleaves of a plant have different ages. Second,the senescence symptom should be measuredwith various senescence parameters and ide-ally with markers that cover various aspectsof senescence physiology. Senescence resultsfrom a sum of various physiological changesand it is often possible that a single param-eter may not reflect senescence but only thechange of a specific physiology related to themeasuring parameter.

Assay of Leaf Senescence

To quantitatively measure the leaf senes-cence symptom, a range of physiologi-cal and molecular parameters can be uti-lized. Well-established senescence markersinclude chlorophyll content, photochemicalefficiency, senescence-associated enzyme ac-tivities, change of protein levels, membraneion leakage, and gene expression, etc. Leafyellowing is a convenient visible indicator ofleaf senescence and reflects mainly chloroplastsenescence of mesophyll cells, which is thefirst step in senescence-associated PCD. Thesurvivorship curve assay based on visual ex-amination of leaf yellowing (the time whenthe half of a leaf turns yellow) provides a re-liable measure, although the assay is some-what subjective. Measuring chlorophyll lossand photochemical efficiency is another con-venient assay for chloroplast senescence (49,74). The activation of catabolic or hydrolyticactivities, such as RNase or peroxidase ac-tivity occurs during leaf senescence (1, 65).Thus, measuring these enzyme activities isalso a reliable and quantitative way to assayleaf senescence. Senescence involves disrup-tion of plasma membrane integrity as the fi-nal step of cell death, which can be conve-niently quantified by monitoring membraneion leakage (74). This provides one of mostreliable assays for senescence-associated cell


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death, although it measures the later step ofsenescence.

Leaf senescence is accompanied by de-creased expression of genes related tophotosynthesis (e.g., CAB2) and protein syn-thesis (e.g., RPS, RBC) and by increasedexpression of senescence-associated genes(SAGs). The expression pattern of thesegenes during leaf development can be mon-itored by RNA gel blot analysis or reversetranscription-polymerase chain reaction (RT-PCR) (74). Microarray analysis would providea quantifiable and global picture of the senes-cence process at the gene expression level witha clue of which downstream pathways of leafsenescence are affected by a specific mutationor by a specific environmental condition (8,11). Microarray data may be further utilizedfor systems-level analysis of leaf senescence.

Genetic Analysis of Leaf Senescence

Two main approaches were utilized for under-standing regulation of leaf senescence: the ge-netic and molecular approaches. The geneticapproach involves isolation and characteriza-tion of mutants that show altered senescencephenotypes. Arabidopsis is a suitable modelplant in this regard (25). Considering thecomplex nature of leaf senescence, it is ex-pected that regulation of senescence involvesmany regulatory elements composed of posi-tive and negative elements to finely tune theinitiation and progression of senescence. Thepositive elements must exist for senescenceto proceed. The negative elements are alsoimportant to prevent senescence from occur-ring prematurely. Many of these regulatoryelements may contribute subtly in the senes-cence phenotype due to redundant functionsin senescence. In addition, senescence is in-evitably affected by the previous developmen-tal stages including leaf formation and growth.Thus, a screening scheme suitably focusedon leaf senescence symptoms was developedand successfully employed for isolating senes-cence mutants. So far, most of the geneticscreening was focused on identifying delayed

senescence mutants from T-DNA or a chem-ical mutant pool, which allowed identifica-tion of various important positive elements ofsenescence (50, 74, 75, 79). Early-senescencemutants screened from T-DNA or chemicalmutant pools would enable identification ofnegative factors involved in the leaf senes-cence process (80). However, this approachshould be taken with the caution that mu-tations with apparent early-senescence symp-toms may not be directly associated with con-trol of senescence because mutations in manyhomeostatic or housekeeping genes could alsogive apparent early-senescence symptoms.

Molecular Approaches toUnderstanding Leaf Senescence

The alternative approach was to identify andcharacterize genes that show enhanced orreduced expression during leaf senescence.Recent technological advances have allowedinvestigation of the SAGs at the genome-widescale (3, 8, 17, 19, 41, 72). For example, aDNA microarray with 13,490 aspen expressedsequence tags (ESTs) was used to analyze thetranscriptom of aspen leaves during autumnsenescence (3). In Arabidopsis, AffymetrixGeneChip arrays representing 24,000 geneswere utilized for analyzing changes in globalexpression pattern during leaf senescence (8,72). This analysis has identified more than800 SAGs, illustrating the dramatic alterationin cellular physiology that underlies thedevelopmental transition to the senescencestage. Unlike the genome-wide microarrayanalysis, microarray analysis of 402 potentialtranscription factors was carried out atdifferent developmental stages and undervarious biotic and abiotic stresses, providinga clue to the transcriptional regulatorynetwork during leaf senescence (11). Similarapproaches for other crop plants shouldallow comparison of molecular pictures ofleaf senescence in different species. Thecollection of T-DNA insertion lines avail-able in Arabidopsis was effectively utilizedfor functional analysis of individual SAGs.


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In particular, functional characterizationof potential regulators such as signaltransduction-related proteins and tran-scription factors was the primary target forthis analysis. Analysis of these mutant lineshas provided and will continue to provideimportant information for understandingregulatory pathways of leaf senescence.

MOLECULAR GENETICREGULATION OF LEAFSENESCENCE

Leaf senescence is an integral part of plantdevelopment and constitutes the final stageof development. The timing of leaf senes-cence is thus controlled by developmental age.

However, the senescence process includingsenescence rate and molecular nature is in-timately influenced by various environmen-tal and internal factors. The environmentalcues that affect leaf senescence include stressessuch as high or low temperature, drought,ozone, nutrient deficiency, pathogen infec-tion, and shading, etc. The internal factors in-clude various phytohormones and reproduc-tive development as well as developmental age(Figure 2). It is obvious that multiple path-ways responding to various internal and exter-nal factors should exist and are interconnectedto form a complex network of regulatory path-ways for senescence (24). It is also obviousthat, although the apparent symptoms of leafsenescence appear similar during senescence,

Macromoleculedegradation

Nutrient salvage& translocation

Detoxification& defense

• Chlorophyll loss/ nitrogen and lipid mobilization• Increase of antioxidants and defense-related genes

Regulatorynetwork

• DNA laddering/ disruption of the nucleus and mitochondria• Disintegration of the plasma and vacuolar membranes

WRKY6WRKY53

NAC1

Onset of senescence

Internal factors

• Hormones

Cytokinin (AHK3, ARR2)Ethylene (EIN2, OLD)Auxin (ARF2)JA (OsDOS)ABASA

• Reproduction

External factors

• UV-B or ozone• Nutrient limitation• Heat or cold• Drought• Shading• Pathogen attack

or wounding

Developmentalage

Figure 2A model for regulatory pathways in leaf senescence. Leaf senescence is considered a complex process inwhich the effects of various internal and external signals are integrated into the developmentalage-dependent senescence pathways. Multiple pathways that respond to various factors are possiblyinterconnected to form regulatory networks. These regulatory pathways activate distinct sets ofsenescence-associated genes, which are responsible for executing the degeneration process and ultimatelylead to cell death.


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the molecular nature of the senescence stateinfluenced by these factors will be distinctive(53).

Leaf senescence should be a finely regu-lated process, considering its potential role inplants’ fitness and the various factors involvedin senescence control. Below we discuss theprogress regarding molecular and genetic un-derstanding of leaf senescence.

Onset of Leaf Senescence

A few of the central and unanswered ques-tions regarding leaf senescence are how theleaf senescence is initiated, what the natureof the threshold that triggers leaf senescenceis, how the developmental age is recognizedto initiate the senescence program, and whatthe nature of the developmental age is. Thereare some indications that lead to answers tothese questions. In plants, sugar status modu-lates and coordinates internal regulators andenvironmental cues that govern growth anddevelopment. Several lines of evidence sug-gest that a high concentration of sugars lowersphotosynthetic activity and induces leaf senes-cence (12, 31, 44, 55). Senescence would betriggered when the level of sugars is abovean acceptable window. In that sense, sugarmetabolic rate would affect leaf longevity andmight be the mechanism that regulates thedevelopmental aging process, as shown in arange of organisms from yeast to mammals(15, 36).

An interesting finding was obtained fromstudies of the oresara 4-1 (ore4-1) mutation,which causes a delay in leaf senescence dur-ing age-dependent senescence, but not inhormone- or dark-induced senescence (75).The ore4-1 mutant has a partial lesion inchloroplast functions, including photosynthe-sis, which results from reduced expression ofthe plastid ribosomal protein small subunit 17(PRPS17) gene. It was suggested that the de-layed leaf senescence phenotype observed inthe ore4-1 mutant is likely due to a reducedmetabolic rate because the chloroplasts, themajor energy source for plant growth via pho-

Aging: an additionof timing to a cell,organ, or a wholeplant that occursthroughoutdevelopment. In thissense, aging wouldbe a majordeterminant ofsenescence but notsenescence itself

tosynthesis, are only partially functional in themutant. Reduced metabolic rate could lead toless oxidative stress, which might be a crucialfactor in senescence.

Leaf senescence should be intimately re-lated to the previous developmental stages ofleaf, such as leaf initiation, growth, and mat-uration. Thus, it is possible that genes con-trolling these processes, including meristem-atic activity, could influence age-dependentsenescence. In this respect, we observed thatthe leaves of the blade on petiole 1-1 (bop1-1) mutant that showed enhanced meristem-atic activity in leaves exhibited a prolongedlife span (21). Exact mechanisms by whichthis gene regulates leaf senescence need to beinvestigated.

Environmental Factors and LeafSenescence

Senescence is an integrated response of plantsto endogenous developmental and externalenvironmental signals. Thus, some of thegenes involved in the response to environ-mental changes are expected to regulate leafsenescence. A comparison of gene expres-sion patterns between stress responses andleaf senescence indicated that considerablecrosstalk exists between these processes. Forexample, among the 43 transcription factorgenes that are induced during senescence, 28genes are also induced by various stresses.Our current understanding of the relation-ship between environmental responses andleaf senescence mostly comes from the studyof senescence response to the phytohormonessuch as abscisic acid (ABA), jasmonic acid( JA), ethylene, and salicylic acid (SA) that areextensively involved in response to variousabiotic and biotic stresses. These stresses af-fect synthesis and/or signaling pathways of thehormones to eventually trigger expression ofstress-responsive genes, which in turn appearsto affect leaf senescence. The involvement ofthese hormonal pathways is discussed below.However, we emphasize the need to directlyexamine the relationship between the stress


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AHK3: ArabidopsisHistidine Kinase 3

Arabidopsis

response regulators(ARRs): classifiedinto two distinctsubtypes, type A andtype B, by thereceiver domainsequences and byC-terminalcharacteristics

Apoplastic phloemunloading pathway:Sucrose is releasedvia a sucrosetransporter from thesieve elements of thephloem in theapoplast, where it isirreversiblyhydrolyzed by anextracellularinvertase

responses and leaf senescence by, for exam-ple, utilizing various stress response mutantsexisting in Arabidopsis.

Involvement of PhytohormonePathways in Leaf Senescence

Hormone signaling pathways often mediateor influence development and environmen-tal responses in plants. For leaf senescence,an especially intimate interplay of many ofthese hormonal pathways is involved alongwith age-controlled senescence. This wouldbe a way for plants to ensure proper con-trol of leaf senescence response to endogenousand/or environmental signals. The hormonalpathways appear to play at all the stages ofleaf senescence, including the initiation phaseof senescence, progression, and the terminalphases. Each plant hormone affects variousdevelopmental and/or environmental eventsin a complex manner. This causes difficultiesin assaying the roles of the hormonal pathwaysin leaf senescence. Nonetheless, the roles ofthese hormones in regulating leaf senescenceare becoming evident through characteriza-tion of genetic mutants and the global gene ex-pression analysis, providing important molec-ular information about how the hormonalsignaling pathways lead to changes in patternof gene expression during leaf senescence.

Cytokinins have many critical functionsin plants, such as the control of cell prolif-eration, shoot formation, and shoot branch-ing. Cytokinins have also been known formany decades to be senescence-delaying hor-mones (59), based on the findings that theendogenous cytokinin level drops during leafsenescence and exogenous application or en-dogenous enhancement of cytokinin contentusing the senescence-specific SAG12 pro-moter delays senescence (16, 42, 51). Con-sistent with the physiological finding thatthe cytokinin level decreases during leafsenescence, genomic-scale molecular analy-sis revealed that genes involved in cytokininsynthesis, a cytokinin synthase and adeno-sine phosphate isopentenyl-transferase (IPT)

genes, are downregulated and a gene for cy-tokinin degradation, cytokinin oxidase, is up-regulated in senescing leaves (8).

How cytokinins affect leaf senescence isstill unknown despite of the dramatic effect ofcytokinin in delaying leaf senescence. A recentdiscovery showed that Arabidopsis HistidineKinase 3 (AHK3), one of the three cytokininreceptors in Arabidopsis, plays a major role incontrolling cytokinin-mediated leaf longevity(35). This conclusion was obtained throughcharacterization of the gain-of-functionArabidopsis mutant, ore12-1, which showsdelayed leaf senescence due to a missense mu-tation in the AHK3 gene. A loss-of-functionmutation of AHK3, but not of the othercytokinin receptors, conferred a reducedsensitivity to cytokinin in cytokinin-mediateddelay of leaf senescence. This report alsoshowed that the phosphorylation of theArabidopsis response regulator 2 (ARR2) me-diated by AHK3 is essential for controllingleaf longevity (Figure 3). The exact mech-anism by which the phosphorylated ARR2leads to induction or repression of genesregulating and/or executing leaf senescenceneeds further investigation.

An interesting link between the antise-nescence effect of cytokinins and primarymetabolism was suggested, based on the find-ing that cytokinin-mediated delay of senes-cence is correlated with the activity ofextracellular invertase, the enzyme function-ally linked in the apoplastic phloem unload-ing pathway (38). When the extracellularinvertase activity was inhibited, cytokinin-mediated delay of leaf senescence was also in-hibited. The result showed that extracellularinvertase plays a role in mediating cytokininaction in delaying leaf senescence, suggestingthat carbohydrate partitioning associated withinvertase activity may be related to cytokinin-mediated delay of leaf senescence. This ob-servation is particularly notable in that regu-lation of leaf senescence is related to changesin source-sink relationships of sugars and inthat a tight link among cytokinin action, pri-mary metabolism, and leaf senescence exists.


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Figure 3Hypothetical model for a function of ORE12/AHK3 in controlling cytokinin-mediated leaf longevity.Although the cytokinin signals may be perceived by the other cytokinin receptors in Arabidopsis, ARR2phosphorylation is specifically mediated by ORE12/AHK3. Thus, the phosphorelay of ORE12/AHK3 toARR2 is a signaling pathway specific to the control of cytokinin-mediated leaf longevity. Thephosphorylated ARR2 then induces downstream cytokinin-responsive genes and, directly or indirectly,leads to induction of a set of target genes responsible for delaying the leaf senescence program, resultingin increased leaf longevity.

Ethylene has long been known as a ma-jor hormone in hastening leaf senescence aswell as fruit ripening and flower senescence(1). Although it was apparent that ethylene isan important positive regulator of leaf senes-cence, the molecular genetic mechanism ofethylene action in leaf senescence is only nowbeing revealed. In many plant species, includ-ing Arabidopsis, the level of ethylene increasesduring leaf senescence. Accordingly, the ethy-lene biosynthetic genes encoding ACC syn-thase, ACC oxdiase, and nitrilase are upreg-

ulated in senescing leaves (72). Two of theArabidopsis mutants, ethylene-resistant 1 (etr1)and ethylene-insensitive 2 (ein2), that are defi-cient in ethylene perception and signal trans-duction, respectively, exhibited significantdelays in leaf senescence, revealing the impor-tance of the endogenous ethylene signalingpathway as a positive regulator in leaf senes-cence. A recent study also showed that En-hanced Disease Resistance 1 (EDR1) mightbe a negative regulator for ethylene-mediatedleaf senescence (64). However, transgenic


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Abscission: theshedding of leaves,flowers, or fruits,usually at a weak areatermed theabscission zone

Arabidopsis and tomato plants that constitu-tively overproduce ethylene do not exhibitearlier-onset leaf senescence, suggesting thatethylene alone is not sufficient to initiate leafsenescence. This is consistent with the pos-tulation that age-dependent factors are re-quired for ethylene-regulated leaf senescence.Furthermore, potential regulators involvedin integrating ethylene signaling into age-dependent pathways have been reported. Theonset of leaf death 1 (old1) mutant of Arabidopsisdisplays a phenotype with earlier-onset senes-cence in an age-dependent manner (33). Theearly-senescence phenotype was further ac-celerated by exposure to ethylene, showingthat the old1 mutation resulted in alternationof both of the age- and ethylene signaling-dependent leaf senescence. However, in theold1etr1 double mutant where ethylene per-ception was blocked by the mutation in theETR1 gene, age-dependent earlier-onset leafsenescence still occurred but was not furtheraccelerated by ethylene treatment. These ob-servations suggested that OLD1 negativelyregulates integration of ethylene signalinginto leaf senescence. Recent studies with sev-eral old mutants that exhibited an alteredsenescence response to ethylene treatmentfurther supported the notion that the effectof ethylene on leaf senescence depends onage-related changes through these OLD genes(32).

ABA is a key plant hormone mediatingplant responses to environmental stresses. Italso functions in plant development such asseed germination and plant growth. Further-more, it has been well known that exogenousapplication of ABA promotes leaf abscissionand senescence (81). However, the role ofABA in leaf senescence has not been clearlydefined aside from some circumstantial evi-dence. The ABA level increases in senescingleaves and exogenously applied ABA inducesexpression of several SAGs (73), which is con-sistent with the effect on leaf senescence. En-vironmental stresses such as drought, high saltcondition, and low temperature positively af-fect leaf senescence, and under these stress

conditions ABA content increases in leaves.Concurrently with the increased ABA levelin senescing leaves (18), the genes encodingthe key enzyme in ABA biosynthesis, 9-cis-epoxycarotenoid dioxygenase (NECD), andtwo aldehyde oxidase genes AAO1 and AAO3show increased expression (8, 72). The ABA-inducible receptor-like kinase gene of Ara-bidopsis, RPK1, was found to be gradually up-regulated during leaf senescence ( J.C. Koo &H.G. Nam, unpublished data). Inducible ex-pression of RPK1 hastened the onset of leafsenescence, supporting a role for ABA in leafsenescence. A recent report argued that ABAinduces accumulation of H2O2 in senescingrice leaf, which in turn accelerates leaf senes-cence (30). Another possibility is that senes-cence accelerated by exogenous ABA treat-ment might cause increased H2O2 generation,since it is well known that there is an increaseof reactive oxygen species during leaf senes-cence. ABA also induces expression of an-tioxidant genes and enhances the activities ofantioxidative enzymes such as superoxide dis-mutase (SOD), ascorbate peroxidase (APOD),and catalase (CAT) (29). These activities mayplay at least a partial role in protecting the cel-lular functions required for progression andcompletion of senescence. It appears that ABAcontrols activities of both the cellular protec-tion activities and senescence activities. Thebalance between these two activities seemsto be important in controlling progression ofleaf senescence and may be adjusted by othersenescence-affecting factors such as age. Acrucial link between ABA and leaf senescencehas yet to be discovered via genetic analysis.

Methyl jasmonate (MeJA) and its precur-sor JA promote senescence in detached oat(Avena sativa) leaves (69). Exogenously ap-plied MeJA to detached Arabidopsis leavesleads to a rapid loss of chlorophyll contentand photochemical efficiency of photosystemII (PSII) and increased expression of SAGssuch as SEN4, SEN5, and γ VPE. A moreconvincing support for the role of JA in leafsenescence comes from the observation thatJA-dependent senescence is defective in the


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JA-insensitive mutant coronatine insensitive 1(coi1), implying that the JA signaling path-way is required for JA to promote leaf senes-cence (23). Functional studies on a nuclear-localized CCCH-type zinc finger protein,OsDOS (Oryza sativa Delay of the Onsetof Senescence), also supports involvement ofMeJA in leaf senescence (37). The expressionof the OsDOS gene was downregulated dur-ing leaf senescence. Notably, RNAi knock-down of OsDOS accelerated age-dependentleaf senescence, whereas its overexpression re-sulted in a marked delay of leaf senescence,showing that OsDOS acts as a negative regu-lator for leaf senescence. A genome-wide ex-pression analysis revealed that many of the JAsignaling-dependent genes in particular wereupregulated in the RNAi transgenic lines butdownregulated in the overexpressing trans-genic lines. This implies that OsDOS acts asa negative regulator of leaf senescence in in-tegrating the JA signaling pathway into age-dependent senescence.

SA is the hormone involved in pathogenresponse and pathogen-mediated cell death.A recent intriguing discovery in leaf senes-cence was the role of SA in age-dependentleaf senescence. The concentration of en-dogenous SA is four times higher in senescingleaves of Arabidopsis. The higher SA level insenescing leaves appears to be involved in up-regulation of several SAGs during leaf senes-cence (45): expression of a number of SAGssuch as PR1a, chitinase, and SAG12 is consid-erably reduced or undetectable in Arabidopsisplants defective in the SA signaling or biosyn-thetic pathway (npr1 and pad4 mutants, andNahG transgenic plants). A surprising discov-ery was derived from transcriptome analysis:The change of transcriptome mediated by theSA pathway is highly similar to that medi-ated by age-dependent senescence. The factthat the SA pathway is specifically involved inage-dependent leaf senescence is further sup-ported by the finding that age-dependent butnot dark-induced leaf senescence is delayedin NahG overexpressing transgenic plants thatproduce dramatically reduced SA levels.

NahG: agene-encodingbacterial salicylatehydroxylase thatdestroys SA byconverting it tocatechol

There is evidence indicating that SAmight be involved in senescence-associatedcell death. Leaves from Arabidopsis pad4 mu-tants that are defective in the SA signal-ing pathway do not appear to undergo celldeath as efficiently as the wild type (45).In this mutant, leaves often remain yellowduring the senescence stage with a much-delayed cell death (57, 58). This result showsa clear involvement of the SA pathway insenescence-associated cell death. A hyperse-nescence mutant hys1, which showed an early-senescence phenotype, was found to be allelicto cpr5, which was isolated based on its con-stitutive expression of defense responses andspontaneous cell death. The enhanced levelsof SA and defense-related gene expressionsmight cause precocious senescence, support-ing a role of SA pathways in the senescence-associated cell death process.

The role of auxin in leaf senescence hasbeen elusive, particularly due to its involve-ment in various aspects of plant develop-ment. However, evidence suggests that auxinis also involved in the senescence process (61).The auxin level increases during leaf senes-cence. Consequently, IAA biosynthetic genesencoding tryptophan synthase (TSA1), IAAldoxidase (AO1), and nitrilases (NIT1-3) areupregulated during age-dependent leaf senes-cence (72). Exogenous application of auxinrepresses transcription of some SAGs (27,47). Together, this implies that the auxinlevel increases during leaf senescence dueto increased expression of auxin biosyntheticgenes, which leads to delayed leaf senescence,leaving auxin as a negatively acting factor ofleaf senescence. It has also been suggested thatchanges in auxin gradients rather than the en-dogenous auxin level itself could be importantin modulating the senescence process (2). Ex-pression of more than half of the genes relatedto auxin transport is reduced during senes-cence (72). This may cause aberrant distribu-tion of auxin following leaf senescence.

Studies on the genetic mutation altered inauxin signaling support the involvement ofauxin in controlling leaf senescence (14, 50).


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AUXIN RESPONSE FACTOR 2 (ARF2) isone of the transcription repressors in the auxinsignaling pathway. Microarray analysis showsthat expression of the ARF2 gene is inducedin senescing leaves. Disruption of ARF2 byT-DNA insertion causes delay in leaf senes-cence. The phenotype canonically puts ARF2as a positive regulator of leaf senescence. Wealso isolated another allele of arf2 from anethylmethane sulfonate (EMS)-mutagenizedpool, which showed delayed leaf senescencealong with an increased sensitivity to the ex-ogenous auxin in hypocotyls growth inhibi-tion. Together, these imply that the reducedARF2 function in the mutant can cause re-duced repression of auxin signaling with in-creased auxin sensitivity, leading to delayedsenescence. However, it has yet to be seenwhether the effect of auxin pathways is di-rectly involved in leaf senescence or whetherit indirectly influences leaf senescence be-cause auxin and the arf2 mutants also causea pleiotropic effect in plant development.

Other Regulatory Genesof Senescence

Besides the regulatory genes mentionedabove, several other regulatory genes of leafsenescence have been identified through ge-netic screening of senescence mutants andthrough functional identification of someSAGs.

Ubiquitin-dependent proteolysis is likelyinvolved in regulation of leaf senescence. TheORE9 gene encodes an F-box protein, a com-ponent of the SCF complex, which acts asan E3 ligase in ubiquitin-dependent prote-olysis. Leaf senescence was delayed in theore9 mutant (74). It was also known thatproteolysis by the N-end rule pathway hasa function in senescence progression. Thedelayed-leaf-senescence 1 (dls1) mutant, which isdefective in arginyl tRNA:protein transferase(R-transferase), showed delayed develop-ment of leaf senescence symptoms (79).R-transferase is a component of the N-endrule proteolytic pathway.

A few regulatory genes identified inour laboratory by genetic screening includeORE7, ORE1, and SOR12. ORE7 is an AT-hook transcription factor that may be in-volved in controlling chromatin architecture.ORE1 is NO APICAL MERISTEM (NAM),ATAF1, and CUP-SHAPED COTYLE-DONS2 (CUC2) (NAC) family transcriptionfactor. SOR12 suppresses the delayed senes-cence phenotype of ORE12/AHK3. It alsoappears that miRNA is involved in control-ling leaf senescence. Functional characteriza-tion of these genes and further genetic iso-lation of the senescence regulatory elementsshould be a critical asset in understanding leafsenescence.

A large number of SAGs have been identi-fied in various plants through microarray anal-ysis. Some of them have been found to encodepotential regulatory factors that are compo-nents of signal perception and transductions,such as transcription factors and receptor-likekinases. Characterization of these potentialregulatory genes led to discovery of a few im-portant senescence regulatory genes and pro-vided some insight into the regulatory mech-anism of leaf senescence.

Genes for 96 transcription factors wereidentified in Arabidopsis to be upregulated atleast threefold in senescing leaves. These be-long to 20 different transcription factor fam-ilies, the largest groups being NAC, WRKY,C2H2-type zinc finger, AP2/EREBP, andMYB proteins. Among the WRKY transcrip-tion factors, AtWRKY53 and WRKY6 havebeen further characterized in relation to leafsenescence. WRKY53 is upregulated at a veryearly stage of leaf senescence but decreasesagain at later stages, implying that WRKY53might play a regulatory role in the early eventsof leaf senescence (26). Putative target genesof WRKY53 include various SAGs, PR genes,stress-related genes, and transcription factorsincluding other WRKY factors. A knockoutline of the WRKY53 gene showed delayedleaf senescence, whereas inducible overex-pression caused precocious senescence, show-ing that it functions as a positive element in


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leaf senescence (43). Identification of directtarget genes of WRKY53 should further re-veal the WRKY53-mediated senescence reg-ulatory pathways. Another WRKY transcrip-tion factor gene, WRKY6, shows high-levelupregulation during leaf senescence as wellas during pathogen infection (60). WRKY6regulates a set of genes through the W-boxsequences in their promoter. Many WRKY6-regulated genes are associated with senes-cence and pathogen response, including thesenescence-induced receptor-like kinase gene(SIRK). Although WRKY6 appears to have afunctional role both in pathogen defense aswell as senescence, the SIRK gene appearedto be expressed only during senescence butnot during pathogen infection. The wrky6knockout mutation alters expression of SAGsbut does not have any apparent effect on leafsenescence. The altered expression of SAGs inthe knockout mutation may not be enough tobe manifested into the apparent change of leafsenescence. It is also likely that functional re-dundancy exists among the WRKY transcrip-tion factors, considering the large number ofmembers in the family.

NAC proteins are one of the largest fami-lies of plant-specific transcription factors withmore than 100 members in Arabidopsis. NACfamily genes play a role in embryo and shootmeristem development, lateral root forma-tion, auxin signaling, and defense response. Atotal of 20 genes encoding the NAC transcrip-tion factor, representing almost one fifth ofthe NAC family members, showed enhancedexpression during natural senescence and indark-induced senescence (20). The T-DNAknockout mutant of AtNAP, a gene encodingan NAC family transcription factor, showedsignificantly delayed leaf senescence. Thus,AtNAP functions as a positive element in leafsenescence. AtNAP orthologs exist in kidneybean and rice and are also upregulated duringleaf senescence. We also isolated a delayed leafsenescence mutant, which is due to a nonsensemutation in one of the NAC transcription fac-tors ( J.H. Kim & H.G. Nam, unpublisheddata). It is likely that several other senescence-

Autophagy: aregulated recyclingprocess wherebycytosol andorganelles areencapsulated invesicles, which arethen engulfed anddigested by lyticvacuoles/lysosomes

upregulated NAC transcription factors play aregulatory role in leaf senescence. Transcrip-tional autoregulation and inter-regulation, aswell as homodimerization and heterodimer-ization, among the NAC family members areimportant mechanisms in regulating NACtranscription factor-mediated developmentalprocesses. Similar mechanisms are expectedto be involved in the NAC transcriptionfactor-mediated regulatory network of leafsenescence. The potential functions of mostleaf senescence-associated transcription fac-tors remain to be elucidated. Functional char-acterization of these genes including the sig-naling pathways they are involved in and thetarget genes they regulate will be invaluable inunderstanding the complex molecular path-ways regulating leaf senescence.

Another example of SAGs with which invivo function was assayed is the autophagygenes. Autophagy is an intracellular processfor vacuolar bulk degradation of cytoplas-mic components and is required for nutrientcycling. Mutants carrying a T-DNA inser-tion within the Arabidopsis autophagy genes,AtAPG7, AtAPG9, and AtAPG18a, exhibitedpremature leaf senescence (13, 22, 77). Inthese mutants, nutrients may be less efficientlyutilized during execution of senescence, orsome of the components needed for pro-gression of senescence may not be efficientlyprovided.

A few of the genes involved in lipidmetabolism have a role in leaf senescence.Reduced expression of the Arabidopsis acylhydrolase gene by antisense RNA interfer-ence in transgenic plants delayed the onsetof leaf senescence, whereas chemically in-duced overexpression of the gene caused pre-cocious senescence (20). In addition, trans-genic plants with reduced expression of asenescence-induced lipase also showed de-layed leaf senescence (67). It is likely that thedelayed senescence in these transgenic lineswith reduced lipase expression is due to pro-longed maintenance of membrane integrity,indicating the importance of membrane in-tegrity during senescence.


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CONCLUSIONS AND FUTURECHALLENGES

With the aid of microarray, we now knowthat more than 800 genes are distinctivelyupregulated during senescence, which illus-trates the dramatic alteration in cellular phys-iology that underlies leaf senescence. Withthe knowledge of the nature of these SAGs,we can now figure out the molecular land-scape of leaf senescence. We need to seethe dynamic changes of the transcriptomealong more detailed windows of leaf senes-cence stages, which will enable identifica-tion of more SAGs. This will also allow usto understand the dynamic changes of thephysiology undergoing senescence. The mi-croarray data could be further examined usingvarious bioinformatic tools for classifying theSAGs, for establishing a hierarchical relation-ship among the SAGs, and for systems-levelanalysis of molecular events underlying senes-cence. The senescence pathways affected byvarious signals are being revealed. Further mi-croarray analyses of leaf senescence in var-ious senescence mutants and under varioussenescence-affecting conditions should reveala detailed molecular level of the senescencepathways. One important challenge will beto investigate how the SAGs are coordinatelyregulated during leaf senescence. DNA mi-croarray and chromatin immunoprecipitationapproaches could be helpful to answering thisquestion.

Although isolating a few key regulatorygenes of leaf senescence greatly aided the un-derstanding of leaf senescence, there are manymore regulatory elements of leaf senescence.Finding the senescence regulatory genes hasbeen and will continue to be one of the mainchallenges. Some regulatory elements couldbe found fairy easily by functionally charac-terizing the potential regulatory SAGs. How-ever, it should be noted that there are manyother senescence regulatory genes that donot belong to SAGs. The in vivo functionof the SAGs can now be easily assayed us-ing the genomic tools available in Arabidop-

sis, including the large collection of T-DNAinsertion lines or the Targeting-InducedLocal Lesions in Genomes (TILLING)approach.

It is encouraging that senescence is nowwell assayed in the realm of genetics. Thegenetic screening of senescence mutants wasfruitful in understanding the genetic regula-tory mode and in isolating senescence regula-tory genes. However, considering the com-plex nature of senescence, current geneticscreening is far from saturated. It will be im-portant to use various mutant pools to iden-tify novel senescence regulatory elements.Chemically mutagenized pools in particularare valuable because they might provide novelalleles that cannot be obtained by T-DNAmutagenesis, as illustrated by the discovery ofORE12/AHK3. Global gene expression anal-ysis of the senescence mutants could provideimportant clues for dissecting the regulatorypathways. Identifying suppressors to knownmutants will be also useful to dissect geneticmechanisms governing senescence processes.More genetic mutants can certainly be iso-lated by designing a more elegant screeningscheme, for example, for mutations defectivein integrating environmental effects into asenescence program.

Leaf senescence occurs at the last step ofleaf development. Accordingly, some genesthat function in senescence could also beinvolved in other biological processes. Themutations in this type of gene may show dif-ficulties in assaying their function in senes-cence because their effects on senescence canbe masked by other early-mutant phenotypes.Through senescence-specific gene silencingor senescence-specific induction, using asenescence-specific promoter or chemicallyinducible promoters will partially circumventthe problem.

Although most of the molecular anal-yses on leaf senescence were based onmRNA expression, it should be noted thatmRNA expression is only one aspect offunctional gene regulation. Other regulatorymechanisms such as protein-level expression,


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protein stability, or localization of regula-tory proteins involved in senescence processshould certainly be involved. An integrated in-formational analysis involving proteomic andmetabolomic analyses during leaf senescencewill eventually be needed to better understandleaf senescence.

One serious pitfall in the current assay forleaf senescence is that senescence symptomsare measured at the organ level. However,within a senescing leaf, individual cells areusually at different stages of developmentalage or senescence. It is also unlikely that allthe cells within an individual leaf undergo co-herent cell death. To better understand thesenescence process, it will be necessary todevelop assays that can monitor senescencesymptoms and senescence-associated celldeath symptoms at the individual cellularlevel.

Leaf senescence is certainly an evolution-arily acquired process and thus the plantsevolved in different ecological settings withdifferent evolutionary tracks will show differ-ences in the pattern and regulation of senes-cence. It would be interesting to do a compar-ative study utilizing the information obtainedfrom Arabidopsis. This may even be pursued invarious ecotypes of Arabidopsis.

Another important challenge in the areaof leaf senescence is determining its biotech-nological applications. Although manipula-tion of leaf senescence can greatly improvecrop yield and other characteristics such asincreased shelf life, the knowledge and mate-rials obtained so far have been poorly utilizedfor this purpose. Considering the potential fu-ture food shortage and the use of plants as asource of bioenergy, improving crop produc-tivity should be a top priority.

SUMMARY POINTS

1. Leaf senescence is a finely regulated and complex process that incorporates multipledevelopmental and environmental signals. Microarray analysis revealed the complexmolecular network of the senescence pathways.

2. Leaf senescence involves age-dependent PCD. Senescence-associated cell death andother PCDs show common as well as distinctive signaling pathways.

3. The genetic scheme was established in screening leaf senescence mutants. Geneticanalysis revealed that leaf senescence is controlled by various negative and positivegenetic elements.

4. More than 800 genes were identified as SAGs, reflecting the dramatic alteration incellular physiology that underlies the leaf senescence. Potential regulatory elementsamong the SAGs were characterized for their function in leaf senescence. The tran-scription factors WRKY53 and AtNAP act as positive regulators of leaf senescence.

5. Metabolic rate appears to be one mechanism involved in age-dependent leafsenescence.

6. A key molecule for cytokinin-mediated leaf longevity was identified as AHK3, one ofthe cytokinin receptors. ARR2 phosphorylation mediated by AHK3 is essential forcontrolling leaf longevity.

7. Signaling pathways of various phytohormones including ABA, SA, JA, and ethyleneare intimately linked to leaf senescence. Interestingly, SA-mediated senescence path-way is highly similar to that of natural leaf senescence, as revealed by microarrayanalysis.


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8. Ubiquitin-dependent proteolysis is likely involved in controlling leaf senescence.Other senescence-regulatory factors include acyl hydrolase, invertase, and autophagy,which suggest involvement of membrane integrity, apoplasitc sugar levels, and nutri-ent recycling, respectively.

ACKNOWLEDGMENTS

We apologize to all our colleagues whose work could not be properly reviewed here becauseof space limitation. The work by H.G.N. was supported in part by MOST (KOSEF) throughthe National Core Research Center for Systems Bio-Dynamics (R15-2004-033-05002-0) andin part by the Crop Functional Genomics Research Program (CG1312). The work by P.O.L.was supported by the Korea Research Foundation Grant funded by the Korea Government(MOEHRD, Basic Research Promotion Fund, KRF-2005–261-C00075).

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Annual Review ofPlant Biology

Volume 58, 2007Contents

FrontispieceDiter von Wettstein � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �xii

From Analysis of Mutants to Genetic EngineeringDiter von Wettstein � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �1

Phototropin Blue-Light ReceptorsJohn M. Christie � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 21

Nutrient Sensing and Signaling: NPKSDaniel P. Schachtman and Ryoung Shin � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 47

Hydrogenases and Hydrogen Photoproduction in OxygenicPhotosynthetic OrganismsMaria L. Ghirardi, Matthew C. Posewitz, Pin-Ching Maness, Alexandra Dubini,

Jianping Yu, and Michael Seibert � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 71

Hidden Branches: Developments in Root System ArchitectureKaren S. Osmont, Richard Sibout, and Christian S. Hardtke � � � � � � � � � � � � � � � � � � � � � � � � � � 93

Leaf SenescencePyung Ok Lim, Hyo Jung Kim, and Hong Gil Nam � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �115

The Biology of Arabinogalactan ProteinsGeorg J. Seifert and Keith Roberts � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �137

Stomatal DevelopmentDominique C. Bergmann and Fred D. Sack � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �163

Gibberellin Receptor and Its Role in Gibberellin Signaling in PlantsMiyako Ueguchi-Tanaka, Masatoshi Nakajima, Ashikari Motoyuki,

and Makoto Matsuoka � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �183

Cyclic Electron Transport Around Photosystem I: Genetic ApproachesToshiharu Shikanai � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �199

Light Regulation of Stomatal MovementKen-ichiro Shimazaki, Michio Doi, Sarah M. Assmann,

and Toshinori Kinoshita � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �219

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The Plant Heterotrimeric G-Protein ComplexBrenda R.S. Temple and Alan M. Jones � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �249

Alternative Splicing of Pre-Messenger RNAs in Plants in theGenomic EraAnireddy S.N. Reddy � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �267

The Production of Unusual Fatty Acids in Transgenic PlantsJohnathan A. Napier � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �295

Tetrapyrrole Biosynthesis in Higher PlantsRyouichi Tanaka and Ayumi Tanaka � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �321

Plant ATP-Binding Cassette TransportersPhilip A. Rea � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �347

Genetic and Epigenetic Mechanisms for Gene Expression andPhenotypic Variation in Plant PolyploidsZ. Jeffrey Chen � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �377

Tracheary Element DifferentiationSimon Turner, Patrick Gallois, and David Brown � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �407

Populus: A Model System for Plant BiologyStefan Jansson and Carl J. Douglas � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �435

Oxidative Modifications to Cellular Components in PlantsIan M. Møller, Poul Erik Jensen, and Andreas Hansson � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �459

Indexes

Cumulative Index of Contributing Authors, Volumes 48–58 � � � � � � � � � � � � � � � � � � � � � � � �483

Cumulative Index of Chapter Titles, Volumes 48–58 � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �488

Errata

An online log of corrections to Annual Review of Plant Biology chapters(if any, 1997 to the present) may be found at http://plant.annualreviews.org/

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Leaf Senescence Pyung Ok Lim (2007)

Documents

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