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Relationship between plant stress tolerance, senescence and life span

Michal Sharabi-Schwager,a Amnon Lers,a Alon Samachb and Ron Porata,* aDepartment of Postharvest Science of Fresh Produce, ARO, The Volcani Center, Bet Dagan, Israel bThe Robert H Smith Institute of Plant Sciences and Genetics in Agriculture, Faculty of Agricultural, Food and Environmental Quality Sciences, The Hebrew University of Jerusalem, Rehovot, Israel Abstract Purpose of review: In many aerobic organisms, including fungi, yeasts, nematodes, fruit flies, mice and humans, it was found that increased resistance to stresses, especially oxidative stress, is correlated with extended longevity, which leads to the development of the “stress resistance” theory of aging. Nevertheless, very little is yet known regarding the accuracy of this theory in plants. Here we re-view recently accumulated evidence supporting the existence of tight correlation between stress tolerance and onset of senescence and determination of life span in plants, which supports the applicability of this theory to plants. Findings: Certain lines of evidence reveal the correlation between plant stress tolerance and regulation of senescence and life span. Firstly, it was found that the Arabidopsis delayed leaf senescence mutants ore1, ore3 and ore9 and the long-lived mutant gigantea ex-hibit enhanced tolerance to oxidative stresses. Secondly, transgenic cotton plants overexpressing the GF14λ regulator gene and Arabi-dopsis plants overexpressing the CBF2 transcriptional activator gene are more tolerant to drought and freeze stresses, respectively, and also show delayed leaf senescence phenotypes and enhanced life spans. Thirdly, Arabidopsis mutants deficient in vitamin C (vtc1) or vitamin E (vte2) are sensitive to oxidative stress, and exhibit premature senescence and reduced seed longevity, respectively. Together, these findings suggest a tight link between stress resistance and longevity in plants, similar to what has been hypothesised in animals. Direction for future research: Confirmation of the correlation between plant stress tolerance and regulation of senescence and life span opens the possibility of using this knowledge in future research and in breeding programs in order to develop new horticultural cultivars with enhanced tolerance to environmental stresses that will most likely include phenotypes with extended longevity and de-layed senescence. Such cultivars will obviously have much improved postharvest storage lives and will suffer less from damage caused by accelerated senescence. Keywords: aging; life span; oxidative stress; senescence; stress tolerance

Abbreviations

*Correspondence to: Dr Ron Porat, Dept. of Postharvest Science, ARO, The Volcani Center, PO Box 6, Bet Dagan 50250, Israel, Tel: +972 3 9683617; Fax: +972 3 9683622; email: rporat@volcani.agri.gov.il Stewart Postharvest Review 2009, 2:4 Published online 01 February 2009 doi: 10.2212/spr.2009.2.4

APX Ascorbate Peroxidase CAT Catalase

ROS Reactive Oxygen Species

SOD Superoxide Dismutase

POX Peroxidase

SAG Senescence-associated Gene

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The “stress resistance” theory of aging In the 1950s Denham Harman suggested that reactive oxygen species (ROS) play an essential role in governing the aging process of aerobic organisms. This suggestion led to the “free radical” theory of aging [1]. Later Sohal and Weindruch [2] and Martin et al. [3*] revised and updated the “free radical” theory of aging and offered the “oxidative stress” theory of aging instead. This modification is based on the existence of a chronic state of oxidative stress in cells of aerobic organ-isms, even under normal physiological conditions, because of an imbalance between production of peroxidants and antioxi-dants. This imbalance leads to accumulation of oxidative damage in a variety of macromolecules. While the rate of accumulation of oxidative damage is steady at first, it accel-erates during aging, resulting in a progressive loss in the functional efficiency of various cellular processes [4]. More recently it was noted that the ability of aerobic organisms to cope with stresses can be used as a predictor of life expec-tancy, which led to the “stress resistance” theory of aging. This theory hypothesises that increased resistance to intrinsic and extrinsic stresses leads to a prolonged life span [5, 6*–8]. The “oxidative stress” and “stress resistance” theories of ag-ing are fully consistent with the well known “calorie restric-tion” theory of aging, since reduction of metabolic activity results in less oxidative damage [2]. The truthfulness of the “oxidative stress” and “stress resistance” theories of aging was demonstrated in various aerobic organisms including yeasts, fungi, nematodes, fruit flies, mice and humans [3, 6*, 9]. Nevertheless, although extensive research has been con-ducted in various aerobic organisms, very little is yet known regarding the applicability of the “stress resistance” theory of aging to the plant kingdom. The “oxidative stress” and “stress resistance” theories of ag-ing in animals relate most particularly to the generation of ROS in mitochondria as a normal by-product of aerobic res-piration that causes oxidative stress conditions [6*]. For ex-ample, a typical human cell metabolises about 1012 molecules of oxygen per day and generates some 3 × 109 molecules of hydrogen peroxide (H2O2) per hour [3*]. In addition to gen-eration of ROS in mitochondria during the oxidative phos-phorylation chain, plants also produce large amounts of ROS in the chloroplasts during photosynthesis and the CO2 fixa-tion process [10**–12]. Furthermore, plants are immobile and fixed in the soil and, therefore, are consistently exposed to environmental stresses such as unfavourable temperatures (heating, chilling and freezing), drought, salinity, flooding, excessive or insufficient irradiation, UV light, ozone, heavy metals, etc. Exposure to such stresses results in massive gen-eration of ROS and interferes with the delicate balance of cellular redox homeostasis [13]. On the whole, their status as photosynthetic organisms and their routine exposure to stresses make plants vulnerable to oxidative stresses. Aging and life span in plants Aging in animals is defined as the progressive loss of func-tion, accompanied by decreasing fertility and increasing mor-

tality with advancing age [14]. In higher plants, aging is most obviously manifested in the senescence of leaves – an indis-pensable process developed to maximise the re-utilisation of nutrients that have been accumulated in senescing leaves that can no longer contribute to the plant [15]. Furthermore, it has been suggested that leaf senescence can be reconciled with other evolutionary theories of the origin of aging in animals [16]. Senescence in plants is an age-dependent deterioration proc-ess that occurs at the cell, tissue, organ or organism level, and leads to death or the end of the life span [17]. Leaf senes-cence is particularly associated with efficient recycling of nutrients that are translocated from senescencing cells to de-veloping parts of the plant; it is a highly regulated and or-dered process that involves cessation of photosynthesis, dis-integration of chloroplasts, breakdown of leaf proteins, loss of chlorophyll and removal of amino acids, and thereby en-ables the rest of the plant (ie, the younger leaves, fruits or flowers) to benefit from the nutrients accumulated during the life span of the leaf [18, 19*]. While leaf senescence relates to a particular organ, whole plant longevity is determined by the complete loss of function and viability of all tissues and organs within the entire plant [17]. Leaf and whole-plant se-nescence are most dramatic in monocarpic plants, which re-produce only once and die at the end of the reproduction stage [20]. Leaf and whole plant senescence occur in an age-dependent manner, but are also governed by complex interactions be-tween various internal and external signals. The internal fac-tors that induce senescence are the age of the leaves and the developmental stage of the plant, including changes in en-dogenous levels of the plant hormones that affect senescence, such as ethylene and cytokinin [19*]. The external factors that affect leaf and plant senescence include exposure to en-vironmental stresses, pathogen infection and shading [19*]. In addition, various studies have indicated that oxidative stress and generation of ROS play a major role in triggering the senescence syndrome [10**, 21]. Effects of environmental stresses on leaf and plant senescence Leaf senescence is accelerated by exposure to environmental stresses that have negative consequences for plant growth and development; they include extreme light or temperatures, radiation, drought, nutrient deficiency, pathogen infection, flooding, and the presence of toxic materials in the air, water or soil [22*]. In fact, exposure to stresses is estimated to be the primary cause of crop loss worldwide, because of imma-ture senescence, which has the potential to reduce the aver-age yield of main crops by more than 50% [23]. Indeed, tran-script profiling studies revealed the occurrence of consider-able overlap in genes responding to both stress responses and leaf senescence [19*]. For example, among 43 transcription factor genes that were found to be induced during senes-cence, 28 were also induced by exposure to various stresses

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[24]. One example is the Senescence-Associated Gene 1 (SAG1), from Arabidopsis that is commonly regulated by both initiation of leaf senescence and exposure to various stresses [25]. Acceleration of leaf senescence is not just a consequence of exposure to stresses, but rather it is a key defence mechanism that contributes to plant survival in the face of unfavourable environmental stress conditions [22*, 26]. In this context, Munne-Bosch and Alegre [26] suggested that acceleration of leaf senescence may contribute to plant survival under drought stress conditions by allowing nutrient remobilisation from senescing leaves to reproductive parts of the plant, thus enabling completion of the life cycle even under stressful conditions. Furthermore, leaf senescence or abscission under drought stress serves the whole plant by minimising water loss through transpiration. A common biochemical process, which most probably pro-vides an important direct link between exposure to various abiotic and biotic stresses and acceleration of leaf senes-cence, is the accumulation of ROS [13, 27*, 28]. ROS are actively produced in plant cells during programmed cell death, and also in response to abiotic stresses and pathogen infection, and they serve as key signal molecules that activate plant defence and senescence processes [11, 12, 21]. Exces-sive formation of ROS, causing so-called “oxidative stress”, leads to induced expression of many senescence-enhanced genes [23], and consequent acceleration of leaf and plant senescence [10**, 21, 29]. Involvement of oxidative stress in regulation of leaf senescence Oxidative stress (manifested in cellular accumulation of ROS) plays two different important roles during leaf senes-cence: in the early stages accumulated ROS serve as impor-tant signalling molecules, and in later stages they are in-volved in molecule degradation. In Arabidopsis, it has been shown that parallel decreases in cytosolic ASCORBATE PER-OXIDASE 1 (APX1) and CATALASE 2 (CAT2) genes expres-sion during bolting are involved in creation of an H2O2 peak that is responsible for triggering the expression of senes-cence-related transcription factors, such as WRKY53, and induction of senescence [30, 31]. At later stages, during the progression of leaf senescence, there is a gradual decline in the activity of various antioxidant enzymes, including CAT, APX and superoxide dismutase (SOD) [10**, 29]. In maize leaves, the H2O2 content and lipid peroxidation increased from the young leaf stage till the senescent leaf stage, and consequent decreases in SOD, APX, peroxidase (POX) and CAT enzyme activities were observed [32]. Furthermore, it was shown that senescence of an early-senescing cultivar, X 3342, was associated with enhanced oxidative stress and rapid decline of antioxidant enzyme activities during the ap-proach to maturity, whereas a late-senescing cultivar, Deccan 103, maintained lower H2O2 content and enhanced activities of SOD (mainly a particular Mn-SOD isoform), APX and

CAT [32]. Similarly, it was shown in tobacco plants that older leaves had lower levels of the antioxidants, vitamin C and glutathione, and persistently lower activities of the anti-oxidative enzymes CAT, Cu/Zn-SOD and APX. These changes lead to lower photo-oxidative-stress tolerance and consequent acceleration of leaf senescence [33]. Taken to-gether, these findings and many others demonstrate that, similarly to what has been found in animal systems, oxidative processes and excessive formation of ROS are important components of leaf and whole-plant senescence syndromes [10**, 21]. Prolonged life-span mutants are more tolerant to oxidative stresses Oxidative stress resistance and potential life span seem to be correlated in many aerobic organisms, ranging from yeasts to mammals [3*, 5, 6*, 14, 15, 34–36]. In this paper we present experimental evidence that plants, too, exhibit a tight correla-tion between oxidative stress tolerance and regulation of lon-gevity and life span. In Arabidopsis, it has been reported that the late-flowering mutant gigantea which has extended longevity is also more tolerant to oxidative stresses than the wild type, as indicated by its increased resistance to hydrogen peroxide and to the superoxide radical-generating herbicide paraquat [37**]. Furthermore, among 11 different late-flowering mutants tested, the gigantea (gi-3) mutant, which showed the longest delay in flowering and had the longest life span, was also the most tolerant to oxidative stresses. The Arabidopsis ore1, ore3 and ore9 (oresara means “long living” in Korean language) mutants exhibit extended leaf longevity. These long-living mutants are also more tolerant to various types of oxidative stresses, as indicated by the in-creased tolerance of both detached leaves and whole plants to various oxidative stress-inducing agents, such as hydrogen peroxide, salicylhydroxamic acid (SHAM), N,N,-diethyldithio carbamic acid (DDC)and methyl viologen (MV) [38**]. Furthermore, the degree of tolerance to oxidative stress was closely proportional to the degree of extension of leaf longevity exhibited by each mutant [38**]. Nevertheless, the activities of the antioxidant enzymes SOD, APX and CAT in these mutants were similar to or even slightly lower than those in wild type plants, therefore, their increased toler-ance to oxidative stress does not appear to be mediated by enhanced activity of these ROS-scavenging enzymes. Overall, these studies of the various long-lived Arabidopsis mutants provide genetic evidence that oxidative stress toler-ance in plants is linked to control of leaf longevity [37**, 38**]. Transgenic plants with enhanced resistance to environmental stresses have longer life-spans According to the “stress resistance” theory of aging, in-creased resistance to stress is correlated with extended leaf

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longevity and overall life span. Here we present research evidence that supports the applicability of this theory to plants, by evaluating leaf senescence and longevity traits in transgenic plants that exhibit increased resistance to environ-mental stresses. Transgenic cotton plants overexpressing the Arabidopsis GF14λ gene encoding the 14-3-3 conserved regulator protein exhibited improved water-stress tolerance and delayed leaf senescence, and a “stay-green” phenotype [39]. The GF14λ transgenic plants maintained enhanced photosynthesis rates under water-deficient conditions, and had a “stay-green” phe-notype: the first 4-6 oldest leaves in the transgenic plants turned yellow about 2 weeks later than similar leaves in con-trol non-transgenic plants [39]. In another study, Rivero et al. [40] introduced the ISOPEN-TENYLTRANSFERASE (IPT) gene, driven by a stress- and senescence-induced promoter, into transgenic tobacco plants. The IPT gene encodes an enzyme that catalyses the rate-limiting step in cytokinin biosynthesis, and its overex-pression results in inhibition of leaf senescence [41]. It has been established that suppression of drought-induced leaf senescence by overexpression of the IPT gene results in a conspicuous increase of drought tolerance that was mani-fested in vigorous growth after a long drought that killed the control plants [40]. Overall, the transgenic plants displayed minimal yield loss even when watered with only 30% of the amount of water used under control conditions [40]. Alto-gether, the findings of this study elucidate the tight relation-ship between enhanced stress (drought) tolerance and delay of leaf senescence.

In current research in our laboratory, we have found that overexpression of the C-repeat/dehydration-responsive ele-ment binding factor 2 (CBF2) transcriptional activator gene in Arabidopsis, which governs cold-regulated gene expres-sion and induction of frost tolerance in the plant [42, 43], also results in a remarkable delay of leaf senescence and exten-sion of the life-span of the plants (Figure 1). As shown in Figure 1, overexpression of the CBF2 gene has only minor effects on plant development, but delays leaf senescence re-markably. When grown at 20˚C, the rosette leaves of wild-type plants began to turn yellow 30 days after germination, while in the CBF2-overexpressing plants this process was delayed by about 3 weeks. Consequently, the total life span of the CBF2-overexpressing plants was approximately 20 to 24 days longer than that of the wild-type plants. Overall, de-tailed evaluation of leaf senescence and life span of the CBF2 overexpressing plants revealed a tight link between enhanced frost stress tolerance, and leaf senescence inhibition and life span extension. Vitamins C and E deficient mutants are sensi-tive to oxidative stress and undergo premature senescence Further support for the role of oxidative stress tolerance in governing longevity and the onset of senescence comes from studies of Arabidopsis mutants deficient in vitamins C and E. Vitamin C (L-ascorbic acid) and vitamin E (tocopherol) are both well known antioxidants, contributing to cellular detoxi-fication of ROS in hydrophilic and lipophilic fractions, re-spectively. It has been found that Arabidopsis vitamin c-1 (vtc1) plants (deficient in L-ascorbic acid because of a mutation in guanoside diphosphate (GDP)-mannose pyrophosphorylase, a key enzyme involved in the vitamin C biosynthetic pathway) exhibit elevated levels of various SAG transcripts as well as increased salicylic acid levels. Accordingly, it was concluded that low vitamin C levels in vtc1 mutants caused the plants to enter at least some stages of leaf senescence prematurely [44*, 45]. Furthermore, it was noted that dark-induced senes-cence occurred more rapidly in leaf discs taken from vtc1 plants than in those from wild-type plants [45]. Similar to what has been observed in the vtc1 mutants, it was also found that antisense inhibition of GDP-mannose pyrophosphorylase expression in transgenic potato plants resulted in reduced levels of vitamin C and acceleration of developmental senes-cence: after 3 months in soil the aerial parts of the transgenic plants completely dried out, whereas at that time wild-type plants had not started to senesce [46]. Finally, it has been reported that exogenous application of ascorbic acid prevents the effects of silver nitrate, a generator of ROS, on the induc-tion of expression of SAGs such as LSC54 and LSC94 [23]. Vitamin E is a quencher of singlet oxygen and it effectively scavenges various ROS and ROS by-products, including lipid peroxyl radicals. Mutants in two vitamin E biosynthesis loci (vte1 and vte2) in Arabidopsis exhibited tocopherol defi-

Figure 1. Phenotypes of wild type (WS ecotype) and CBF2-overexpressing Arabidopsis plants after 38 days of growth at 22ºC. The picture on the left (A) shows that overexpression of the CBF2 gene had only minor effects on the developmental stage of the plant but had a remarkable effect of delaying rosette leaf senescence. The picture on the right (B) is an enlargement of the rosette leaves. The wild-type plants are on the left side and the CBF2-overexpressing plants on the right side of each picture.

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ciency and significantly reduced seed longevity compared with the wild-type seeds [47]. Moreover, the vte1 and vte2 plants were also shown to be more sensitive to oxidative stress, suggesting that vitamin E is essential to prevent lipid peroxidation damage during seed storage and for protection of the young seedlings during germination and early develop-ment [47]. Conclusions The “stress resistance” theory of aging claims that increased resistance to internal and environmental stresses leads to pro-longed life span in eukaryotic organisms. In this paper, we reviewed observations supporting the existence of tight corre-lation between plant stress tolerance and the timing of onset of leaf senescence and determination of life span. Especially worth noticing is the relationship between oxidative stress tolerance and regulation of senescence processes: long-lived Arabidopsis mutants appeared to be more tolerant than wild-type plants to oxidative stress, and mutants deficient in anti-oxidative molecules (vitamin E and C) suffered from prema-ture senescence and diminished longevity. Furthermore, transgenic plants with increased tolerance to environmental stresses had delayed leaf senescence phenotypes and en-hanced life spans. In the future, this information regarding the validity of the “stress resistance” theory of aging in plants may be utilised in breeding programs to develop new horti-cultural cultivars with enhanced tolerance to environmental stresses. Such enhanced tolerance will most likely encompass prolonged longevity and delayed senescence phenotypes. Such cultivars will obviously have much extended posthar-vest storage lives and will suffer less from wastage caused by accelerated senescence. Acknowledgments This manuscript is contribution no. 537/08 from the Agricul-tural Research Organization, The Volcani Center, Bet Dagan, Israel. References Papers of interest have been indicated as: * Marginal importance ** Essential reading 1 Harman DJ. Aging: a theory based on free radical and radiation chemis-

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