TY - JOUR
AU - Munné-Bosch, Sergi
AB - Abstract The life cycle of a leaf can be characterized as consisting of different stages: from primordial leaf initiation in the shoot apical meristem (SAM) to leaf senescence. Leaf development, from early leaf growth to senescence, is tightly controlled by plant development and the environment. Here, we primarily focus on summarizing current evidence indicating that photo-oxidative stress occurs at the two extremes of a leaf’s lifespan. Some recent studies clearly indicate that—as happens in senescing leaves—emerging new leaves suffer from photo-oxidative stress, which suggests that oxidative stress plays a key role at both ends of the leaf life cycle. We discuss the causes and consequences of suffering from photo-oxidative stress during leaf development, paying attention to the particularities of this process at the two extremes of leaf development. Of particular importance is the current evidence showing mechanisms that maintain an adequate cellular reactive oxygen species/antioxidant (redox) balance that allows growth and prevents oxidative damage in young emerging leaves, while later on photo-oxidative stress induces cell death in senescing leaves. Also of interest is the fact that reductions in the efficiency of photosystem II photochemistry may not necessarily indicate photo-oxidative stress in emerging leaves. In this review, we summarize current knowledge of photoinhibition, photoprotection, and photo-oxidative stress at the two ends of the leaf life cycle: early leaf growth and leaf senescence. Antioxidants, leaf growth, leaf senescence, oxidative stress, photoinhibition, photoprotection, redox regulation Introduction Leaf development is extremely plastic. Not only are the shape and complexity of leaves extremely varied between species, but they also are within an individual plant. Depending on the developmental stage and growth conditions, there can also be pronounced variations in leaf shape, size, and longevity. All leaves within an individual compete for light, water, and nutrients; therefore, their growth is in harmony with the architecture of the plant, which at the same time determines the life history traits and longevity of each leaf. All leaves will be exposed to a specific micro-environment and certain developmental pressures—such as interindividual and intershoot competition for resources—that will determine their development. The life cycle of a leaf can be divided into different stages. It starts with primordial initiation in the shoot apical meristem (SAM), followed by the primary morphogenesis stage—when cell division/proliferation occurs—and a secondary morphogenesis characterized by cell expansion (Donnelly et al., 1999). Leaf initiation and early leaf growth (including both cell division and expansion) are tightly controlled by endogenous factors that include hormones, reactive oxygen species (ROS), sugars, and other regulators that converge on the regulation of transcription factors and gene expression (Werner and Schmülling, 2009; Traas and Monéger, 2010). These early stages are also subject to modulation by environmental factors such as light, water, and nutrient availability, and temperature, which allow the plant to optimize growth according to its environmental conditions (Yoshida et al., 2011). During the initiation stage, leaf primordia are considered to be a heterotrophic organ as the apparatus for photosynthesis has not yet been developed and all the photoassimilates and nutrients needed for leaf development come from other organs. As its ontogenetic development proceeds, the leaf is formed and gradually becomes autotrophic. At this stage, although emerging leaves are already photosynthetically active, they still depend on imported photoassimilates for growth. Some time is needed before the leaf switches from being a carbon sink to a carbon source (Turgeon, 1989). The leaf then grows until it reaches a certain size and shape. It is generally assumed that a leaf is mature when it has expanded to its full leaf area. At this stage, the leaf has become a net carbon exporter (Fig. 1). Fig. 1. View largeDownload slide Interplay between emerging and senescing leaves (A) and comparison of photosynthetic activity in emerging and senescing leaves (B). Fig. 1. View largeDownload slide Interplay between emerging and senescing leaves (A) and comparison of photosynthetic activity in emerging and senescing leaves (B). Senescence is considered to be the last stage in leaf development. Highly regulated changes at the molecular, cellular, biochemical, and physiological levels cause the leaf to die. Before dying, however, the leaf fulfils an essential function during senescence: nutrient remobilization, including not only mobilizing essential nutrients for the plant—such as nitrogen—but also providing substantial amounts of carbon, mainly in the form of sucrose, for other plant parts (leaf primordia, emerging new leaves, reproductive organs, or storage organs). Leaf senescence is regulated by the same endogenous and environmental factors as is early leaf growth (Fig. 2). Thus, ROS also play an essential role in the regulation of the process in concert with other endogenous regulators—such as hormones—and act as signalling molecules that translate information from environmental cues (Munné-Bosch et al., 2013). Senescence initiation proceeds through a series of signalling cascades that lead to changes in gene expression of the so-called senescence-associated genes (SAGs). As a result, re-organization starts and catabolic activities increase, causing the leaf to undergo a source–sink transition, whereby part of the photoassimilates and nutrients that the leaf had been accumulating during its development are remobilized and distributed to other parts of the plant. After nutrient remobilization is complete, leaf senescence eventually results in the death of the organ, which may be followed or not—depending on the species and conditions—by abscission (Lim et al., 2007; Fig. 2). Fig. 2. View largeDownload slide Factors modulating leaf growth and senescence in plants. Fig. 2. View largeDownload slide Factors modulating leaf growth and senescence in plants. In this review, we focus on the role of photo-oxidative stress both at early stages of leaf growth and during leaf senescence. We consider early leaf growth to be the stages at which the leaf is photosynthetically active but still depends on imported photoassimilates for net growth. During leaf senescence, we focus on the processes involved in the initiation, re-organization, and terminal phases. Furthermore, we aim at characterizing such processes beyond the information gathered in the model plant Arabidopsis thaliana and include recent literature on the topic obtained in perennials. Early leaf growth and senescence differ greatly between annual and perennial plants, as does the growth strategy adopted. The leaves of annual plants have a shorter lifespan and senescence is usually induced by reproduction, although environmental factors can undoubtedly modulate the process. In these plants, all the life history traits will ultimately be focused on rapidly producing seeds. The leaves of perennial plants generally live longer and their senescence is generally modulated more strongly by environmental cues, rather than by reproduction; although flower and fruit production can also play a major role. The perennial strategy is also effective at producing seeds; not by using different plant generations as in annual plants, but by the same individual producing seeds for long periods of time. Since the plant produces new shoots every spring, the energy stored in the plant parts that have survived through the winter will be successfully used for growth and reproduction. In trees, for example, structure can be built up year after year so that the tree becomes larger and capable of producing more fruit and seed than the previous year, out-competing other plants for light, water, nutrients, and space (Iwasa and Cohen, 1989). We summarize here recent studies that clearly indicate that new, emerging leaves show transient photo-oxidative stress, exactly as happens during senescence. However, oxidative damage and death occur during the terminal phase of senescence. Thus, we focus here on the particularities of photo-oxidative stress at the two extremes of the life cycle of leaves, and discuss the differences that lead to different outcomes; all particularly focused on photoinhibition, photoprotection, and photo-oxidative stress. Photoinhibition and photoprotection in emerging leaves Light plays a dual role in the regulation of leaf growth (Fig. 3). On one hand, it plays a major role in photomorphogenesis via the induction of phytochrome function and signalling; while on the other, light energy is used for photosynthesis. Both processes (photomorphogenesis and photosynthesis) can, however, converge in the regulation of leaf growth by modulating ROS production in a complex manner. Stirnberg et al. (2012) have shown that Arabidopsis mutants with a defect in a gene encoding the transposase-related transcription factor FAR-RED ELONGATED HYPOCOTYL3 (FHY3), which is known to be involved in the far-red light-dependent regulation of seedling de-etiolation, present oxidative stress-related phenotypes showing retarded leaf growth and cell death. Interestingly, this phenotype was found to require the AUXIN-RESISTANT1 gene, and turned out to be independent of phytochrome A (phyA). In another study, Danon et al. (2006) showed that cryptochrome 1 (cry1) mediates singlet oxygen-induced programmed cell death (PCD). Unexpectedly, the light-dependent release of singlet oxygen alone was not sufficient to induce PCD of the conditional fluorescent (flu) mutant of Arabidopsis, but had to act in concert with a second concurrent blue light reaction mediated by cry1. Taken together, these results indicate that photoreceptor function may be finely modulated during plant development to prevent oxidative damage and cell death during leaf initiation and early leaf growth. Fig. 3. View largeDownload slide Reactive oxygen species (ROS) play multiple roles depending on the developmental stage of the leaves. Fig. 3. View largeDownload slide Reactive oxygen species (ROS) play multiple roles depending on the developmental stage of the leaves. Furthermore, emerging new leaves are sensitive to many environmental insults since their photosynthetic apparatus is not fully developed. During the early stages of leaf development, the photosynthetic rate gradually increases, as does stomatal conductance. The photosynthetic apparatus is under construction, so low CO2 assimilation rates occur concomitantly with stomatal closure during early stages of leaf growth (Freeland, 1952; Choinski and Johnson, 1993; Greer and Halligan, 2001). Consequently, since chloroplasts may be exposed to excess excitation energy, photoinhibition can occur (Fig. 4). Indeed, some studies have reported that the Fv/Fm ratio, which is an indicator of the maximum efficiency of photosystem II (PSII) photochemistry, is lower in young expanding leaves than in fully expanded leaves (Jiang et al., 2005; Maayan et al., 2008; Lepedus et al., 2011), thereby confirming that while the photosynthetic machinery is being formed leaves are very sensitive to photoinhibition. This photoinhibition can result from immature chloroplasts and therefore photosynthetic apparatus, leading to a reduced efficiency of PSII photochemistry, or to transient ROS accumulation in chloroplasts. Fig. 4. View largeDownload slide Formation of reactive oxygen species (ROS) in chloroplasts (A), photoinhibition at the two extremes of the leaf lifespan (B), and summary of the photoprotection mechanisms operating in emerging and senescing leaves (C). Fig. 4. View largeDownload slide Formation of reactive oxygen species (ROS) in chloroplasts (A), photoinhibition at the two extremes of the leaf lifespan (B), and summary of the photoprotection mechanisms operating in emerging and senescing leaves (C). It is well known that excess light can trigger the production of ROS via the photosynthetic electron transport chain (Asada, 2006). In those conditions, a superoxide anion (O–2) is produced as a consequence of the direct reduction of oxygen by ferredoxin in the Mehler reaction in PSI. However, the interaction between oxygen and a chlorophyll molecule in the triplet state (3Chl*) can generate the ROS that is generally the most damaging in chloroplasts: singlet oxygen (1O2; Fig. 4). ROS generated in chloroplasts can react and oxidize a large number of molecules, including photosynthetic pigments, sugars, lipids, nucleic acids, and several proteins—such as the D1 protein subunit of PSII, which causes photoinhibition (Takahashi and Badger, 2011). This inhibition of photosynthesis—which is reflected in reductions in the Fv/Fm ratio in young expanding leaves—will, however, not result in irreversible damage to the photosynthetic apparatus; so efficient repair of the D1 protein is expected. D1 protein levels measured during the first stages of leaf growth revealed a small amount of the protein, which increased while the young leaf expanded, to achieve a fully functional PSII (Maayan et al., 2008; Lepedus et al., 2011). Another common indicator of whether young leaves suffer photo-oxidative stress is bulk protein and lipid oxidation caused by ROS, which are measured as levels of total protein carbonyl and malondialdehyde (a lipid oxidation product), respectively. Lepedus et al. (2011) found that the development of the photosynthetic apparatus in expanding leaves of Norway maple (Acer platanoides L.) correlated negatively with the levels of protein carbonyls and positively with lipid peroxidation; that is, emerging leaves showed increased protein, but not increased lipid oxidation compared with fully expanded leaves. However, other studies have shown a negative correlation between leaf development and levels of malondialdehyde (Juvany et al., 2012), thus suggesting that oxidative stress occurs in emerging leaves, but that the oxidative target may differ between species and/or growth conditions. In addition to the fact that the photosynthetic apparatus is under construction and is therefore more susceptible to photoinhibition, emerging leaves are highly susceptible to photodamage because they normally initiate at the top of a branch where they receive more direct sunlight than expanded leaves further down. Unfortunately, however, to our knowledge, no studies have been carried out to disentangle the effects of an immature photosynthetic apparatus from those of the conditions expanding leaves are exposed to. Indeed, such studies might prove difficult since different climatic conditions will in turn affect growth rates and therefore mask the results. In any case, compelling evidence clearly indicates that it is vital that young emerging leaves have good photoprotection mechanisms. Otherwise, photodamage (understood as irreversible damage to the photosynthetic apparatus) would inhibit photosynthesis and this would cause a reduction in growth and productivity that would affect either the renewal of leaves in perennials or the chance of survival in annual plants. Emerging leaves construct the new photosynthetic apparatus progressively, thereby avoiding excess energy in newly formed chloroplasts. The levels of chlorophyll therefore increase steadily during leaf expansion (Jiang et al., 2005; Maayan et al., 2008; Lepedus et al., 2011). Although the lack of efficient photosynthetic machinery means that emerging new leaves may be exposed to considerable photoinhibition, low amounts of chlorophyll limit light absorption and therefore potential photodamage. However, it is clear from the results discussed previously that emerging leaves need additional mechanisms to prevent photodamage that could be caused by increased levels of ROS production in chloroplasts. Furthermore, as young leaves are usually exposed to higher irradiance than mature leaves, they need increased photoprotective ability. One of the most important mechanisms employed against high irradiance is the xanthophyll cycle-dependent dissipation of excess energy as heat. Non-photochemical quenching (NPQ) of chlorophyll fluorescence is most extensive at the very early stages of leaf maturation (Jiang et al., 2005; Lepedus et al., 2011), and young, expanding leaves have relatively larger xanthophyll pools and a greater de-epoxidation state of the xanthophyll cycle (DPS) than fully expanded leaves (Jiang et al., 2006), which suggests a protective role against excesses of light. A greater DPS and high NPQ values have been correlated with an increased thermal dissipation of excess energy in chloroplasts and therefore increased photoprotection capacity in several species (Demmig-Adams and Adams, 1992). Recently it has additionally been shown that xanthophylls are essential during leaf growth not only as a photoprotection mechanism but also because they are involved in PSI biogenesis (Dall’Osto et al., 2013). α-Tocopherol has antioxidant and photoprotective effects in leaves. It works by preventing lipid peroxidation and scavenging ROS, mainly neutralizing 1O2 (Kruk et al., 2005). However, it does not seem to play a role in protection against excessive light in young leaves, as they present low levels of α-tocopherol (Lepedus et al., 2011; Juvany et al., 2012). Szymanska and Kruk (2008) reported high levels of γ-tocopherol in young leaves of runner bean (Phaseolus coccineus) that decreased with leaf age, in contrast to α-tocopherol. Their study suggests that γ-tocopherol may play a role as an antioxidant, replacing the low levels of α-tocopherol. Furthermore, a red transitional coloration has been detected in young leaves in some species, indicating the accumulation of anthocyanins (Choinski and Wise, 1999; Juvany et al., 2012). Liakopoulos et al. (2006) found that anthocyanins in the epidermis of young grapevine (Vitis vinifera) leaves decreased the risk of photoinhibition. It has been suggested that anthocyanins may play a photoprotective role by modifying the quantity of incident light on chloroplasts (Steyn et al., 2002; Manetas et al., 2003; Hughes et al., 2005). This could indicate that some species accumulate anthocyanins in emerging new leaves as another photoprotection mechanism; although this is still controversial. Another element involved in photoprotection are the early light-induced proteins (ELIPs), which seem to be essential in light energy dissipation (Montané and Kloppstech, 2000) and in photo-oxidative stress protection (Hutin et al., 2003). Accumulation of these proteins has been reported under several stress conditions, such as high light stress (Zeng et al., 2002; Sävenstrand et al., 2004; Tzvetkova-Chevolleau et al., 2007). Maayan et al. (2008) and Pinto et al. (2011) showed that the expression of ELIPs in young leaves is correlated with low photosynthetic activity, whereas very low levels of these proteins or complete non-expression was found in mature leaves. This is consistent with an increased protective demand in emerging leaves. Finally, current ongoing research aims to identify new mechanisms of photoprotection in the chloroplasts of emerging leaves. For example, Li et al. (2011) have shown that ZEBRA NECROSIS, which encodes a thylakoid-bound protein of unknown function, is required to protect developing chloroplasts from ROS and excess light, especially during the assembly of thylakoid protein complexes. At very early stages of leaf growth, low levels of ascorbate and ascorbate peroxidase (APX) activity have also been reported (Lepedus et al., 2011); such activity is essential for hydrogen peroxide removal (Foyer and Noctor, 2011). Low tocopherol and ascorbate levels, together with reduced APX activity suggest that there is a time window for increased ROS accumulation in emerging leaves. However, during the development of the photosynthetic apparatus in soybean (Glycine max), high levels of the antioxidant enzymatic protection system have also been reported, including high levels of APX (Jiang et al., 2005). It is possible that in this last study, the time window for reduced APX activity was not detected due to the time frame used for the sampling points. Be that as it may, it is clear that despite the multiple mechanisms involved in photoprotection, leaves suffer from photo-oxidative stress at very early stages of growth. However, this stress is rapidly buffered by the development of efficient antioxidant machinery while the leaf expands and develops. Photoinhibition and photoprotection in senescing leaves Leaf senescence constitutes the last developmental stage in the life of a leaf and it is characterized by highly regulated processes at the physiological, biochemical, and molecular levels. Although senescence is controlled mainly by leaf age, it can be induced by many environmental stresses, particularly those leading to excess excitation energy in chloroplasts, such as drought, excess light, heat stress, or salinity. Once senescence is induced, chloroplasts are one of the first organelles to be targeted for breakdown, while mitochondria and nuclei maintain their integrity until the terminal phase. Hence, the photosynthetic apparatus is rapidly dismantled, starting with chlorophyll degradation, a decrease in photosynthesis, and enhanced photoinhibition, which can be detected by low Fv/Fm ratios (Wingler et al., 2006; Abreu and Munné-Bosch, 2009). Another sign of leaf senescence is an increase in the levels of ROS. It has been extensively reported that during the first steps of leaf senescence following chlorophyll degradation ROS increase rapidly (Smart, 1994; Buchanan et al., 2000). This rapid ROS production leads to pigment, protein, and lipid oxidation; oxidative processes that are needed for nutrient remobilization (Hörstensteiner and Feller, 2002). Finally, oxidative processes in combination with other mechanisms lead to leaf death (Zimmermann and Zentgraf, 2005). Therefore, oxidative stress plays multiple roles in senescing leaves; it is known to induce leaf senescence, but ROS production (such as that of singlet oxygen, one of the most potentially damaging molecules formed in chloroplasts during photo-oxidative processes; Triantaphylidès et al., 2008) should be controlled in both space and time in senescing chloroplasts by efficient antioxidant machinery (Munné-Bosch et al., 2001; Zimmerman and Zentgraf, 2005). Otherwise, the terminal phase will be induced rapidly (before nutrient remobilization occurs), and the principal function of senescence in leaves will not be fulfilled. Although senescence is usually seen as a purely degenerative process leading to death, it has a positive effect on the plant through the remobilization and recycling of nutrients to other plant parts, and may consequently be considered a survival strategy under adverse climatic conditions (Munné-Bosch and Alegre, 2004). Consequently, photoprotection of the photosynthetic apparatus plays a major role in controlling the timing and progression of senescence; not only when senescence is initiated, but also modulating the exact period of nutrient remobilization in chloroplasts (re-organization phase) and compromising chloroplast function when these organelles are no longer needed in the terminal phase, thereby inducing cell death. As occurs in emerging leaves, the most flexible and quantitatively important photoprotection mechanism (in terms of the amount of excess energy dissipated) in senescing leaves is the xanthophyll cycle-dependent dissipation of excess energy as heat. In senescing leaves, the chloroplasts are dismantled. This includes the degradation of the pigment antennae of PSII and PSI; therefore, the amount of photosynthetic pigments, including xanthophylls, decreases. How, then, can the xanthophyll cycle-dependent energy dissipation increase in senescing leaves? The xanthophyll cycle pool (VZA: the sum of violaxanthin, zeaxanthin, and antheraxanthin) decreases, but violaxanthin levels decrease more than those of zeaxanthin, so that the DPS (given as Z+0.5×A/VZA) increases (Munné-Bosch and Peñuelas, 2003; Duarte et al., 2012). The DPS, rather than zeaxanthin accumulation, has been correlated with the thermal dissipation of excess energy in chloroplasts (Demmig-Adams and Adams, 1992). Furthermore, an increase in xanthophyll cycle pigments relative to chlorophyll is generally observed in senescent leaves, thus indicating an increased photoprotection capacity relative to the amount of light absorbed by chlorophyll (Lu et al., 2003). It should be borne in mind that only a few molecules of zeaxanthin per reaction centre of PSII are needed, in combination with a pH gradient across the thylakoid membrane, for efficient photoprotection (Heber et al., 2001). Wingler et al. (2004) showed that the overall plant NPQ increases with leaf age in Arabidopsis, and NPQ remained high in the base of rosette leaves at very advanced phases of development. In that study, minimum fluorescence (F0) temporarily increased at the tips of the inner rosette leaves from where the high F0 spread to the base preceding cell death, thus indicating distinct spatial patterns of photoprotection in senescing leaves. Furthermore, Dai et al. (2004) showed that, at the beginning of senescence or under low light, wheat (Triticum aestivum) leaves were able to dissipate excess light energy via xanthophyll cycle-dependent NPQ; however, the xanthophyll cycle was insufficient to protect leaves against photodamage under strong light, when the leaves became severely senescent. Taken together, these studies indicate complex spatiotemporal regulation of photoprotective processes within the plant, in which NPQ increases at early stages of leaf senescence to decrease later. This suggests that NPQ is needed in periods of nutrient remobilization, while it decreases during the terminal phase when photoprotection is no longer needed. Generally, preferential loss of chlorophyll a is reported in senescing leaves, leading to a decrease in the chlorophyll a/b ratio, therefore suggesting a preferential loss of chlorophyll a-containing proteins, which are closely associated with the reaction centres, rather than a loss of light-harvesting proteins (Rosenthal and Camm, 1997; Munné-Bosch and Peñuelas, 2003). Nonetheless, senescence does not always occur equally in all species in terms of photosynthetic pigment degradation. Krupinska et al. (2012) reported an increase in the chlorophyll a/b ratio at a late phase of senescence concomitantly with a decline in the level of the Lhcb1 apoprotein of the light-harvesting complex (LHC) and in the level of the corresponding transcript. Ultrastructural studies revealed the presence of chloroplasts with long, single or pairwise thylakoids that lacked large grana stacks. The authors hypothesized that the early degradation of grana thylakoids harbouring the major LHC reduced the risk of photoinhibition and might be causally related to the high yield of the barley variety studied. ELIPs, which have predominantly been found involved in photoprotection in emerging leaves (see the previous section), could also have such a role in senescing leaves. Binyamin et al. (2001) suggested that ELIPs may act as pigment carriers, binding free chlorophyll during senescence in the same manner as during stress conditions, and helping in maintaining chloroplast function, thus delaying senescence. It has been suggested that anthocyanins protect the photosynthetic apparatus from excess light during senescence (Hoch et al., 2001). Anthocyanins, which accumulate in the leaf epidermis in most anthocyanin-bearing plant species, are thought to function as photoprotective screens, preventing overexcitation of the photosynthetic system by reducing the amount of light absorbed by mesophyll chloroplasts. However, the results to date differ between species and study conditions. In a study under field and laboratory conditions of Cornus sanguinea and Parthenocissus quinquefolia, which display considerable variation in both anthocyanin and chlorophyll concentrations during autumn, Manetas and Buschmann (2011) showed that the possible photoprotection conferred by anthocyanins may be of limited advantage, and even in the best of cases may occur only under adverse environmental conditions. Neither was conclusive evidence of enhanced photoprotection in anthocyanin-bearing leaves obtained by Merzlyak et al. (2008), who studied the optical properties of leaves from Norway maple (Acer platanoides), cotoneaster (Cotoneaster alaunica), hazel (Corylus avellana), Siberian dogwood (Cornus alba), and Virginia creeper (Parthenocissus quinquefolia), differing in pigment composition and at different stages of ontogenesis. Hughes (2011) noted that, although red leaves tend to show symptoms of shade acclimation relative to green leaves, consistent with a photoprotective function, winter-red and winter-green species often inhabit the same high-light environments, and exhibit similar photosynthetic capacities, which indicates that factors dictating interspecific winter leaf coloration remain unclear. Apart from NPQ and anthocyanins, studies of antioxidant protection have also revealed interesting patterns of photoprotection during leaf senescence. García-Plazaola et al. (2003) studied photoprotection mechanisms during autumnal senescence both in leaves exposed to sunlight and in those kept in the shade of woody plants with different ecological characteristics and senescence patterns, including a shade-intolerant and early successional species (Betula alba), a shade-tolerant and late successional species (Corylus avellana), and an N-fixing tree with low N resorption efficiency (Alnus glutinosa). As a general senescence pattern, the authors found that nitrogen resorption preceded autumn and started in mid-summer; furthermore, it occurred in parallel with a slight and continuous ascorbate, chlorophyll, and carotenoid degradation. Munné-Bosch and Peñuelas (2003) also found decreased ascorbate and tocopherol concentrations in mastic tree senescing leaves, which occurred concomitantly with increased lipid peroxidation. Tocopherol levels generally increase in senescing leaves (García-Plazaola et al., 2003), but, if sampling includes the last phases of senescence, tocopherol levels decrease (Juvany et al., 2012). Consistent with these results, Abbasi et al. (2009) found that tocopherol-deficient tobacco (Nicotiana tabacum) RNAi (RNA interference) transgenic lines show accelerated senescence. A considerable decrease of the ascorbate content in chloroplasts was also found during leaf senescence of pea (Pisum sativum) plants, with only dehydroascorbate being detectable in senescing leaves, thus specifically indicating ascorbate oxidation in chloroplasts during senescence (Palma et al., 2006). In contrast, glutathione levels in chloroplasts remained unaltered or increased slightly—depending on N availability—in senescing leaves, but in all cases the reduction state of glutathione increased, thus suggesting a differential antioxidant behaviour between ascorbate and glutathione in chloroplasts of senescing leaves. This latter study is of particular interest since analyses of antioxidant metabolites were performed in isolated organelles. This is particularly relevant for ascorbate and gluthatione, since these antioxidants—in contrast to tocopherols and carotenoids—are not exclusively found in chloroplasts. Therefore, ascorbate and glutathione levels in leaves do not necessarily indicate what happens in chloroplasts and are therefore not indicative of photo-oxidative stress. In summary, it appears that a severe loss of antioxidant protection occurs in chloroplasts during the latest phases of leaf senescence, coincident with reductions in the NPQ. Therefore, antioxidant protection will be generally decreased together with the capacity to dissipate excess excitation energy in chloroplasts, consequently leading to photo-oxidative damage during the terminal phase (Fig. 4). Photo-oxidative stress and redox signalling As explained in the previous sections, photoinhibition can cause photo-oxidative stress in both emerging and senescing leaves, thereby eventually leading to redox signalling protective responses in the former and oxidative damage and death in the latter. ROS may trigger acclimation responses which counteract the environmental change, to maintain or increase the photosynthetic electron transport efficiency. Many such responses may involve targeted changes in nuclear gene expression and require two-way communication between the chloroplasts and nucleus. Recently, Kravchik and Bernstein (2013) showed that oxidative stress induced by salinity induces expression of genes involved in antioxidant protection in young leaves of maize (Zea mays). Furthermore, it has been shown that the cellular redox state can change the activity of chloroplast DNA replication (Kabeya and Miyagishima, 2013); hence, ROS play an important role during leaf growth. However, while several studies have researched the role of photo-oxidative stress and redox signalling in senescing leaves, to date none has focused on examining changes in gene expression induced by photo-oxidative stress in emerging leaves. During the early senescing phases, efficient antioxidant machinery is needed to prevent premature death due to oxidative damage. The up-regulation of antioxidant genes during senescence answers such a need (Gepstein et al., 2003; Buchanan-Wollaston et al., 2005; van der Graaff et al., 2006). Oxidative stress itself could trigger the expression of genes related to its own detoxification. Some studies reported that various genes encoding antioxidant enzymes are induced by H2O2 (Neill et al., 2002). Gechev et al. (2002) reported that moderate doses of H2O2 induce antioxidant enzymes that protect tobacco from oxidative stress. Furthermore, Navabpour et al. (2003) showed that some of the genes involved in antioxidant protection during senescence are indeed induced by oxidative stress. One of them is the LSC803 gene, which encodes glutathione peroxidase, an enzyme directly related to H2O2 detoxification (Apel and Hirt, 2004). Other antioxidant biosynthesis genes and detoxification-related genes up-regulated during senescence (Gepstein et al., 2003) are also induced by oxidative stress (Desikan et al., 2001). Some studies have also reported the up-regulation of many SAGs involved in the degradation of macromolecules, and the mobilization and transport of metabolites, suggesting that they may play a role in the mobilization of nutrients to the rest of the plant (Gepstein et al., 2003; Buchanan-Wollaston et al., 2005; van der Graaff et al., 2006). Transcriptomic analysis of oxidative stress-regulated genes in Arabidopsis (Desikan et al., 2001) shows that oxidative stress can also induce the expression of genes related to macromolecular degradation and recycling, thereby playing an essential role in the re-organization phase. Finally, several studies indicate that ROS, such as H2O2, are involved in the induction of PCD (de Pinto et al., 2012). Furthermore, Guo (2012) reviewed and compared genes identified in previous studies as being involved in senescence processes from different species, including Populus, Arabidopsis, and wheat (Andersson et al., 2004; Buchanan-Wollaston et al., 2005; Gregersen and Holm, 2007). The author reports that at the gene expression level, the developmental process of senescence seems to be conserved among species and not to differ much between dicots and monocots, or between annual and perennial plants. Furthermore, it has been shown by different means of retrograde signalling that photo-oxidative stress, and therefore ROS produced in chloroplasts, contributes to the regulation of nuclear genes in senescing leaves (for a review, see Pfannschimdt and Munné-Bosch, 2013). However, although several studies report on massive changes in gene expression during early leaf growth (Schmid et al., 2005; Efroni et al., 2008; Rehrauser, 2010), it is unknown to what extent photo-oxidative stress in chloroplasts contributes to ROS-regulated gene expression in emerging leaves; therefore it is not possible to establish common or differential patterns of photo-oxidative stress effects on gene expression in emerging and senescing leaves, an aspect that warrants further research. Rather, results obtained thus far on photoinhibition, photoprotection, and photo-oxidative stress reveal interesting common patterns of behaviour, but also important differences between emerging and senescing leaves. Particularities of photo-oxidative stress in emerging and senescing leaves: a summary Results on photoinhibition, photoprotection, and photo-oxidative stress reveal complex but characteristic spatiotemporal response patterns in emerging and senescing leaves. Here, we summarize both the common and the different responses in emerging and senescing leaves, so as to identify common strategies at the two ends of the leaf life cycle. Young, expanding leaves are more susceptible to photoinhibition than fully expanded, mature leaves. This susceptibility to photoinhibition is particularly apparent at very early stages of growth, when chloroplasts receive large amounts of light but the photoprotection and antioxidant machinery is not yet completely built, so that excess excitation energy in the chloroplasts cannot be fully dissipated. For this short time window during early leaf development, oxidative stress occurs, but is not translated into oxidative damage, in terms of irreversible oxidative injury. Rather, it is expected that this transient oxidative stress serves a signalling function for protection. Similarly to what occurs in emerging leaves, mechanisms of photoprotection—such as the xanthophyll cycle-dependent dissipation of excess energy—and antioxidant protection are activated in senescing leaves. In this case, however, photoprotection mechanisms are operative during the re-organization phase; when photoassimilate and nutrient remobilization is accomplished, severe photoinhibition occurs as a result of the failure of photoprotection mechanisms. Hence, the same mechanisms are operative in both leaf types, but the timing is completely different, as if reflected in a mirror: (i) photoinhibition occurs both very early in emerging leaves and very late in senescing leaves; and (ii) photoprotection is activated later in the growth phase, while it declines in advanced senescence (Fig. 4). Photoinhibition is therefore maximal at the two extremes of the leaf life cycle because both leaf types have the same problem: incomplete photosynthetic apparatus. The causes, however, differ: emerging leaves are developing that apparatus, while senescing leaves are dismantling it; both are therefore sensitive to photoinhibition and photo-oxidative stress. The final result is completely different in the two cases: oxidative stress in emerging leaves plays a protective, presumably signalling, role, while oxidative stress at very advanced stages of senescence results in oxidative damage and death. Conclusions and perspectives In this review, we have shown that photoinhibition and photo-oxidative stress occur at the two extremes of the leaf life cycle, not only in senescing leaves but also at the very start of leaf expansion. It appears that this photo-oxidative stress is transiently induced both in emerging leaves and in the initial stages of senescence, but during the last stages of senescence the oxidative stress will be sustained in time and cause oxidative damage and death. Photoprotection mechanisms play a key role in the occurrence of photo-oxidative stress in both emerging and senescing leaves. Photo-oxidative stress occurs while photoprotection mechanisms are still not fully operative in emerging leaves, but its cellular signalling function is still unknown. While photo-oxidative stress is known to induce expression of SAGs and therefore to play a key role in senescence, ROS formed in chloroplasts are presumed to play a protective role in redox signalling in emerging leaves; however, evidence for this is lacking. Indeed, it is highly probable that the transient photo-oxidative stress in emerging leaves serves to make a more efficient photosynthetic apparatus, by acting as a signal to construct a functional system that will be more resistant to environmental injuries later when the leaf is fully expanded. However, it is also possible that this photo-oxidative stress plays no protective signalling role and serves as a selective pressure on emerging new leaves, so that the more susceptible leaves do not progress. This second hypothesis is more plausible for perennial plants, in which very young expanding leaves from different shoots compete for resources. Finally, the importance of studying leaf senescence by considering the whole leaf developmental programme should be emphasized, since history traits of the same and neighbouring leaves undoubtedly affect the spatiotemporal senescence programme within the plant. A recent study has shown that repeated exposures to strong light resulted in the acclimation to high light and oxidative stress not only of the exposed leaves, but also of young emerging leaves (Gordon et al., 2012). Furthermore, epigenetic changes triggered by specific events encountered by leaves during their early life history—such as a specific stress imprint during the early phases of growth—are also likely to determine the timing of senescence. It remains, however, to be examined to what extent photo-oxidative stress suffered during early leaf growth affects the timing and/or progression of senescence in plants. To date, all the studies have focused on establishing how a number of abiotic stresses can affect senescence after short periods of time and not on whether a stress imprint at an early stage of leaf development can affect senescence much later in time. Abbreviations: Abbreviations: APX ascorbate peroxidase ELIP early light-induced protein NPQ non-photochemical quenching PCD programmed cell death PS photosystem ROS reactive oxygen species SAG senescence-associated gene SAM shoot apical meristem. Acknowledgements Support for the research in the laboratory of SM-B is received through grants BFU2012-32057 and CSD2008-00040 from the Ministry of Economy and Competitivity of the Spanish Government, and the ICREA Academia prize funded by the Generalitat de Catalunya. We are very grateful to Toffa Evans (University of Barcelona) for English corrections. We are also indebted to two anonymous reviewers for their insight and comments on the manuscript. References Abbasi A Saur A Hennig P Tschiersch H Hajirezaei M Hofius D Sonnewald U Voll LM . 2009. Tocopherol deficiency in transgenic tobacco (Nicotiana tabacum L.) plants leads to accelerated senescence. Plant, Cell and Environment  32, 144– 157. Google Scholar CrossRef Search ADS   Abreu ME Munné-Bosch S . 2009. Salicylic acid deficiency in NahG transgenic lines and sid2 mutants increases seed yield in the annual plant Arabidopsis thaliana. Journal of Experimental Botany  60, 1261– 1271. Google Scholar CrossRef Search ADS PubMed  Apel K Hirt H . 2004. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology  55, 373– 399. Google Scholar CrossRef Search ADS PubMed  Andersson A Keskitalo J Sjodin A et al.   . 2004. A transcriptional timetable of autumn senescence. Genome Biology  5, R24. Google Scholar CrossRef Search ADS PubMed  Asada K . 2006. Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiolgy  141, 391– 396. Google Scholar CrossRef Search ADS   Binyamin L Falah M Portnoy V Soudry E Gepstein S . 2001. The early light-induced protein is also produced during leaf senescence of Nicotiana tabacum. Planta  212, 591– 597. Google Scholar CrossRef Search ADS PubMed  Buchanan BB Gruissem W Jones RL . 2000. Biochemistry and molecular biology of plants . Rockville, MD: American Society of Plant Physiologists. Buchanan-Wollaston V Page T Harrison E et al.   . 2005. Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. The Plant Journal  42, 567– 585. Google Scholar CrossRef Search ADS PubMed  Choinski JS Johnson JM . 1993. Changes in photosynthesis and water status of developing leaves of Brachystegis spiciformis Benth. Tree Physiology  13, 17– 27. Google Scholar CrossRef Search ADS PubMed  Choinski JS Wise RR . 1999. Leaf growth and development in relation to gas exchange in Quercus marilandica Muenchh. Journal of Plant Physiology  154, 302– 309. Google Scholar CrossRef Search ADS   Dai J Gao H Dai Y Zou Q . 2004. Changes in activity of energy dissipating mechanisms in wheat flag leaves during senescence. Plant Biology  6, 171– 177. Google Scholar CrossRef Search ADS PubMed  Dall’Osto L Piques M Ronzani M Molesini B Alboresi A Cazzaniga S Bassi R . 2013. The Arabidopsis nox mutant lacking carotene hydroxylase activity reveals a critical role for xanthophylls in photosystem I biogenesis. The Plant Cell  25, 591– 608. Google Scholar CrossRef Search ADS PubMed  Danon A Coll NS Apel K . 2006. Cryptochrome-1-dependent execution of programmed cell death induced by singlet oxygen in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA  103, 17036– 17041. Google Scholar CrossRef Search ADS   Demmig-Adams B Adams WW III . 1992. Photoprotection and other responses of plants to high light stress. Annual Review of Plant Biology and Plant Molecular Biology  43, 599– 626. Google Scholar CrossRef Search ADS   de Pinto MC Locato V de Gara L . 2012. Redox regulation in plant programmed cell death. Plant, Cell and Environment  35, 234– 244. Google Scholar CrossRef Search ADS   Desikan R Mackerness SA Hancock JT Neill SJ . 2001. Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiology  127, 159– 172. Google Scholar CrossRef Search ADS PubMed  Donnelly PM Bonetta D Tsukaya H Dengler RE Dengler NG . 1999. Cell cycling and cell enlargement in developing leaves of Arabidopsis. Developmental Biology  215, 407– 419. Google Scholar CrossRef Search ADS PubMed  Duarte B Couto T Marques JC Caçador I . 2012. Scirpus maritimus leaf pigment profile and photochemistry during senescence: implications on carbon sequestration. Plant Physiology and Biochemistry  57, 238– 244. Google Scholar CrossRef Search ADS PubMed  Efroni I Blum E Goldsshmidt A Eshed Y . 2008. A protracted and dynamic maturation schedule underlies Arabidopsis leaf development. The Plant Cell  20, 2293– 2306. Google Scholar CrossRef Search ADS PubMed  Foyer CH Noctor G . 2011. Ascorbate and glutathione: the heart of the redox hub. Plant Physiology  155, 2– 18. Google Scholar CrossRef Search ADS PubMed  Freeland RO . 1952. Effect of age of leaves upon the rate of photosynthesis in some conifers. Plant Physiology  27, 685– 690. Google Scholar CrossRef Search ADS PubMed  García-Plazaola JI Hernández A Becerril JM . 2003. Antioxidant and pigment composition during autumnal leaf senescence in woody deciduous species differing in their ecological traits. Plant Biology  5, 557– 566. Google Scholar CrossRef Search ADS   Gechev T Gadjev I van Breusegem F Inzé D Dukiandjiev S Toneva V Minkov I . 2002. Hydrogen peroxide protects tobacco from oxidative stress by inducing a set of antioxidant enzymes. Cellular and Molecular Life Sciences  59, 708– 714. Google Scholar CrossRef Search ADS PubMed  Gepstein S Sabehi G Carp MJ Hajouj T Nesher MFO Yariv I Dor C Bassani M . 2003. Large-scale identification of leaf senescence-associated genes. The Plant Journal  36, 629– 642. Google Scholar CrossRef Search ADS PubMed  Gordon MJ Carmody M Albrecht V Pogson B . 2012. Systemic and local responses to repeated HL stress-induced retrograde signalling in Arabidopsis. Frontiers in Plant Science  3, 303. Google Scholar PubMed  Greer DH Halligan EA . 2001. Photosynthetic and fluorescence light responses for kiwifruit leaves at different stages of development on vines grown at two different photon flux densities. Australian Journal of Plant Physiology  28, 373– 382. Gregersen PL Holm PB . 2007. Transcriptome analysis of senescence in the flag leaf of wheat (Triticum aestivum L.). Plant Biotechnology Journal  5, 192– 206. Google Scholar CrossRef Search ADS PubMed  Guo Y . 2012. Towards systems biological understanding of leaf senescence. Plant Molecular Biology  (in press). Heber U Bukhov NG Suvalov VA Kkobayashi Y Lange OL . 2001. Protection of the photosynthetic apparatus against damage by excessive illumination in homoiohydric leaves and poikilohydric mosses and lichens. Journal of Experimental Botany  52 1999– 2006. Google Scholar CrossRef Search ADS PubMed  Hoch WA Zeldin EL McCown BH . 2001. Physiological significance of anthocyanins during autumnal leaf senescence. Tree Physiology  21, 1– 8. Google Scholar CrossRef Search ADS PubMed  Hörtensteiner S Feller U . 2002. Nitrogen metabolism and remobilization during senescence. Journal of Experimental Botany  53, 927– 937. Google Scholar CrossRef Search ADS PubMed  Hughes NM . 2011. Winter leaf reddening in ‘evergreen’ species. New Phytologist  190, 573– 581. Google Scholar CrossRef Search ADS PubMed  Hughes NM Neufeld HS Burkey KO . 2005. Functional role of anthocyanins in high-light winter leaves of the evergreen herb Galax urceolata. New Phytologist  168, 575– 587. Google Scholar CrossRef Search ADS PubMed  Hutin C Nussaume L Moise N Moya I Kloppstech K Havaux M . 2003. Early light-induced proteins protect Arabidopsis from photooxidative stress. Proceedings of the National Academy of Sciences, USA  15, 4921– 4926. Google Scholar CrossRef Search ADS   Iwasa Y Cohen D . 1989. Optimal growth schedule of a perennial plant. American Naturalist  133, 480– 505. Google Scholar CrossRef Search ADS   Jiang CD Gao HY Zou Q Jiang GM Li LH . 2006. Leaf orientation, photorespiration and xanthophyll cycle protect young soybean leaves against high irradiance in field. Environmental and Experimental Botany  55, 87– 96. Google Scholar CrossRef Search ADS   Jiang CD Li PM Gao HY Zou Q Jiang GM Li LH . 2005. Enhanced photoprotection at the early stages of leaf expansion in field-grown soybean plants. Plant Science  168, 911– 919. Google Scholar CrossRef Search ADS   Juvany M Muller M Munné-Boch S . 2012. Leaves of field-grown mastic trees suffer oxidative stress at two extremes of their lifespan. Journal of Integrative Plant Biology  54, 584– 594. Google Scholar CrossRef Search ADS PubMed  Kabeya Y Miyagishima S . 2013. Chloroplast DNA replication is regulated by the redox state independently of chloroplast division in Chlamydomonas reinhardtii. Plant Physiology  161, 2102– 2112. Google Scholar CrossRef Search ADS PubMed  Kravchik M Bernstein N . 2013. Effects of salinity on the transcriptome of growing maize leaf cells point at cell-age specificity in the involvement of the antioxidative response in cell growth restriction. BMC Genomics  14, 24. Google Scholar CrossRef Search ADS PubMed  Kruk J Holländer-Czytko H Oettmeier W Trebst A . 2005. Tocopherol as singlet oxygen scavenger in photosystem II. Journal of Plant Physiology  162, 749– 757. Google Scholar CrossRef Search ADS PubMed  Krupinska K Mulisch M Hollmann J Tokarz K Zschiesche W Kage H Humbeck K Bilger W . 2012. An alternative strategy of dismantling of the chloroplasts during leaf senescence observed in a high-yield variety of barley. Physiologia Plantarum  144, 189– 200. Google Scholar CrossRef Search ADS PubMed  Lepedus H Gaca V Viljevac M Kovac S Fulgosi H Simic D Jurkovic V Cesar V . 2011. Changes in photosynthetic performance and antioxidative strategies during maturation of Norway maple (Acer platanoides L.) leaves. Plant Physiology and Biochemistry  49, 368– 376. Google Scholar CrossRef Search ADS PubMed  Li J Pandeya D Nath K et al.   . 2010. ZEBRA-NECROSIS, a thylakoid-bound protein, is critical for the photoprotection of developing chloroplasts during early leaf development. The Plant Journal  62, 713– 725. Google Scholar CrossRef Search ADS PubMed  Liakopoulos G Nikolopoulos D Klouvatou A Vekkos KA Manetas Y Karabourniotis G . 2006. The photoprotective role of epidermal anthocyanins and surface pubescence in young leaves of grapevine (Vitis vinifera). Annals of Botany  98, 257– 265. Google Scholar CrossRef Search ADS PubMed  Lim PO Kim HJ Nam HG . 2007. Leaf senescence. Annual Review of Plant Biology  58, 115– 136. Google Scholar CrossRef Search ADS PubMed  Lu Q Wen X Lu C Zhang Q Kuang T . 2003. Photoinhibition and photoprotection in senescent leaves of field-grown wheat plants. Plant Physiology and Biochemistry  58, 749– 754. Google Scholar CrossRef Search ADS   Maayan I Shaya F Ratner K Mani Y Lavee S Avidan B Shahak Y Ostersetzer-Biran O . 2008. Photosynthetic activity during olive (Olea europaea) leaf development correlates with plastid biogenesis and Rubisco levels. Physiologia Plantarum  134, 547– 558. Google Scholar CrossRef Search ADS PubMed  Manetas Y Buschmann C . 2011. The interplay of anthocyanin biosynthesis and chlorophyll catabolism in senescing leaves and the question of photosystem II photoprotection. Photosynthetica  49, 515– 522. Google Scholar CrossRef Search ADS   Manetas Y Petropoulou Y Psaras GK Drinia A . 2003. Exposed red (anthocyanic) leaves of Quercus coccifera display shade characteristics. Functional Plant Biology  30, 265– 270. Google Scholar CrossRef Search ADS   Merzlyak MN Chivkunova OB Solovchenko AE Naqvi KR . 2011. Light absorption by anthocyanins in juvenile, stressed, and senescing leaves. Journal of Experimental Botany  59, 3903– 3911. Google Scholar CrossRef Search ADS   Montané MH Kloppstech K . 2000. The family of light harvesting related proteins (LHCs, ELIPs, HLIPs). Was the harvesting of light their primary function? Gene  258, 1– 8. Google Scholar CrossRef Search ADS PubMed  Munné-Bosch S Alegre L . 2004. Die and let live: leaf senescence contributes to plant survival under drought stress. Functional Plant Biology  31, 203– 216. Google Scholar CrossRef Search ADS   Munné-Bosch S Juvany-Marí T Alegre L . 2001. Drought-induced senescence is characterized by a loss of antioxidant defences in chloroplasts. Plant, Cell and Environment  24, 1319– 1327. Google Scholar CrossRef Search ADS   Munné-Bosch S Peñuelas J . 2003. Photo- and antioxidative protection during summer leaf senescence in Pistacia lentiscus L. grown under Mediterranean field conditions. Annals of Botany  92, 385– 391. Google Scholar CrossRef Search ADS PubMed  Munné-Bosch S Queval G Foyer CH . 2013. The impact of global change factors on redox signaling underpinning stress tolerance. Plant Physiology  161, 5– 19. Google Scholar CrossRef Search ADS PubMed  Navabpour S Morris K Allen R Harrison E Mackerness SA Buchanan-Wollaston V . 2003. Expression of senescence-enhanced genes in response to oxidative stress. Journal of Experimental Botany  54, 2285– 2292. Google Scholar CrossRef Search ADS PubMed  Neill SJ Desikan R Clarke A Hurst RD Hancock JT . 2002. Hydrogen peroxide and nitric oxide as signalling molecules in plants. Journal of Experimental Botany  53, 1237– 1247. Google Scholar CrossRef Search ADS PubMed  Palma JM Jiménez A Sandalio LM Corpas FJ Lundqvist M Gómez M Sevilla F del Río LA . 2006. Antioxidative enzymes from chloroplasts, mitochondria, and peroxisomes during leaf senescence of nodulated pea plants. Journal of Experimental Botany  57, 1747– 1758. Google Scholar CrossRef Search ADS PubMed  Pfannschmidt T Munné-Bosch S . 2013. Plastidial signaling during the plant life cycle. In: Biswal B Krupinska K Biswal UC, eds. Advances in photosynthesis and respiration, Vol. 36: plastid development in leaves during growth and senescence . Dordrecht, The Netherlands: Springer(in press). Pinto F Berti M Olivares D Sierralta WD Hinrichsen P Pinto M . 2011. Leaf development, low temperature and light stress control of the expression of early light-inducible proteins (ELIPs) in Vitis vinifera L. Environmental and Experimental Botany  72, 278– 283. Google Scholar CrossRef Search ADS   Rehrauser H Aquino C Gruissem W et al.   . 2010. AGRONOMICS1: a new resource for Arabidopsis transcriptome profiling. Plant Physiology  152, 487– 499. Google Scholar CrossRef Search ADS PubMed  Rosenthal SI Camm EL . 1997. Photosynthetic decline and pigment loss during autumn foliar senescence in western larch (Larix occidentalis). Tree Physiology  17, 767– 775. Google Scholar CrossRef Search ADS PubMed  Sävenstrand H Olofsson M Samuelsson M Strid Å . 2004. Induction of early light-inducible protein gene expression in Pisum sativum after exposure to low levels of UV-B irradiation and other environmental stresses. The Plant Cell  22, 532– 536. Google Scholar CrossRef Search ADS   Schmid M Davison TS Henz SR Pape UJ Demar M Vingron M Schölkopf B Weigel D Lohmann JU . 2005. A gene expression map of Arabidopsis thaliana. Nature Genetics  37, 501– 506. Google Scholar CrossRef Search ADS PubMed  Smart C . 1994. Gene expression during leaf senescence. New Phytologist  126, 419– 448. Google Scholar CrossRef Search ADS   Steyn WJ Wand SJE Holcroft DM Jacobs G . 2002. Anthocyanins in vegetative tissues: a proposed unified function in photoprotection. New Phytologist  155, 349– 361. Google Scholar CrossRef Search ADS   Stirnberg P Zhao S Williamson L Ward S Leyser O . 2012. FHY3 promotes shoot branching and stress tolerance in Arabidopsis in an AXR1-dependent manner. The Plant Journal  71, 907– 920. Google Scholar CrossRef Search ADS PubMed  Szymanska R Kruk J . 2008. γ-Tocopherol dominates in young leaves of runner bean (Phaseolus coccineus) under a variety of growing conditions: the possible functions of γ-tocopherol. Phytochemistry  69, 2142– 2148. Google Scholar CrossRef Search ADS PubMed  Takahashi S Badger MR . 2011. Photoprotection in plants: a new light on photo-system II damage. Trends in Plant Science  16, 53– 60. Google Scholar CrossRef Search ADS PubMed  Triantaphylidès C Krischke M Hoeberichts FA Ksas B Gresser G Havaux M Van Breusegem F Mueller MJ . 2008. Singlet oxygen is the major reactive oxygen species involved in photooxidative damage to plants. Plant Physiology  148, 960– 968. Google Scholar CrossRef Search ADS PubMed  Traas J Monéger F . 2010. Systems biology of organ initiation at the shoot apex. Plant Physiology  152, 420– 427. Google Scholar CrossRef Search ADS PubMed  Turgeon R . 1989. The sink–source transition in leaves. Annual Review of Plant Physiology and Plant Molecular Biology  40, 119– 138. Google Scholar CrossRef Search ADS   Tzvetkova-Chevolleau T Frank F Alawady AE Dalla’Osto L Carrière F Bassi R Grimm B Nassaume L Havaux M . 2007. The light stress-indiced protein ELIP2 is a regulator of chlorophyll synthesis in Arabidopsis thaliana. The Plant Journal  50, 795– 809. Google Scholar CrossRef Search ADS PubMed  van der Graaff E Schwacke R Schneider A Desimone M Flugge U-I Kunze R . 2006. Transcription analysis of Arabidopsis membrane transporters and hormone pathways during developmental and induced leaf senescence. Plant Physiology  141, 776– 792. Google Scholar CrossRef Search ADS PubMed  Werner T Schmülling T . 2009. Cytokinin action in plant development. Current Opinion in Plant Biology  12, 527– 538. Google Scholar CrossRef Search ADS PubMed  Wingler A Marès M Pourtau N . 2004. Spatial patterns and metabolic regulation of photosynthetic parameters during leaf senescence. New Phytologist  161, 781– 789. Google Scholar CrossRef Search ADS   Wingler A Purdy S MacLean JA Pourtau N . 2006. The role of sugars in integrating environmental signals during the regulation of leaf senescence. Journal of Experimental Botany  57, 391– 399. Google Scholar CrossRef Search ADS PubMed  Yoshida S Mandel T Kuhlemeier C . 2011. Stem cell activation by light guides plant organogenesis. Genes and Development  25, 1439– 1450. Google Scholar CrossRef Search ADS PubMed  Zeng Q Chen X Wood AJ . 2002. Two early light-inducible protein (ELIP) cDNAs from the resurrection plant Tortula ruralis are differentially expressed in response to desiccation, rehydration, salinity and high-light. Jorunal of Experimental Botany  53, 1197– 1205. Google Scholar CrossRef Search ADS   Zimmermann P Zentgraf U . 2005. The correlation between oxidative stress and leaf senescence during plant development. Cellular and Molecular Biology Letters  10, 515– 534. Google Scholar PubMed  © The Author [2013]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved. For permissions, please email: journals.permissions@oup.com
TI - Photo-oxidative stress in emerging and senescing leaves: a mirror image?
JF - Journal of Experimental Botany
DO - 10.1093/jxb/ert174
DA - 2013-07-03
UR - https://www.deepdyve.com/lp/oxford-university-press/photo-oxidative-stress-in-emerging-and-senescing-leaves-a-mirror-image-ZGP8hJfwFF
SP - 3087
EP - 3098
VL - 64
IS - 11
DP - DeepDyve
ER -