JXB Advance Access published online on March 10, 2009
Journal of Experimental Botany, doi:10.1093/jxb/erp067
eXtra Botany |
Sugars, senescence, and ageing in plants and heterotrophic organisms
1Research Department of Genetics, Evolution and Environment, Darwin Building, University College London, Gower Street, London WC1E 6BT, UK
2Unité de la Nutrition Azotée des Plantes, UR511, INRA Versailles, Route de St Cyr, F-78000 Versailles, France
3Department of Plant Sciences and Plant Pathology, Montana State University, Bozeman, MT 59717-3150, USA
* To whom correspondence should be addressed: E-mail: a.wingler{at}ucl.ac.uk
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Abstract |
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 Top Abstract Evidence for an involvement...Supplementary dataReferences |
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Although an involvement of metabolic signals in the regulation of plant senescence has been demonstrated in a range of studies, the exact signalling pathways remain largely unresolved. For leaves, evidence supports a role of sugar accumulation in the initiation and/or acceleration of senescence. However, regulation of senescence or ageing may respond to different metabolic signals in heterotrophic plant organs and heterotrophic organisms. In animals and yeast, dietary restriction results in increased lifespan. In this article, the metabolic regulation of leaf senescence is compared with the effects of dietary restriction. Similarities and differences in the signalling pathways are discussed, including the role of autophagy, TOR (target of rapamycin), Sir2 (silent information regulator-2), and SnRK1 (sucrose non-fermenting-1-related protein kinase-1).
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Evidence for an involvement of sugars in the regulation of leaf senescence |
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TopAbstractEvidence for an involvement...Supplementary dataReferences |
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Leaf senescence is a plastic process that can be triggered by a variety of external and internal factors (Buchanan-Wollaston et al., 2003). Senescence reduces photosynthetic carbon fixation, but is important for the recycling of nitrogen and other nutrients, for example, resulting in increased grain protein (Uauy et al., 2006). Due to its position at the crossroads of carbon and nitrogen metabolism, senescence is regulated by carbon and nitrogen signals. Increasing evidence suggests a role for hexose accumulation in ageing leaves as a signal for either senescence initiation or acceleration in annual plants (Masclaux et al., 2000; Moore et al., 2003; Masclaux-Daubresse et al., 2005; Parrott et al., 2005, 2007; Pourtau et al., 2006; Wingler and Roitsch, 2008).
Recently, the role of sugar accumulation or starvation in leaf senescence has been critically evaluated by van Doorn (2008). This author has pointed out that little is known about sugar concentrations and senescence regulation in different tissues and cells. While we agree with the view that sugars may not always be the direct cause of leaf senescence, sufficient evidence supports the notion that sugar signalling plays a role in senescence regulation in a complex network with a variety of other signals, for example, resulting from biotic or abiotic stress (Wingler and Roitsch, 2008).
In addition to sugar accumulation, dark treatment induces leaf yellowing. This treatment can result in starvation, but is also likely to signal via light signalling pathways. It is not surprising that expression of genes involved in downstream processes, such as proteolysis, overlap between senescence initiated by different treatments that result in sugar accumulation or starvation. The senescence-specific cysteine protease gene SAG12 has been shown to be induced (Pourtau et al., 2006; Parrott et al., 2007) or repressed (Noh and Amasino, 1999) by sugars during senescence, but the behaviour of single genes, which may respond after senescence has been initiated, cannot necessarily tell us whether senescence is sugar- or starvation-induced. Comparison of overall changes of the transcriptome (Buchanan-Wollaston, 2005; Wingler and Roitsch, 2008) is a better way of testing whether senescence is regulated by starvation, darkness or sugar accumulation.
To compare different treatments, microarray results for experiments using the Arabidopsis Affymetrix ATH1 array were clustered (Fig. 1). Global changes in response to glucose treatment (Pourtau et al., 2006) clustered closely with changes during developmental leaf senescence (Schmid et al., 2005) when glucose was supplied to intact plants in combination with low nitrogen supply, but less closely in combination with high nitrogen supply, a treatment that does not induce visible senescence. Accumulation of sugars due to a mutation in the SUC2 sucrose transporter gene (pho3 mutant; Lloyd and Zakhleniuk, 2004) clustered with the experiments in which glucose was supplied externally. Interestingly, gene expression changes during dark-induced senescence (Lin and Wu, 2004) did not cluster with developmental senescence, but with the effect of starvation in cell cultures (Contento et al., 2004). This supports the view that high sugar/low nitrogen conditions and not starvation and/or dark trigger changes in gene expression that are characteristic of developmental leaf senescence.
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Changes in gene expression induced by steam girdling of barley leaves (Parrott et al., 2007), which results in internal sugar accumulation, demonstrate that this regulation is not restricted to Arabidopsis leaves. However, in contrast to leaves, senescence or senescence-like symptoms (including enhanced proteolysis) are delayed by sugar feeding in isolated heterotrophic plant tissues such as root tips (James et al., 1993), suggesting that different signalling responses are triggered by the carbohydrate status of auto- and heterotrophic plant tissues. To understand such differences fully, a systematic comparison of the transcriptomic responses of plant cell cultures, dark-incubated leaves and different types of heterotrophic tissues to carbohydrate status would be beneficial.
The role of autophagy in the metabolic regulation of leaf senescence
Autophagy is an evolutionarily conserved process contributing to the degradation of macromolecules in animals, yeasts, and plants. In animals and yeasts, autophagy is a regulated process for the removal of damaged proteins and organelles. In plants, autophagy has been shown to occur during sucrose starvation, nitrogen deficiency, and senescence (Bassham et al., 2006). Recently, it has been demonstrated that autophagy is required for the senescence-dependent degradation of Rubisco (Ishida et al., 2008). Mutations in autophagy genes can, however, result in accelerated rather than delayed senescence (Thompson et al., 2005), suggesting that autophagy is essential for nutrient remobilization before the onset of visible senescence and, possibly, for waste removal as in animals. While autophagy is generally considered to be induced by sugar starvation, statistical analysis using MapMan (Usadel et al., 2005) to identify gene ontologies that respond differently to a treatment than the remaining genes on the array indicates that expression of autophagy genes is not only induced by senescence, dark treatment, and starvation, but also by treatment with glucose in the presence of low nitrogen (see Supplementary Table S1 at JXB online). By contrast, glucose does not induce autophagy genes in the presence of high nitrogen supply. Together with the observation that mutants in autophagy genes are hypersensitive to nitrogen deficiency as well as carbon starvation (Thompson et al., 2005), this indicates that the carbon/nitrogen balance may play an important role in the induction of autophagy. Although autophagy was induced in all treatments resulting in senescence, which autophagy genes were induced varied between the different treatments (see Supplementary Table S2 at JXB online).
Another interesting link between carbon availability, senescence, and autophagy has recently been established by Baena-Gonzáles et al. (2007). This work has demonstrated that the protein kinase SnRK1 (sucrose non-fermenting-1-related protein kinase-1) is involved in the signalling response to carbon depletion. Overexpression of KIN10, encoding the catalytic subunit of SnRK1, increased the expression of normally sugar-repressed genes involved in catabolic pathways and also led to the induction of autophagy genes. Interestingly, KIN10-overexpressing plants showed delayed flowering and senescence. This is consistent with the view that increased carbon availability and not starvation is involved in the initiation of senescence.
Parallels between the metabolic regulation of leaf senescence and the effect of dietary restriction on ageing in heterotrophic organisms
Parallels can be drawn between the metabolic regulation of leaf senescence and the extension of life span by dietary restriction in heterotrophic organisms. While leaf senescence can be monitored as a decline in chlorophyll or photosynthetic function, ageing in heterotrophic organisms is usually a demographic measure, i.e. based on the change in the fraction of individuals alive over time. Although it is more difficult to determine the exact time at which a leaf is dead, senescence usually results in the death of a leaf and can also be monitored as leaf longevity.
Dietary restriction, for example, by dilution of growth media or reduced availability of food, has been shown to extend life span in a large range of organisms, including yeasts, invertebrates, and mammals (reviewed by Mair and Dillin, 2008). Some of the regulatory pathways may be conserved between plants and heterotrophic organisms. For example, SnRK1 is related to Snf1 (sucrose non-fermenting-1) in yeast and AMPK (AMP-activated protein kinase) in animals. In addition to the plant SnRK1 (Baena-Gonzáles et al., 2007), Snf1 (Bitterman et al., 2003) and AMPK (Mair and Dillin, 2008) have been linked to extended life span and dietary restriction.
When energy supply is low, AMPK inhibits processes, such as protein synthesis, by the inhibition of TOR (target of rapamycin). Reduced TOR signalling can result in increased life span (Mair and Dillin, 2008). This suggests a complicated web of interactions between proteins involved in co-ordinating energy status, sugar content, nitrogen availability, cell fate, and longevity. However, the existence of a similar web of interaction remains to be demonstrated in plants (Baena-Gonzáles and Sheen, 2008). Conditional silencing of the Arabidopsis TOR kinase induced early leaf yellowing, chlorophyll degradation, and accumulation of high soluble sugar concentrations. In the same plants, the activity of enzyme markers for nitrogen remobilization was increased, indicating that, in plants, TOR is needed to restrain senescence and nutrient recycling (Deprost et al., 2007).
In addition to the proposed function of reduced TOR signalling in extended life span in response to dietary restriction, it is now well known that, in animals and yeasts, decreased nutrient availability can stimulate autophagy in part by the inhibition of TOR signalling (Finkel et al., 2007). In Caenorhabditis elegans, RNAi inhibition of autophagy genes, in turn, prevented the extension of life span by TOR inhibition or dietary restriction (Hansen et al., 2008). However, the role of autophagy in animals is complex in the sense that it constitutes a stress adaptation that avoids cell death and suppresses apoptosis, whereas, in other circumstances, it constitutes an alternative cell-death pathway (Maiuri et al., 2007). A parallel can be seen in plants, where, despite the role of autophagy in senescence, mutants in autophagy show accelerated senescence and cell death (Thompson et al., 2005). Further characterization of Arabidopsis mutants in autophagy genes could shed more light on the interaction between carbon supply, TOR signalling, and leaf longevity in plants.
Another possible parallel between the regulation of leaf senescence and the effect of dietary restriction on ageing is the involvement of the NAD/NADH ratio. The Arabidopsis onset of leaf death5 (old5) mutant that shows early senescence has recently been identified as a mutant in quinolinate synthase, an enzyme required for the de novo synthesis of NAD (Schippers et al., 2008). In heterotrophic organisms, Sir2 (silent information regulator-2), an NAD-dependent histone deacetylase, is involved in life-span extension in response to dietary restriction. In yeast, low glucose supply has been suggested to extend life span by reducing the NADH concentration and thereby activating Sir2 (Lin et al. 2004). Less is known about the role of Sir2 in plants, but it has been shown that down-regulation of the rice Sir2 orthologue results in premature cell death resembling the hypersensitive response to pathogens (Huang et al., 2007).
While, in yeasts, ageing can be delayed by decreased glucose supply (Bitterman et al., 2003), similar to the proposed role of hexose signalling in leaf senescence, dietary restriction in Drosophila is more responsive to reduced protein or amino acid rather than to reduced sugar supply (Mair et al., 2005; Lee et al., 2008). This is opposite to the effect of nitrogen on plants, where high nitrogen supply inhibits the senescence-inducing effect of glucose (Pourtau et al., 2006). In conclusion, although the molecular processes involved in the regulation of senescence/ageing in response to metabolic signals may be conserved, the signals which they respond to may have diversified reflecting the metabolic requirement (autotrophic/heterotrophic, inorganic/organic nitrogen supply) of different organisms.
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Supplementary data |
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TopAbstractEvidence for an involvement...Supplementary dataReferences |
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Supplementary data can be found at JXB online.
Supplementary Table S1. Statistical analysis of changes in the expression of autophagy genes in Arabidopsis in response to different treatments.
Supplementary Table S2. Changes in the expression of autophagy genes in Arabidopsis in response to different treatments.
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