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First published online November 10, 2006; 10.1104/pp.106.091355 Plant Physiology 143:434-446 (2007) © 2007 American Society of Plant Biologists OPEN ACCESS ARTICLE
Genetic Variation Suggests Interaction between Cold Acclimation and Metabolic Regulation of Leaf Senescence1,[W],[OA]Unité de Nutrition Azotée des Plantes, Institut National de la Recherche Agronomique, F–78026 Versailles cedex, France (C.M.-D., T.L.); Department of Biology, University College London, London WC1E 6BT, United Kingdom (S.P., N.P., A.W.); and Unité de Recherche en Génomique Végétale/Institut National de la Recherche Agronomique/Centre National de la Recherche Scientifique, Université d'Evry Val d'Essonne, F–91057 Evry cedex, France (L.T., J.-P.R.)
The extent to which leaf senescence is induced by nitrogen deficiency or by sugar accumulation varies between natural accessions of Arabidopsis (Arabidopsis thaliana). Analysis of senescence in plants of the Bay-0 x Shahdara recombinant inbred line (RIL) population revealed a large variation in developmental senescence of the whole leaf rosette, which was in agreement with the extent to which glucose (Glc) induced senescence in the different lines. To determine the regulatory basis of genetic differences in the Glc response, we investigated changes in gene expression using Complete Arabidopsis Transcriptome MicroArray (CATMA) analysis. Genes whose regulation did not depend on the genetic background, as well as genes whose regulation was specific to individual RILs, were identified. In RIL 310, a line that does not show the typical senescence response to Glc, stress response genes, especially those responding to cold stress, were induced by Glc. We therefore tested whether cold acclimation delays senescence by reducing sugar sensitivity. In cold-acclimated plants, leaf senescence was severely delayed and Glc did not induce the typical senescence response. Together, our results suggest that cold acclimation extends rosette longevity by affecting metabolic regulation of senescence, thereby allowing vernalization-dependent plants to survive the winter period. The role of functional chloroplasts and of nitrogen and phosphate availability in this regulation is discussed.
The timing of leaf senescence is an important life history trait. Early onset of senescence could severely impair photosynthetic carbon gain, whereas late senescence could inhibit senescence-dependent nutrient recycling (Himelblau and Amasino, 2001  ), which is important for the growth of young leaves and for fruit and seed formation (Levey and Wingler, 2005; Wingler et al., 2005). When plants are aging, their shoot carbon-to-nitrogen ratio increases as a result of nitrogen dilution. Physiological studies have shown that peaks in sugar content in tobacco (Nicotiana tabacum) and Arabidopsis (Arabidopsis thaliana) leaves coincide with the onset of senescence (Masclaux et al., 2000; Diaz et al., 2005). In addition, an external supply of Glc results in leaf yellowing (Wingler et al., 2004), indicating an induction of senescence by sugar accumulation. Affymetrix GeneChip analysis of gene expression has confirmed that Glc induces changes in gene expression that are typical of developmental leaf senescence (Pourtau et al., 2006).
In Arabidopsis, considerable variation in the regulation of senescence can be found in accessions from different geographic origins (Levey and Wingler, 2005
Using RILs from the Bay-0 x Sha population with different senescence phenotypes, we have shown that amino acid and sugar content can be used as markers for the timing and extent of senescence of the first six leaves during nitrogen starvation (Diaz et al., 2005
Natural variation has also been described for freezing tolerance of Arabidopsis accessions. QTL analysis using a Landsberg erecta x Cape Verde Islands population showed that allelic variation in a transcription factor gene, C-repeat binding factor (CBF) 2, which is involved in the regulation of cold acclimation, underlies a major QTL for freezing tolerance (Alonso-Blanco et al., 2005 To investigate the basis of natural variation in the metabolic regulation of senescence, we determined the effect of sugar supply on metabolite content and on gene expression in RILs with contrasting sugar response. Complete Arabidopsis Transcriptome MicroArray (CATMA) analysis indicated that cold-responsive genes were induced by Glc in the sugar-insensitive RIL 310. We also investigated the impact of cold acclimation on the regulation of senescence.
Senescence of the Leaf Rosette
RILs with contrasting senescence phenotypes have previously been identified in the Bay-0 x Sha population based on the senescence of their first six leaves during nitrogen starvation (Diaz et al., 2005
Typical Arabidopsis Genes That Are Regulated by Glc during Senescence
The difference in senescence response to Glc between the RILs indicates genetic variation in the regulation of senescence. To identify genes that are commonly regulated, independent of the genetic background, we used CATMA analysis to determine changes in gene expression in response to Glc. CATMA combines a large dynamic range with good sensitivity and high specificity (Hilson et al., 2004 The set of coregulated genes can be used to determine gene functions that are up- or down-regulated during Glc-induced senescence (Fig. 3 ). About one-fourth of down-regulated genes were photosynthetic genes, mainly those involved in the light reactions, but also genes for Calvin cycle enzymes. In particular, genes encoding PSI proteins were overrepresented in the group of down-regulated genes compared to all pathways. There were also more genes for transport and cell wall composition down- than up-regulated. Pathways overrepresented in the group of up-regulated genes include several transcription factor genes in the RNA bin and genes involved in signaling. Genes for protein synthesis, degradation, and modification and for secondary metabolism were also induced by Glc. Only three stress genes (two down-regulated and one up-regulated) were found in the list of genes showing common regulation in all RILs.
It was surprising that typical senescence-associated genes (SAGs), such as SAG12 and production of anthocyanin pigment 2 (PAP2), were also induced in RIL 310 despite the lack of the typical Glc response. Indeed, induction of SAG12 was only statistically significant in one of the biological replicates. In addition, the regulation of typical SAGs in RIL 310 varied between different experiments. Whereas induction of SAG12 and PAP2 by Glc was confirmed for RIL 45, RIL 232, and the parental lines Bay-0 and Sha in an independent experiment, SAG12 was expressed in the absence of Glc in RIL 310 (Supplemental Fig. S1). This is in agreement with chlorosis of the first leaves often observed in the absence of Glc in RIL 310 (Fig. 1B).
To investigate what caused the differences in the senescence response to Glc, genes whose regulation was specific to the RILs were identified (Supplemental Table S1). For the line with an intermediate senescence phenotype, RIL 232, the number of specific genes was small (29 in total; nine genes repressed and 20 genes induced by Glc treatment). More genes were specifically regulated in the RILs with extreme senescence phenotypes; 183 genes were specifically regulated in RIL 45 and most of these genes were repressed (156 repressed, 27 induced). For RIL 310, 233 specifically regulated genes were found (98 repressed and 135 induced).
A large number of stress genes were up-regulated by Glc in RIL 310. To investigate further how RIL 310 is affected by stress, we analyzed the stress response of the genes induced by Glc in RIL 310 using Genevestigator (Zimmermann et al., 2004
Despite its delayed senescence phenotype and high photosynthetic efficiency on Glc, an unexpectedly large number of photosynthetic genes were down-regulated by Glc in RIL 310 (Table II ). Most of these genes are chloroplast-encoded genes involved in the light reactions of photosynthesis. In addition to photosynthetic genes, genes for protein synthesis in the chloroplasts, both chloroplast and nuclear encoded, were repressed by Glc.
A separate group of photosynthetic genes (21 genes) was down-regulated by Glc in RIL 45 (Supplemental Table S1). In the case of RIL 45, this effect is in agreement with the strong senescence response of RIL 45 to Glc. Another interesting feature of gene regulation in RIL 45 was that three usually sugar-inducible genes involved in the response to biotic stress were repressed by Glc (At1g75040 = PR5; At2g43570, a chitinase gene; At1g73260, a Kunitz family protein).
Because Glc only induces senescence in combination with low, but not high, nitrogen supply (Wingler et al., 2004
Growth in the presence of Glc resulted in a slight, but insignificant, increase in amino acid content in Bay-0, Sha, RIL 310, and RIL 232 (Fig. 5 ). The relative content of Glu and Asp and of minor amino acids (data not shown) largely followed the changes in total amino acids and was thus not affected to a great extent by Glc treatment. There were, however, clear effects on the proportion of Arg and Pro. Whereas the relative content of Arg decreased in all lines with sugar feeding, Pro accumulated. There was also an increase in the proportion of Val in all lines, whereas Asn was reduced after growth on Glc in the more senescent lines Bay-0 and RIL 45.
In RIL 310, the total amino acid content was higher than in the other lines. This effect was statistically significant in comparison with all lines but RIL 232. The most striking difference between RIL 310 and the other lines was an increased Gly-to-Ser ratio on medium without Glc, which could indicate increased rates of photorespiration. High ammonium content in RIL 310 (data not shown) supports this assumption. In the absence of Glc, Arg content was also increased in RIL 310. In addition, RIL 310 contained more Gln than the other lines. Overall, the higher total amino acid content and increase in Gln suggest that internal nitrogen availability was high in RIL 310.
In addition to sugar accumulation, nitrogen starvation can induce leaf senescence and regulation of senescence mainly depends on the relative availability of nitrogen and carbon (Pourtau et al., 2004
Effect of Cold Acclimation
Because leaves that have developed in the cold do not show the typical down-regulation of photosynthesis in response to sugar accumulation (Strand et al., 1997
Whole-rosette senescence varied considerably between lines, but similar line-specific differences were found after growth in compost and on Glc-containing agar medium (Fig. 1). Fv/Fm data (Fig. 7) confirmed our previous observation that senescence is very strongly induced by Glc in RIL 45, but not in RIL 310, with RIL 232 showing an intermediate phenotype (Diaz et al., 2005 ). Surprisingly, the whole-rosette senescence phenotype is opposite to senescence of the first six leaves of plants grown at low nitrogen supply (Diaz et al., 2005). Whereas the first six leaves of RIL 310 senesce early in the absence of Glc, this line then continues to produce dark-green, late-senescing leaves and flowers late. In contrast, the first leaves of RIL 45 senesce late, but this line produces fewer leaves and flowers early, resulting in a reduced lifespan. The contrasting senescence characteristics of the first leaves and leaves formed later during development show that the regulation of senescence can vary depending on leaf position. Zentgraf et al. (2004) found that gene expression is not only influenced by leaf age, but also by plant age, indicating that leaves of different positions senesce in different ways. This may also help explain the conundrum of why an inverse relationship was found between QTL for senescence of the first six leaves and carbohydrate content (Calenge et al., 2006), despite the ability of sugars to induce senescence.
Leaf senescence is a complex process that can be triggered by a range of environmental and age-related factors. It is therefore not surprising that, depending on the cause of leaf senescence, different pathways are induced. Buchanan-Wollaston et al. (2005)
So far, gene expression profiling during senescence has focused on single accessions. Our results on the variation of senescence between the RILs and parental lines (Fig. 1) do, however, suggest that regulation of senescence can vary significantly, not only in response to different environmental conditions, but also depending on the genetic background. In an experiment comparing gene expression with and without salicylic acid treatment in several Arabidopsis accessions, Kliebenstein et al. (2006)
We also identified genes that were regulated in the same way in all lines. These can serve as a core set of genes that respond to sugars during senescence (Fig. 3). For RIL 45, RIL 232, and the parental accessions Bay-0 and Sha, the response of these genes was confirmed in an independent experiment (Supplemental Fig. S1). However, some variation in gene expression in the absence of Glc was found in RIL 310, which, when grown without sugar, often showed chlorosis of the first leaves. Especially for the up-regulated genes, there was also a good agreement of CATMA results shown here with the Affymetrix GeneChip data on sugar-induced senescence in the Ws-2 accession. Although the dynamic range of CATMA is larger than that of the Affymetrix ATH1 GeneChip (Allemeersch et al., 2005
Senescence is not induced in Arabidopsis plants grown on Glc in the presence of high nitrogen supply (Wingler et al., 2004
The late-senescing line RIL 310 had the highest amino acid content of all lines (Fig. 5) and also high protein content (data not shown). In particular, high content of Arg (on medium without Glc) and Gln (on both media) suggests that nitrogen storage capacity is high in RIL 310. This could explain why this line does not respond to Glc in the same way as the other lines, despite containing large amounts of Glc, Fru, and Suc (Fig. 4). Although, the relative Pro content (as a proportion of total amino acids) was higher in Bay-0 than in RIL 310 after growth on Glc, the absolute Pro content was highest in RIL 310 due to the overall increased amino acid content in this line. In addition to a high carbon-to-nitrogen ratio, stress conditions, such as cold stress or drought, induce Pro synthesis by induction of P5CS (Svensson et al., 2006
The Gly-to-Ser ratio can serve as a predictive marker of senescence (Diaz et al., 2005
In the presence of Glc, RIL 310 had the highest chlorophyll content (Fig. 1) and functional chloroplasts, as indicated by the Fv/Fm values (Table III
; Fig. 7). The down-regulation of genes for photosynthesis, plastid protein synthesis, and chloroplast-encoded genes in RIL 310 (Table II) is therefore difficult to interpret. However, synthesis of chloroplast-encoded proteins is not necessarily related to transcript abundance. In Chlamydomonas, a drop of 90% in chloroplast transcript did not affect synthesis of chloroplast proteins (Eberhard et al., 2002
In RIL 310, cold-response genes were induced by Glc (Table I; Supplemental Fig. S1). Complex interactions exist between chloroplast function and cold acclimation. Functional chloroplasts are required for cold acclimation and also for regulation of the majority of cold-responsive genes, probably because the induction of cold acclimation depends on PSII excitation pressure (Ensminger et al., 2006 ). Using barley (Hordeum vulgare) mutants in chloroplast development, Svensson et al. (2006) showed that only 11% of genes regulated by cold treatment in wild-type barley were also regulated to a similar extent in mutants in chloroplast development. Maintained chloroplast function could explain why cold-responsive genes were more strongly induced by Glc in RIL 310 than in the other lines, which showed stronger senescence-dependent decline in photosynthesis. In barley, up-regulation of genes under CBF control is, however, not chloroplast dependent (Svensson et al., 2006). Nine genes involved in redox regulation were also specifically regulated in RIL 310 (Supplemental Table S1). This could, for example, indicate induction of the cold response due to oxidative stress (Prasad et al., 1994; Svensson et al., 2006) or a redox signal. Furthermore, induction of some of the cold-responsive genes by Glc in all lines may suggest that cold-dependent sugar accumulation could be part of a feed-forward loop in the cold acclimation pathway. It is possible that this sugar effect is mediated by changes in amino acid content, such as Pro or Arg (Fig. 5).
Our results show that senescence is severely delayed in plants grown at 5°C, both in compost and on Glc-containing agar medium (Figs. 1, 2, and 7). This is in agreement with the observation that leaves that have developed in the cold do not show repression of photosynthesis, despite sugar accumulation (Strand et al., 1997 Transfer of seedlings to 5°C resulted in a temporary decline in Fv/Fm in all lines, showing that, without acclimation, RIL 310 was not more cold tolerant than the other lines. In addition, the presence of Glc had no impact on the extent of the decline in Fv/Fm. This suggests that only part of the typical cold acclimation response was induced by Glc in RIL 310, resulting in decreased sugar sensitivity, but not in increased cold hardening. Because changes in amino acid content could be involved in this regulation, it would be interesting to determine the effect of cold acclimation on senescence in response to varied nitrogen availability.
In contrast to nitrogen deficiency, phosphate deficiency decreases sugar sensitivity (Nielsen et al., 1998 In conclusion, our results show that leaf senescence is controlled by interactions between sugar and nitrogen signaling with the cold acclimation pathway. Chloroplast signals, as well as phosphorus availability, are likely to affect this signaling interaction.
Plant Material
RILs with contrasting senescence phenotypes (Diaz et al., 2005
For growth under low and high nitrogen conditions, seeds were stratified and sown as described by Diaz et al. (2005)
Maximal photosynthetic efficiency (Fv/Fm) was determined nondestructively for the whole rosettes of Arabidopsis plants using a pulse-modulated imaging fluorometer (FluorCam 700MF; Photon Systems Instruments) as described by Wingler et al. (2004)
Two independent biological replicates were cultivated for 25 d on agar medium. Leaf rosettes of approximately 12 plants for each replicate were harvested at midday by removing the roots and inflorescences with a razor blade and immediately frozen in liquid nitrogen. Total RNA was extracted according to Logemann et al. (1987)
Microarray hybridizations were performed with CATMA (Crowe et al., 2003
Statistical analysis was based on two dye swaps per comparison, one for each replicate. For each array, the raw data comprised the logarithm of median feature pixel intensity at wavelengths 635 nm (red) and 532 nm (green). No background was subtracted. In the following description, log-ratio refers to the differential expression between the different treatments. It is either log2 (red/green) or log2 (green/red) according to the experimental design. An array-by-array normalization was performed to remove systematic biases. First, we excluded spots that were considered to show badly formed features by the experimenter. Then we performed a global intensity-dependent normalization using the LOESS procedure (Yang et al., 2002
Pathways that are overrepresented in response to Glc compared to all pathways were determined using the Overview function of MapMan (Usadel et al., 2005
For RT-PCR, plant material was harvested after growth on agar medium as for CATMA analysis, however, at day 30, due to the slightly later onset of senescence in this particular experiment. RNA was extracted by homogenizing plant material in TRIzol reagent (Invitrogen) using a FP220 ribolyzer (Q-Biogene). RNA was isolated according to the TRIzol protocol (Invitrogen). cDNA was synthesized as in Pourtau et al. (2006) For plants grown on unfertilized compost and watered with 2 or 10 mM nitrate, whole rosettes were harvested at days 27 and 36 after sowing. The cycle numbers in the PCR reaction were 28 cycles for GER1 (At1g72610), 32 cycles for the jacalin gene (At2g39330), 30 cycles for ASN2 (At5g65010), 28 cycles for GS2 (At5g35630), and 30 cycles for SAG12 (At5g45890). PCR products were quantified after gel imaging using a Bio-Rad GelDoc 1000 camera (Bio-Rad) and the MultiGauge FujiFilm image analyzer (Fujifilm) and corrected using the signal obtained for 18S rRNA (At3g41768 and At2g01010; constitutive control).
Leaf rosettes for sugar and amino acid analysis were harvested after 30 d at midday. Roots and inflorescences were cut off and the rosettes frozen in liquid nitrogen. Sugars were extracted in hot (80°C) 80% ethanol and determined using enzymatic essays according to Stitt et al. (1989)
Amino acid content in leaf rosettes was determined after extraction in 2% 5-sulfosalicylic acid (50 mg mL–1fresh weight). Total amino acid content was assayed by the Rosen colorimetric method using Gln as a reference (Rosen, 1957
The following materials are available in the online version of this article.
We thank Thushyanthi Sivagnanam (University College London) for excellent technical assistance. We also wish to thank Åsa Strand (Umeå University) for helpful suggestions concerning the interactions between cold acclimation and chloroplast function. Received October 17, 2006; accepted November 7, 2006; published November 10, 2006.
1 This work was supported by the Biotechnology and Biological Sciences Research Council (research grant no. 31/P16341) and a PhD studentship from the Natural Environment Research Council, United Kingdom. The Insititut National de la Recherche Agronomique and the Centre National de la Recherche Scientifique provided extra financial support for the Complete Arabidopsis Transcriptome MicroArray. 
2 Present address: Unité Mixte de Recherches 6553, Centre National de la Recherche Scientifique, Ecobio, Université de Rennes 1, Campus Scientifique de Beaulieu, Bat. 14A, F–35042 Rennes cedex, France. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Astrid Wingler (a.wingler{at}ucl.ac.uk).
[W] The online version of this article contains Web-only data.
[OA] Open Access articles can be viewed online without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.106.091355 * Corresponding author; e-mail a.wingler{at}ucl.ac.uk; fax 44–20–7679–7096.
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1-pyrroline-5-carboxylate synthetase (P5CS), a rate-limiting enzyme in the synthesis of Pro from Glu, is induced, resulting in increased Pro formation and reduced Glu availability for Arg synthesis (Verma and Zhang, 1999
