Effect of sugar-induced senescence on gene expression and implications for the regulation of senescence in Arabidopsis

Abstract

There has been some debate whether leaf senescence is induced by sugar starvation or by sugar accumulation. External supply of sugars has been shown to induce symptoms of senescence such as leaf yellowing. However, it was so far not clear if sugars have a signalling function during developmental senescence. Glucose and fructose accumulate strongly during senescence in Arabidopsis thaliana (L.) Heynh. leaves. Using Affymetrix GeneChip analysis we determined the effect of sugar-induced senescence on gene expression. Growth on glucose in combination with low nitrogen supply induced leaf yellowing and changes in gene expression that are characteristic of developmental senescence. Most importantly, the senescence-specific gene SAG12, which was previously thought to be sugar-repressible, was induced over 900-fold by glucose. Induction of SAG12, which is expressed during late senescence, demonstrates that processes characteristic for late stages are sugar-inducible. Two MYB transcription factor genes, PAP1 and PAP2, were identified as senescence-associated genes that are induced by glucose. Moreover, growth on glucose induced genes for nitrogen remobilisation that are typically enhanced during developmental senescence, including the glutamine synthetase gene GLN1;4 and the nitrate transporter gene AtNRT2.5. In contrast to wild-type plants, the hexokinase-1 mutant gin2-1 did not accumulate hexoses and senescence was delayed. Induction of senescence by externally supplied glucose was partially abolished in gin2-1, indicating that delayed senescence was a consequence of decreased sugar sensitivity. Taken together, our results show that Arabidopsis leaf senescence is induced rather than repressed by sugars.

Dynamic Acclimation of Photosynthesis Increases Plant Fitness in Changing Environments

“…Previous studies have shown that this gene is induced under conditions of sugar feeding and during sugar-induced senescence (Gonzali et al, 2006;Li et al, 2006;Pourtau et al, 2006). In vitro evidence shows that this gene product is a functional sugar phosphate/phosphate translocator, with activity for triose-and hexose-Ps (Knappe et al, 2003).…”

“…It functions in vitro to transport both Glc-6-P and triose-P in exchange for phosphate (Knappe et al, 2003). Reported expression levels have typically been low, though it has been identified as being up-regulated in response to sugar feeding (Gonzali et al, 2006;Li et al, 2006) and during leaf senescence (Pourtau et al, 2006). In the Col-0 ecotype, which is unable to acclimate dynamically but which expresses the GPT2 gene, it was reported that gpt22 mutants grow normally (Niewiadomski et al, 2005).…”

Comprehensive Dissection of Spatiotemporal Metabolic Shifts in Primary, Secondary, and Lipid Metabolism during Developmental Senescence in Arabidopsis

“…However, their roles in senescence remain controversial (Noodén, 1980;Yoshida, 2003;van Doorn, 2004van Doorn, , 2008Wingler et al, 2006Wingler et al, , 2009, since both sugar starvation and addition can induce SAG expression (Gan and Amasino, 1997;Fujiki et al, 2000Fujiki et al, , 2001van Doorn, 2004). Furthermore, although the decline of photosynthesis that occurs during senescence should lead to a decrease of sugar levels, an increase of sugars during senescence was reported in several plant species, including Arabidopsis (Masclaux et al, 2000;Quirino et al, 2001;Stessman et al, 2002;Diaz et al, 2005;Masclaux-Daubresse et al, 2005, 2007Pourtau et al, 2006;Wingler et al, 2006Wingler et al, , 2012. These data are in accordance with the results obtained here in the wholeplant experiment, where we observed an increase of sugar levels in leaves during developmental senescence (Fig.…”

“…Therefore, in order to consider the evidence of specific roles for metabolites in senescence, a more precise analysis of metabolite levels in different tissues and cell types during the process of senescence is required. Although, to date, a number of targeted metabolite profiles, particularly those focused on lipids as seed storage compounds (Yang and Ohlrogge, 2009;Seltmann et al, 2010) and sugars, amino acids, and nutrient ions (Masclaux et al, 2000;Quirino et al, 2001;Stessman et al, 2002;Diaz et al, 2005;Masclaux-Daubresse et al, 2005, 2007Pourtau et al, 2006;Wingler et al, 2006Wingler et al, , 2012, have been generated from maturing and senescing tissues, a broad overview of metabolic changes during senescence, including the interactions between various metabolic pathways, is still lacking. Therefore, we performed a metabolomics study to obtain comprehensive metabolite profiles, including primary and secondary metabolites and lipids, over the course of developmental senescence in rosette leaves before and after bolting and siliques of Arabidopsis in order to investigate the metabolic response and spatiotemporal distribution of metabolites during senescence at the whole-plant level and within single leaves.…”

Acclimation of metabolism to light in Arabidopsis thaliana: the glucose 6‐phosphate/phosphate translocator GPT2 directs metabolic acclimation

“…2010) and during senescence (Pourtau et al . 2006). Taken together, these results are consistent with GPT2 expression being induced in response to an accumulation of sugars in the cell.…”