Pathway analysis of the transcriptome and metabolome of salt sensitive and tolerant poplar species reveals evolutionary adaption of stress tolerance mechanisms

Abstract

BackgroundPopulus euphratica is a salt tolerant and Populus × canescens a salt sensitive poplar species. Because of low transcriptional responsiveness of P. euphratica to salinity we hypothesized that this species exhibits an innate activation of stress protective genes compared with salt sensitive poplars. To test this hypothesis, the transcriptome and metabolome of mature unstressed leaves of P. euphratica and P. × canescens were compared by whole genome microarray analyses and FT-ICR-MS metabolite profiling.ResultsDirect cross-species comparison of the transcriptomes of the two poplar species from phylogenetically different sections required filtering of the data set. Genes assigned to the GO slim categories 'mitochondria', 'cell wall', 'transport', 'energy metabolism' and 'secondary metabolism' were significantly enriched, whereas genes in the categories 'nucleus', 'RNA or DNA binding', 'kinase activity' and 'transcription factor activity' were significantly depleted in P. euphratica compared with P. × canescens. Evidence for a general activation of stress relevant genes in P. euphratica was not detected. Pathway analyses of metabolome and transcriptome data indicated stronger accumulation of primary sugars, activation of pathways for sugar alcohol production, and faster consumption of secondary metabolites in P. euphratica compared to P. × canescens. Physiological measurements showing higher respiration, higher tannin and soluble phenolic contents as well as enrichment of glucose and fructose in P. euphratica compared to P. × canescens corroborated the results of pathway analyses.ConclusionP. euphratica does not rely on general over-expression of stress pathways to tolerate salt stress. Instead, it exhibits permanent activation of control mechanisms for osmotic adjustment (sugar and sugar alcohols), ion compartmentalization (sodium, potassium and other metabolite transporters) and detoxification of reactive oxygen species (phenolic compounds). The evolutionary adaptation of P. euphratica to saline environments is apparently linked with higher energy requirement of cellular metabolism and a loss of transcriptional regulation.

Metabolic Interaction between Anthocyanin and Lignin Biosynthesis Is Associated with Peroxidase FaPRX27 in Strawberry Fruit

“…Combining metabolite profiling data with gene expression analyses has provided unique and comprehensive overviews of the transcriptional regulation of metabolic shifts, responses to plant hormones, as well as adaption of stress tolerance mechanisms (YonekuraSakakibara et al, 2008;Janz et al, 2010;Kogel et al, 2010;Stushnoff et al, 2010;Rohrmann et al, 2011;Zifkin et al, 2012). In this study, a custom-made oligonucleotidebased microarray platform (Roche-NimbleGen) was employed for the comprehensive investigation of differential gene expression in strawberry varieties that were selected by metabolite profiling analysis due to their opposite levels of phenolics ( Fig.…”

Life at the extreme: lessons from the genome

“…In some cases, they have been inferred from the primary sequences of well-characterized genes, such as the 37-amino-acid stretch in L -myo-inositol-1-phosphate synthase, which distinguishes the salt-tolerant wild rice ( Porteresia coarctata ) from domesticated rice ( Oryza sativa ) [11], or the single-amino-acid variation in AtHKT1;1 (which encodes the high-affinity K + transporter 1) that distinguishes coastal from inland clines of Arabidopsis [12]. In other cases, they have been implicated by the constitutively higher expression - in the absence of stress - of genes that are induced by stress in Arabidopsis , as in the resurrection plant Craterostigma plantagineum [13], the salt-tolerant poplar Populus euphratica [14], or the Arabidopsis relatives T. parvula and Thellungiella salsuginea (formerly T. halophila ) [15-17]. …”

Linking the Salt Transcriptome with Physiological Responses of a Salt-Resistant Populus Species as a Strategy to Identify Genes Important for Stress Acclimation

“…The complete protocols for probe labeling and hybridization, normalized data, and raw data files are available from the ArrayExpress database (www.ebi.ac.uk/arrayexpress/) under the accessions of E-MEXP-2095. By the use of P. euphratica arrays, problems that may arise by low hybridization efficiencies caused by sequence divergence are avoided (Janz et al, 2010).…”

“…Using microarrays with this collection of stress-responsive genes, Brosché et al (2005) found that leaves of mature desert-grown P. euphratica trees acclimated to high salinity show only a few differentially expressed genes compared with tapwatered control trees. Salt-acclimated Euphrat poplars show less gene regulation than salt-sensitive poplar species (Ding et al, 2010), probably because transporters important to control excessive salt accumulation and the flavonoid/phenylpropanoid pathway, which may counteract negative salt effects by controlling reactive oxygen species, are constitutively upregulated in the tolerant poplar species (Janz et al, 2010). However, it is still unclear which early molecular responses are required to adjust the metabolism to life at a new level of osmotic balance and ionic stress.…”