Shedding light on an extremophile lifestyle through transcriptomics

Abstract

Summary• The tropical intertidal ecosystem is defined by trees -mangroves -which are adapted to an extreme and extremely variable environment. The genetic basis underlying these adaptations is, however, virtually unknown. Based on advances in pyrosequencing, we present here the first transcriptome analysis for plants for which no prior genomic information was available. We selected the mangroves Rhizophora mangle (Rhizophoraceae) and Heritiera littoralis (Malvaceae) as ecologically important extremophiles employing markedly different physiological and life-history strategies for survival and dominance in this extreme environment.• For maximal representation of conditional transcripts, mRNA was obtained from a variety of developmental stages, tissues types, and habitats. For each species, a normalized cDNA library of pooled mRNAs was analysed using GSFLX pyrosequencing.• A total of 537 635 sequences were assembled de novo and annotated as > 13 000 distinct gene models for each species. Gene ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) orthology annotations highlighted remarkable similarities in the mangrove transcriptome profiles, which differed substantially from the model plants Arabidopsis and Populus.• Similarities in the two species suggest a unique mangrove lifestyle overarching the effects of transcriptome size, habitat, tissue type, developmental stage, and biogeographic and phylogenetic differences between them.

Life at the extreme: lessons from the genome

“…Interestingly, despite these species having different life histories and physiological strategies in their adaptation to tropical intertidal habitats, their transcriptomes showed strikingly similar allocations in GO and Kyoto Encyclopedia of Genes and Genomes (KEGG) functional categories, suggesting convergent evolution as 'mangroves' [26]. …”

“…In Lobularia maritima (sweet alyssum), a salt-tolerant coastal relative of Arabidopsis [49], 35% of the salt-induced transcriptome is 'unknown', as are half of the salt-stress-induced transcripts from a facultative halophyte, Festuca rubra ssp. litoralis [50] and nearly 55% of the contigs in two mangrove transcriptomes ( R. mangle and H. littoralis ) [26]. …”

“…Without sequence similarities on which to base annotation, 'orphan genes' usually lack assignable functions [10,26]. Clearly, this is a major obstacle to elucidating the genetic basis for any characteristic, not just for understanding stress tolerance, and overcoming this is an important target.…”

Applications of next generation sequencing in molecular ecology of non-model organisms

“…As an example of this, (Dassanayake et al, 2009) used transcriptome characterization of two species of mangrove to investigate convergent evolution of gene expression. Shared transcriptomic profiles between species may of course be a result of a common evolutionary origin or a joint distribution (Nuzhdin et al, 2004).…”

Genome Structures and Halophyte-Specific Gene Expression of the Extremophile Thellungiella parvula in Comparison with Thellungiella salsuginea (Thellungiella halophila) and Arabidopsis

“…What appears to emerge is the existence of a small number of novel genes (Vinocur and Altman, 2005), while novel uses of kingdom-wide existing genes and proteins seem to provide the bulk of the mechanisms that form the basis of the stress-tolerance phenotype. Increasingly, halophyte transcriptomes are being analyzed and contrasted to glycophytic relatives (Kore-eda et al, 2004;Gong et al, 2005;Zouari et al, 2007;Dassanayake et al, 2009;Guo et al, 2009;Chelaifa et al, 2010). With the advent of numerous ongoing whole genome sequencing projects and comparisons throughout the plant kingdom, a multifaceted approach becomes possible.…”