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

Abstract

The genome of Thellungiella parvula, a halophytic relative of Arabidopsis (Arabidopsis thaliana), is being assembled using Roche-454 sequencing. Analyses of a 10-Mb scaffold revealed synteny with Arabidopsis, with recombination and inversion and an uneven distribution of repeat sequences. T. parvula genome structure and DNA sequences were compared with orthologous regions from Arabidopsis and publicly available bacterial artificial chromosome sequences from Thellungiella salsuginea (previously Thellungiella halophila). The three-way comparison of sequences, from one abiotic stress-sensitive species and two tolerant species, revealed extensive sequence conservation and microcolinearity, but grouping Thellungiella species separately from Arabidopsis. However, the T. parvula segments are distinguished from their T. salsuginea counterparts by a pronounced paucity of repeat sequences, resulting in a 30% shorter DNA segment with essentially the same gene content in T. parvula. Among the genes is SALT OVERLY SENSITIVE1 (SOS1), a sodium/proton antiporter, which represents an essential component of plant salinity stress tolerance. Although the SOS1 coding region is highly conserved among all three species, the promoter regions show conservation only between the two Thellungiella species. Comparative transcript analyses revealed higher levels of basal as well as salt-induced SOS1 expression in both Thellungiella species as compared with Arabidopsis. The Thellungiella species and other halophytes share conserved pyrimidine-rich 5# untranslated region proximal regions of SOS1 that are missing in Arabidopsis. Completion of the genome structure of T. parvula is expected to highlight distinctive genetic elements underlying the extremophile lifestyle of this species.

Life at the extreme: lessons from the genome

“…and other halophytes that are absent in Arabidopsis . These differences in regions that are not transcribed are correlated with differences in expression observed for SOS1 in Thellungiella [15,16]. …”

“…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]. …”

“…The T. parvula genome is of particular interest because chromosomal assemblies that approach the coverage of A. thaliana are available. Moreover, because the Thellungiella species share many of the characteristics that led to the acceptance of Arabidopsis as a model (size, growth habit, seed amount, mutants, and transformation ability), they have been recognized as excellent candidates for comparative genomics studies [15,22]. …”

“…At this point, there are few genomes complete enough to allow detailed comparisons, essentially only T. parvula and A. thaliana . In these two, although the gene spaces show extensive overall colinearity, there are also major translocations of gene-rich regions and extensive changes in intergenic sequences [10,15]. Beyond this, there are three promising, potentially adaptive linkages to explore.…”

The integration of activity in saline environments: problems and perspectives

“…With respect to salinity, following the sequencing of the genomes of two halophytic Arabidopsis relatives (Thellungiella parvula and T. salsuginea), it became evident that genes associated with abiotic stress responses and ion transport had been tandem duplicated in the halophytes in significantly higher numbers than in Arabidopsis (Dassanayake et al 2011;Oh et al 2012;Wu et al 2012). These duplications, although showing a high degree of sequence similarity to their Arabidopsis equivalents, have essentially no similarity in their promoter regions and substantially different expression patterns even in the absence of salt (Oh et al 2010). How their epigenomes or populations of small interfering RNAs differ has yet to be examined, but these are undoubtedly involved in their different responses to stressful environments.…”