Drought is one of the main abiotic stresses, which affects plant growth, development, and crop yield. Plant response to drought implies carbon allocation to sink organs and sugar partitioning between different cell compartments, and thereby requires the involvement of sugar transporters (SUTs). Among them, the early response to dehydration six-like (ESL), with 19 members in Arabidopsis thaliana, form the largest subfamily of monosaccharide transporters (MSTs) still poorly characterized. A common feature of these genes is their involvement in plant response to abiotic stresses, including water deficit. In this context, we carried out morphological and physiological phenotyping of A. thaliana plants grown under well-watered (WW) and water-deprived (WD) conditions, together with the expression profiling of 17 AtESL genes in rosette leaves. The drought responsiveness of 12 ESL genes, 4 upregulated and 8 downregulated, was correlated to different water statuses of rosette leaves. The differential expression of each of the tandem duplicated AtESL genes in response to water stress is in favor of their plausible functional diversity. Furthermore, transfer DNA (T-DNA) insertional mutants for each of the four upregulated ESLs in response to water deprivation were identified and characterized under WW and WD conditions. To gain insights into global sugar exchanges between vacuole and cytosol under water deficit, the gene expression of other vacuolar SUTs and invertases (AtTMT, AtSUC, AtSWEET, and AtβFRUCT) was analyzed and discussed.

Carbon management by plants involves the activity of many sugar transporters, which play roles in sugar subcellular partitioning and reallocation at the whole organism scale. Among these transporters, the early response to dehydration six-like (ESL) monosaccharide transporters (MSTs) are still poorly characterized although they represent one of the largest sugar transporter subfamilies. In this study, we used an evolutionary genomic approach to infer the evolutionary history of this multigenic family. No ESL could be identified in the genomes of rhodophytes, chlorophytes, and the brown algae Ectocarpus siliculosus, whereas one ESL was identified in the genome of Klebsormidium nitens providing evidence for the early emergence of these transporters in Streptophytes. A phylogenetic analysis using the 519 putative ESL proteins identified in the genomes of 47 Embryophyta species and being representative of the plant kingdom has revealed that ESL protein sequences can be divided into three major groups. The first and second groups originated in the common ancestor of all spermaphytes [ζ: 340 million years ago (MYA)] and of angiosperms (ε: 170–235 MYA), respectively, and the third group originated before the divergence of rosids and asterids (γ/1R: 117 MYA). In some eudicots (Vitales, Malpighiales, Myrtales, Sapindales, Brassicales, Malvales, and Solanales), the ESL family presents remarkable expansions of gene copies associated with tandem duplications. The analysis of non-synonymous and synonymous substitutions for the dN/dS ratio of the ESL copies of the genus Arabidopsis has revealed that ESL genes are evolved under a purifying selection even though the progressive increase of dN/dS ratios in the three groups suggests subdiversification phenomena. To further explore the possible acquisition of novel functions by ESL MSTs, we identified the gene structure and promoter cis-acting elements for Arabidopsis thaliana ESL genes. The expression profiling of Arabidopsis ESL unraveled some gene copies that are almost constitutively expressed, whereas other gene copies display organ-preferential expression patterns. This study provides an evolving framework to better understand the roles of ESL transporters in plant development and response to environmental constraints.