Transcriptome differences between two sister desert poplar species under salt stress

Zhang et al. BMC Genomics 2014, 15:337 http://www.biomedcentral.com/1471-2164/15/337 RESEARCH ARTICLE Open Access Transcriptome differences between two sister desert poplar species under salt stress Jian Zhang1, Jianju Feng1,2, Jing Lu1, Yongzhi Yang1, Xu Zhang1, Dongshi Wan1 and Jianquan Liu1* Abstract Background: Populus euphratica Oliv and P. pruinosa Schrenk (Salicaceae) both grow in dry desert areas with high summer temperatures. However, P. euphratica is distributed in dry deserts with deep underground water whereas P. pruinosa occurs in deserts in which there is underground water close to the surface. We therefore hypothesized that these two sister species may have evolved divergent regulatory and metabolic pathways during their interaction with different salt habitats and other stresses. To test this hypothesis, we compared transcriptomes from callus exposed to 24 h of salt stress and control callus samples from both species and identified differentially expressed genes (DEGs) and alternative splicing (AS) events that had occurred under salt stress. Results: A total of 36,144 transcripts were identified and 1430 genes were found to be differentially expressed in at least one species in response to salt stress. Of these DEGs, 884 and 860 were identified in P. euphratica and P. pruinosa, respectively, while 314 DEGs were common to both species. On the basis of parametric analysis of gene set enrichment, GO enrichment in P. euphratica was found to be significantly different from that in P. pruinosa. Numerous genes involved in hormone biosynthesis, transporters and transcription factors showed clear differences between the two species in response to salt stress. We also identified 26,560 AS events which were mapped to 8380 poplar genomic loci from four libraries. GO enrichments for genes undergoing AS events in P. euphratica differed significantly from those in P. pruinosa. Conclusions: A number of salt-responsive genes in both P. euphratica and P. pruinosa were identified and candidate genes with potential roles in the salinity adaptation were proposed. Transcriptome comparisons of two sister desert poplar species under salt stress suggest that these two species may have developed different genetic pathways in order to adapt to different desert salt habitats. The DEGs that were found to be common to both species under salt stress may be especially important for future genetic improvement of cultivated poplars or other crops through transgenic approaches in order to increase tolerance of saline soil conditions. Keywords: P. euphratica, P. pruinosa, Salt tolerance, Salinity stress, Transcriptome, Differentially expressed genes, Alternative splicing Background Salinity and drought stresses are the two most important environmental factors limiting plant growth and development in semiarid and arid areas [1]. Over 100 countries in the world have been identified as being affected by salinity [2], and the scale of the problem seems to be increasing at an alarming rate [3]. Salinity, together with drought, has far-reaching implications for food security, economic sustainability and the irreplaceable biodiversity of any affected area, and it is anticipated that these * Correspondence: 1 State Key Laboratory of Grassland and Agro-Ecosystems, School of Life Sciences, Lanzhou University, Lanzhou 730000, Gansu, China Full list of author information is available at the end of the article challenges will be exacerbated by the projected impact of climate change. The effects of water-insufficiency stresses have been studied extensively; they limit water and micronutrient uptake and lead to closure of stomata, decline in carbon metabolism, stunted growth, ion/salt toxicity and reduced yield [3,4]. For plants to survive under such conditions, they must sense and respond to these abiotic stresses rapidly and in a complex manner [5], through signalling and regulatory pathways [3,4,6] mediated by abscisic acid [7] or ethylene [8], generally resulting in altered expression of transcription factors [9], and in many cases in increased expression of genes encoding products required for osmoregulation, cell protection and/or acclimation [10-15]. These modifications © 2014 Zhang et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. Zhang et al. BMC Genomics 2014, 15:337 http://www.biomedcentral.com/1471-2164/15/337 may lead to changes in signal transduction, ionic homeostasis, scavenging of reactive oxygen species, accumulation of compatible solutes and growth regulation [3,6,16-18]. A common strategy for the identification of overall changes in gene expression under salt stress is to compare the transcriptomes of the targeted species or cultivars using microarrays and/or RNA-Seq technologies [19]. A plethora of comparisons between salt-sensitive and salt-tolerant cultivars of model and non-model plant species, including Arabidopsis [20-22], rice [23], poplar [24-27], tomato [28], potato [29], Medicago truncatula [30], sugarcane [31] and olive [32], have been reported to date. These studies have identified more than 30 families of transcription factors and numerous enzyme-encoding genes involved in responses to salt stress [33,34]. However, overall changes in gene expression and physiological responses to salt stress vary greatly between different species, particularly between sensitive and non-sensitive pairs of related species [35-39]. It is often difficult to ascertain whether these differences were caused by divergence during the course of evolution or were brought about through adaptive differentiation. It is therefore of interest to compare the overall changes in gene expression that occur in sister species under salt stress, as this will minimise phylogenetic effects. Here we examine differences in the transcriptomes of two sister desert poplar species under salt stress. Populus serves as a model for elucidating physiological and molecular mechanisms of stress tolerance in tree species [40-42]. Both P. euphratica and P. pruinosa grow in dry deserts with high summer temperatures [43-46]. Both species can tolerate high salinity and survive NaCl concentrations of more than 300 mM [47] in nutrient solution, and P. euphratica has been used as a model species for studying abiotic responses to salt or drought stress [27,48-50]. In addition to differences in leaf and hair morphology between the two species, they also occur in different types of habitat. P. euphratica is found in dry deserts with deep underground water while P. pruinosa is distributed in deserts where the underground water is closer to the surface, and therefore more accessible, but also saltier near ancient or extant rivers. It is likely that these two species (...truncated)