The ecological genomic basis of salinity adaptation in Tunisian Medicago truncatula

Abstract

BackgroundAs our world becomes warmer, agriculture is increasingly impacted by rising soil salinity and understanding plant adaptation to salt stress can help enable effective crop breeding. Salt tolerance is a complex plant phenotype and we know little about the pathways utilized by naturally tolerant plants. Legumes are important species in agricultural and natural ecosystems, since they engage in symbiotic nitrogen-fixation, but are especially vulnerable to salinity stress.ResultsOur studies of the model legume Medicago truncatula in field and greenhouse settings demonstrate that Tunisian populations are locally adapted to saline soils at the metapopulation level and that saline origin genotypes are less impacted by salt than non-saline origin genotypes; these populations thus likely contain adaptively diverged alleles. Whole genome resequencing of 39 wild accessions reveals ongoing migration and candidate genomic regions that assort non-randomly with soil salinity. Consistent with natural selection acting at these sites, saline alleles are typically rare in the range-wide species' gene pool and are also typically derived relative to the sister species M. littoralis. Candidate regions for adaptation contain genes that regulate physiological acclimation to salt stress, such as abscisic acid and jasmonic acid signaling, including a novel salt-tolerance candidate orthologous to the uncharacterized gene AtCIPK21. Unexpectedly, these regions also contain biotic stress genes and flowering time pathway genes. We show that flowering time is differentiated between saline and non-saline populations and may allow salt stress escape.ConclusionsThis work nominates multiple potential pathways of adaptation to naturally stressful environments in a model legume. These candidates point to the importance of both tolerance and avoidance in natural legume populations. We have uncovered several promising targets that could be used to breed for enhanced salt tolerance in crop legumes to enhance food security in an era of increasing soil salinization.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-1160) contains supplementary material, which is available to authorized users.

Salt tolerance during germination and seedling growth of wild wheat Aegilops tauschii and its impact on the species range expansion

“…We note that the observed association between seedling growth ability under stress and early flowering in Ae. tauschii parallels a case in Medicago in which flowering time was shown to play a major role in adaptation to saline soils9. Ae.…”

“…However, in the process of species range expansion, migrating individuals/populations may have to overcome several stressful abiotic factors other than climate conditions in order to survive and propagate in the new habitats. Edaphic stress is one of the key abiotic factors that may serve as a selective agent in the evolution of local adaptation89. In natural settings, plants’ germination, vegetative growth, root and aboveground architecture, metabolism, and reproduction may be strongly influenced by soil’s shallowness and poor drainage (physical conditions), as well as water and nutrient deficiency, acidity, alkalinity, salinity, and metal toxicity (chemical conditions).…”

Validating Genome-Wide Association Candidates Controlling Quantitative Variation in Nodulation

“…In standard forward genetic screens, a mutant phenotype is identified based on the effects seen within individual organisms, something that will bias these screens toward detecting genes of large effect. Forward genetic screens are likely to miss genes of small phenotypic effects, such as those that contribute to naturally occurring quantitative variation in nodulation (Stanton-Geddes et al, 2013; Friesen et al, 2014). Identification of these genes of subtle effect will provide a fuller understanding of the symbiosis between legumes and rhizobia, and may provide targets for selection in important agronomic legumes.…”

Population Genomics for Understanding Adaptation in Wild Plant Species

“…The strategy was similar in both cases, using contrasts between populations on serpentine and granite soils or diploid and tetraploid populations, and this approach should be informative for A. halleri as well, where there are many populations that have evolved metal hyperaccumulation and tolerance. Contrasts between populations growing on saline and nonsaline soils also supported the identification of candidate loci involved in salinity adaptation in Medicago truncatula (43,44).…”

“…The major exception is Arabidopsis thaliana, which was not only the first plant but also one of the first species overall for which rich genome-wide and subsequently whole-genome polymorphism data became available (22,30,45,61,74,99,112,114,131,132). Information on other wild species that are not closely related to crops is emerging only very slowly (18,37,43,44,47,59,121,161). This presumably reflects funding priorities, which emphasize new resources for breeding, but it represents a missed opportunity if one wants to understand how wild species adapt to natural environments.…”