Salinity adaptation in date palm (Phoenix dactylifera): evidence for selective sweeps at Salt Overly Sensitive (SOS) genes

Abstract

The date palm is a high salinity tolerant fruit tree grown mainly in the region spanning from North Africa to parts of South Asia. Climate change models of this region indicate the possibility of increasing salinity in the future. The Salt Overly Sensitive (SOS) pathway is crucial for salinity tolerance in plants, serving as a primary defense mechanism by facilitating sodium exclusion. To better understand date palms' salt tolerance, we analyzed variation in SOS pathway genes in a set of 197 date palm genomes collected from across the range of cultivation. Here, we show evidence for selective sweeps in multiple SOS pathway genes. A single major pdSOS1 haplotype is at very high frequency in Eastern and Western subpopulations, with a minor, likely ancestral haplotype still present in both geographical locations. Allele-specific gene expression analysis showed differences in salt-treated roots between swept and ancestral haplotypes. Interestingly, sequence-based analysis of the pdSOS1 haplotype suggested a second, much earlier introgression event between P. theophrasti and date palm, though direction is unclear. This event happened before both the selective sweep and the previously reported recent introgression to date palm. We identified a MITE transposable element inserted into a pdSOS1 intron on the swept haplotype, and a similar insertion was found in an intron of the SOS2 paralog pdCIPK8. Both insertions are unique to date palm among Phoenix species. The pdCIPK8 haplotype containing the MITE is also at high frequency in both populations. Further analysis showed evidence for a selective sweep spanning the pdSOS3 region in the western population that shares similarity to an Eastern haplotype spanning the promoter region only. Slower extended haplotype homozygosity decay surrounding the genes in the western population suggests that the swept haplotype originated in the East and spread to the West in all cases. Altogether, our data provide evidence of selective sweeps in the date palm SOS pathway and may go to explaining how this species has developed such high salinity tolerance.