Candidate Genes for the High-Altitude Adaptations of Two Mountain Pine Taxa

Abstract

Mountain plants, challenged by vegetation time contractions and dynamic changes in environmental conditions, developed adaptations that help them to balance their growth, reproduction, survival, and regeneration. However, knowledge regarding the genetic basis of species adaptation to higher altitudes remain scarce for most plant species. Here, we attempted to identify such corresponding genomic regions of high evolutionary importance in two closely related European pines, Pinus mugo and P. uncinata, contrasting them with a reference lowland relative—P. sylvestris. We genotyped 438 samples at thousands of single nucleotide polymorphism (SNP) markers, tested their genetic differentiation and population structure followed by outlier detection and gene ontology annotations. Markers clearly differentiated the species and uncovered patterns of population structure in two of them. In P. uncinata three Pyrenean sites were grouped together, while two outlying populations constituted a separate cluster. In P. sylvestris, Spanish population appeared distinct from the remaining four European sites. Between mountain pines and the reference species, 35 candidate genes for altitude-dependent selection were identified, including such encoding proteins responsible for photosynthesis, photorespiration and cell redox homeostasis, regulation of transcription, and mRNA processing. In comparison between two mountain pines, 75 outlier SNPs were found in proteins involved mainly in the gene expression and metabolism.

Evolutionary targets of gene expression divergence in a complex of closely related pine species

“…We observed generally lower intraspecific variation in expression of markers in individuals of dwarf mountain pine and the other two species occasionally showed bipolar spread of the transcription estimates. These results contrast with the pattern observed in a broad set of genome-wide SNP markers (Zaborowska et al, 2021), where P. mugo showed the highest intraspecific diversity among these three taxa. However, due to the limited sample sizes used here, much of the variation among the pine species remains unexplored.…”

“…Counts of DEGs exhibited interesting patterns showing similar numbers of genes in comparisons of P. mugo and P. uncinata vs P. sylvestris (26), P mugo vs P. uncinata (28), and P. uncinata vs P. sylvestris (26), while triple that number was observed in the comparison of P. mugo and P. sylvestris (90). The pattern denotes asymmetric relations between Scots pine and two mountain pines, consistent with most available data (e.g., Wachowiak et al, 2015;Zaborowska et al, 2021). The number of markers that unite the mountain pines and discriminate them from Scots pine ((M vs PS) U (U vs PS): 14) was not much larger than the numbers of DEGs specific to each of them ((M vs PS) U (M vs UN): 8 and (U vs PS) U (U vs M): 2).…”

“…Pines from the P. mugo complex and P. sylvestris diverged about 5 million years BP (Wachowiak et al, 2011;). However, they are genetically similar, and previous studies showed little differentiation between the taxa at karyotype (Bogunić et al, 2011), mitochondrial and plastid genomes (Heuertz et al, 2010;Dzialuk et al, 2017;Zaborowska et al, 2019;Sokołowska et al, 2021), nuclear loci (Monteleone et al, 2006;Wachowiak et al, 2013;Zaborowska et al, 2021), and candidate genes that showed low (<0.1%) net genetic divergence between the taxa (Wachowiak et al, 2013). So far, only singular species diagnostic markers have been found at mitochondrial, plastid, and nuclear regions (Wachowiak et al, 2000;Kormut'ák et al, 2005;Żukowska & Wachowiak, 2017;Zaborowska et al, 2019).…”

“…Comparative transcriptome analysis of these pines (Wachowiak et al, 2015) revealed thousands of polymorphic markers that were used for the development of SNP genotyping array (Perry et al, 2020), which has since been used to identify loci significantly associated with key adaptive traits, including growth and phenology (Perry et al, 2022). Genomic studies support the phylogenetically close relationship between two mountain pine taxa as compared to Scots pine and reveal some candidate regions under selection during the species evolution (Zaborowska et al, 2021).…”

Genomic Insights into High-Altitude Adaptation: A Comparative Analysis of Roscoea alpina and R. purpurea in the Himalayas

“…The development of high-throughput sequencing technology has greatly accelerated genomic research and identification of key genes and promoted the adaptive evolution and ecological research of non-model organisms [19,20]. This technology is also beneficial for further exploring the adaptation of non-model plants to high elevation [8,9,21,22].…”