Genome of Crucihimalaya himalaica , a close relative of Arabidopsis , shows ecological adaptation to high altitude

Abstract

Crucihimalaya himalaica, a close relative ofArabidopsisandCapsella, grows on the Qinghai–Tibet Plateau (QTP) about 4,000 m above sea level and represents an attractive model system for studying speciation and ecological adaptation in extreme environments. We assembled a draft genome sequence of 234.72 Mb encoding 27,019 genes and investigated its origin and adaptive evolutionary mechanisms. Phylogenomic analyses based on 4,586 single-copy genes revealed thatC. himalaicais most closely related toCapsella(estimated divergence 8.8 to 12.2 Mya), whereas both species form a sister clade toArabidopsis thalianaandArabidopsis lyrata, from which they diverged between 12.7 and 17.2 Mya. LTR retrotransposons inC. himalaicaproliferated shortly after the dramatic uplift and climatic change of the Himalayas from the Late Pliocene to Pleistocene. Compared with closely related species,C. himalaicashowed significant contraction and pseudogenization in gene families associated with disease resistance and also significant expansion in gene families associated with ubiquitin-mediated proteolysis and DNA repair. We identified hundreds of genes involved in DNA repair, ubiquitin-mediated proteolysis, and reproductive processes with signs of positive selection. Gene families showing dramatic changes in size and genes showing signs of positive selection are likely candidates forC. himalaica’s adaptation to intense radiation, low temperature, and pathogen-depauperate environments in the QTP. Loss of function at the S-locus, the reason for the transition to self-fertilization ofC. himalaica, might have enabled its QTP occupation. Overall, the genome sequence ofC. himalaicaprovides insights into the mechanisms of plant adaptation to extreme environments.

Genomic basis of parallel adaptation varies with divergence inArabidopsisand its relatives

“…To address our hypothesis at deeper phylogenetic scales, we performed a meta-analysis of gene-and function-level parallelism by complementing our data with gene candidate lists from six genome-wide studies of alpine adaptation from the Brassicaceae family [36][37][38][39][40][41] (species diverging 0.5 -18 millions of years ago 48,49 , Supplementary Tables 8, 9). We found significant parallelism both at the level of candidate genes (overlaps between 19 % of species pairs were significant, all within the Arabidopsis genus, p < 0.05, Fisher's exact test, Fig.…”

“…Arabidopsis halleri subsp. gemmifera from Japan 41 , aly: Arabidopsis lyrata from Northern Europe 39 , ath: Arabidopsis thaliana from Alps 38 , chi: Crucihimalaya himalaica 36 , lme: Lepidium meyenii 40 .…”

“…We gathered lists of gene candidates from all available studies focused on alpine adaptation in Brassicaceae [36][37][38][39][40][41] , i.e., adaptation towards treeless high-elevation habitats addressed by studies of whole genome sequence data ( Supplementary Table 8). We unified (merged) the gene candidate lists if multiple altitudinal gradients were screened within a species (except for A. halleri from Europe and Japan which were kept as separate units due to extraordinarily high spatial and genetic divergence of these two lineages) 61 .…”

“…Here, we aimed to test this hypothesis and investigate whether allele reuse is a major mechanism. We used replicated instances of adaptation to a challenging alpine environment, spanning a range of divergence from populations to tribes within the plant family Brassicaceae [36][37][38][39][40][41] (Fig. 1a).…”

De novo sequencing of the transcriptome reveals regulators of the floral transition in Fargesia macclureana (Poaceae)

“…The transcriptomic profiles of Posidonia oceanica also showed a strong metabolic activation of hormones in the heat stress-induced flowering plants [45]. Signal transduction-related genes were also found to have undergone both significant positive selection and expansion events on the adaptive evolution of Crucihimalaya himalaica [34] and cyanobacterium Trichormus sp. NMC-1 [46] on the QTP.…”