Transcriptome Signatures of Selection, Drift, Introgression, and Gene Duplication in the Evolution of an Extremophile Endemic Plant

Abstract

Plants on serpentine soils provide extreme examples of adaptation to environment, and thus offer excellent models for the study of evolution at the molecular and genomic level. Serpentine outcrops are derived from ultramafic rock and have extremely low levels of essential plant nutrients (e.g., N, P, K, and Ca), as well as toxic levels of heavy metals (e.g., Ni, Cr, and Co) and low moisture availability. These outcrops provide habitat to a number of endemic plant species, including the annual mustard Caulanthus amplexicaulis var. barbarae (Cab) (Brassicaceae). Its sister taxon, C. amplexicaulis var. amplexicaulis (Caa), is intolerant to serpentine soils. Here, we assembled and annotated comprehensive reference transcriptomes of both Caa and Cab for use in protein coding sequence comparisons. A set of 29,443 reciprocal best Blast hit (RBH) orthologs between Caa and Cab was compared with identify coding sequence variants, revealing a high genome-wide dN/dS ratio between the two taxa (mean = 0.346). We show that elevated dN/dS likely results from the composite effects of genetic drift, positive selection, and the relaxation of negative selection. Further, analysis of paralogs within each taxon revealed the signature of a period of elevated gene duplication (∼10 Ma) that is shared with other species of the tribe Thelypodieae, and may have played a role in the striking morphological and ecological diversity of this tribe. In addition, distribution of the synonymous substitution rate, dS, is strongly bimodal, indicating a history of reticulate evolution that may have contributed to serpentine adaptation.

Evolutionary Analysis of the YABBY Gene Family in Brassicaceae

“…As extreme cases, YAB5 was absent (while five other members were all duplicated) in Lepidium sativum, YAB3 was absent in Leavenworthia alabamica, and all three YABBY genes, i.e., FIL, YAB2, and INO, were simultaneously absent in Stanleya pinnata, indicating that the species might have undergone particular natural constraints during its evolution, a hypothesis supported by the fact that Stanleya pinnata can develop normally in a wide range of hard edaphic environments such as soils with high sodium, boron, or selenium content or serpentine soils [70][71][72]. Interestingly, the WGD event in Stanleya pinnata was estimated to have occurred ~10.65 Mya [67], similar to that (~10 Mya) of Caulanthus amplexicaulis [65], but the fates of duplicate YABBY genes were very different between the two species, both of which belong to the Thelypodiae tribe. These variations in the number and composition of different types of YABBY genes observed in certain Brassicaceae species may have partially contributed to the high morphological disparity that was observed among Brassicaceae species [73].…”

“…Among the 37 Brassicaceae species, 17 (including A. thaliana) each contained a set of six basic YABBY genes, i.e., one FIL, one YAB2, one YAB3, one YAB5, one INO, and one CRC, whereas one (named Sisymbrium irio) contained a set of six basic YABBY genes plus an additional YAB2 member originated by duplication by tandem in the genome. This set of six basic YABBY genes was perfectly duplicated in Caulanthus amplexicaulis and triplicated in Camelina sativa, caused obviously by recent whole-genome duplication (WGD) and triplication (WGT), respectively, which occurred during the evolutionary history of their genomes [65,66]. The remaining 19 species each contained a variable number of YABBY genes with a variable composition, which is a consequence of WGD or WGT that occurred in these species followed by the extensive loss of duplicated or triplicated genes in the process of rediploidization [67].…”

“…For example, we can deduce from the trees that the five FIL and six YAB2 from Eruca vesicaria were the result of a WGT event followed by another more recent WGD event (Figure S2A,B), the 18 YABBY genes from Camelina sativa were the result of a very recent WGT event, and the 12 YABBY genes from Caulanthus amplexicaulis were the result of a more ancient WGD event. It was estimated that the WGT event (by hybridization of the three sub-genomes in quick succession) in Camelina sativa occurred very recently, probably emerging during the rapid expansion of agricultural practices ~5-10,000 ya [65], while the WGD event in Caulanthus amplexicaulis occurred ~10 Mya [66]. Interestingly, no duplicate YABBY gene was lost in Caulanthus amplexicaulis despite the ~10 million years of evolution, indicating that the YABBY genes of Caulanthus amplexicaulis underwent a relaxed selection during evolution.…”

Development of 15 microsatellite loci in the endangered Streptanthus glandulosus subsp. niger (Brassicaceae)

“…Evidence from transcriptome sequencing indicates that a common ancestor to S. glandulosus subsp. niger and other members of the tribe Thelypodieae underwent a major (possibly whole genome) duplication event ~8–10 mya (Kagale et al., ; Hawkins et al., ). A diploid chromosome number of 2 n = 28 is almost universally conserved across the tribe (Warwick and Al‐Shehbaz, ).…”

High-resolution Hi-C maps highlight multiscale chromatin architecture reorganization during cold stress in Brachypodium distachyon

“…3 E). For example, Bradi2g20510 ( CRT3 ) encodes calreticulin, which plays a role in calcium ion homeostasis and tolerance to abiotic stress [ 30 ]. When it gained a TAD boundary, its expression increased under cold stress conditions (Fig.…”