Insights into the plateau adaptation of Salvia castanea by comparative genomic and WGCNA analyses

• Salvia castanea evolved the special underground stem with “trunk-branches” developmental pattern. • Significantly expanded and contracted OGGs, SSGs, and PSGs contribute to morphogenesis and QTP adaptation of S. castanea. • Tomenta of leaves and periderm of underground stem are like armors protecting S. castanea against QTP environment. • Secondary metabolites mainly RA and T-IIA realize the functions of armors. • NAC29 and TGA22 were identified as key TFs involved in regulating T-IIA and RA biosynthesis. Salvia castanea , a wild plant species is adapted to extreme Qinghai-Tibetan plateau (QTP) environments. It is also used for medicinal purposes due to high ingredient of tanshinone IIA (T-IIA). Despite its importance to Chinese medicinal industry, the mechanisms associated with secondary metabolites accumulation (i.e. T-IIA and rosmarinic acid (RA)) in this species have not been characterized. Also, the role of special underground tissues in QTP adaptation of S. castanea is still unknown. We explored the phenomenon of periderm-like structure in underground stem center of S. castanea with an aim to unravel the molecular evolutionary mechanisms of QTP adaptation in this species. Morphologic observation and full-length transcriptome of S. castanea plants were conducted. Comparative genomic analyses of S. castanea with other 14 representative species were used to reveal its phylogenetic position and molecular evolutionary mechanisms. RNA-seq and WGCNA analyses were applied to understand the mechanisms of high accumulations of T-IIA and RA in S. castanea tissues . Based on anatomical observations, we proposed a “trunk-branches” developmental model to explain periderm-like structure in the center of underground stem of S. castanea. Our study suggested that S. castanea branched off from cultivated Danshen around 16 million years ago. During the evolutionary process, significantly expanded orthologous gene groups, 24 species-specific and 64 positively selected genes contributed to morphogenesis and QTP adaptation in S. castanea . RNA-seq and WGCNA analyses unraveled underlying mechanisms of high accumulations of T-IIA and RA in S. castanea and identified NAC29 and TGA22 as key transcription factors. We proposed a “trunk-branches” developmental model for the underground stem in S. castanea. Adaptations to extreme QTP environment in S. castanea are associated with accumulations of high secondary metabolites in this species.