Green revolution gene drives adaptation of Arabidopsis to the extremely high altitude

To elucidate the process of adaptation, particularly the traits subject to natural selection and the molecular mechanisms underlying their natural variation, is one of the primary objectives of evolutionary biology. The uplifted landscape offers an excellent framework for understanding how organisms adapt to dramatic climatic gradients. To investigate the genetic basis of plant adaptation to the extremely high altitude, we first compared the genomic and phenotypic variations of two closely related Arabidopsis thaliana accessions from high altitude (Xizang, also known as "Tibet") and low altitude (Yunnan), respectively. The Xizang population represents a relict group characterized by a small effective population size. Notably, the Xizang genome has more transposable elements (TEs) and more gene loss-of-function (LoF) mutations. Differentially expressed genes were enriched in biological processes of cellular response to oxygen-containing compound, regulation of defense response, and response to light intensity. Intriguingly, the phenotypic selection analysis revealed that silique density was under natural selection. Furthermore, we genetically mapped and validated that the LoF mutation of GA20ox1, the homologous gene of green revolution in rice, resulted in a higher silique density in Xizang Arabidopsis. Given that GA20ox1 is linked to Arabidopsis adaptation to the Alps Mountains, its parallel evolution plays an important role in the adaptation to Alpine habitats. Overall, our results highlight that identifying adaptive traits and elucidating the molecular mechanisms underlying natural variation of these traits is crucial for unraveling the mystery of adaptive evolution and has significant implications for crop breeding.