Evolution of phosphate metabolism in Tibetan wild barley to adapt to aluminum stress

Aims: Aluminum (Al) toxicity in acid soil significantly reduces plant growth, agricultural productivity and ecosystem health. The Al-tolerant barley cultivars were reported to mainly rely on the Al-activated efflux of citrate from root apices, but the key mechanisms for Al tolerance may differ for wild relatives of barley adapted to acid soil. Methods: Here, we investigated plant Al tolerance from evolutionary physiological, molecular, and ecological perspectives. Results: Phylogenetic analysis of Al tolerance-associated gene families showed that most of these genes were conserved from streptophyte algae to angiosperms, indicating land plants have evolved gradually in adaption to Al-rich acid soil during plant terrestrialization. Vacuolar phosphate transporter SPX-major facility superfamily (SPX-MFS) and inorganic phosphate transporter 1 family (PHT1s) of streptophyte algae showed high genetic similarity to land plants. PHT1s exhibited a significant expand during the evolution from streptophyte algae to liverworts and then eudicots. Al-tolerant Tibetan wild barley accession, XZ29 showed high levels of P-containing glycolytic intermediates including Glu-6-P, Fru-6-P, 3-PGA, 2-PGA and PEP under Al stress. Some primary metabolites were evolutionarily conserved in liverwort, gymnosperm and three tested angiosperms. Furthermore, we found that Al-induced Pi efflux from root elongation zone to chelate rhizosphere Al3+, and immobilization of Al with P at the inner epidermal layer of root mature zone to reduce Al accumulation in the cortical layer in barley. Conclusions: These results indicated that Tibetan wild barley has evolved unique P transport and metabolism for the adaptation to harsh conditions in eastern and southeastern Tibet where acid soils contain high P.