Miscanthus sinensis dominates in Andosol through strong phosphorus acquisition that enhances water-use efficiency and nitrogen fixation

Andosol was unsuitable for crop production without large inputs of phosphorus fertilizer due to high levels of active aluminum making phosphorus insoluble. However, Miscanthus sinensis has dominated Andosol for centuries, and how it sustains growth despite severe phosphorus-deficiency remains unclear. Under varied phosphorus treatments, pot experiments were conducted to investigate phosphorus acquisition in Miscanthus sinensis, along with its impact on water-use efficiency and nitrogen fixation. Among the species tested, only Miscanthus sinensis showed relatively higher phosphorus acquisition in Andosol than in vermiculite, as reflected by a marked increase in biomass production (0.96 and 0.11 g plant-1, respectively). This provides the first experimental evidence that Miscanthus sinensis possesses a superior capability to utilize phosphorus sources in Andosol. This capability was further confirmed by its effective utilization of sparingly soluble phosphorus forms (Al-P, Fe-P, Ca-P, and Ca-Phy) in a vermiculite medium, where biomass production was comparable to that under phosphorus fertilizer supply. It was further observed that when C4 monocots, including Miscanthus sinensis, failed to acquire sufficient phosphorus, their characteristic higher water-use efficiency compared with C3 dicots disappeared. Specifically, water-use efficiency in Miscanthus sinensis increased from 3.2 to 7.1 g kg-1 across phosphorus treatments, whereas C3 dicots showed smaller variations (radish: 1.2-2.8, soybean: 4.0-5.1, and peanut: 5.1-6.2 g kg-1). Regression analysis showed that phosphorus concentration explained a large proportion of the variation in water-use efficiency among C4 monocots (Chinese silver grass, bahiagrass, and guinea grass) (R2 = 0.67), but not in C3 dicots (R2 = 0.04), indicating that phosphorus status is critical for maintaining the C4 trait. Furthermore, using 15N-enriched fertilizer, we estimated that 3.4-15.9% of nitrogen in Miscanthus sinensis was derived from the atmosphere, and this contribution was also strongly dependent on phosphorus availability. Our findings suggest that phosphorus acquisition contributes to maintaining high water-use efficiency and enhancing N2 fixation in Miscanthus sinensis, thereby supporting its dominance in nutrient-poor Andosol. This study improves our understanding of plant nutritional strategies under nutrient-limited conditions.