Leaf manganese concentrations reveal phosphorus-mining strategies and trait diversification of Myrtaceae in south-eastern Australia.

Abstract

Background and aims: Phosphorus (P)-impoverished soils shape plant adaptation in biodiverse ecosystems worldwide, from Australian heathlands to Amazonian rainforests to southern China's karst regions. While non-mycorrhizal lineages like Proteaceae and Cyperaceae use carboxylate exudation that mobilise P, and are celebrated for such strategies, the mechanisms allowing mycorrhizal Myrtaceae-especially eucalypts-to thrive in these soils without fungal assistance remain unclear. Given Myrtaceae's dominance in P-impoverished Australian ecosystems, a key question arises: How do mycorrhizal plants succeed in P-impoverished environments without relying on fungal symbiosis? We challenge the paradigm that carboxylate-driven P acquisition is exclusive to non-mycorrhizal species.

Methods: Using leaf manganese concentrations ([Mn]) as a proxy for carboxylate exudation, we assessed trait diversification across Myrtaceae genera. We collected leaf and soil samples from 34 species of eucalypt (Angophora, Blakella, Corymbia, Eucalyptus) and other Myrtaceae from 18 sites in south-eastern Australia.

Key results: Our findings reveal consistently high leaf [Mn] in many Myrtaceae, comparable to that in known carboxylate-releasing species, indicating intensive P mining. This suggests convergent evolution of carboxylate exudation in mycorrhizal Myrtaceae, fundamentally reshaping our understanding of nutrient acquisition in symbiotic plants. Significant interspecific variation was observed, with Angophora showing markedly higher [Mn] than Eucalyptus, suggesting divergent P-acquisition strategies within Myrtaceae. Weak phylogenetic signals for leaf [Mn] and [P] in eucalypts imply repeated evolutionary change in these traits, similar to what is known in other Australian species adapted to P scarcity.

Conclusions: By demonstrating carboxylate-driven P mining in mycorrhizal Myrtaceae, we redefine the mechanisms behind their dominance in low-P environments. Trait diversity-linked to variation in carboxylate-mediated P acquisition and plant-soil feedbacks-likely drives niche differentiation and genus-level distribution across south-eastern Australia. Connecting leaf [Mn] to carboxylate-driven P mining advances our understanding of trait evolution in Myrtaceae and provides a framework for predicting plant-soil interactions in P-impoverished ecosystems globally.