Yan Li, Hayes Patrick E, Nge Francis J, Rogers Erin I E, Wright Ian J, Ranathunge Kosala, Ellsworth David S, Lambers Hans
School of Biological Sciences, The University of Western Australia, 35 Stirling Highway, Perth, WA, 6009, Australia.
National Herbarium of New South Wales, Botanic Gardens of Sydney, Locked Bag 6002, Mount Annan, NSW 2567, Australia.
Ann Bot. 2025 Jun 17. doi: 10.1093/aob/mcaf129.
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.
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.
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.
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.
缺磷土壤影响着全球生物多样性生态系统中植物的适应性,从澳大利亚的石南荒原到亚马逊雨林,再到中国南方的喀斯特地区。虽然像山龙眼科和莎草科这样的非菌根谱系通过分泌羧酸盐来活化磷,并因其策略而备受赞誉,但菌根桃金娘科植物,尤其是桉树,在没有真菌帮助的情况下在这些土壤中茁壮成长的机制仍不清楚。鉴于桃金娘科在澳大利亚缺磷生态系统中的优势地位,一个关键问题出现了:菌根植物如何在不依赖真菌共生的情况下在缺磷环境中取得成功?我们对羧酸盐驱动的磷获取是非菌根物种所特有的这一范式提出了挑战。
我们以叶片锰浓度([Mn])作为羧酸盐分泌的指标,评估了桃金娘科各属的性状多样性。我们从澳大利亚东南部18个地点的34种桉树(包括拟桉属、布拉克桉属、伞房桉属、桉属)和其他桃金娘科植物中采集了叶片和土壤样本。
我们的研究结果表明,许多桃金娘科植物的叶片[Mn]始终很高,与已知的羧酸盐释放物种相当,这表明它们在大量获取磷。这表明菌根桃金娘科植物中羧酸盐分泌存在趋同进化,从根本上重塑了我们对共生植物养分获取的理解。观察到显著的种间差异,拟桉属的[Mn]明显高于桉属,这表明桃金娘科内部存在不同的磷获取策略。桉树叶片[Mn]和[P]的系统发育信号较弱,这意味着这些性状发生了反复的进化变化,类似于其他适应低磷环境的澳大利亚物种。
通过证明菌根桃金娘科植物中羧酸盐驱动的磷获取,我们重新定义了它们在低磷环境中占优势的背后机制。与羧酸盐介导的磷获取和植物 - 土壤反馈变化相关的性状多样性,可能驱动了澳大利亚东南部的生态位分化和属级分布。将叶片[Mn]与羧酸盐驱动的磷获取联系起来,加深了我们对桃金娘科性状进化的理解,并为预测全球缺磷生态系统中的植物 - 土壤相互作用提供了一个框架。