Convergent losses of arbuscular mycorrhizal symbiosis in carnivorous plants

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Abstract

Across evolutionary scales, lineages acquire and lose traits and associated genes. Most land plants form arbuscular mycorrhizal (AM) symbiosis, an ancient trait for enhanced nutrition that was convergently lost in some clades. Carnivory, another nutritional trait, is a more recent adaptation that has convergently arisen in several angiosperm orders. The two biotic interactions similarly help plants acquire mineral nutrients, raising the question of whether they can coexist. However, the mycorrhizal status of carnivorous plants has long remained speculative. Here, we surveyed the occurrence of AM-associated genes in five angiosperm orders harbouring carnivorous species, revealing convergent losses of the AM trait either coincident with or predating the emergence of carnivory. Exceptionally, the carnivorous plant speciesRoridula gorgoniasretains symbiosis-related genes and forms arbuscules upon inoculation assays, demonstrating the two nutritional strategies, although rare, can coexist. The youngest carnivorous lineage,Brocchinia reducta, showed signatures of the early stages of AM trait loss, as reflected by its gene retention and AM colonization patterns. An AM-associatedCHITINASEgene encodes a digestive enzyme in the Australian pitcher plantCephalotus, suggesting gene co-option. These findings illuminate the largely unexplored processes by which plant nutritional strategies evolve and supplant one another over time.

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