Phyllosphere fungal diversity generates pervasive nonadditive effects on plant performance

• Published in: The New phytologist Vol. 243; no. 6; pp. 2416 - 2429
• Main Authors: Almeida, Brianna K., Tran, Elan H., Afkhami, Michelle E.
• Format: Journal Article
• Language: English
• Published: England Wiley Subscription Services, Inc 01-09-2024
• Subjects: antagonism; Biodiversity; Collections; Community composition; Consortia; foliar microbiome; Fungi; Fungi - physiology; Inoculation; microbial interactions; Microbiomes; Microbiota - physiology; nonadditive; Phyllosphere; Plant Leaves - microbiology; Plants; Productivity; Species diversity; Synergism; synthetic consortia; synergism; nonadditive; microbial interactions; foliar microbiome; antagonism; synthetic consortia
• ISSN: 0028-646X; 1469-8137; 1469-8137
• DOI: 10.1111/nph.19792

Summary
Plants naturally harbor diverse microbiomes that can dramatically impact their health and productivity. However, it remains unclear how fungal microbiome diversity, especially in the phyllosphere, impacts intermicrobial interactions and consequent nonadditive effects on plant productivity.
Combining manipulative experiments, field collections, culturing, microbiome sequencing, and synthetic consortia, we experimentally tested for the first time how foliar fungal community diversity impacts plant productivity. We inoculated morning glories (Ipomoea hederifolia L.) with 32 phyllosphere consortia of either low or high diversity or with single fungal taxa, and measured effects on plant productivity and allocation.
We found the following: (1) nonadditive effects were pervasive with 56% of fungal consortia interacting synergistically or antagonistically to impact plant productivity, including some consortia capable of generating acute synergism (e.g. > 1000% increase in productivity above the additive expectation), (2) interactions among ‘commensal’ fungi were responsible for this nonadditivity in diverse consortia, (3) synergistic interactions were approximately four times stronger than antagonistic effects, (4) fungal diversity affected the magnitude but not frequency or direction of nonadditivity, and (5) diversity affected plant performance nonlinearly with the highest performance in low‐diversity treatments.
These findings highlight the importance of interpreting plant–microbiome interactions under a framework that incorporates intermicrobial interactions and nonadditive outcomes to understand natural complexity.
See also the Commentary on this article by Whitaker, 243: 2050–2051.