An evolutionary perspective on increasing net benefits to crops from symbiotic microbes

Authors: DENISON, FORD - University Of Minnesota; Muller, Katherine

Submitted to: Evolutionary Applications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/6/2022
Publication Date: 4/14/2022
Citation: Denison, F.R., Muller, K.E. 2022. An evolutionary perspective on increasing net benefits to crops from symbiotic microbes. Evolutionary Applications. https://doi.org/10.1111/eva.13384.
DOI: https://doi.org/10.1111/eva.13384

Interpretive Summary: Problem statement: Over the past 20 years, extensive resources have been devoted to research and products aiming to improve agronomic benefits from beneficial microbes. However, progress has been underwhelming, due in part to flawed research targets and methodology. Accomplishment: This essay synthesizes previous and ongoing research on beneficial microbes in agriculture through a lens of evolutionary theory. We recommend research targets and strategies that are likely to advance the field. Contribution: We hope scientists working on beneficial microbes in agriculture will adopt our recommendations and avoid wasting more research dollars on ineffective studies.

Technical Abstract: Plant-imposed, fitness-reducing sanctions against less-beneficial symbionts have been documented for rhizobia, mycorrhizal fungi, and fig wasps. Although most of our examples are for rhizobia, we argue that the evolutionary persistence of mutualism in any symbiosis would require such sanctions, if there are multiple strains per host plant. We therefore discuss methods that could be used to develop and assess crops with stricter sanctions. These include methods to screen strains for greater mutualism and to identify crop genotypes that impose stronger selection for mutualism. Single-strain experiments that measure costs as well as benefits have shown that diversion of resources by rhizobia can reduce nitrogen-fixation efficiency (N per C) and that some legumes can increase this efficiency by manipulating their symbionts. Plants in the field always host multiple strains with possible synergistic interactions, so benefits from different strains might best be compared by regressing plant growth or yield on each strain’s abundance in a mixture. However, results from this approach have not yet been published. To measure legacy effects of stronger sanctions on future crops, single-genotype test crops could be planted in a field that recently had replicated plots with different genotypes of the sanction-imposing crop. Enhancing agricultural benefits from symbiosis may require accepting tradeoffs that constrained past natural selection, such as tradeoffs between current and future benefits.