The genetic identity of neighboring plants in intraspecific mixtures modulates disease susceptibility of both wheat and rice

PLoS Biol. 2023 Sep 12;21(9):e3002287. doi: 10.1371/journal.pbio.3002287. eCollection 2023 Sep.

Abstract

Mixing crop cultivars has long been considered as a way to control epidemics at the field level and is experiencing a revival of interest in agriculture. Yet, the ability of mixing to control pests is highly variable and often unpredictable in the field. Beyond classical diversity effects such as dispersal barrier generated by genotypic diversity, several understudied processes are involved. Among them is the recently discovered neighbor-modulated susceptibility (NMS), which depicts the phenomenon that susceptibility in a given plant is affected by the presence of another healthy neighboring plant. Despite the putative tremendous importance of NMS for crop science, its occurrence and quantitative contribution to modulating susceptibility in cultivated species remains unknown. Here, in both rice and wheat inoculated in greenhouse conditions with foliar fungal pathogens considered as major threats, using more than 200 pairs of intraspecific genotype mixtures, we experimentally demonstrate the occurrence of NMS in 11% of the mixtures grown in experimental conditions that precluded any epidemics. Thus, the susceptibility of these 2 major crops results from indirect effects originating from neighboring plants. Quite remarkably, the levels of susceptibility modulated by plant-plant interactions can reach those conferred by intrinsic basal immunity. These findings open new avenues to develop more sustainable agricultural practices by engineering less susceptible crop mixtures thanks to emergent but now predictable properties of mixtures.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Agriculture
  • Crops, Agricultural
  • Disease Susceptibility
  • Oryza* / genetics
  • Triticum / genetics

Grants and funding

This work was supported by the Agence Nationale de la Recherche (ANR-16-IDEX-0006 AMUSER to CV), the CASDAR program (“BURRITOS” project to JBM), the INRAE LIA program (Plantomix project to JBM), the European Research Council (ERC) (Starting Grant Project “Ecophysiological and biophysical constraints on domestication in crop plants” ERC-StG-2014-639706-CONSTRAINTS to CV) and the National Natural Science Foundation of China (Grants 31801792 and 31960554 to HH). RP is supported by a PhD grant from Institut Agro. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.