A high diversity of mechanisms endows ALS-inhibiting herbicide resistance in the invasive common ragweed (Ambrosia artemisiifolia L.)

Ingvild Loubet,Christophe Délye,Valérie Le Corre,Benoit Barrès,Laëtitia Caddoux,Fanny Pernin,Séverine Michel,Séverine Fontaine

doi:10.1038/s41598-021-99306-9

Abstract

Ambrosia artemisiifolia L. (common ragweed) is a globally invasive, allergenic, troublesome arable weed. ALS-inhibiting herbicides are broadly used in Europe to control ragweed in agricultural fields. Recently, ineffective treatments were reported in France. Target site resistance (TSR), the only resistance mechanism described so far for ragweed, was sought using high-throughput genotyping-by-sequencing in 213 field populations randomly sampled based on ragweed presence. Additionally, non-target site resistance (NTSR) was sought and its prevalence compared with that of TSR in 43 additional field populations where ALS inhibitor failure was reported, using herbicide sensitivity bioassay coupled with ALS gene Sanger sequencing. Resistance was identified in 46 populations and multiple, independent resistance evolution demonstrated across France. We revealed an unsuspected diversity of ALS alleles underlying resistance (9 amino-acid substitutions involved in TSR detected across 24 populations). Remarkably, NTSR was ragweed major type of resistance to ALS inhibitors. NTSR was present in 70.5% of the resistant plants and 74.1% of the fields harbouring resistance. A variety of NTSR mechanisms endowing different resistance patterns evolved across populations. Our study provides novel data on ragweed resistance to herbicides, and emphasises that local resistance management is as important as mitigating gene flow from populations where resistance has arisen.

Highlights

Ambrosia artemisiifolia L. is a globally invasive, allergenic, troublesome arable weed
Our work unravelled an unexpected diversity of herbicide resistance mechanisms in common ragweed in France
Common ragweed is a striking example of multiple, parallel evolution where a diversity of Target site resistance (TSR) and/or non-target site resistance (NTSR) mechanisms are selected for locally, and combined within populations as well as within individual plants

Summary

Introduction

Ambrosia artemisiifolia L. (common ragweed) is a globally invasive, allergenic, troublesome arable weed. ALS-inhibiting herbicides are broadly used in Europe to control ragweed in agricultural fields. Target site resistance (TSR), the only resistance mechanism described so far for ragweed, was sought using high-throughput genotypingby-sequencing in 213 field populations randomly sampled based on ragweed presence. Non-target site resistance (NTSR) was sought and its prevalence compared with that of TSR in 43 additional field populations where ALS inhibitor failure was reported, using herbicide sensitivity bioassay coupled with ALS gene Sanger sequencing. NTSR was ragweed major type of resistance to ALS inhibitors. The use of synthetic herbicides to control weeds since the middle of the twentieth century contributed to increase global crop yields. Following the intensive use of herbicides to control weeds, a number of weed species evolved mechanisms allowing them to survive and successfully reproduce in treated fields. Herbicide resistance can be defined as the natural, inheritable ability of mutant weed genotypes to survive herbicide concentrations that kill or inhibit the development of wild-type genotypes of the same species (sensitive genotypes), and/or as the outcome of the adaptive evolution of weeds as a result of selection for reduced sensitivity under herbicide selective pressure[2]

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Conclusion