Multiple modes of convergent adaptation in the spread of glyphosate-resistant Amaranthus tuberculatus

Abstract

The selection pressure exerted by herbicides has led to the repeated evolution of herbicide resistance in weeds. The evolution of herbicide resistance on contemporary timescales in turn provides an outstanding opportunity to investigate key questions about the genetics of adaptation, in particular, the relative importance of adaptation from new mutations, standing genetic variation, or geographic spread of adaptive alleles through gene flow. Glyphosate-resistant Amaranthus tuberculatus poses one of the most significant threats to crop yields in the midwestern United States (1), with both agricultural populations and herbicide resistance only recently emerging in Canada (2, 3). To understand the evolutionary mechanisms driving the spread of resistance, we sequenced and assembled the A. tuberculatus genome and investigated the origins and population genomics of 163 resequenced glyphosate-resistant and susceptible individuals from Canada and the USA. In Canada, we discovered multiple modes of convergent evolution: in one locality, resistance appears to have evolved through introductions of preadapted US genotypes, while in another, there is evidence for the independent evolution of resistance on genomic backgrounds that are historically nonagricultural. Moreover, resistance on these local, non-agricultural backgrounds appears to have occurred predominantly through the partial sweep of a single haplotype. In contrast, resistant haplotypes arising from the midwestern US show multiple amplification haplotypes segregating both between and within populations. Therefore, while the remarkable species-wide diversity of A. tuberculatus has facilitated geographic parallel adaptation of glyphosate resistance, more recently established agricultural populations are limited to adaptation in a more mutation-limited framework.

Molecular mechanisms of adaptive evolution revealed by global selection for glyphosate resistance

“…() demonstrated multiple origins of glyphosate resistance in populations of Conyza canadensis in the Central Valley of California. Recently, multiple origins of glyphosate resistance were identified in A. tuberculatus by whole‐genome resequencing, showing both the introduction of glyphosate resistance into Canada from the USA as well as independent evolution of glyphosate resistance in other populations in Canada (Kreiner et al ., ). Others have shown that glyphosate resistance traits can be spread through hybridization between related Amaranthus species (Gaines et al ., ; Nandula et al ., ).…”

Mechanisms of evolved herbicide resistance

“…Draft genomes have recently been obtained for some of our most important herbicide-resistant weeds, including A. tuberculatus (156), C. canadensis (157), B. scoparia (64), R. raphanistrum (158), E. crus-galli (159), and E. indica (160). Although some of these genomes are still highly fragmented, those of A. tuberculatus, C. canadensis, and E. crus-galli have N50s greater than 1.5 Mb (N50 is the length of a computationally-assembled contiguous sequence for which 50% of the sequences in an assembly are longer and 50% are shorter; longer N50 indicates a better assembly).…”

The EccDNA Replicon: A Heritable, Extranuclear Vehicle That Enables Gene Amplification and Glyphosate Resistance in Amaranthus palmeri

“…The high degree of synteny and collinearity between Angiosperms can offer insights into the genomic origin(s) of the eccDNA replicon. The eccDNA replicon was aligned to the two closely related species grain amaranth (Amaranthus hypochondriacus) and waterhemp (Amaranthus tuberculatus), each with a haploid chromosome number (n=16) and pseudochromosome-scale reference genome assemblies (Lightfoot et al, 2017;Kreiner et al, 2019). Both comparator genome assemblies have a single copy of the EPSPS gene located near the middle of scaffold 5 (Figure 3).…”