Genes encoding cytochrome P450 monooxygenases and glutathione S-transferases associated with herbicide resistance evolved before the origin of land plants

Abstract

Cytochrome P450 (CYP) monooxygenases and glutathione S-transferases (GST) are enzymes that catalyse chemical modifications of a range of organic compounds. Herbicide tolerance is associated with higher levels of CYP and GST gene expression in some herbicide-resistant weed populations compared to sensitive populations of the same species. By comparing the protein sequences of 9 representative species of the Archaeplastida - the lineage which includes red algae, glaucophyte algae, chlorophyte algae, and streptophytes - and generating phylogenetic trees, we identified the CYP and GST proteins that existed in the common ancestor of the Archaeplastida. All CYP clans and all but one land plant GST classes present in land plants evolved before the divergence of streptophyte algae and land plants from their last common ancestor. We also demonstrate that there are more genes encoding CYP and GST proteins in land plants than in algae. The larger numbers of genes among land plants largely results from gene duplications in CYP clans 71, 72, and 85 and in the GST Phi and Tau classes. Enzymes that either chemically alter herbicides or confer herbicide resistance belong to CYP clans 71 and 72 and the GST Phi and Tau classes. These results demonstrate that the clan and class diversity in extant plant CYP and GST proteins evolved in the Proterozoic before the divergence of land plants and streptophyte algae from a last common ancestor. Then, early in embryophyte evolution during the Palaeozoic, gene duplication in four of the twelve CYP clans, and in two of the fourteen GST classes, led to the large numbers of CYP and GST proteins found in extant land plants. It is among the genes of CYP clans 71 and 72 and GST classes Phi and Tau that alleles conferring herbicide resistance evolved in the last fifty years.