Loss-of-function in GIGANTEA confers resistance to PPO-inhibiting herbicide tiafenacil through transcriptional activation of antioxidant genes in Arabidopsis

Abstract

Herbicides play a crucial role in maintaining crop productivity by reducing competition between weeds and crops. Protoporphyrinogen oxidase (PPO)-inhibiting herbicides trigger the photooxidative damage that destroys cell membranes. Tiafenacil is a recently developed pyrimidinedione-type PPO-inhibiting herbicide that has low IC50 values in plants and is less toxic in humans compared to other PPO inhibitors. Previous reports confirmed that mutations in Arabidopsis circadian clock-controlled gene GIGANTEA (GI) were insensitive to phytooxidants, including chloroplast biogenesis inhibitors and herbicides. Here, we examined whether GI regulates the resistance to tiafenacil. Both gi mutant alleles, gi-1 and gi-2, were resistant to tiafenacil with survival rates of 97% and 83%, respectively, under 1 µM tiafenacil treatments, while 56% of wild-type and GI-overexpressing plants (GI-OX) survived. Both gi mutants were insensitive to tiafenacil-induced inhibition of photosystem efficiency and alleviated photooxidative damage. The gi mutants showed significant increases in transcriptional expressions and enzyme activities of antioxidants compared to wild-type and GI-OX. Moreover, loss-of-function in GI enhanced resistance to tiafenacil-containing commercial herbicide Terrad’or Plus®. Collectively, based on our results together with previous reports, mutations in GI confer resistance to herbicides with different MoAs and would be a crucial molecular target for non-target-site resistance strategies to develop herbicide-resistant crops.