Trace concentrations of imazethapyr (IM) affect floral organs development and reproduction in Arabidopsis thaliana: IM-induced inhibition of key genes regulating anther and pollen biosynthesis

Abstract

Understanding how herbicides affect plant reproduction and growth is critical to develop herbicide toxicity model and refine herbicide risk assessment. Although our knowledge of herbicides toxicity mechanisms at the physiological and molecular level in plant vegetative phase has increased substantially in the last decades, few studies have addressed the herbicide toxicity problematic on plant reproduction. Here, we determined the long-term (4-8 weeks) effect of a chiral herbicide, imazethapyr (IM), which has been increasingly used in plant crops, on floral organ development and reproduction in the model plant Arabidopsis thaliana. More specifically, we followed the effect of two IM enantiomers (R- and S-IM) on floral organ structure, seed production, pollen viability and the transcription of key genes involved in anther and pollen development. The results showed that IM strongly inhibited the transcripts of genes regulating A. thaliana tapetum development (DYT1: DYSFUNCTIONAL TAPETUM 1), tapetal differentiation and function (TDF1: TAPETAL DEVELOPMENT AND FUNCTION1), and pollen wall formation and developments (AMS: ABORTED MICROSPORES, MYB103: MYB DOMAIN PROTEIN 103, MS1: MALE STERILITY 1, MS2: MALE STERILITY 2). Since DYT1 positively regulates 33 genes involved in cell-wall modification (such as, TDF1, AMS, MYB103, MS1, MS2) that can catalyze the breakdown of polysaccharides to facilitate anther dehiscence, the consistent decrease in the transcription of these genes after IM exposure should hamper anther opening as observed under scanning electron microscopy. The toxicity of IM on anther opening further lead to a decrease in pollen production and pollen viability. Furthermore, long-term IM exposure increased the number of apurinic/apyrimidinic sites (AP sites) in the DNA of A. thaliana and also altered the DNA of A. thaliana offspring grown in IM-free soils. Toxicity of IM on floral organs development and reproduction was generally higher in the presence of the R-IM enantiomer than of the S-IM enantiomer. This study unraveled several IM toxicity targets and mechanisms at the molecular and structural level linked to the toxicity of IM trace concentrations on A. thaliana reproduction.

Exposure to trace amounts of sulfonylurea herbicide tribenuron-methyl causes male sterility in 17 species or subspecies of cruciferous plants

“…Thus, an application of ALS-inhibiting gametocides on model plant A. thaliana to replace manual emasculation will be of interest to geneticists when they wish to make many genetic crosses. The results of the present study, combined with previous studies [12–14, 23, 24], suggest the possible use of other sulfonylurea chemicals as gametocides for cruciferous plants. The alternate use of other gametocides can resolve the concerns of insensitivity to tribenuron-methyl in some special genotypes.…”

“…A previous study also reported that a foliar spray of 15 ng of tribenuron-methyl per plant of A. thaliana had a gametocidal effect [23]. In addition, exposure to trace concentrations of imazethapyr, an ALS-inhibitor, had unstable gametocidal effects on Brassica plants [13] and affected floral organ development and reproduction in A. thaliana [24]. Thus, an application of ALS-inhibiting gametocides on model plant A. thaliana to replace manual emasculation will be of interest to geneticists when they wish to make many genetic crosses.…”

Effects of Herbicides on Flowering

“…Petal, anther, and pollen deformations have been reported for Brassica spp. flowers exposed to low doses of glyphosate (Londo et al 2014), and anther malformations and pollen quality reductions have been reported for imazethapyr (Qian et al 2015). Malformations including reduced disk diameter ( Tanacetum vulgare , Leucanthemum vulgare ) and ray floret length ( L. vulgare ) following application of drift relevant doses of glyphosate have been documented for 2 nontarget Asteraceae species (Strandberg et al 2017).…”

Herbicide-related signaling in plants reveals novel insights for herbicide use strategies, environmental risk assessment and global change assessment challenges

“…Mechanisms of primary sensing of xenobiotic structures, which have been characterized in animal cells, have however remained elusive in the case of plant cells (Ramel et al, 2012), even if various situations of plant-xenobiotic interactions suggest that such primary sensing may also exist in plant cells (Ramel et al, 2012). Qian et al (2015aQian et al ( , 2015b have shown that low levels of imazethapyr induced major metabolic and molecular changes in flowers or in roots. However, these imazethapyr treatments were carried out at IC50 concentrations yielding some level of toxicity.…”