A transposon surveillance mechanism that safeguards plant male fertility during stress

Abstract

Although plants are able to withstand a range of environmental conditions, spikes in ambient temperature can impact plant fertility causing reductions in seed yield and significant economic losses1,2. Therefore, understanding the precise molecular mechanisms that underpin plant fertility under environmental constraints is critical to safeguard future food production3. Here, we identified two Argonaute-like proteins whose activities are required to sustain male fertility in maize plants under high temperatures. We found that MALE-ASSOCIATED ARGONAUTE 1 and 2 (MAGO1 and MAGO2) associate with temperature-induced phased secondary small RNAs in pre-meiotic anthers and are essential to control the activity of retrotransposons in male meiocyte initials. Biochemical and structural analyses revealed how MAGO2 activity and its interaction with retrotransposon RNA targets are modulated through the dynamic phosphorylation of a set of highly conserved surface-located serine residues. Our results demonstrate that an Argonaute-dependent RNA-guided surveillance mechanism is critical in plants to sustain male fertility under environmentally constrained conditions by controlling the mutagenic activity of transposons in male germ cells.