miR472 deficiency enhances Arabidopsis thaliana defence without reducing seed production

After having co-existed in plant genomes for at least 200 million years, the products of microRNA (miRNA) and Nucleotide-Binding Leucine Rich Repeat protein (NLR) genes formed a regulatory relationship in the common ancestor of modern gymnosperms and angiosperms. From then on, DNA polymorphisms occurring at miRNA target sequences within NLR transcripts must have been compensated by mutations in the corresponding mature miRNA sequence, therefore maintaining that regulatory relationship. The potential evolutionary advantage of such regulation remains largely unknown and might be related to two mutually non-exclusive scenarios: miRNA-dependent regulation of NLR levels might prevent defence mis-activation with negative effects on plant growth and reproduction; or reduction of active miRNA levels in response to pathogen derived molecules (PAMPS and silencing suppressors) might rapidly release otherwise silent NLR transcripts for rapid translation and thereby enhance defence. Here, we used Arabidopsis thaliana plants deficient for miR472 function to study the impact of releasing its NLR targets on plant growth and reproduction and on defence against the fungal pathogen Plectospharaella cucumerina. We show that miR472 regulation has a dual role, participating both in the tight regulation of plant defence and growth. MIM472 lines, with reduced active miR472, are more resistant to pathogens and, correlatively, have reduced relative growth compared to wild-type plants. However, despite MIM472 lines flower at the same time than their wild-type, the end of their reproductive phase is delayed, and they exhibit higher adult biomass, resulting in similar seed yield as the wild-type. Our study highlights how negative consequences of defence activation might be compensated by changes in phenology and that miR472 reduction is an integral part of plant defence responses.