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. The potential evolutionary advantage of such regulation remains largely unknown and might be related to two nonexclusive scenarios: (i) miRNA-dependent regulation of NLR levels might prevent defense mis-activation with negative effects on plant growth and reproduction or (ii) reduction of active miRNA levels in response to pathogen-derived molecules (pathogen-associated molecular patterns [PAMPs] and silencing suppressors) might rapidly release otherwise silent NLR transcripts for rapid translation and thereby enhance defense. 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 defense against the fungal pathogen Plectosphaerella cucumerina. We show that miR472 regulation has a dual role, participating both in the tight regulation of plant defense and growth. MIM472 lines, with reduced active miR472, are more resistant to pathogens and, correlatively, have reduced relative growth compared with wild-type plants, although the end of their reproductive phase is delayed, exhibiting higher adult biomass and similar seed yield as the wild-type. Our study highlights how negative consequences of defense activation might be compensated by changes in phenology and that miR472 reduction is an integral part of plant defense responses. [Formula: see text] Copyright © 2024 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.
Keywords: defense; development; evolution; microRNA; nucleotide-binding leucine-rich repeat protein; pathogen sensor; trade-off.