98195-5065 (G.A.M., T.L., C.Q.)The crucial role of microRNAs in plant development is exceedingly well supported; their importance in environmental robustness is studied in less detail. Here, we describe a novel, environmentally dependent phenotype in hypomorphic argonaute1 (ago1) mutants and uncover its mechanistic underpinnings in Arabidopsis (Arabidopsis thaliana). AGO1 is a key player in microRNA-mediated gene regulation. We observed transparent lesions on embryonic leaves of ago1 mutant seedlings. These lesions increased in frequency in full-spectrum light. Notably, the lesion phenotype was most environmentally responsive in ago1-27 mutants. This allele is thought to primarily affect translational repression, which has been linked with the response to environmental perturbation. Using several lines of evidence, we found that these lesions represent dead and dying tissues due to an aberrant hypersensitive response. Although all three canonical defense hormone pathways (salicylic acid, jasmonate, and jasmonate/ethylene pathways) were up-regulated in ago1 mutants, we demonstrate that jasmonate perception drives the lesion phenotype. Double mutants of ago1 and coronatine insensitive1, the jasmonate receptor, showed greatly decreased frequency of affected seedlings. The chaperone HEAT SHOCK PROTEIN 90 (HSP90), which maintains phenotypic robustness in the face of environmental perturbations, is known to facilitate AGO1 function. HSP90 perturbation has been shown previously to upregulate jasmonate signaling and to increase plant resistance to herbivory. Although single HSP90 mutants showed subtly elevated levels of lesions, double mutant analysis disagreed with a simple epistatic model for HSP90 and AGO1 interaction; rather, both appeared to act nonadditively in producing lesions. In summary, our study identifies AGO1 as a major, largely HSP90-independent, factor in providing environmental robustness to plants. ARGONAUTE1 (AGO1) is an ancient, highly conserved essential protein. One of 10 functionally distinct AGO proteins in the plant Arabidopsis (Arabidopsis thaliana), AGO1 uses microRNAs (miRNAs) to decrease the expression of target genes. AGO1 and the miRNA pathway are crucial for many regulatory processes throughout development and in response to environmental stimuli. As frequent components of feedforward loops, miRNAs also play important roles in controlling gene expression noise and maintaining the phenotypic robustness of specific traits in several organisms, including plants ( Lempe et al., 2013).AGO1 and miRNAs also are critical for proper plant responses to abiotic stress. The expression levels of miRNAs respond to heat shock, cold, drought, oxidative stress, UV light exposure, and hypoxia (Sunkar et al., 2012). For example, in response to drought, the expression of miR169 decreases and the expression of its target gene, encoding the transcription factor NFYA5, increases in Arabidopsis (Li et al., 2008). Increased expression of NFYA5 supports plant survival in drought conditions. Transgenic plants ove...