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Pathogenicity and molecular mechanisms of the identified variants were studied in yeast and patient\u2010derived fibroblasts.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>Twelve cases (4%) were found to carry novel variants in <jats:italic>AFG3L2,<\/jats:italic> a gene that has been associated with autosomal dominant spinocerebellar ataxia 28 (SCA28). Half of cases were familial with a dominant inheritance, whereas the others were sporadic, including <jats:italic>de novo<\/jats:italic> mutations. Biallelic mutations were found in 3 probands with severe syndromic optic neuropathy, acting as recessive or phenotype\u2010modifier variants. All the DOA\u2010associated <jats:italic>AFG3L2<\/jats:italic> mutations were clustered in the ATPase domain, whereas SCA28\u2010associated mutations mostly affect the proteolytic domain. The pathogenic role of DOA\u2010associated <jats:italic>AFG3L2<\/jats:italic> mutations was confirmed in yeast, unraveling a mechanism distinct from that of SCA28\u2010associated <jats:italic>AFG3L2<\/jats:italic> mutations. Patients' fibroblasts showed abnormal OPA1 processing, with accumulation of the fission\u2010inducing short forms leading to mitochondrial network fragmentation, not observed in SCA28 patients' cells.<\/jats:p><\/jats:sec><jats:sec><jats:title>Interpretation<\/jats:title><jats:p>This study demonstrates that mutations in <jats:italic>AFG3L2<\/jats:italic> are a relevant cause of optic neuropathy, broadening the spectrum of clinical manifestations and genetic mechanisms associated with <jats:italic>AFG3L2<\/jats:italic> mutations, and underscores the pivotal role of OPA1 and its processing in the pathogenesis of DOA. 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