Abstract
During adaptive radiation, mitochondria have coevolved with their hosts, leading to gain or loss of subunits and assembly factors of respiratory complexes. Plant complex I harbors ∼40 nuclear and 9 mitochondrial-encoded subunits and requires stepwise assembly for integrating different intermediates via assembly factors. In mammalian, the mitochondrial complex I intermediate assembly (MCIA) complex is required for building the membrane arm module. However,plants have lost almost all of the MCIA components, arising a hypothesis that plants follow an ancestral pathway to assemble the membrane arm subunits. Here, we characterize a maize crumpled seed mutant crp1, which encodes an ortholog of human complex I assembly factor 1, zNDUFAF1, the only evolutionarily conserved MCIA subunit in plants. It indeed localizes to mitochondria and accumulates in two intermediate complexes that contain complex I membrane arm subunits. Disruption of zNDUFAF1 results in severe defects in complex I assembly and activity, a cellular bioenergetic shift to aerobic glycolysis, and mitochondrial vacuolation. Moreover, we find that zNDUFAF1, the putative mitochondrial import inner membrane translocase ZmTIM17-1 and isovaleryl-CoA dehydrogenase ZmIVD1 mutually interact, coprecipitate from mitochondria, and comigrate in the same assembling intermediates. Perturbations of either ZmTIM17-1 or ZmIVD1 lead to the diminish of complex I stability and activity, and defective seeds. Thus, they probably form a MCIA-like complex that is essential for complex I biogenesis and seed development. Our findings suggest that plants and mammals recruit MCIA subunits independently for complex I assembly, revealing the importance of parallel evolution in mitochondria adaptation to their hosts.