The Mitochondrial Iron Regulated (MIR) gene is Oryza genus-specific and evolved before the speciation of major AA-genome lineages

Abstract

Rice (Oryza sativa L.) is both a model species and an economically relevant crop. The Oryza genus comprises 25 species, which constitute a genetic reservoir for cultivated rice breeding. Genomic data is available for several Oryza species, making it a good model for genetics and evolution within closely related species. The Mitochondrial Iron Regulated (MIR) gene was previously implicated in O. sativa Fe deficiency response, and was considered an orphan gene present only in rice. Here we show that MIR is also found in other Oryza species that belong to the AA genome group. We characterized the evolutionary pattern of MIR genes within the Oryza genus. Our data suggest that MIR originated de novo from non-coding sequences present only in AA genome species, but these sequences in turn are derived from an exon fragment of Raffinose Synthase genes, present in several groups of monocots. We also show that all species that have a putative functional MIR conserve their regulation by Fe deficiency, with the exception of Oryza barthii. In O. barthii, the MIR coding sequence was translocated to a different chromosomal position and separated from its regulatory region, which led to a lack of Fe deficiency responsiveness. Moreover, we show that MIR co-expression subnetwork cluster in O. sativa is responsive to Fe deficiency, evidencing the importance of the newly originated gene in Fe uptake. This work establishes that MIR is not an orphan gene as previously proposed, but a de novo originated gene within the Oryza genus. We also showed that MIR is undergoing genomic changes in at least one species (O. barthii), which can impact its role in Fe deficiency.