Abstract
Main conclusion
The MIR gene is not an Oryza sativa orphan gene, but an Oryza genus-specific gene that evolved before AA lineage speciation by a complex origination process.
Abstract
Rice (Oryza sativa L.) is a model species and an economically relevant crop. The Oryza genus comprises 25 species, with genomic data available for several Oryza species, making it a model for genetics and evolution. The Mitochondrial Iron-Regulated (MIR) gene was previously implicated in the 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 Oryza sativa complex, which have AA genome type and constitute the primary gene pool for O. sativa breeding. Our data suggest that MIR originated in a stepwise process, in which sequences derived from an exon fragment of the raffinose synthase gene were pseudogenized into non-coding, which in turn originated the MIR gene de novo. All species with a putative functional MIR gene 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, leading to a lack of Fe deficiency responsiveness. Moreover, the 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 genus Oryza. We also showed that MIR is undergoing genomic changes in one species (O. barthii), with an impact on Fe deficiency response.
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source of the non-conding sequence present in chromosome 6 of almost all Oryza sativa complex, AA genome species. This event may have happened before Oryza sativa complex last common ancestor divergence, but seems to be lost to all but Oryza sativa complex species within Oryza (except O. meridionalis—which diverged earlier than O. glumaepatula—and O. longistaminata—which diverged later than O. glumaepatula). Given that O. glumaepatula has the regions where the non-coding sequence from chromosome 4 and chromosome 6 are found, but has only the chromosome 6 sequence, we suggest that the chromosome 6 was generated first, and was the source of MIR de novo origination—an event that occurred after O. glumeapatula speciation. After MIR origination, the sequence in chromosome 6 was also duplicated to generate the non-coding sequence in chromosome 4. The change in the chromosomal position of ObarMIR and the separation of its regulatory sequence is shown. It should be noted that the raffinose synthase gene also underwent duplication during the evolution of the monocot lineage. Coding exons are shown as rectangles; the MIR exon and the exon that originated the chromosome 6 non-coding region is shown in red, whereas other exons of raffinose synthase gene are shown in blue. Non-coding sequences originated from raffinose synthase exon are shown as white rectangles. The promoter region of MIR is shown as a thick line. Duplication events are highlighted by a yellow star
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Abbreviations
- MIR :
-
Mitochondrial Iron Regulated
- IDE1:
-
Iron deficiency element1
- IDEF1:
-
Iron deficiency element-binding factor1
- –Fe:
-
Fe deficiency
- MYA:
-
Million years ago
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Acknowledgements
This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-Brasil (CAPES)-Finance Code 001 and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), which granted fellowships to BHNO, AW, JPF and FKR. We also thank Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul. The authors would like to especially thank Tracy Punshon, from the Dartmouth College, USA, for proofreading the manuscript.
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de Oliveira, B.H.N., Wairich, A., Turchetto-Zolet, A.C. et al. The Mitochondrial Iron-Regulated (MIR) gene is Oryza genus specific and evolved before speciation within the Oryza sativa complex. Planta 251, 94 (2020). https://doi.org/10.1007/s00425-020-03386-2
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DOI: https://doi.org/10.1007/s00425-020-03386-2