Horizontal gene transfers dominate the functional mitochondrial gene space of a holoparasitic plant

GARCIA, LAURA E.; EDERA, ALEJANDRO A.; PALMER, JEFFREY D.; SATO, HECTOR; SANCHEZ-PUERTA, M. VIRGINIA

NEW PHYTOLOGIST

WILEY-BLACKWELL PUBLISHING, INC

Año: 2021

0028-646X

Although horizontal gene transfer (HGT) is common in angiosperm mitochondrial DNAs(mtDNAs), few cases of functional foreign genes have been identified. The one outstandingcandidate for large-scale functional HGT is the holoparasite Lophophytum mirabile, whosemtDNA has lost most native genes but contains intact foreign homologs acquired fromlegume host plants. To investigate the extent to which this situation results from functional replacement ofnative by foreign genes, functional mitochondrial gene transfer to the nucleus, and/or loss ofmitochondrial biochemical function in the context of extreme parasitism, we examined theLophophytum mitochondrial and nuclear transcriptomes by deep paired-end RNA sequenc-ing. Most foreign mitochondrial genes in Lophophytum are highly transcribed, accuratelyspliced, and efficiently RNA edited. By contrast, we found no evidence for functional genetransfer to the nucleus or loss of mitochondrial functions in Lophophytum. Many functionalreplacements occurred via the physical replacement of native genes by foreign genes. Someof these events probably occurred as the final act of HGT itself. Lophophytum mtDNA has experienced an unprecedented level of functional replacementof native genes by foreign copies. This raises important questions concerning population-ge-netic and molecular regimes that underlie such a high level of foreign gene takeover.