Pervasive horizontal gene transfer in the mitochondrial genomes of holoparasites (Balanophoraceae)

ROULET ME.; CERIOTTI LF.; SANCHEZ-PUERTA, MV.

Congreso; Primer Congreso Latinoamericano de Evolución (CLEVOL); 2021

Plant vascular connections established in a host-parasite relationship allow the passage of water, nutrients, and nucleic acids. This intimate contact promotes the exchange of genetic information between unrelated species, a process named Horizontal Gene Transfer (HGT). Plant mitochondrial genomes (mtDNAs) are frequently impacted by HGT. We deciphered the mtDNA of two holoparasitic angiosperms Ombrophytum subterraneum and Lophophytum leandri (Balanophoraceae). These plants grow in Argentina parasitizing roots of Asteraceae and Fabaceae species, respectively. Both mtDNAs are organized in a multichromosomal structure consisting of c.50 circular chromosomes, similar to the mtDNA of the relative Lophophytum mirabile. However, no chromosome equivalence is found among the three species and the similarity searches between the mtDNA of L.leandri and L.mirabile revealed only 46% of shared regions and even less (16%) when comparing L.leandri with Ombrophytum. Comprehensive phylogenetic analyses showed that L.leandri mtDNA harbors 5 foreign and 15 chimeric protein genes as a result of HGT from its legume hosts. Besides, twelve Ombrophytum protein genes were associated with Asteraceae species and no chimerism was detected. In Ombrophytum mtDNA, all foreign genes coexist with native homologs in contrast to the situation in Lophophytum mtDNA where foreign genes replaced the native counterpart. The overall impact of the HGT including noncoding regions indicates that L.leandri mtDNA presents 48.3% foreign legume sequences distributed across the chromosomes and Ombrophytum carries 14% from Asteraceae concentrated in only 9 chromosomes. Besides, we found evidence for ancient HGT events, in which foreign legume mitochondrial sequences were acquired before the divergence of both Lophophytum species.