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Multichromosomal structure and foreign tracts in the Ombrophytum subterraneum (Balanophoraceae) mitochondrial genome

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Abstract

Horizontal gene transfer (HGT) is frequent in parasitic plant mitochondria as a result of vascular connections established in host-parasite relationships. Recent studies of the holoparasitic plant Lophophytum mirabile (Balanophoraceae) revealed the unprecedented acquisition of a large amount of mitochondrial sequences from its legume host. We focused on a close relative, the generalist holoparasite Ombrophytum subterraneum, to examine the incidence of HGT events in the mitochondrial genome (mtDNA). The mtDNA of O. subterraneum assembles into 54 circular chromosomes, only 34 of which contain the 51 full-length coding regions. Numerous foreign tracts (totaling almost 100 kb, ~ 14% of the mtDNA), including 12 intact genes, were acquired by HGT from the Asteraceae hosts. Nine chromosomes concentrate most of those regions and eight are almost entirely foreign. Native homologs of each foreign gene coexist in the mtDNA and are potentially functional. A large proportion of shorter regions were related to the Fabaceae (a total of ~ 110 kb, 15.4%), some of which were shared with L. mirabile. We also found evidence of foreign sequences donated by angiosperm lineages not reported as hosts (Apocynaceae, Euphorbiaceae, Lamiaceae, and Malvales). We propose an evolutionary hypothesis that involves ancient transfers from legume hosts in the common ancestor of Ombrophytum and Lophophytum followed by more recent transfer events in L. mirabile. Besides, the O. subterraneum mtDNA was also subjected to additional HGT events from diverse angiosperm lineages, including large and recent transfers from the Asteraceae, and also from Lamiaceae.

Key message

The O. subterraneum mtDNA harbors foreign mitochondrial regions from diverse angiosperms, including 14 and 15% acquired from host lineages Asteraceae and Fabaceae. Twelve intact foreign genes coexist with native homologs.

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Acknowledgements

We thank A.A. Edera for help with scripts and graphs and J.D. Palmer for critical reading of the manuscript. This work was supported by Agencia Nacional de Promoción Científica y Tecnológica (Grant No PICT-0691) and Universidad Nacional de Cuyo (Grant No 06/A724) to M.V.S.P, and by NSF (Grant No 1062432) to Indiana University, which supports the computer cluster.

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  1. IBAM, Universidad Nacional de Cuyo, CONICET, Facultad de Ciencias Agrarias, Almirante Brown 500, M5528AHB, Chacras de Coria, Mendoza, Argentina

    M. Emilia Roulet, Laura E. Garcia, Carolina L. Gandini, Gabriela Ponce & M. Virginia Sanchez-Puerta

  2. Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Cuyo, Padre Jorge Contreras 1300, M5502JMA, Mendoza, Argentina

    Laura E. Garcia, Gabriela Ponce & M. Virginia Sanchez-Puerta

  3. Facultad de Ciencias Agrarias, Universidad Nacional de Jujuy, Cátedra de Botánica General–Herbario JUA, Alberdi 47, 4600, San Salvador de Jujuy, Jujuy, Argentina

    Hector Sato

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  1. M. Emilia Roulet
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Contributions

MER and MVSP designed the study, analyzed the data and wrote the manuscript. H.S. was involved in sample collection and taxonomic identification. LEG and GP performed host and parasite DNA extraction and purification and participated in the analysis. CLG assembled the mtDNA and helped with scripts for data analyses.

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Correspondence to M. Virginia Sanchez-Puerta.

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Roulet, M.E., Garcia, L.E., Gandini, C.L. et al. Multichromosomal structure and foreign tracts in the Ombrophytum subterraneum (Balanophoraceae) mitochondrial genome. Plant Mol Biol 103, 623–638 (2020). https://doi.org/10.1007/s11103-020-01014-x

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