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Evolution of an Ancient Microsatellite Hotspot in the Conifer Mitochondrial Genome and Comparison with Other Plants

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Abstract

In plants, mitochondrial sequence tandem repeats (STRs) have been associated with intragenomic recombination, a process held responsible for evolutionary outcomes such as gene regulation or cytoplasmic male-sterility. However, no link has been established between the recurrent accumulation of STRs and increased mutation rates in specific regions of the plant mtDNA genome. Herein, we surveyed this possibility by comparing, in a phylogenetic context, the variation of a STR-rich mitochondrial intron (nad5-4) with eleven mtDNA genes devoid of STRs within Abies (Pinaceae) and its related genera. This intron has been accumulating repeated stretches, generated by at least three-independent insertions, before the split of the two Pinaceae subfamilies, Abietoideae and Pinoideae. The last of these insertions occurred before the divergence of Abies and produced, exclusively within this genus, a tenfold increase of both the indel and substitution rates in the STR hotspot of the intron. The regions flanking the STRs harbored mutation rates as low as those estimated in mitochondrial genes devoid of repeated stretches. Further searches in complete plant mtDNA genomes, and previous studies reporting polymorphic mtSTRs, revealed that repeated stretches are common in all sorts of plants, but their accumulation in STR hotspots appears to be taxa specific. Our study suggests a new mutagenic role for repeated sequences in the plant mtDNA.

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Acknowledgments

We are grateful to J. Beaulieu, I. Gamache (Canadian Forest Service), C. Sayre (VanDusen Botanical Garden), F.T. Ledig (Univ. California-Davis), S.C. González-Martínez (CIFOR-INIA), P. Delgado, D. Gernandt, A. Keiman, Y. Nava, C. Saenz, and Glenn R. Furnier (Insts. of Biology and Ecology-UNAM) for valuable help during sample collections, and to S. Senneville, S. Gerardi (Univ. Laval), K. Budde, Y. Kurt, and M. Zabal (CIFOR-INIA) for assistance in the laboratory. Further thanks are extended to B. Morton, P. Canard and two anonymous reviewers for constructive comments on a previous draft of this manuscript. This research was financially supported by grants from the Ministère du développement économique de l’innovation et de l’exportation of Québec, the Natural Sciences and Engineering Research Council of Canada (Discovery program), the Consejo Nacional de Ciencia y Tecnología (CONACYT, Grants 153305 and 167826), the Comisión Nacional para el Conocimiento y el uso de la Biodiversidad (CONABIO, grant B138), and the Programa de Apoyo a las Divisiones de Estudios de Postgrado (PADEP-UNAM) and the Dirección General de Asuntos del Personal Académico (IN224309-3, IN202712 and IC200411) from the Universidad Nacional Autónoma de México.

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  1. Departamento de Ecología Evolutiva, Instituto de Ecología, Universidad Nacional Autónoma de México, Ciudad Universitaria, Circuito Exterior, Apartado Postal 70-275, Mexico, DF, Mexico

    Juan P. Jaramillo-Correa, Erika Aguirre-Planter & Luis E. Eguiarte

  2. Canada Research Chair in Forest and Environmental Genomics, Forest Research Centre and Institute for Systems and Integrative Biology, Université Laval, Quebec, QC, G1V 0A6, Canada

    Juan P. Jaramillo-Correa, Damase P. Khasa & Jean Bousquet

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  1. Juan P. Jaramillo-Correa
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Correspondence to Juan P. Jaramillo-Correa.

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Jaramillo-Correa, J.P., Aguirre-Planter, E., Eguiarte, L.E. et al. Evolution of an Ancient Microsatellite Hotspot in the Conifer Mitochondrial Genome and Comparison with Other Plants. J Mol Evol 76, 146–157 (2013). https://doi.org/10.1007/s00239-013-9547-2

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