Abstract

Due to the endosymbiotic origin of organelles, a pattern of coevolution and coadaptation between organellar and nuclear genomes is required for proper cell function. In this review, we focus on the impact of cytonuclear interaction on the reproductive isolation of plant species. We give examples of cases where species exhibit barriers to reproduction which involve plastid-nuclear or mito-nuclear genetic incompatibilities, and describe the evolutionary processes at play. We also discuss potential mechanisms of hybrid fitness recovery such as paternal leakage. Finally, we point out the possible interplay between plant mating systems and cytonuclear coevolution, and its consequence on plant speciation.

Highlights

  • Speciation is the evolutionary process that leads to the differentiation of distinct species from an ancestral population

  • The longer the species have diverged, the more they are expected to be reproductively isolated due to genetic differences, i.e., different fixed substitutions [4]. These mutations might have been directly selected by natural selection, for example if they confer a better adaptation to a given habitat, rendering the hybrid maladapted to both parental habitats

  • Accelerated rate of plastid evolution increases the propensity for CN incompatibilities (CNIs) as it leads to a faster coevolution of organellar and nuclear genomes within populations [20,54,55]

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Summary

Introduction

Speciation is the evolutionary process that leads to the differentiation of distinct species from an ancestral population. The longer the species have diverged, the more they are expected to be reproductively isolated due to genetic differences, i.e., different fixed substitutions [4]. These mutations might have been directly selected by natural selection, for example if they confer a better adaptation to a given habitat, rendering the hybrid maladapted to both parental habitats. We will assess how organellar genomes and their interaction with the nucleus can be involved in the process of speciation and reproductive isolation. Hybrids from reciprocal crosses often reveal an asymmetry in the level of reproductive isolation. Recent studies provide accumulative evidence of the frequent role of cytoplasmic genomes in adaptation and speciation in plants (reviewed in [9,11,12])

Coevolution between Nuclear and Organellar Genomes
Cytonuclear Incompatibilities
Acceleration of Organellar Genome Evolution Enhances the Propensity of CNIs
CNIs as the Result of Intergenomic Conflict—the CMS Case
Cytonuclear Coevolution and Environment
CNI Can Contribute to Speciation
Inheritance Patterns of the Organellar Genomes
Heteroplasmy
Paternal Leakage Rescues from Cytonuclear Incompatibilities
Findings
How Could Mating Systems Favor or Limit CNI?
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