Abstract

The transfer of genetic material from the mitochondria and plastid to the nucleus gives rise to nuclear integrants of mitochondrial DNA (NUMTs) and nuclear integrants of plastid DNA (NUPTs). This frequently occurring DNA transfer is ongoing and has important evolutionary implications. In this review, based on previous studies and the analysis of NUMT/NUPT insertions of more than 200 sequenced plant genomes, we analyzed and summarized the general features of NUMTs/NUPTs and highlighted the genetic consequence of organellar DNA insertions. The statistics of organellar DNA integrants among various plant genomes revealed that organellar DNA-derived sequence content is positively correlated with the nuclear genome size. After integration, the nuclear organellar DNA could undergo different fates, including elimination, mutation, rearrangement, fragmentation, and proliferation. The integrated organellar DNAs play important roles in increasing genetic diversity, promoting gene and genome evolution, and are involved in sex chromosome evolution in dioecious plants. The integrating mechanisms, involving non-homologous end joining at double-strand breaks were also discussed.

Highlights

  • Three genetic compartments coexist in the plant cells: the nucleus and two cytoplasmic organelles, namely, chloroplast and mitochondria

  • The organelle-derived DNAs in the nucleus are designated as nuclear integrants of plastid DNA (NUPTs) and nuclear integrants of mitochondrial DNA (NUMTs)

  • Sequence analysis revealed that such terminal micro-identities have been presented for NUMT integrants in humans [99,100], indicating that organellar fragments integrating into the nuclear genome via nonhomologous end-joining mechanism (NHEJ) during double-stranded break (DSB) repair process might be a common mechanism conserved in eukaryotic organisms

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Summary

Introduction

Three genetic compartments coexist in the plant cells: the nucleus and two cytoplasmic organelles, namely, chloroplast (plastid) and mitochondria. Mitochondrion and chloroplast DNA have been integrated to the nuclear genome with high frequency, whereas other types of transfer occur rarely. With the rapid development of high-throughput sequencing technology, the plastid, mitochondrial, and nuclear genomes of a number of plant species have been deciphered. This makes the large-scale analysis of NUPTs and NUMTs in plants be possible. The characterization of nuclear organellar DNAs in plants adds new insights into the role of NUPTs and NUMTs in genome structure and evolution. We summarized recent advances in organelle-derived sequences and genome evolution in plants, with focus on the evolutionary fate of these insertions and the roles of NUPTs/NUMTs in the structure and evolution of plant genomes

Characterization of Organellar DNA-Derived Sequences in Plants
Number and Size Distribution
Modification Pattern
Transfer Rate of Organellar DNA to Nucleus
Elimination
Fragmentation
Rearrangement
Proliferation
Contribution to the Genetic Diversity
Effects on Gene Structure and Evolution
Roles Played in the Sex Chromosome Evolution
Mechanisms of Organellar DNA Integration
Findings
Conclusions and Perspective

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