Abstract
Besides the nuclear genome, plants possess two small extra chromosomal genomes in mitochondria and chloroplast, respectively, which contribute a small fraction of the organelles’ proteome. Both mitochondrial and chloroplast DNA have originated endosymbiotically and most of their prokaryotic genes were either lost or transferred to the nuclear genome through endosymbiotic gene transfer during the course of evolution. Due to their immobile nature, plant nuclear and organellar genomes face continuous threat from diverse exogenous agents as well as some reactive by-products or intermediates released from various endogenous metabolic pathways. These factors eventually affect the overall plant growth and development and finally productivity. The detailed mechanism of DNA damage response and repair following accumulation of various forms of DNA lesions, including single and double-strand breaks (SSBs and DSBs) have been well documented for the nuclear genome and now it has been extended to the organelles also. Recently, it has been shown that both mitochondria and chloroplast possess a counterpart of most of the nuclear DNA damage repair pathways and share remarkable similarities with different damage repair proteins present in the nucleus. Among various repair pathways, homologous recombination (HR) is crucial for the repair as well as the evolution of organellar genomes. Along with the repair pathways, various other factors, such as the MSH1 and WHIRLY family proteins, WHY1, WHY2, and WHY3 are also known to be involved in maintaining low mutation rates and structural integrity of mitochondrial and chloroplast genome. SOG1, the central regulator in DNA damage response in plants, has also been found to mediate endoreduplication and cell-cycle progression through chloroplast to nucleus retrograde signaling in response to chloroplast genome instability. Various proteins associated with the maintenance of genome stability are targeted to both nuclear and organellar compartments, establishing communication between organelles as well as organelles and nucleus. Therefore, understanding the mechanism of DNA damage repair and inter compartmental crosstalk mechanism in various sub-cellular organelles following induction of DNA damage and identification of key components of such signaling cascades may eventually be translated into strategies for crop improvement under abiotic and genotoxic stress conditions. This review mainly highlights the current understanding as well as the importance of different aspects of organelle genome maintenance mechanisms in higher plants.
Highlights
In plants, mitochondria and chloroplast are double membrane bound semi autonomous organelles having self contained genetic materials and equipped with the associated molecular machinery for regulation of gene expression (Gutman and Niyogi, 2009; Smith and Keeling, 2015; Gray, 2017; Peralta-Castro et al, 2020)
Since their discovery about half a century ago, significant progress has been made on the sequencing and characterization of mitochondrial and chloroplast genome
It has long been considered that bona fide DNA damage repair mechanism is absent in both plant mitochondria and chloroplast genomes
Summary
Mitochondria and chloroplast are double membrane bound semi autonomous organelles having self contained genetic materials (mt-DNA and cp-DNA, respectively) and equipped with the associated molecular machinery for regulation of gene expression (Gutman and Niyogi, 2009; Smith and Keeling, 2015; Gray, 2017; Peralta-Castro et al, 2020). The endosymbiotic origin of mitochondria and chloroplast from cyanobacteria and α-proteobacteria, respectively has indicated the presence of prokaryotic mode of replication and repair machineries in both the organelles (Ahmad and Nielsen, 2020) These replication or recombination/repair proteins, which participate in genome stability maintenance mechanisms in mitochondria and chloroplast, are encoded by either of these organellar genomes (Morley et al, 2019; Brieba, 2019). More than 95% of chloroplast proteins, including those associated with the maintenance of cp-DNA have been shown to be encoded by the nuclear genome (Green, 2011), which contains all the required genetic information for chloroplast functioning and plant survival (Woodson and Chory, 2008) Both mitochondria and chloroplast genomes have been shown to experience considerable magnitude of homologous recombination and gene conversion events between comparable DNA sequences (Maréchal and Brisson, 2010; Wu et al, 2020). This review mainly summarizes the current understanding of different aspects of organelle genome maintenance mechanisms in higher plants along with the possible applications of genetic manipulations of organellar genomes in crop improvement
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