An Insight Into the Mechanism of Plant Organelle Genome Maintenance and Implications of Organelle Genome in Crop Improvement: An Update

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.

RETRACTED: UPL5 modulates WHY2 protein distribution in a Kub-site dependent ubiquitination in response to [Ca2+]cyt-induced leaf senescence

“… 30 , 31 , 44 WHY2 protein in potato and WHY1 and WHY3 proteins in Arabidopsis are also involved in maintaining low mutation rates and structural integrity of mitochondrial and chloroplast genomes. 27 , 28 , 29 , 45 The crystal structure of Solanum tuberosum WHY2, a close homolog of Arabidopsis WHY2, revealed that WHIRLY proteins bind to single-strand DNA to promote accurate repair of DNA double-strand breaks over an error-prone repair pathway 29 . We supposed that the allocation of WHY2 between cytoplasm and plastid by UPL5 is involved in maintaining plastid genome stability.…”

Challenges Facing CRISPR/Cas9-Based Genome Editing in Plants

“…Although the plant plastid transformation has been successful, there are also limitations associated with its use, such as the frequent inability to obtain progeny harboring the transgene, as well as the need for specialized instruments ( Piatek et al, 2018 ; Arimura et al, 2020 ). Importantly, organellar genome editing might now be achievable by expressing genes encoding sequence-specific nucleases in the organelles or in the nucleus ( Mahapatra et al, 2021 ; Hanson et al, 2013 ). The introduction of a transgene into the mitochondrial or chloroplast genome is mediated by homologous recombination and thus relies on DSB formation in the organellar genome ( Li et al, 2021a ; Mahapatra et al, 2021 ).…”

“…Importantly, organellar genome editing might now be achievable by expressing genes encoding sequence-specific nucleases in the organelles or in the nucleus ( Mahapatra et al, 2021 ; Hanson et al, 2013 ). The introduction of a transgene into the mitochondrial or chloroplast genome is mediated by homologous recombination and thus relies on DSB formation in the organellar genome ( Li et al, 2021a ; Mahapatra et al, 2021 ). Genome editing based on the sequence-specific nucleases ZFNs, TALENs, and CRISPR/Cas9 leads to precise DSBs that may therefore increase the efficiency of genome editing in these plant organelles.…”

Plant mitochondrial introns as genetic markers - conservation and variation

“…Plant genetic information is distributed among nuclear, plastid and mitochondrial genomes ( Mahapatra et al., 2021 ; Camus et al., 2022 ), and genetic markers for each genome provide complementary tools for investigations of inheritance and evolution ( Qiu et al., 1999 ; Duminil and Besnard, 2021 ; Besse, 2021 ; Camus et al., 2022 ). Although genome sequencing is the gold standard for such studies, convenient PCR-based markers retain utility and appeal ( Egan et al., 2012 ; Hodel et al., 2016 ; Besse, 2021 ).…”