Plant Organellar DNA Polymerases Evolved Multifunctionality through the Acquisition of Novel Amino Acid Insertions

Abstract

The majority of DNA polymerases (DNAPs) are specialized enzymes with specific roles in DNA replication, translesion DNA synthesis (TLS), or DNA repair. The enzymatic characteristics to perform accurate DNA replication are in apparent contradiction with TLS or DNA repair abilities. For instance, replicative DNAPs incorporate nucleotides with high fidelity and processivity, whereas TLS DNAPs are low-fidelity polymerases with distributive nucleotide incorporation. Plant organelles (mitochondria and chloroplast) are replicated by family-A DNA polymerases that are both replicative and TLS DNAPs. Furthermore, plant organellar DNA polymerases from the plant model Arabidopsis thaliana (AtPOLIs) execute repair of double-stranded breaks by microhomology-mediated end-joining and perform Base Excision Repair (BER) using lyase and strand-displacement activities. AtPOLIs harbor three unique insertions in their polymerization domain that are associated with TLS, microhomology-mediated end-joining (MMEJ), strand-displacement, and lyase activities. We postulate that AtPOLIs are able to execute those different functions through the acquisition of these novel amino acid insertions, making them multifunctional enzymes able to participate in DNA replication and DNA repair.

Genetic dissection of marker trait associations for grain micro-nutrients and thousand grain weight under heat and drought stress conditions in wheat

“…Stably identified MTA for TGW under different treatments and combined BLUP, AX-94926681 located on chromosome 6A, was identified with transcript TraesCS6A02G402600. The locus codes for three major enzymes ribonuclease H-like and exonuclease and RNase T/DNA polymerase III were identified and are related to the enzymes responsible for nucleic acid metabolism, replication, homologous recombination, DNA repair, transposition ( Majorek et al., 2014 ), epigenetic changes at RNAPIII ( Hummel and Liu, 2022 ), and the repair of double-stranded breaks in Arabidopsis thaliana ( Peralta-Castro et al., 2020 ). Their presence as an integral part of the membrane and property of DNA binding further confirms the results based on gene ontology.…”

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

“…However, despite the continuous assault of oxidative damage, sequence drift in both plant mitochondrial and chloroplast genomes remains very low, indicating the presence of an efficient organellar DNA damage repair system. Recently, several studies have demonstrated that as like nuclear genome, the BER pathway also participates in the repair of oxidative DNA damages in the organellar genome ( Boesch et al, 2009 ; Gredilla, 2010 ; Boesch et al, 2011 ; Prakash and Doublié, 2015 ; Peralta-Castro et al, 2020 ). BER in plants is a crucial genome defense pathway, comprising of sequential steps, including excision of the damaged DNA base, splitting of the sugar-phosphate backbone of DNA at the AP (apurinic/apyrimidinic) site, reorganizing the resulting DNA ends, filling of gaps through DNA replication and finally DNA strand ligation ( Roldán-Arjona et al, 2019 ).…”

“…In plants, 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 ). Both chloroplast and mitochondrial DNA have originated endosymbiotically from cyanobacteria and α-proteobacteria, respectively ( Sagan, 1967 ; Dyall et al, 2004 ; Chevigny et al, 2020 ).…”

“…To maintain genome integrity under adverse conditions, plant mitochondria and chloroplast have evolved with an extensive regulatory mechanisms to counteract the deleterious effects of DNA damage ( Maréchal and Brisson, 2010 ; Oldenburg and Bendich, 2015 ; Ahmad and Nielsen, 2020 ). Plant mitochondria and chloroplast have been found to possess well-developed base excision repair (BER) pathways, comparable to the nuclear genome to cope up with different forms of oxidative DNA damages ( Boesch et al, 2009 ; Peralta-Castro et al, 2020 ). Besides oxidative lesions, double-strand breaks (DSBs), which are also generated in the organellar genome either spontaneously or in response to other stress signals, are predominantly repaired by various homology-dependent repair pathways, as unlike the nuclear genome, both the organelles lack the non-homologous end-joining NHEJ pathways ( Maréchal and Brisson, 2010 ).…”

Oxidative and Glycation Damage to Mitochondrial DNA and Plastid DNA during Plant Development

“…DNA molecules, however, are susceptible to damage of two types. Endogenous damage occurs when DNA polymerase makes mistakes [ 1 ], and when metabolic byproducts react with the DNA, either oxidatively or by glycation reactions [ 2 ]. Exogenous damage can be caused by radiation and toxins [ 3 ].…”