Signaling from Plastid Genome Stability Modulates Endoreplication and Cell Cycle during Plant Development

Abstract

Highlights d Plastid genome instability alters endoreplication and cell cycle d Plastid genome instability results in increased expression of cell-cycle-related genes d SOG1 mediates the activation of cell-cycle-related genes by plastid genome instability d ROS is required for communication of plastid genome with endoreplication and cell cycle

RADA is a main branch migration factor in plant mitochondrial recombination and its defect leads to mtDNA instability and cell cycle arrest

“…We also checked whether radA plants could have increased rearrangements of the cpDNA, as described for Arabidopsis why1why3 and why1why3reca1 Arabidopsis mutants, and for maize cptK1 (Duan et al, 2020; Le Ret et al, 2018; Zampini et al, 2015). Analysis by PCR using divergent primers has been used before to detect increased rearrangements of the cpDNA (Duan et al, 2020; Marechal et al, 2009). But in our hands, after testing six pairs of primers described in the literature we just obtained either negative or irreproducible results.…”

“…In plants, SMR genes encode inhibitors of CDK-cyclin complexes that are transcriptionally induced in response to changing conditions, integrating environmental and metabolic signals with cell cycle control (Dubois et al, 2018; Hudik et al, 2014; Yi et al, 2014). Interestingly, chloroplastic defects have been shown to induce cell cycle arrest through the induction of SMR5 and SMR7 (Duan et al, 2020; Hudik et al, 2014). How these genes are activated remains to be fully elucidated, but the mechanism could involve the activation of the DNA damage response (DDR).…”

“…The cell cycle is an energy demanding process that can be arrested by defects in respiration or photosynthesis (Riou-Khamlichi et al, 2000). Several studies have shown that chloroplastic defects lead to altered cell cycle regulation including reduced cell proliferation and premature endoreduplication (Duan et al, 2020; Hudik et al, 2014; Pedroza-Garcia et al, 2019). That seems to be also the case in radA, as suggested by the increased size of epidermal cells and confirmed by determination of nuclear ploidy, analysis of EdU incorporation and mitotic activity, although in this case endoreduplication was reduced in the radA mutant.…”

“…But just functional deficiency of OXPHOS complexes does not per se activate regulators of cell cycle, since in mutants of complex I there was no evidence for the activation of genes such as SMR5 or SMR7 (Meyer et al, 2009). In several chloroplast-deficient mutants such as crl or the triple reca1why1why3 , ROS accumulation is thought to activate the DNA Damage Response master regulator SOG1, leading to cell cycle arrest and activation of DNA repair (Duan et al, 2020; Hudik et al, 2014; Pedroza-Garcia et al, 2019). Indeed, DDR mutants and particularly sog1 are hypersensitive to genotoxins targeting organelles (Pedroza-Garcia et al, 2019) and ROS accumulation leads to SOG1 activation through its phosphorylation by the ATM kinase (Yi et al, 2014).…”

A new take on organelle‐mediated stress sensing in plants

“…Enhanced nuclear endoreplication and altered cell cycle regulation occur in response to chemical and genetic disruption of the plastid genome (Duan et al ., 2020). This phenomenon requires the gene SOG1 , a putative nuclear transcription factor responsive to DNA damage (Duan, et al ., 2020). Plastid genome disruption triggers increased ROS to effect this response and, remarkably, SOG1 interacts with Sucrose Nonfermenting‐Related Kinase 1 ( SnRK1 ) (Hamasaki et al ., 2019), reiterating the linkage of plastid status with energy homeostasis.…”