RUG3 and ATM synergistically regulate the alternative splicing of mitochondrial nad2 and the DNA damage response in Arabidopsis thaliana

Abstract

The root apical meristem (RAM) determines both RAM activity and the growth of roots. Plant roots are constantly exposed to adverse environmental stresses that can cause DNA damage or cell cycle arrest in the RAM; however, the mechanism linking root meristematic activity and RAM size to the DNA damage response (DDR) is unclear. Here, we demonstrate that a loss of function in RCC1/UVR8/GEF-Like 3 (RUG3) substantially augmented the DDR and produced a cell cycle arrest in the RAM in rug3 mutant, leading to root growth retardation. Furthermore, the mutation of RUG3 caused increased intracellular reactive oxygen species (ROS) levels, and ROS scavengers improved the observed cell cycle arrest and reduced RAM activity level in rug3 plants. Most importantly, we detected a physical interaction between RUG3 and ataxia telangiectasia mutated (ATM), a key regulator of the DDR, suggesting that they synergistically modulated the alternative splicing of nad2. Our findings reveal a novel synergistic effect of RUG3 and ATM on the regulation of mitochondrial function, redox homeostasis, and the DDR in the RAM, and outline a protective mechanism for DNA damage repair and the restoration of mitochondrial function that involves RUG3-mediated mitochondrial retrograde signaling and the activation of an ATM-mediated DDR pathway.

Role of pyrimidine salvage pathway in the maintenance of organellar and nuclear genome integrity

“…A plethora of retrograde signalling routes have been described ( de Souza et al ., ), however, and further studies will be needed to determine how they are connected to the DDR. Recently, in Arabidopsis, it was shown that the N‐terminal of ATM interacts with RUG3, a mitochondria protein, and that this interaction occurs within organelles, possibly to control the organelle DDR (Su et al ., ). In line with these findings, we observed that DDR components are required for plant tolerance to organelle DNA damage.…”

Analysis of the Roles of the Arabidopsis nMAT2 and PMH2 Proteins Provided with New Insights into the Regulation of Group II Intron Splicing in Land-Plant Mitochondria

“…Other proteins that influence the splicing of group II introns in plant organelles include pentatricopeptide repeat (PPR) proteins, chloroplast RNA maturation (CRM)-related factors (i.e., the mCSF1 protein), members of the plant organellar RNA recognition (PORR) family, mitochondrial transcription termination factor (mTERF) related proteins and several other factors, which are seemingly unique to eukaryotes and are thus expected to evolve from the host genomes to function in organellar group II intron splicing in plants (reviewed in, e.g., [ 12 , 14 , 15 , 30 ]). Some of the proteins, such as nMAT2 [ 33 ], PMH2 [ 37 ] and mCSF1 [ 40 ], are required for the processing of a larger set of introns, while other factors such as PPR proteins (see, e.g., [ 41 , 42 , 43 , 44 , 45 , 46 , 47 , 48 , 49 ]) and mTERF15 [ 50 ] appear to be more specific, influencing the splicing of a single or only a few group II introns [ 14 ].…”

Alternative splicing results in a lack of starch synthase IIa-D in Chinese wheat landrace

“…Pre-mRNA splicing produces extensive proteomic and regulatory diversity during development. Accurate modulation of pre-mRNA splicing is essential for normal cellular functions in wheat, rice, and Arabidopsis (Fang et al 2017;Xia et al 2017;Marquez et al 2012;Su et al 2017). In plants, approximately 20% of the genes have multiple isoforms of transcripts that play various role in photosynthesis, disease resistance, flowering, quality, and other physiology processes (Wang et al 2006;Barbazuk et al 2008;Reddy 2007;Sestili et al 2015).…”