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The Plant DNA Damage Response: Signaling Pathways Leading To The Plant DNA Damage Response: Signaling Pathways Leading to Growth Inhibition and Putative Role in Response to Stress Conditions Maher-Un Nisa, Ying Huang, Moussa Benhamed, Cécile Raynaud To cite this version: Maher-Un Nisa, Ying Huang, Moussa Benhamed, Cécile Raynaud. The Plant DNA Damage Response: Signaling Pathways Leading to Growth Inhibition and Putative Role in Response to Stress Conditions. Frontiers in Plant Science, Frontiers, 2019, 10, 10.3389/fpls.2019.00653. hal-02351967 HAL Id: hal-02351967 https://hal.archives-ouvertes.fr/hal-02351967 Submitted on 26 May 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License fpls-10-00653 May 17, 2019 Time: 15:12 # 1 REVIEW published: 17 May 2019 doi: 10.3389/fpls.2019.00653 The Plant DNA Damage Response: Signaling Pathways Leading to Growth Inhibition and Putative Role in Response to Stress Conditions Maher-Un Nisa, Ying Huang, Moussa Benhamed and Cécile Raynaud* Institute of Plant Sciences Paris-Saclay, IPS2, CNRS-INRA-University of Paris Sud, Paris-Diderot and Evry, University of Paris-Saclay, Gif-sur-Yvette, France Maintenance of genome integrity is a key issue for all living organisms. Cells are constantly exposed to DNA damage due to replication or transcription, cellular metabolic activities leading to the production of Reactive Oxygen Species (ROS) or even exposure to DNA damaging agents such as UV light. However, genomes remain extremely stable, thanks to the permanent repair of DNA lesions. One key mechanism contributing to genome stability is the DNA Damage Response (DDR) that activates DNA repair Edited by: pathways, and in the case of proliferating cells, stops cell division until DNA repair is Kaoru Okamoto Yoshiyama, complete. The signaling mechanisms of the DDR are quite well conserved between Tohoku University, Japan organisms including in plants where they have been investigated into detail over the Reviewed by: Thomas Eekhout, past 20 years. In this review we summarize the acquired knowledge and recent VIB-UGent Center for Plant Systems advances regarding the DDR control of cell cycle progression. Studying the plant DDR Biology, Belgium Naoki Takahashi, is particularly interesting because of their mode of development and lifestyle. Indeed, Nara Institute of Science plants develop largely post-embryonically, and form new organs through the activity and Technology (NAIST), Japan of meristems in which cells retain the ability to proliferate. In addition, they are sessile *Correspondence: organisms that are permanently exposed to adverse conditions that could potentially Cécile Raynaud [email protected] induce DNA damage in all cell types including meristems. In the second part of the review we discuss the recent findings connecting the plant DDR to responses to biotic Specialty section: and abiotic stresses. This article was submitted to Plant Cell Biology, Keywords: cell cycle checkpoint, DNA damage, biotic and abiotic stress, genome integrity, plants a section of the journal Frontiers in Plant Science Received: 01 April 2019 INTRODUCTION Accepted: 30 April 2019 Published: 17 May 2019 Maintenance of genome integrity is essential in all living organisms. It is required for proper Citation: development and for faithful transmission of the genetic information from one generation to Nisa M-U, Huang Y, Benhamed M the next. Yet, cells are constantly subjected to DNA damage. One major source of mutations and Raynaud C (2019) The Plant DNA is DNA metabolism itself, both during DNA replication and DNA repair. The error rate of the Damage Response: Signaling replication machinery is estimated in the range of 10−7 to 10−8. This low error rate results from Pathways Leading to Growth −6 −8 Inhibition and Putative Role the fidelity of replicative polymerases, which have an error rate between 10 and 10 , and the in Response to Stress Conditions. successful excision of 90–99% of mis-paired bases thanks to the proof-reading activity of these Front. Plant Sci. 10:653. complexes (Kunkel, 2004). DNA repair processes can also introduce errors, with a similar rate as doi: 10.3389/fpls.2019.00653 replication when they involve proof-reading polymerases, or with a higher rate when they involve Frontiers in Plant Science| www.frontiersin.org 1 May 2019| Volume 10| Article 653 fpls-10-00653 May 17, 2019 Time: 15:12 # 2 Nisa et al. DNA Damage and Stress Response alternative polymerases (Kunkel, 2004; Jain et al., 2018). Finally, Response (DDR) allows activation of cell cycle checkpoints unrepaired lesions can block the main replicative polymerases; and of specific DNA repair mechanisms (Yoshiyama et al., in that case, TransLesion Synthesis (TLS) Polymerases, take over 2013b; Hu et al., 2016). The DDR is highly conserved between (Uchiyama et al., 2009). They interact with each other, and are eukaryotes with some variations that will be briefly discussed thought to form a large complex at stalled forks to allow choosing below. Its ultimate outcome will depend on the severity of the best suited polymerase for each type of lesion (Powers and the DNA lesions and the efficiency of the repair process: cell Washington, 2018). Their ability to replicate DNA passed lesions cycle activity can resume if lesions are successfully repaired, makes them error-prone: their substitution rate when replicating but more severe DNA damage can induce endoreduplication undamaged templates is comprised between 10−3 and 10−1 (Adachi et al., 2011). This process corresponds to several rounds (Kunkel, 2004). In addition, DNA demethylation can also cause of DNA replication without mitosis, leading to an increase in mutations because it requires nucleotide removal followed by nuclear DNA content; it is widely distributed in plants such Base Excision Repair (BER) (He et al., 2011). as in Arabidopsis leaves or stems, fruits, and endosperm in Being sessile organisms, plants are constantly exposed to cereals (Galbraith et al., 1991), and is associated with cell stress conditions that can also damage their DNA. Indeed, differentiation and enlargement (Kondorosi et al., 2000). In the plants need light to grow photo-autotrophically, but UV light context of the DDR, it is thus seen as a permanent differentiation, induces DNA damage, notably in the form of cyclobutane thereby avoiding the proliferation of cells with damaged DNA. pyrimidines (CPDs). Likewise, the photosynthetic apparatus Interestingly, endoreduplication also exists in animals although generates Reactive Oxygen Species (ROS), especially when plants it is not as common as in plants, and can be triggered by DNA are exposed to excess light, either because the intensity is very damage, and could thus be a conserved response in eukaryotes high, or when other external conditions such as heat or drought (Fox and Duronio, 2013). Finally, depending on the cell type and reduce the plant’s capacity to consume the reducing power the severity of damage, DDR activation can result in programmed produced by light absorption in photosystems (Noctor and Foyer, cell death (PCD) (Furukawa et al., 2010). Interestingly, plant 2016). Very few studies have estimated the frequency of DNA stem cells are particularly sensitive to DNA damage and prone lesions in plant cells. In Human cells, DNA lesions caused by to enter cell death (Fulcher and Sablowski, 2009), suggesting spontaneous hydrolysis or ROS occur at a frequency ranging that specific mechanisms are at work to protect meristems from from a few hundreds to over 105 per cell, depending on the accumulating mutations. type of damage (Bray and West, 2005). In maize, the number The DDR signaling pathway has received extensive attention of apurinic/apyrimidic sites formed in root tips during the first in Mammals due to its relevance in the field of cancer research, 20 h of seed imbibition was estimated to 3.75 × 105 per genome but has also been studied into details in plants for about 15– and per cell. Thus, although detailed quantification of DNA 20 years. In this review we will summarize the recent advances on damage occurring in plant cells is missing, DNA damage can the plant DDR. We will focus exclusively on the DDR signaling be considered as a frequent event under normal conditions, and events and cell cycle regulation, but will not discuss the complex likely even more so in response to various stress conditions. mechanisms involved in DNA repair that have been reviewed In spite of the high frequency of DNA damage occurring in elsewhere (Manova and Gruszka, 2015; Spampinato, 2017). Next, plant cells, the estimated mutation rate is very low. Through we will explore the emerging connection between DDR and whole genome sequencing of Arabidopsis lines propagated from biotic and abiotic stress responses. Indeed, even though DDR is single seed descent for 25–30 generations, the genome-wide likely activated in response to a wide range of stress conditions average mutation rate was estimated around 7 × 10−9 per site per and could account for some of the negative effects of stress on generation (Ossowski et al., 2010; Weng et al., 2019). This figure cell division, it has to date little been studied in the context of corresponds to less than one single mutation in the entire genome plant response to stress, with most studies using genotoxic to per generation, and is at least 10 times lower than the error rate trigger the DDR. of the replication machinery for a single cell cycle. This provides striking evidence for the efficiency with which DNA Damage is detected and repaired in the cell.
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