ALT1, a Snf2 Family Chromatin Remodeling ATPase, Negatively Regulates Alkaline Tolerance through Enhanced Defense against Oxidative Stress in Rice

Guo, Mingxin; Wang, Ruci; Wang, Juan; Hua, Kai; Wang, Yueming; Liu, Xiaoqiang; Yao, Shanguo

doi:10.1371/journal.pone.0112515

Cited by 47 publications

(34 citation statements)

References 61 publications

(88 reference statements)

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“…The only SNF2 family member investigated outside Arabidopsis is the ATPase ALT1 in rice (Oryza sativa), which regulates alkaline tolerance through the modulation of genes involved in reactive oxygen species metabolism and DNA repair. In spite of this rather indirect involvement in DDR, it is interesting that the same nucleosome remodeler acts in both ROS and DNA damage response, strengthening the link between these two stresses (Guo et al, 2014).…”

Section: Chromatin-remodeling Complexes Connected With Ddrmentioning

confidence: 99%

DNA Damage Repair in the Context of Plant Chromatin

Donà

Scheid

2015

Plant Physiol.

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The integrity of DNA molecules is constantly challenged. All organisms have developed mechanisms to detect and repair multiple types of DNA lesions. The basic principles of DNA damage repair (DDR) in prokaryotes and unicellular and multicellular eukaryotes are similar, but the association of DNA with nucleosomes in eukaryotic chromatin requires mechanisms that allow access of repair enzymes to the lesions. This is achieved by chromatin-remodeling factors, and their necessity for efficient DDR has recently been demonstrated for several organisms and repair pathways. Plants share many features of chromatin organization and DNA repair with fungi and animals, but they differ in other, important details, which are both interesting and relevant for our understanding of genome stability and genetic diversity. In this Update, we compare the knowledge of the role of chromatin and chromatin-modifying factors during DDR in plants with equivalent systems in yeast and humans. We emphasize plant-specific elements and discuss possible implications.A DNA molecule in a eukaryotic chromosome has a diameter of 2 nm but a length in the range of centimeters. Being 10 7 times longer than it is wide would make it highly sensitive to breakage if it were not organized in compact and dynamic chromatin, with nucleosomes as basic units followed by multiple higher order levels of organization. Within this packaging, replication and transcription constitute an endogenous mechanical strain, while exposure of cells to physical or chemical hazard creates a wide range of DNA damage induced by external factors, including photoproducts, pyrimidine dimers, interstrand crosslinking, and single and double-strand breaks (DSBs). All organisms possess mechanisms that repair DNA molecules. DNA damage repair (DDR) systems for the various types of damage are overlapping as well as complementary, and their prevalence depends on the organism, the stage of the cell cycle, the site and the amount of damage, and the availability of intact templates. A coarse categorization distinguishes nucleotide excision repair, base excision repair, nonhomologous end joining (NHEJ), and homologous recombination (HR). Many schematic models for these DDR pathways describe the action and interaction of several repair components, but they are usually misleading in one aspect: DNA strands are illustrated as straight lines, neglecting the emerging role of chromatin for the location and the fate of DNA lesions. More realistically, we should envisage DNA lesions in the chromatin context like the leakage or burst of an in-ground pipe. Recognizing the defect, localizing it, excavating the broken parts, cleaning the ends, reconnecting them, and restoring the original state are mirrored in the subsequent steps of DDR: signaling, labeling, accessing, resecting, religating, and reassembling. Chromatin is expected to especially affect the access, resection, and restoration of the original arrangement, and several factors that can dissolve higher order structures, slide, evict, or exchange ...

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Section: Chromatin-remodeling Complexes Connected With Ddrmentioning

confidence: 99%

DNA Damage Repair in the Context of Plant Chromatin

Donà

Scheid

2015

Plant Physiol.

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“…High pH conditions impose severe damage stress on rice seedling growth by causing serious root cell injury and death, which, consequently, results in whole-plant wilting and even death ( Lv et al, 2013 ; Guo et al, 2014 ; Wei et al, 2015 ). However, the molecular mechanism responsible for root damage by alkaline stress remains largely unknown.…”

Section: Introductionmentioning

confidence: 99%

“…However, the molecular mechanism responsible for root damage by alkaline stress remains largely unknown. Recently, Guo et al (2014) identified a rice mutant, alkaline tolerance 1 ( alt1 ), with enhanced tolerance to alkaline stress ( Guo et al, 2014 ). Map-based cloning of alt1 revealed that ALT1 encodes a Snf2 family chromatin remodeling ATPase.…”

Section: Introductionmentioning

confidence: 99%

Root Damage under Alkaline Stress Is Associated with Reactive Oxygen Species Accumulation in Rice (Oryza sativa L.)

et al. 2017

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Alkaline stress (high pH) severely damages root cells, and consequently, inhibits rice (Oryza sativa L.) seedling growth. In this study, we demonstrate the accumulation of reactive oxygen species (ROS) in root cells under alkaline stress. Seedlings of two rice cultivars with different alkaline tolerances, ‘Dongdao-4’ (moderately alkaline-tolerant) and ‘Jiudao-51’ (alkaline-sensitive), were subjected to alkaline stress simulated by 15 mM sodium carbonate (Na2CO3). Alkaline stress greatly reduced seedling survival rate, shoot and root growth, and root vigor. Moreover, severe root cell damage was observed under alkaline stress, as shown by increased membrane injury, malondialdehyde accumulation, and Evan’s Blue staining. The expression of the cell death-related genes OsKOD1, OsHsr203j, OsCP1, and OsNAC4 was consistently upregulated, while that of a cell death-suppressor gene, OsBI1, was downregulated. Analysis of the ROS contents revealed that alkaline stress induced a marked accumulation of superoxide anions (O2•-) and hydrogen peroxide (H2O2) in rice roots. The application of procyanidins (a potent antioxidant) to rice seedlings 24 h prior to alkaline treatment significantly alleviated alkalinity-induced root damage and promoted seedling growth inhibition, which were concomitant with reduced ROS accumulation. These results suggest that root cell damage, and consequently growth inhibition, of rice seedlings under alkaline stress is closely associated with ROS accumulation. The antioxidant activity of superoxide dismutase, catalase, peroxidase, and ascorbate peroxidase increased under alkaline stress in the roots, probably in response to the cellular damage induced by oxidative stress. However, this response mechanism may be overwhelmed by the excess ROS accumulation observed under stress, resulting in oxidative damage to root cells. Our findings provide physiological insights into the molecular mechanisms of alkalinity-induced damage to root cells, and will contribute to the improvement of alkaline stress tolerance in rice plants.

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“…The RNAi construct was generated by inserting a hairpin sequence with two 552‐bp cDNA inverted repeats targeting the sequence from 5214–5765 bp downstream of the start codon of CRR1 . The 552‐bp fragment was ligated into pZH2Bi and driven by the ubiquitin promoter (Guo et al ., ). For analyzing the promoter activity of CRR1 , the 2.1‐kb promoter region of the CRR1 gene was amplified from WT genomic DNA.…”

Section: Methodsmentioning

confidence: 97%

CRR1 encoding callose synthase functions in ovary expansion by affecting vascular cell patterning in rice

et al. 2016

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The ovary of rice undergoes rapid expansion immediately after fertilization, and this process determines the final sink strength potential of caryopses. To date, work on rice grain development has mainly focused on endosperm filling, whereas information on the essential elements for ovary expansion remains limited. We report here a functional analysis of the ovary expansion retarded mutant crr1 in rice. Map-based cloning revealed that CRR1 encodes a protein homologous to the Arabidopsis callose synthases AtGSL8 and AtGSL10. Point mutation in crr1 resulted in alternative splicing, which led to the formation of the truncated crr1 protein without the β-glucan synthase domain. Iodine staining showed that there were few starch granules and these were unevenly distributed in the pericarp of crr1, and a 5,6-carboxyfluorescein diacetate transport assay revealed that carbohydrates were less efficiently unloaded from the lateral vasculature into the developing caryopsis. CRR1 transcripts were detected in all plant organs, with the highest level found in receptacles, which are mainly composed of vascular tissues. Analysis of pCRR1::GUS transgenic plants showed that CRR1 was specifically expressed in vascular bundle cells. Consistently, loss of function of CRR1 led to disordered patterns of vascular cells in the ovaries and receptacles of the mutant. Furthermore, a small portion of cells in the vascular bundles of crr1 showed defective cell wall formation, and callose deposition was specifically reduced at the plasmodesmata (PD) of cells with aberrant walls. Our results suggest that CRR1 performs a pivotal role in determining initial ovary expansion in rice, possibly via the PD-mediated permeability of cell fate determinants for vascular cell differentiation.

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ALT1, a Snf2 Family Chromatin Remodeling ATPase, Negatively Regulates Alkaline Tolerance through Enhanced Defense against Oxidative Stress in Rice

Cited by 47 publications

References 61 publications

DNA Damage Repair in the Context of Plant Chromatin

DNA Damage Repair in the Context of Plant Chromatin

Root Damage under Alkaline Stress Is Associated with Reactive Oxygen Species Accumulation in Rice (Oryza sativa L.)

CRR1 encoding callose synthase functions in ovary expansion by affecting vascular cell patterning in rice

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