Proteasomal degradation of BRAHMA promotes Boron tolerance in Arabidopsis

Sakamoto, Takuya; Tsujimoto-Inui, Yayoi; Sotta, Naoyuki; Hirakawa, Takeshi; Matsunaga, Tomoko; Fukao, Yoichiro; Matsunaga, Satoru; Fujiwara, Toru

doi:10.1038/s41467-018-07393-6

Cited by 50 publications

(57 citation statements)

References 57 publications

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“…Therefore, cell wall-mediated boron toxicity alone may not explain the toxic effects of excess boron on these systems, especially animal cells. Excess boronassociated DNA damage has been reported as a consequence of boron toxicity among eukaryotes (Sakamoto et al, 2018). In addition, we showed that transcriptional signals related to RNA metabolism were substantially affected in A. thaliana, while S. parvula orthologs showed a stress-prepared expression level prior to the stress ( Figure 4A, 6A, and 6B).…”

Section: Why Is Excess Boron Toxic To Plants?mentioning

confidence: 56%

Cross species multi-omics reveals cell wall sequestration and elevated global transcription as mechanisms of boron tolerance in plants

Wang

DiTusa

et al. 2020

Preprint

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Boron toxicity is a worldwide problem for crop production, yet we have only a limited understanding of the genetic responses and adaptive mechanisms to this environmental stress in plants. Here we identified responses to excess boron in boron stress-sensitive Arabidopsis thaliana and its boron stress-tolerant extremophyte relative Schrenkiella parvula using comparative genomics, transcriptomics, metabolomics, and ionomics. S. parvula maintains a lower level of total boron and free boric acid in its roots and shoots and sustains growth for longer durations than A. thaliana when grown with excess boron. S. parvula likely excludes boron more efficiently than A. thaliana, which we propose is partly driven by BOR5, a boron transporter that we functionally characterized in the current study. Both species allocate significant transcriptomic and metabolomic resources to enable their cell walls to serve as a partial sink for excess boron, particularly discernable in A. thaliana shoots. We provide evidence that the S. parvula transcriptome is pre-adapted to boron toxicity, exhibiting substantial overlap with the boron-stressed transcriptome of A. thaliana. Our transcriptomic and metabolomics data also suggest that RNA metabolism is a primary target of boron toxicity. Cytoplasmic boric acid likely forms complexes with ribose and ribose-containing compounds critical to RNA and other primary metabolic functions. A model depicting some of the cellular responses that enable a plant to grow in the presence of normally toxic levels of boron is presented.

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Section: Why Is Excess Boron Toxic To Plants?mentioning

confidence: 56%

Cross species multi-omics reveals cell wall sequestration and elevated global transcription as mechanisms of boron tolerance in plants

Wang

DiTusa

et al. 2020

Preprint

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“…Interestingly, while BRM was enriched near transcriptional start sites (TSS) of target genes as expected, many target genes were bound at their 3 end, especially at 3 regions that have promoter-like structures such as TATA boxes, high H3K4me3 levels, low H3K27me3 and di-methylated lysine 9 on H3 (H3K9me2) levels, and high antisense transcriptional activity. However, BRM does not co-localize with the H3K27me3 mark [22] but with H3K9 and H3K14 acetylation marks [27].…”

Section: Genome-wide Functions Of Brm In Plantsmentioning

confidence: 87%

“…BRM stability is also involved in DNA double-strand breaks (DSBs) tolerance in Arabidopsis [27]. High levels of boron induce DSBs.…”

Section: Brm Has Roles In Abiotic Stress and Hormone Pathwaysmentioning

confidence: 99%

Unwinding BRAHMA Functions in Plants

Thouly

Masson

Lai

et al. 2020

Genes

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The ATP-dependent Switch/Sucrose non-fermenting (SWI/SNF) chromatin remodeling complex (CRC) regulates the transcription of many genes by destabilizing interactions between DNA and histones. In plants, BRAHMA (BRM), one of the two catalytic ATPase subunits of the complex, is the closest homolog of the yeast and animal SWI2/SNF2 ATPases. We summarize here the advances describing the roles of BRM in plant development as well as its recently reported chromatin-independent role in pri-miRNA processing in vitro and in vivo. We also enlighten the roles of plant-specific partners that physically interact with BRM. Three main types of partners can be distinguished: (i) DNA-binding proteins such as transcription factors which mostly cooperate with BRM in developmental processes, (ii) enzymes such as kinases or proteasome-related proteins that use BRM as substrate and are often involved in response to abiotic stress, and (iii) an RNA-binding protein which is involved with BRM in chromatin-independent pri-miRNA processing. This overview contributes to the understanding of the central position occupied by BRM within regulatory networks controlling fundamental biological processes in plants.

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“…Inhibition of cell division in the RAM is a critical cause of B toxicity in roots. In roots of Arabidopsis thaliana , high-B treatment decreases the RAM size through inhibition of cell division activity (Sakamoto et al, 2011, 2018; Aquea et al, 2012). The reduction in cell division activity is also observed in root tips of Vicia faba treated with a high B concentration (Liu et al, 2000), The inhibition of cell division is attributed to DNA damage caused by high-B stress in the RAM (Sakamoto et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

“…The reduction in cell division activity is also observed in root tips of Vicia faba treated with a high B concentration (Liu et al, 2000), The inhibition of cell division is attributed to DNA damage caused by high-B stress in the RAM (Sakamoto et al, 2011). We previously reported that a chromosomal protein complex (condensin II) and a regulatory particle AAA-ATPase 5a (RPT5a) of 26S proteasome (26SP) are essential for amelioration of high-B-dependent DNA damage and the maintenance of RAM size in A. thaliana (Sakamoto et al, 2011, 2018).…”

Section: Introductionmentioning

confidence: 99%

The 26S Proteasome Is Required for the Maintenance of Root Apical Meristem by Modulating Auxin and Cytokinin Responses Under High-Boron Stress

et al. 2019

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Boron (B), an essential micronutrient, causes adverse effects on the growth and development of plants when highly accumulated. By the analysis of Arabidopsis mutants hypersensitive to high-boron (high-B) stress, we have shown that 26S proteasome (26SP) is required to maintain the morphology of the root apical meristem (RAM) under high-B stress. To further understand the molecular function of 26SP in tolerance to high-B stress in the RAM, in this study we investigated the pathways regulated by 26SP using a 26SP subunit mutant, rpt5a , which is hypersensitive to high-B stress. Expression of RPT5a was induced by high-B stress in the entire RAM accompanied by its strong expression in the stele, including the stem cells. Analysis of stele organization in the rpt5a mutant revealed that 26SP is especially important for maintenance of the stele under high-B stress condition (3 mM B treatment). Expression analyses of an auxin-response reporter revealed that auxin responses were enhanced in the stele and the stem cell niche by high-B stress, especially in the rpt5a mutant. In contrast, the expression of TCS::GFP representing cytokinin signaling in the stem cell niche was unchanged in the wild type and extremely weak in the rpt5a mutant, irrespective of B condition. The drastically aberrant auxin and cytokinin responses in the rpt5a mutant under high-B stress were supported by transcriptome analysis using root tips. These results suggest that the collapse of hormonal crosstalk in the stele including the stem cells occurred in the rpt5a mutant, especially under high-B stress. Treatment with the auxin signaling inhibitor α-(phenyl ethyl-2-one)-indole-3-acetic acid (PEO-IAA) reduced sensitivity to high-B stress in the wild type and restored the RAM morphology in the rpt5a mutant under the high-B stress condition. In addition, cytokinin treatment conferred the rpt5a mutant with tolerance to high-B stress in RAM morphology. It is concluded that 26SP containing RPT5a is required for maintenance of auxin/cytokinin balance in the stele, which is crucial for preventing defects in RAM morphology under high-B stress.

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Proteasomal degradation of BRAHMA promotes Boron tolerance in Arabidopsis

Cited by 50 publications

References 57 publications

Cross species multi-omics reveals cell wall sequestration and elevated global transcription as mechanisms of boron tolerance in plants

Cross species multi-omics reveals cell wall sequestration and elevated global transcription as mechanisms of boron tolerance in plants

Unwinding BRAHMA Functions in Plants

The 26S Proteasome Is Required for the Maintenance of Root Apical Meristem by Modulating Auxin and Cytokinin Responses Under High-Boron Stress

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