Arsenite Elicits Anomalous Sulfur Starvation Responses in Barley

Reid, Robert J.; Gridley, Kate L.; Kawamata, Yuta; Zhu, Yan

doi:10.1104/pp.113.216937

Cited by 21 publications

(13 citation statements)

References 42 publications

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“…As(III) and As(V) increase the intracellular thiol content in arsenic hyperaccumulator plants (Bleeker et al, 2006); As(V) reductase activity is therefore a prerequisite for arsenic tolerance and accumulation. CK also represses sulfur transporters (Maruyama-Nakashita et al, 2004), and As(III) causes severe sulfur starvation and induces expression of sulfur transporters (Reid et al, 2013). These data support the idea that sulfur is critical for increased biosynthesis of PC and other thiol-related compounds, which leads to arsenic accumulation.…”

Section: Discussionsupporting

confidence: 72%

Cytokinin determines thiol-mediated arsenic tolerance and accumulation in Arabidopsis thaliana

et al. 2016

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The presence of arsenic in soil and water is a constant threat to plant growth in many regions of the world. Phytohormones act in the integration of growth control and stress response, but their role in plant responses to arsenic remains to be elucidated. Here, we show that arsenate [As(V)], the most prevalent arsenic chemical species in nature, causes severe depletion of endogenous cytokinins (CKs) in the model plant Arabidopsis (Arabidopsis thaliana). We found that CK signaling mutants and transgenic plants with reduced endogenous CK levels showed an As(V)-tolerant phenotype. Our data indicate that in CK-depleted plants exposed to As(V), transcript levels of As(V)/phosphate-transporters were similar or even higher than in wild-type plants. In contrast, CK depletion provoked the coordinated activation of As(V) tolerance mechanisms, leading to the accumulation of thiol compounds such as phytochelatins and glutathione, which are essential for arsenic sequestration. Transgenic CK-deficient Arabidopsis and tobacco lines show a marked increase in arsenic accumulation. Our findings indicate that CK is an important regulatory factor in plant adaptation to arsenic stress.Since the inception of life, arsenic in the biosphere has been a constant challenge to the survival of life forms. Although all organisms on earth have developed strategies to cope with this extremely toxic metalloid (Rosen, 2002;Tripathi et al., 2007), arsenic currently poses a major worldwide environmental problem (Naujokas et al., 2013).Arsenate [As(V)] is the most abundant chemical form of arsenic. Due to its structural similarity to phosphate (Pi), it is easily incorporated into plants and other organisms through Pi transporters. Once taken up by the cell, As(V) is rapidly reduced to arsenite [As(III)] by As (V) reductases. As(III) is either extruded from the cytoplasm or is sequestered by phytochelatins (PCs) and other related thiol-containing compounds and is compartmentalized into vacuoles (Tripathi et al., 2007).In plants, when As(V) is perceived, Pi transporters are rapidly downregulated, and thiol compound accumulation increases concomitantly to cope with the metalloid. These two responses are key As(V) tolerance strategies for natural plant populations (Meharg and Macnair 1992;Bleeker et al., 2006). Accumulation of PC and other related thiol-containing compounds is widely used by plants for heavy metal detoxification. PCs are synthesized from glutathione (GSH) by the enzyme PHYTOCHELATIN SYNTHASE1 (PCS1). As(V) induces PCS1, together with two other genes involved in GSH biosynthesis: g-GLUTAMYLCYSTEINE SYNTHETASE and GLUTATHIONE SYNTHETASE (GSH2; Sung et al., 2009). In addition, As(III) activates GSH and PC accumulation; As(V) reductase activity is thus essential for arsenic tolerance (Bleeker et al., 2006). Arabidopsis thaliana ARSENATE REDUCTASE QTL1 (AtARQ1, At2g21045; also termed HAC1; Chao et al., 2014), an As(V) reductaseencoding gene, is also transcriptionally regulated by As(V) (Sánchez-Bermejo et al., 2014). Arsenic tolerance thus ...

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Section: Discussionsupporting

confidence: 72%

Cytokinin determines thiol-mediated arsenic tolerance and accumulation in Arabidopsis thaliana

et al. 2016

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“…These studies demonstrate the importance of PCs in plant metal/metalloid detoxification. Previous studies on S nutrition and As stresses indicate that up-regulation of SULTR-mediated S uptake is likely to be important for plant As tolerance (Sung et al 2009;Jobe et al 2012;Reid et al 2013;Srivastava et al 2014). These observations imply the significance of S nutrition and transport for supporting substantial synthesis of such Cys-containing metabolites.…”

Section: Discussionmentioning

confidence: 80%

“…The up-regulation of SULTR homologs in response to As stress has also been observed in other species such as barley (Hordeum vulgare L.) and rice (Reid et al 2013;Srivastava et al 2014). In barley, total S concentration in tissues is increased by As exposure and its accumulation, which is accompanied by the induction of the SULTR homolog (HvST1) expression and the increase of thiol levels (Reid et al 2013). These suggest that As stresses enhance S uptake by up-regulating SULTR transporters, and we hypothesize that proper S uptake and supply for S-metabolic pathways, including the PC-synthetic pathway, are important for achieving As tolerance of plants.…”

Section: Introductionmentioning

confidence: 68%

“…In A. thaliana, SULTR1;2 is the primary S uptake transporter in roots (Shibagaki et al 2002;Yoshimoto et al 2002Yoshimoto et al , 2007Barberon et al 2008), and its expression is strongly induced by As stress along with the expression of other S-assimilation genes (Sung et al 2009;Jobe et al 2012). The up-regulation of SULTR homologs in response to As stress has also been observed in other species such as barley (Hordeum vulgare L.) and rice (Reid et al 2013;Srivastava et al 2014). In barley, total S concentration in tissues is increased by As exposure and its accumulation, which is accompanied by the induction of the SULTR homolog (HvST1) expression and the increase of thiol levels (Reid et al 2013).…”

Section: Introductionmentioning

confidence: 91%

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Enhanced arsenic sensitivity with excess phytochelatin accumulation in shoots of a SULTR1;2 knockout mutant of Arabidopsis thaliana (L.) Heynh

Nishida

Duan

Ohkama‐Ohtsu

et al. 2016

Soil Science and Plant Nutrition

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One mechanism of arsenic detoxification in plants is synthesis of phytochelatins from glutathione in a sulfur-dependent manner. This study examined the contribution of a sulfate transporter, SULTR1;2, in arsenic tolerance in terms of sulfur metabolism in Arabidopsis thaliana (L.) Heynh. Comparative analysis of SULTR mutants showed that defective mutations of SULTR1;2 resulted in an increased arsenic sensitivity, in both shoots and roots, establishing that SULTR1;2 is required for arsenic tolerance. We subsequently quantified total sulfur content and levels of sulfur compounds (phytochelatins, glutathione, cysteine) in a SULTR1;2 mutant, sel1-8. Arsenic treatments increased sulfur uptake of sel1-8, but the mutant was unable to maintain the proper basal level of sulfur. Despite drastic reduction of total sulfur content, the mutant accumulated substantial or rather excess phytochelatins in shoots under arsenic stress conditions. The levels of glutathione and cysteine in shoots were lower in sel1-8 than in the wild type, possibly representing partial disorder of sulfur nutrition under limited sulfur supply. Taken together, we propose that SULTR1;2 contributes to arsenic tolerance by maintaining proper sulfur nutrient status at high demand for sulfur by phytochelatins-synthetic pathway, and/or optimal level of phytochelatin synthesis in shoots.

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“…Synthesis of glutathione is strongly dependent on sulphur (S) supply; hence, the pathway of sulphate assimilation was activated ( Fig. 4a), including a high-affinity sulphate transporter and ATP-sulphurylase, which are known to be involved in As tolerance and accumulation (Wangeline et al, 2004;Nocito et al, 2006;Reid et al, 2013). Moreover, the ABC-type transporter involved in the transport of glutathione complexes into the vacuole (Ghosh et al, 1999) was activated.…”

Section: New Phytologistmentioning

confidence: 99%

Unraveling the effect of arsenic on the model Medicago–Ensifer interaction: a transcriptomic meta‐analysis

et al. 2014

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SummaryThe genetic regulation underlying the effect of arsenic (As(III)) on the model symbiosis Medicago-Ensifer was investigated using a combination of physiological (split-roots), microscopy and genetic (microarrays, qRT-PCR and composite plants) tools.Nodulation was very sensitive to As(III) (median inhibitory dose (ID50) = 20 lM). The effect on root elongation and on nodulation was local (nonsystemic). A battery of stress (salt, drought, heat shock, metals, etc.)-related genes were induced. Glutathione played a pivotal role in tolerance/detoxification, together with secondary metabolites ((iso)flavonoids and phenylpropanoids). However, antioxidant enzymes were not activated.Concerning the symbiotic interaction, molecular evidence suggesting that rhizobia alleviate As stress is for the first time provided. Chalcone synthase (which is involved in the first step of the legume-rhizobia cross-talk) was strongly enhanced, suggesting that the plants are biased to establish symbiotic interactions under As(III) stress. In contrast, 13 subsequent nodulation genes (involved in nodulation factors (Nod factors) perception, infection, thread initiation and progression, and nodule morphogenesis) were repressed.Overexpression of the ethylene responsive factor ERN in composite plants reduced root stress and partially restored nodulation, whereas overexpression of the early nodulin ENOD12 enhanced nodulation both in the presence and, particularly, in the absence of As, without affecting root elongation. Several transcription factors were identified, which could be additional targets for genetic engineering aiming to improve nodulation and/or alleviate root stress induced by this toxic.

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Arsenite Elicits Anomalous Sulfur Starvation Responses in Barley

Cited by 21 publications

References 42 publications

Cytokinin determines thiol-mediated arsenic tolerance and accumulation in Arabidopsis thaliana

Cytokinin determines thiol-mediated arsenic tolerance and accumulation in Arabidopsis thaliana

Enhanced arsenic sensitivity with excess phytochelatin accumulation in shoots of a SULTR1;2 knockout mutant of Arabidopsis thaliana (L.) Heynh

Unraveling the effect of arsenic on the model Medicago–Ensifer interaction: a transcriptomic meta‐analysis

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