The Role of the Plasma Membrane H+-ATPase in Plant Responses to Aluminum Toxicity

Zhang, Jiarong; Ji, Wei; Li, Dongxu; Kong, Xiangying; Rengel, Zed; Chen, Limei; Yang, Ye; Cui, Xiuming; Chen, Qi

doi:10.3389/fpls.2017.01757

Cited by 82 publications

(57 citation statements)

References 100 publications

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“…These results further support the hypothesis that PM H 1 -ATPase activity contributes to the defective V-ATPase-induced root Al resistance. The PM H 1 -ATPase mediates H 1 efflux into the apoplast (Gaxiola et al, 2007;Zhang et al, 2017). To examine whether PM-ATPase activity affects apoplastic pH in wild-type and vha-a2 vha-a3 mutant roots during Al exposure, we measured the pH value in the nonbuffer solutions containing 250 mM Al 31 on which the wild type or the vha-a2 vha-a3 mutant was grown, and we found that the vha-a2 vha-a3 mutant caused a more significant pH decrease than the wild type after 3 h of incubation (Supplemental Fig.…”

Section: V-atpase and V-ppase Activity Are Repressed Upon Al Stressmentioning

confidence: 99%

“…The AHA genes are differentially expressed in Arabidopsis tissues, and eight of them (AHA1-AHA4, AHA7, AHA8, AHA10, and AHA11) are expressed in roots (Ueno et al, 2005). Despite the fact that apoplastic acidification is generally observed upon Al stress (Zhang et al, 2017), little is known about how PM H 1 -ATPase is linked to Al response in Arabidopsis. The PM H 1 -ATPase activity has been hypothesized to be related to the activity of vacuolar H 1 pump (Li et al, 2005;Cho et al, 2012), which is constituted by V-ATPase and V-PPase (Gaxiola et al, 2007).…”

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confidence: 99%

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A Defective Vacuolar Proton Pump Enhances Aluminum Tolerance by Reducing Vacuole Sequestration of Organic Acids

et al. 2019

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Plants cope with aluminum (Al) toxicity by secreting organic acids (OAs) into the apoplastic space, which is driven by proton (H 1) pumps. Here, we show that mutation of vacuolar H 1-translocating adenosine triphosphatase (H 1-ATPase) subunit a2 (VHA-a2) and VHA-a3 of the vacuolar H 1-ATPase enhances Al resistance in Arabidopsis (Arabidopsis thaliana). vha-a2 vha-a3 mutant plants displayed less Al sensitivity with less Al accumulation in roots compared to wild-type plants when grown under excessive Al 31. Interestingly, in response to Al 31 exposure, plants showed decreased vacuolar H 1 pump activity and reduced expression of VHA-a2 and VHA-a3, which were accompanied by increased plasma membrane H 1 pump (PM H 1-ATPase) activity. Genetic analysis of plants with altered PM H 1-ATPase activity established a correlation between Al-induced increase in PM H 1-ATPase activity and enhanced Al resistance in vha-a2 vha-a3 plants. We determined that external OAs, such as malate and citrate whose secretion is driven by PM H 1-ATPase, increased with PM H 1-ATPase activity upon Al stress. On the other hand, elevated secretion of malate and citrate in vha-a2 vha-a3 root exudates appeared to be independent of OAs metabolism and tolerance of phosphate starvation but was likely related to impaired vacuolar sequestration. These results suggest that coordination of vacuolar H 1-ATPase and PM H 1-ATPase dictates the distribution of OAs into either the vacuolar lumen or the apoplastic space that, in turn, determines Al tolerance capacity in plants.

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Section: V-atpase and V-ppase Activity Are Repressed Upon Al Stressmentioning

confidence: 99%

mentioning

confidence: 99%

A Defective Vacuolar Proton Pump Enhances Aluminum Tolerance by Reducing Vacuole Sequestration of Organic Acids

et al. 2019

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“…Interestingly, our results showed that both H 2 S and NO are required for Al‐stimulated GmMATE expression (Figure a). In addition to citrate transporter, PM H + ‐ATPase was also reported to be responsible for Al‐induced citrate secretion in plants (Zhang et al, ). PM H + ‐ATPase can exclude H + outside the cell membrane to create an electrochemical gradient, thus providing a driving force for the activation of secondary transporters.…”

Section: Discussionmentioning

confidence: 99%

Interactions between hydrogen sulphide and nitric oxide regulate two soybean citrate transporters during the alleviation of aluminium toxicity

Wang

Zhang

et al. 2019

Plant Cell & Environment

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Hydrogen sulphide (H 2 S) is emerging as an important signalling molecule involved in plant resistance to various stresses. However, the underlying mechanism of H 2 S in aluminium (Al) resistance and the crosstalk between H 2 S and nitric oxide (NO) in Al stress signalling remain elusive. Citrate secretion is a wide-spread strategy for plants against Al toxicity. Here, two citrate transporter genes, GmMATE13 and GmMATE47, were identified and characterized in soybean. Functional analysis in Xenopus oocytes and transgenic Arabidopsis showed that GmMATE13 and GmMATE47 mediated citrate exudation and enhanced Al resistance. Al treatment triggered H 2 S generation and citrate exudation in soybean roots. Pretreatment with an H 2 S donor significantly elevated Al-induced citrate exudation, reduced Al accumulation in root tips, and alleviated Al-induced inhibition of root elongation, whereas application of an H 2 S scavenger elicited the opposite effect. Furthermore, H 2 S and NO mediated Al-induced GmMATE expression and plasma membrane (PM) H + -ATPase activity and expression. Further investigation showed that NO induced H 2 S production by regulating the key enzymes involved in biosynthesis and degradation of H 2 S. These findings indicate that H 2 S acts downstream of NO in mediating Al-induced citrate secretion through the upregulation of PM H + -ATPase-coupled citrate transporter cotransport systems, thereby conferring plant resistance to Al toxicity.

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“…This can result in changes in cytoplasmic Ca 2+ homeostasis, which controls cell signaling, metabolism and cell-growth processes including root development 110 . Al 3+ stress induces changes in the expression and activity of the plasma membrane H + -ATPase that controls cytosolic pH and membrane potentials 111 .…”

Section: Discussionmentioning

confidence: 99%

Effects of green seaweed extract onArabidopsisearly development suggest roles for hormone signalling in plant responses to algal fertilisers

Ghaderiardakani

Collas

Damiano

et al. 2018

Preprint

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The growing population requires sustainable, environmentally-friendly crops. The plant growthenhancing properties of algal extracts have suggested their use as biofertilisers. The mechanism(s) by which algal extracts affect plant growth are unknown.We examined the effects of extracts from the common green seaweed Ulva intestinalis on germination and root development in the model land plant Arabidopsis thaliana. Ulva extract concentrations above 0.1% inhibited Arabidopsis germination and root growth. Ulva extract <0.1% stimulated root growth. All concentrations of Ulva extract inhibited lateral root formation.An abscisic-acid-insensitive mutant, abi1, showed altered sensitivity to germination-and root growth-inhibition inhibition. Ethylene-and cytokinin-insensitive mutants were partly insensitive to germination-inhibition. This suggests that different mechanisms mediate each effect of Ulva extract on early Arabidopsis development and that multiple hormones contribute to germinationinhibition.Elemental analysis showed that Ulva contains high levels of Aluminium ions (Al 3+ ). Ethylene and cytokinin have been suggested to function in Al 3+ -mediated root growth inhibition: our data suggest that if Ulva Al 3+ levels inhibit root growth, this is via a novel mechanism. We suggest

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The Role of the Plasma Membrane H+-ATPase in Plant Responses to Aluminum Toxicity

Cited by 82 publications

References 100 publications

A Defective Vacuolar Proton Pump Enhances Aluminum Tolerance by Reducing Vacuole Sequestration of Organic Acids

A Defective Vacuolar Proton Pump Enhances Aluminum Tolerance by Reducing Vacuole Sequestration of Organic Acids

Interactions between hydrogen sulphide and nitric oxide regulate two soybean citrate transporters during the alleviation of aluminium toxicity

Effects of green seaweed extract onArabidopsisearly development suggest roles for hormone signalling in plant responses to algal fertilisers

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