Plant Adaptation to Acid Soils: The Molecular Basis for Crop Aluminum Resistance

Kochian, Leon V.; Piñeros, Miguel A.; Liu, Jiping; Magalhães, J. V. de

doi:10.1146/annurev-arplant-043014-114822

Cited by 746 publications

(751 citation statements)

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“…Transgenic approaches have been identified as potentially powerful methods to increase the Al tolerance of plants in acidic soils (Ryan et al, 2011;Kochian et al, 2015). Thus far, a number of genes involved in different biological processes (including organic acid metabolism, stress response, and organic acid transport) have been successfully introduced into plants, with the resultant transgenic plants showing enhanced Al tolerance (Ryan et al, 2011).…”

Section: Discussionmentioning

confidence: 99%

A Formate Dehydrogenase Confers Tolerance to Aluminum and Low pH

et al. 2016

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Formate dehydrogenase (FDH) is involved in various higher plant abiotic stress responses. Here, we investigated the role of rice bean (Vigna umbellata) VuFDH in Al and low pH (H + ) tolerance. Screening of various potential substrates for the VuFDH protein demonstrated that it functions as a formate dehydrogenase. Quantitative reverse transcription-PCR and histochemical analysis showed that the expression of VuFDH is induced in rice bean root tips by Al or H + stresses. Fluorescence microscopic observation of VuFDH-GFP in transgenic Arabidopsis plants indicated that VuFDH is localized in the mitochondria. Accumulation of formate is induced by Al and H + stress in rice bean root tips, and exogenous application of formate increases internal formate content that results in the inhibition of root elongation and induction of VuFDH expression, suggesting that formate accumulation is involved in both H + -and Al-induced root growth inhibition. Over-expression of VuFDH in tobacco (Nicotiana tabacum) results in decreased sensitivity to Al and H + stress due to less production of formate in the transgenic tobacco lines under Al and H + stresses. Moreover, NtMATE and NtALS3 expression showed no changes versus wild type in these over-expression lines, suggesting that herein known Al-resistant mechanisms are not involved. Thus, the increased Al tolerance of VuFDH over-expression lines is likely attributable to their decreased Al-induced formate production. Taken together, our findings advance understanding of higher plant Al toxicity mechanisms, and suggest a possible new route toward the improvement of plant performance in acidic soils, where Al toxicity and H + stress coexist.

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Section: Discussionmentioning

confidence: 99%

A Formate Dehydrogenase Confers Tolerance to Aluminum and Low pH

et al. 2016

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“…aquaporin | nodulin 26-like protein | aluminum tolerance | organic acid exudation | malate A luminum (Al) toxicity is a major constraint for crop yields on acid soils worldwide (1)(2)(3)(4). To cope with Al stress, plants have adopted several resistance mechanisms, including (i) an Al exclusion mechanism in which plants release organic acids (OAs) from the root apex into the rhizosphere to chelate toxic Al 3+ ions and prevent them from entering into root cells, and (ii) an internal Al tolerance mechanism by which Al is sequestered in the vacuole of the root cell and/or translocated to the shoot for sequestration in leaf cell vacuoles (1,2,5).…”

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confidence: 99%

NIP1;2 is a plasma membrane-localized transporter mediating aluminum uptake, translocation, and tolerance in Arabidopsis

Wang

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Members of the aquaporin (AQP) family have been suggested to transport aluminum (Al) in plants; however, the Al form transported by AQPs and the roles of AQPs in Al tolerance remain elusive. Here we report that NIP1;2, a plasma membrane-localized member of the Arabidopsis nodulin 26-like intrinsic protein (NIP) subfamily of the AQP family, facilitates Al-malate transport from the root cell wall into the root symplasm, with subsequent Al xylem loading and root-toshoot translocation, which are critical steps in an internal Al tolerance mechanism in Arabidopsis. We found that NIP1;2 transcripts are expressed mainly in the root tips, and that this expression is enhanced by Al but not by other metal stresses. Mutations in NIP1;2 lead to hyperaccumulation of toxic Al 3+ in the root cell wall, inhibition of root-to-shoot Al translocation, and a significant reduction in Al tolerance. NIP1;2 facilitates the transport of Al-malate, but not Al 3+ ions, in both yeast and Arabidopsis. We demonstrate that the formation of the Al-malate complex in the root tip apoplast is a prerequisite for NIP1;2-mediated Al removal from the root cell wall, and that this requires a functional root malate exudation system mediated by the Al-activated malate transporter, ALMT1. Taken together, these findings reveal a critical linkage between the previously identified Al exclusion mechanism based on root malate release and an internal Al tolerance mechanism identified here through the coordinated function of NIP1;2 and ALMT1, which is required for Al removal from the root cell wall, root-to-shoot Al translocation, and overall Al tolerance in Arabidopsis.aquaporin | nodulin 26-like protein | aluminum tolerance | organic acid exudation | malate

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“…Recently, Kopittke et al (2015) reported that 75 mM Al reduced root growth of soybean after only 5 min, with Al being toxic by binding to the walls of outer cells, which directly inhibited their loosening in the elongation zone, and concluded that the primary lesion of Al is apoplastic. Therefore, the rapid dynamics of root growth to Al stress indicates that Al first inhibits root cell expansion and elongation and later on also cell division (Horst et al, 2010;Kochian et al, 2015). And also, Horst et al (1999) indicated that the cell wall-plasma membrane-cytoskeleton continuous system plays a role in the regulation of Al toxicity.…”

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confidence: 99%

Jasmonic Acid Enhances Al-Induced Root Growth Inhibition

Yang

et al. 2016

Plant Physiol.

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Phytohormones such as ethylene and auxin are involved in the regulation of the aluminum (Al)-induced root growth inhibition. Although jasmonate (JA) has been reported to play a crucial role in the regulation of root growth and development in response to environmental stresses through interplay with ethylene and auxin, its role in the regulation of root growth response to Al stress is not yet known. In an attempt to elucidate the role of JA, we found that exogenous application of JA enhanced the Al-induced root growth inhibition. Furthermore, phenotype analysis with mutants defective in either JA biosynthesis or signaling suggests that JA is involved in the regulation of Al-induced root growth inhibition. The expression of the JA receptor CORONATINE INSENSITIVE1 (COI1) and the key JA signaling regulator MYC2 was up-regulated in response to Al stress in the root tips. This process together with COI1-mediated Al-induced root growth inhibition under Al stress was controlled by ethylene but not auxin. Transcriptomic analysis revealed that many responsive genes under Al stress were regulated by JA signaling. The differential responsive of microtubule organization-related genes between the wild-type and coi1-2 mutant is consistent with the changed depolymerization of cortical microtubules in coi1 under Al stress. In addition, ALMT-mediated malate exudation and thus Al exclusion from roots in response to Al stress was also regulated by COI1-mediated JA signaling. Together, this study suggests that root growth inhibition is regulated by COI1-mediated JA signaling independent from auxin signaling and provides novel insights into the phytohormone-mediated root growth inhibition in response to Al stress.

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Plant Adaptation to Acid Soils: The Molecular Basis for Crop Aluminum Resistance

Cited by 746 publications

References 145 publications

A Formate Dehydrogenase Confers Tolerance to Aluminum and Low pH

A Formate Dehydrogenase Confers Tolerance to Aluminum and Low pH

NIP1;2 is a plasma membrane-localized transporter mediating aluminum uptake, translocation, and tolerance in Arabidopsis

Jasmonic Acid Enhances Al-Induced Root Growth Inhibition

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