A Zinc Finger Transcription Factor ART1 Regulates Multiple Genes Implicated in Aluminum Tolerance in Rice

Yamaji, Naoki; Huang, Chao‐Feng; Nagao, Satoko; Yano, Masahiro; Satō, Yutaka; Nagamura, Yoshiaki; Feng, Jian

doi:10.1105/tpc.109.070771

Cited by 355 publications

(365 citation statements)

References 43 publications

(61 reference statements)

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“…The primary Al avoidance mechanism involves exclusion of Al from the growing root tip via the exudation of Al-chelating OAs into the rhizosphere, where the OAs form nontoxic OA-Al complexes which do not enter the root. Over the past decade, some key cellular/molecular components for both the Al tolerance and exclusion mechanisms have been identified in plants (6)(7)(8)(9)(10)(11)(12).…”

mentioning

confidence: 99%

Natural variation underlies alterations in Nramp aluminum transporter ( NRAT1 ) expression and function that play a key role in rice aluminum tolerance

Liu

Dong

et al. 2014

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

149

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Aluminum (Al) toxicity is a major constraint for crop production on acid soils which compose ∼40% of arable land in the tropics and subtropics. Rice is the most Al-tolerant cereal crop and offers a good model for identifying Al tolerance genes and mechanisms. Here we investigated natural variation in the rice Nramp aluminum transporter (NRAT1) gene encoding a root plasma membrane Al uptake transporter previously hypothesized to underlie a unique Al tolerance mechanism. DNA sequence variation in the NRAT1 coding and regulatory regions was associated with changes in NRAT1 expression and NRAT1 Al transport properties. These sequence changes resulted in significant differences in Al tolerance that were found to be associated with changes in the Al content of root cell wall and cell sap in 24 representative rice lines from a rice association panel. Expression of the tolerant OsNRAT1 allele in yeast resulted in higher Al uptake than did the sensitive allele and conferred greater Al tolerance when expressed in transgenic Arabidopsis. These findings indicate that NRAT1 plays an important role in rice Al tolerance by reducing the level of toxic Al in the root cell wall and transporting Al into the root cell, where it is ultimately sequestered in the vacuole. Given its ability to enhance Al tolerance in rice and Arabidopsis, this work suggests that the NRAT1 gene or its orthologs may be useful tools for enhancing Al tolerance in a wide range of plant species.aluminum transport | cell wall aluminum

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mentioning

confidence: 99%

Natural variation underlies alterations in Nramp aluminum transporter ( NRAT1 ) expression and function that play a key role in rice aluminum tolerance

Liu

Dong

et al. 2014

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

149

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“…Rice, which is the most aluminumresistant cereal crop, employs multiple strategies to achieve high aluminum resistance. The rice aluminum stress-responsive transcriptional factor, ART1, regulates expression of 31 downstream genes (Yamaji et al, 2009). In addition to gene-based aluminum tolerance strategies, some external factors can also affect aluminum resistance, such as external phytohormone application.…”

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confidence: 99%

Coordination between Apoplastic and Symplastic Detoxification Confers Plant Aluminum Resistance

et al. 2013

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Whether aluminum toxicity is an apoplastic or symplastic phenomenon is still a matter of debate. Here, we found that three auxin overproducing mutants, yucca, the recessive mutant superroot2, and superroot1 had increased aluminum sensitivity, while a transfer DNA insertion mutant, xyloglucan endotransglucosylase/hydrolases15 (xth15), showed enhanced aluminum resistance, accompanied by low endogenous indole-3-acetic acid levels, implying that auxin may be involved in plant responses to aluminum stress. We used yucca and xth15 mutants for further study. The two mutants accumulated similar total aluminum in roots and had significantly reduced cell wall aluminum and increased symplastic aluminum content relative to the wild-type ecotype Columbia, indicating that altered aluminum levels in the symplast or cell wall cannot fully explain the differential aluminum resistance of these two mutants. The expression of Al sensitive1 (ALS1), a gene that functions in aluminum redistribution between the cytoplasm and vacuole and contributes to symplastic aluminum detoxification, was less abundant in yucca and more abundant in xth15 than the wild type, consistent with possible ALS1 function conferring altered aluminum sensitivity in the two mutants. Consistent with the idea that xth15 can tolerate more symplastic aluminum because of possible ALS1 targeting to the vacuole, morin staining of yucca root tip sections showed more aluminum accumulation in the cytosol than in the wild type, and xth15 showed reduced morin staining of cytosolic aluminum, even though yucca and xth15 had similar overall symplastic aluminum content. Exogenous application of an active auxin analog, naphthylacetic acid, to the wild type mimicked the aluminum sensitivity and distribution phenotypes of yucca, verifying that auxin may regulate aluminum distribution in cells.Together, these data demonstrate that auxin negatively regulates aluminum tolerance through altering ALS1 expression and aluminum distribution within plant cells, and plants must coordinate exclusion and internal detoxification to reduce aluminum toxicity effectively.

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“…The difference in Al-induced secretion in different plant species may be attributed to the expression level of these MATE genes although the exact mechanisms regulating the gene expression is unknown. Recently, a C2H2-type zinc finger transcription factor, STOP1 in Arabidopsis and ART1 in rice (Iuchi et al 2007;Yamaji et al 2009), which regulate AtMATE and OsFRDL2, respectively, have been identified (Liu et al 2009;Yamaji et al 2009). Identification of similar transcription factor in rye may help understand the molecular mechanism of Al tolerance in rye and difference in organic acid secretion between different species.…”

Section: Discussionmentioning

confidence: 99%

“…Following primers, which were designed based on the sequences of HvAACT1 and OsFRDL2 (Furukawa et al 2007;Yamaji et al 2009), were used to amplify fragments from rye cDNA by PCR; 5 0 -ACGGTGGTGCTTGGTCTCTT-3 0 (forward) and 5 0 -CAGG TGCTAGCTACGGTCCTG-3 0 (reverse) for ScFRDL1, 5 0 -TGC ATCAATGGCTGCACGGC-3 0 (forward) and 5 0 -GCAGTCC CTATCCTTAAGAATCCTGC-3 0 (reverse) for ScFRDL2. The fragmentary PCR products were cloned into pGEM-T-Easy vector and the sequences were determined (ABI3130 Genetic Analyser; Applied Biosystems, Foster City, CA, USA).…”

Section: Cloning Of Mate Genes From Ryementioning

confidence: 99%

Isolation and characterisation of two MATE genes in rye

Yokosho

Yamaji

Feng

2010

Functional Plant Biol.

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114

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Abstract. Multidrug and toxic compound extrusion (MATE) proteins are widely present in bacteria, fungi, plants and mammals. Recent studies have showed that a group of plant MATE genes encodes citrate transporter, which are involved in the detoxification of aluminium or translocation of iron from the roots to the shoots. In this study, we isolated two homologous genes (ScFRDL1 and ScFRDL2) from this family in rye (Secale cereale L.). ScFRDL1 shared 94.2% identity with HvAACT1, an Al-activated citrate transporter in barley (Hordeum vulgare L.) and ScFRDL2 shared 80.6% identity with OsFRDL2, a putative Al-responsive protein in rice (Oryza sativa L.). Both genes were mainly expressed in the roots, however, they showed different expression patterns. Expression of ScFRDL1 was unaffected by Al treatment, but upregulated by Fe-deficiency treatment. In contrast, expression of ScFRDL2 was greatly induced by Al but not by Fe deficiency. The Al-induced up-regulation of ScFRDL2 was found in both the root tips and basal roots. Furthermore, the expression pattern of ScFRDL2 was consistent with citrate secretion pattern. Immunostaining showed that ScFRDL1 was localised at all cells in the root tips and central cylinder and endodermis in the basal root. Taken together, our results suggest that ScFRDL1 was involved in efflux of citrate into the xylem for Fe translocation from the roots to the shoots, while ScFRDL2 was involved in Al-activated citrate secretion in rye.

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A Zinc Finger Transcription Factor ART1 Regulates Multiple Genes Implicated in Aluminum Tolerance in Rice

Cited by 355 publications

References 43 publications

Natural variation underlies alterations in Nramp aluminum transporter ( NRAT1 ) expression and function that play a key role in rice aluminum tolerance

Natural variation underlies alterations in Nramp aluminum transporter ( NRAT1 ) expression and function that play a key role in rice aluminum tolerance

Coordination between Apoplastic and Symplastic Detoxification Confers Plant Aluminum Resistance

Isolation and characterisation of two MATE genes in rye

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