Characterization of the Complex Regulation of <i>AtALMT1</i> Expression in Response to Phytohormones and Other Inducers

Kobayashi, Yuriko; Sugimoto, Miki; Lakshmanan, Venkatachalam; Iuchi, Satoshi; Kobayashi, Masatomo; Bais, Harsh P.; Koyama, Hiroyuki

doi:10.1104/pp.113.218065

Cited by 80 publications

(67 citation statements)

References 44 publications

(51 reference statements)

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“…Yang et al 2011). The AtALMT1 was also reported to be regulated by phytohormones such as auxin and abscisic acid (Kobayashi et al 2013). Under the circumstances, if Al ions affect auxin distribution at the root apex as suggested previously (Kollmeier et al 2000;Abdalla 2008;Hong et al 2008), Al ions could indirectly control auxininducible genes including SUT1 and ALMT1, and hence inhibit root growth.…”

Section: Ntsut1 Confers Al Tolerancementioning

confidence: 76%

Sucrose transporter NtSUT1 confers aluminum tolerance on cultured cells of tobacco (Nicotiana tabacumL.)

Sameeullah

Sasaki

Yamamoto

2013

Soil Science and Plant Nutrition

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The role of plasma membrane-localized sucrose transporter (NtSUT1) was investigated using cultured tobacco cell (Nicotiana tabacum L.) line BY-2. The wild type (WT) cells were first transformed with the NtSUT1 gene or its fragments cloned from tobacco cell line SL to form the over-expression (OX) and suppression (RNAi) cell lines, respectively. Using OX and RNAi transgenics, the role of NtSUT1 in growth capacity of actively growing cells and in aluminum (Al)-treated cells was examined. During the logarithmic phase of growth in nutrient medium containing 2,4-dichlorophenoxyacetic acid (2,4-D), both the rate of sucrose uptake measured with radio-tracer and the content of soluble sugars were higher in OX and lower in RNAi cell lines compared to WT. Overall, the content of soluble sugars negatively correlated with the time necessary for doubling mass (fresh weight). When cells were treated without (control) or with Al in a simple medium containing calcium, sucrose and 2-(N-morpholino)ethanesulfonic acid (MES; pH 5.0) for up to 18 h, the expression of NtSUT1 under its native promoter, or under the control of strong constitutive cauliflower mosaic virus (CaMV) 35S promoter, was strongly dependent on the presence of 2,4-D. Thereafter, the cells were preferentially treated in the presence of 2,4-D. During 6 h after a start of the control treatment, sucrose uptake rates were, compared to WT, slightly higher and lower in OX and RNAi lines respectively. The addition of Al reduced the sucrose uptake rates of OX and WT to the level of RNAi line, indicating that Al inhibits sucrose uptake via NtSUT1. During the post-Al culture of control and Al-treated cells in a nutrient medium, sucrose uptake rates were much higher in OX compared to WT and RNAi lines, which closely and positively correlated with the growth capacity of the cells. Judging from the growth capacity of Al-treated cells relative to that of control cells, OX cells were more tolerant to Al than WT and RNAi. In summary, we conclude that over-expression of NtSUT1 confers higher growth capacity in actively growing cells as well as in Al-treated cells.

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Section: Ntsut1 Confers Al Tolerancementioning

confidence: 76%

Sucrose transporter NtSUT1 confers aluminum tolerance on cultured cells of tobacco (Nicotiana tabacumL.)

Sameeullah

Sasaki

Yamamoto

2013

Soil Science and Plant Nutrition

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“…7). While it remains to be investigated whether our transgenic tobacco plants are also resistant to the attack of bacterial pathogens, the expression of Arabidopsis for Aluminum-activated Malate Transporter1 has been documented to be involved in both Al tolerance and pathogen resistance (Rudrappa et al, 2008;Lakshmanan et al, 2012;Kobayashi et al, 2013). In our previous study, a pathogenesis-related gene was found to be up-regulated by Al stress in rice bean .…”

Section: Discussionmentioning

confidence: 89%

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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“…The complex transcriptional regulation of these orthologs is consistent with the pleiotropic roles of the root-excreted malate. Transcription of the Arabidopsis ortholog AtALMT1 is activated by Al and by other signal inducers, including a type of microbe-associated molecular pattern peptide, flagellin22 (Kobayashi et al, 2013a). GmALMT1 expression is induced by multiple stressors, namely Al, phosphorus deficiency, and low pH (Liang et al, 2013).…”

mentioning

confidence: 99%

“…promoter function (Kobayashi et al, 2013a). In addition, several bioinformatic procedures have been developed to predict cis-elements (Tompa et al, 2005;Zou et al, 2011).…”

mentioning

confidence: 99%

SENSITIVE TO PROTON RHIZOTOXICITY1, CALMODULIN BINDING TRANSCRIPTION ACTIVATOR2, and Other Transcription Factors Are Involved inALUMINUM-ACTIVATED MALATE TRANSPORTER1Expression

et al. 2015

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In Arabidopsis (Arabidopsis thaliana) the root apex is protected from aluminum (Al) rhizotoxicity by excretion of malate, an Al chelator, by ALUMINUM-ACTIVATED MALATE TRANSPORTER1 (AtALMT1). AtALMT1 expression is fundamentally regulated by the SENSITIVE TO PROTON RHIZOTOXICITY1 (STOP1) zinc finger protein, but other transcription factors have roles that enable Alinducible expression with a broad dynamic range. In this study, we characterized multiple cis-elements in the AtALMT1 promoter that interact with transcription factors. In planta complementation assays of AtALMT1 driven by 59 truncated promoters of different lengths showed that the promoter region between -540 and 0 (the first ATG) restored the Al-sensitive phenotype of atalm1 and thus contains ciselements essential for AtALMT1 expression for Al tolerance. Computation of overrepresented octamers showed that eight regions in this promoter region contained potential cis-elements involved in Al induction and STOP1 regulation. Mutation in a position around -297 from the first ATG completely inactivated AtALMT1 expression and Al response. In vitro binding assays showed that this region contained the STOP1 binding site, which accounted for the recognition by four zinc finger domains of the protein. Other positions were characterized as cis-elements that regulated expression by repressors and activators and a transcription factor that determines root tip expression of AtALMT1. From the consensus of known cis-elements, we identified CALMODULIN-BINDING TRANSCRIPTION ACTIVATOR2 to be an activator of AtALMT1 expression. Al-inducible expression of AtALMT1 changed transcription starting sites, which increased the abundance of transcripts with a shortened 59 untranslated region. The present analyses identified multiple mechanisms that regulate AtALMT1 expression.

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Characterization of the Complex Regulation of AtALMT1 Expression in Response to Phytohormones and Other Inducers

Cited by 80 publications

References 44 publications

Sucrose transporter NtSUT1 confers aluminum tolerance on cultured cells of tobacco (Nicotiana tabacumL.)

Sucrose transporter NtSUT1 confers aluminum tolerance on cultured cells of tobacco (Nicotiana tabacumL.)

A Formate Dehydrogenase Confers Tolerance to Aluminum and Low pH

SENSITIVE TO PROTON RHIZOTOXICITY1, CALMODULIN BINDING TRANSCRIPTION ACTIVATOR2, and Other Transcription Factors Are Involved inALUMINUM-ACTIVATED MALATE TRANSPORTER1Expression

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