Identification of STOP1-Like Proteins Associated With Aluminum Tolerance in Sweet Sorghum (Sorghum bicolor L.)

Huang, Sheng; Gao, Jie; You, Jun; Liang, Yanan; Guan, Kexing; Yan, Siqi; Zhan, Meiqi; Yang, Zhenming

doi:10.3389/fpls.2018.00258

Cited by 44 publications

(46 citation statements)

References 44 publications

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“…In previous works by others, the cellular localization of Arabidopsis STOP1 and STOP1 homologs was assessed by transient expression in onion cells, Arabidopsis protoplasts, protoplasts derived from rice callus, tobacco leaves or Nicotiana benthamiana leaves. In all these assays, the STOP1 proteins, fused to the GFP, were localized in the nucleus (Sawaki et al ., , ; Yamaji et al ., ; Fan et al ., ; Wang et al ., ; Che et al ., ; Daspute et al ., ; Huang et al ., ; Wu et al ., ). In these assays, the growth media used were not Pi deficient or particularly enriched in Fe or Al 3+ .…”

Section: Discussionmentioning

confidence: 99%

Under phosphate starvation conditions, Fe and Al trigger accumulation of the transcription factor STOP1 in the nucleus of Arabidopsis root cells

et al. 2019

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Summary Low‐phosphate (Pi) conditions are known to repress primary root growth of Arabidopsis at low pH and in an Fe‐dependent manner. This growth arrest requires accumulation of the transcription factor STOP1 in the nucleus, where it activates the transcription of the malate transporter gene ALMT1; exuded malate is suspected to interact with extracellular Fe to inhibit root growth. In addition, ALS3 – an ABC‐like transporter identified for its role in tolerance to toxic Al – represses nuclear accumulation of STOP1 and the expression of ALMT1. Until now it was unclear whether Pi deficiency itself or Fe activates the accumulation of STOP1 in the nucleus. Here, by using different growth media to dissociate the effects of Fe from Pi deficiency itself, we demonstrate that Fe is sufficient to trigger the accumulation of STOP1 in the nucleus, which, in turn, activates the expression of ALMT1. We also show that a low pH is necessary to stimulate the Fe‐dependent accumulation of nuclear STOP1. Furthermore, pharmacological experiments indicate that Fe inhibits proteasomal degradation of STOP1. We also show that Al acts like Fe for nuclear accumulation of STOP1 and ALMT1 expression, and that the overaccumulation of STOP1 in the nucleus of the als3 mutant grown in low‐Pi conditions could be abolished by Fe deficiency. Altogether, our results indicate that, under low‐Pi conditions, Fe2/3+ and Al3+ act similarly to increase the stability of STOP1 and its accumulation in the nucleus where it activates the expression of ALMT1.

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Section: Discussionmentioning

confidence: 99%

Under phosphate starvation conditions, Fe and Al trigger accumulation of the transcription factor STOP1 in the nucleus of Arabidopsis root cells

et al. 2019

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“…Beside, in Arabidopsis, AtMATE gene expression is regulated by AtSTOP1 (sensitive to proton rhizotoxicity 1) and AtSTOP2 as well as AtALMT1 (Iuchi et al, 2007;Liu et al, 2009;Kobayashi et al, 2014). Similarly, in other plant species, the genes encoding STOP1-like transcription factors (TFs) regulate MATE gene expression (Yamaji et al, 2009;Ohyama et al, 2013;Sawaki et al, 2014;Fan et al, 2015;Huang et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

A single‐population GWAS identified AtMATE expression level polymorphism caused by promoter variants is associated with variation in aluminum tolerance in a local Arabidopsis population

et al. 2020

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Organic acids (OA) are released from roots in response to aluminum (Al), conferring an Al tolerance to plants that is regulated by OA transporters such as ALMT (Al‐activated malate transporter) and multi‐drug and toxic compound extrusion (MATE). We have previously reported that the expression level polymorphism (ELP) of AtALMT1 is strongly associated with variation in Al tolerance among natural accessions of Arabidopsis. However, although AtMATE is also expressed following Al exposure and contributes to Al tolerance, whether AtMATE contributes to the variation of Al tolerance and the molecular mechanisms of ELP remains unclear. Here, we dissected the natural variation in AtMATE expression level in response to Al at the root using diverse natural accessions of Arabidopsis. Phylogenetic analysis revealed that more than half of accessions belonging to the Central Asia (CA) population show markedly low AtMATE expression levels, while the majority of European populations show high expression levels. The accessions of the CA population with low AtMATE expression also show significantly weakened Al tolerance. A single‐population genome‐wide association study (GWAS) of AtMATE expression in the CA population identified a retrotransposon insertion in the AtMATE promoter region associated with low gene expression levels. This may affect the transcriptional regulation of AtMATE by disrupting the effect of a cis‐regulatory element located upstream of the insertion site, which includes AtSTOP1 (sensitive to proton rhizotoxicity 1) transcription factor‐binding sites revealed by chromatin immunoprecipitation‐qPCR analysis. Furthermore, the GWAS performed without the accessions expressing low levels of AtMATE, excluding the effect of AtMATE promoter polymorphism, identified several candidate genes potentially associated with AtMATE expression.

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“…To date, at least 12 STOP1‐like plant proteins have been characterised and related to Al and proton tolerance (Fan et al ., ; Huang et al . ).…”

Section: Resultsmentioning

confidence: 97%

GhSTOP1, a C2H2 type zinc finger transcription factor is essential for aluminum and proton stress tolerance and lateral root initiation in cotton

et al. 2018

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The Aluminum (Al) and proton (H ) ions are major acid soil stress factors deleteriously affecting plant root growth and crop yield. In our preliminary studies, cotton seedlings (Gossypium hirsutum L.) displayed very sensitive phenotypes to Al and H rhizotoxicities. Based on previous Arabidopsis results, we aimed to characterize the Al stress responsive Sensitive to Proton rhizotoxicity 1 (GhSTOP1) transcription system in cotton by RNAi mediated down-regulation. With the help of seed embryo apex explants, we developed transgenic cotton plants overexpressing a GhSTOP1-RNAi cassette with NPTII selection. Kanamycin tolerant T1 seedlings were further considered for Al and H stress tolerance studies. Down-regulation of the GhSTOP1 displayed increased sensitivity to Al and proton rhizotoxicities and the root growth was significantly reduced in RNAi-lines. The expression profile of GhALMT1 (Aluminum-activated Malate Transporter 1), GhMATE (Multidrug and Toxic Compound Extrusion), GhALS3 (Aluminum Sensitive 3) and the key genes involved in the GABA shunt were downregulated in the transgenic RNAi lines. Additionally, the lateral root initiation process was delayed and the expression of GhNAC1 which is involved in lateral root initiation was also suppressed in transgenic lines. Besides, overexpression of GhSTOP1 in Arabidopsis accelerated root growth and AtMATE and AtALMT1 expression under Al stress conditions. These analyses indicate that the GhSTOP1 is necessary for the expression of several genes which are necessary for acid soil tolerance mechanisms and lateral root initiation. This article is protected by copyright. All rights reserved.

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Identification of STOP1-Like Proteins Associated With Aluminum Tolerance in Sweet Sorghum (Sorghum bicolor L.)

Cited by 44 publications

References 44 publications

Under phosphate starvation conditions, Fe and Al trigger accumulation of the transcription factor STOP1 in the nucleus of Arabidopsis root cells

Under phosphate starvation conditions, Fe and Al trigger accumulation of the transcription factor STOP1 in the nucleus of Arabidopsis root cells

A single‐population GWAS identified AtMATE expression level polymorphism caused by promoter variants is associated with variation in aluminum tolerance in a local Arabidopsis population

GhSTOP1, a C2H2 type zinc finger transcription factor is essential for aluminum and proton stress tolerance and lateral root initiation in cotton

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