Al-induced and -activated Signals in Aluminium Resistance

Editorial

22 June 2022

Editorial: Al-Induced and -Activated Signals in Aluminium Resistance

Hiroyuki Koyama

Chao-Feng Huang

Miguel A. Piñeros

and

Yoko Yamamoto

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0 citations

Editors

Hiroyuki Koyama

Gifu University

Chao-Feng Huang

Shanghai Center for Plant Stress Biology, Shanghai Institute for Biological Sciences, Chinese Academy of Sciences (CAS)

Miguel A Pineros

Robert W. Holley Center for Agriculture and Health, Agricultural Research Service (USDA)

Yoko Yamamoto

Okayama University

Impact

Original Research

17 December 2021

Expression GWAS of PGIP1 Identifies STOP1-Dependent and STOP1-Independent Regulation of PGIP1 in Aluminum Stress Signaling in Arabidopsis

Raj Kishan Agrahari

, 11 more and

Yuriko Kobayashi

To elucidate the unknown regulatory mechanisms involved in aluminum (Al)-induced expression of POLYGALACTURONASE-INHIBITING PROTEIN 1 (PGIP1), which is one of the downstream genes of SENSITIVE TO PROTON RHIZOTOXICITY 1 (STOP1) regulating Al-tolerance genes, we conducted a genome-wide association analysis of gene expression levels (eGWAS) of PGIP1 in the shoots under Al stress using 83 Arabidopsis thaliana accessions. The eGWAS, conducted through a mixed linear model, revealed 17 suggestive SNPs across the genome having the association with the expression level variation in PGIP1. The GWAS-detected SNPs were directly located inside transcription factors and other genes involved in stress signaling, which were expressed in response to Al. These candidate genes carried different expression level and amino acid polymorphisms. Among them, three genes encoding NAC domain-containing protein 27 (NAC027), TRX superfamily protein, and R-R-type MYB protein were associated with the suppression of PGIP1 expression in their mutants, and accordingly, the system affected Al tolerance. We also found the involvement of Al-induced endogenous nitric oxide (NO) signaling, which induces NAC027 and R-R-type MYB genes to regulate PGIP1 expression. In this study, we provide genetic evidence that STOP1-independent NO signaling pathway and STOP1-dependent regulation in phosphoinositide (PI) signaling pathway are involved in the regulation of PGIP1 expression under Al stress.

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13 citations

ALMT1 expression is independently activated by iron (Fe) and Al but both mechanisms’ response can interact to enhance ALMT1 response in the root tip. (A) WT, stop133 and stop1127 seedlings, carrying the pALMT1:GUS reporter, were grown 4 days on phosphate-rich medium (P500) and transferred on a P10 medium pH 5.7 at the indicated concentrations of FeCl2. After 3 days, the Δ root growth of the primary roots was measured, and (B) seedlings were stained for GUS activity for 1 h. As a negative control of the GUS staining, the root tip of the two stop1127 seedlings. Scales = 100 μm. Mean ± SD (n = 13–18 seedlings). (C) WT, stop133, and stop1127 seedlings, carrying the pALMT1:GUS reporter, were grown 4 days on a phosphate-rich medium and transferred on a P10 medium with 5 μM AlCl3 at pH 5.7 at the indicated medium. After 3 days, the Δ root growth of the primary roots was measured, and (D) seedlings were stained for GUS activity for 1 h. As a negative control of the GUS staining, the root tip of the two stop1127 seedlings. Scales = 100 μm. Mean ± SD (n = 13–18 seedlings). (E) Four day-old WT, stop133, and stop1127 seedlings (carrying the pALMT1:GUS reporter) were grown 4 days on a P500Fe10 medium and then transferred 3 days on low-phosphate (10 μM KH2PO4) at the indicated condition before the GUS staining for 2.5 h. Three representative root tips are shown per condition. (F) WT, stop133, and stop1127 seedlings were grown 4 days on a phosphate-rich medium and transferred on P10Fe10 medium with the indicated concentrations of AlCl3, and the primary roots were measured. Mean ± SD (n = 8–14 seedlings).

Original Research

03 May 2022

Uncoupling Aluminum Toxicity From Aluminum Signals in the STOP1 Pathway

Léa Le Poder

, 6 more and

Thierry Desnos

4,367 views

10 citations

Original Research

02 December 2021

Genome-Wide Identification and Gene Expression Analysis of Acyl-Activating Enzymes Superfamily in Tomato (Solanum lycopersicum) Under Aluminum Stress

Jian Feng Jin

, 4 more and

Jian Li Yang

In response to changing environments, plants regulate gene expression and subsequent metabolism to acclimate and survive. A superfamily of acyl-activating enzymes (AAEs) has been observed in every class of creatures on planet. Some of plant AAE genes have been identified and functionally characterized to be involved in growth, development, biotic, and abiotic stresses via mediating diverse metabolic pathways. However, less information is available about AAEs superfamily in tomato (Solanum lycopersicum), the highest value fruit and vegetable crop globally. In this study, we aimed to identify tomato AAEs superfamily and investigate potential functions with respect to aluminum (Al) stress that represents one of the major factors limiting crop productivity on acid soils worldwide. Fifty-three AAE genes of tomato were identified and named on the basis of phylogenetic relationships between Arabidopsis and tomato. The phylogenetic analysis showed that AAEs could be classified into six clades; however, clade III contains no AAE genes of tomato. Synteny analyses revealed tomato vegetable paralogs and Arabidopsis orthologs. The RNA-seq and quantitative reverse-transcriptase PCR (qRT-PCR) analysis indicated that 9 out of 53 AAEs genes were significantly up- or downregulated by Al stress. Numerous cis-acting elements implicated in biotic and abiotic stresses were detected in the promoter regions of SlAAEs. As the most abundantly expressed gene in root apex and highly induced by Al, there are many potential STOP1 cis-acting elements present in the promoter of SlAAE3-1, and its expression in root apex was specific to Al. Finally, transgenic tobacco lines overexpressing SlAAE3-1 displayed increased tolerance to Al. Altogether, our results pave the way for further studies on the functional characterization of SlAAE genes in tomato with a wish of improvement in tomato crop in the future.

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14 citations

Mutation of RAE2 decreases the expression of STOP1-regulated genes. (A) Decreased LUC signal of pAtALMT1:LUC in rae2 mutant compared with wild type (WT). Bar = 7 mm. (B–F) Reduced mRNA expression of STOP1-regulated genes in rae2 and rae3/hpr1, which include LUC reporter gene (B), AtALMT1 (C), AtMATE (D), ALS3 (E), and RAE1 (F). (G–I) Comparison of the expression levels of non-STOP1-target genes in WT, rae2, and rae3, which include AtSTAR1 (G), STOP1 (H), and ALS1 (I). Seven-day-old seedlings were exposed to 0 (–Al) or 30 μM Al (+Al) for 12 h, and then the roots were excised for the expression analysis. Data shown are means ± SD of three biological replicates. Different letters at each treatment indicate the values significantly different (P < 0.05, ANOVA followed by Tukey’s test).

Original Research

12 July 2021

The THO/TREX Complex Component RAE2/TEX1 Is Involved in the Regulation of Aluminum Resistance and Low Phosphate Response in Arabidopsis

Yi-Fang Zhu

, 2 more and

Chao-Feng Huang

The C2H2-type zinc finger transcription factor SENSITIVE TO PROTON RHIZOTOXICITY 1 (STOP1) plays a critical role in aluminum (Al) resistance and low phosphate (Pi) response mainly through promoting the expression of the malate transporter-encoding gene ARABIDOPSIS THALIANA ALUMINUM ACTIVATED MALATE TRANSPORTER 1 (AtALMT1). We previously showed that REGULATION OF ATALMT1 EXPRESSION 3 (RAE3/HPR1), a core component of the THO/TREX complex, is involved in the regulation of nucleocytoplasmic STOP1 mRNA export to modulate Al resistance and low Pi response. Here, we report that RAE2/TEX1, another core component of the THO complex, is also involved in the regulation of Al resistance and low Pi response. Mutation of RAE2 reduced the expression of STOP1-downstream genes, including AtALMT1. rae2 was less sensitive to Al than rae3, which was consistent with less amount of malate secreted from rae3 roots than from rae2 roots. Nevertheless, low Pi response was impaired more in rae2 than in rae3, suggesting that RAE2 also regulates AtALMT1-independent pathway to modulate low Pi response. Furthermore, unlike RAE3 that regulates STOP1 mRNA export, mutating RAE2 did not affect STOP1 mRNA accumulation in the nucleus, although STOP1 protein level was reduced in rae2. Introduction of rae1 mutation into rae2 mutant background could partially recover the deficient phenotypes of rae2. Together, our results demonstrate that RAE2 and RAE3 play overlapping but distinct roles in the modulation of Al resistance and low Pi response.

3,950 views

15 citations

Original Research

31 August 2021

Comparative Inter- and IntraSpecies Transcriptomics Revealed Key Differential Pathways Associated With Aluminium Stress Tolerance in Lentil

Chandan Kumar Singh

, 10 more and

Ashutosh Sarker

4,192 views

9 citations

Original Research

25 June 2021

Novel Sources of Tolerance to Aluminium Toxicity in Wild Cicer (Cicer reticulatum and Cicer echinospermum) Collections

Wendy Vance

, 3 more and

Richard W. Bell

In acid soils, the toxic form of aluminium, Al³⁺, significantly inhibits root growth and elongation, leading to less water and nutrient uptake. Previous research had shown differential Al toxicity tolerance among cultivated Cicer arietinum L. (chickpea); however, the potential for developing tolerant cultivars is limited by the narrow genetic diversity of cultivated chickpeas. Recent collections from Turkey of wild Cicer species, Cicer reticulatum, and Cicer echinospermum, have increased the available gene pool significantly, but there has been no large-scale screening of wild Cicer for acid tolerance or Al³⁺ toxicity tolerance. This study evaluated 167 wild Cicer and 17 Australian chickpea cultivars in a series of screenings under controlled growth conditions. The pH of 4.2 and Al concentrations of 15 and 60 μM Al were selected for large-scale screening based on dose response experiments in a low ionic strength nutrient solution. The change in root length showed better discrimination between tolerant and sensitive lines when compared with shoot and root dry weights and was used as a selection criterion. In a large-scale screening, 13 wild Cicer reticulatum accessions had a higher root tolerance index (≥50%), and eight had higher relative change in root length (≥40%) compared with PBA Monarch, which showed greater tolerance among the Australian domestic cultivars screened. In general, C. reticulatum species were found to be more tolerant than C. echinospermum, while genetic population groups Ret_5, Ret_6, and Ret_7 from Diyarbakir and Mardin Province were more tolerant than other groups. Among C. echinospermum, Ech_6 from the Siv-Diyar collection site of the Urfa Province showed better tolerance than other groups. In this first detailed screening of aluminium toxicity tolerance in the new wild Cicer collections, we identified accessions that were more tolerant than current domestic cultivars, providing promising germplasm for breeding programs to expand chickpea adaptation to acid soils.