Transcriptomic variation among six Arabidopsis thaliana accessions identified several novel genes controlling aluminium tolerance

Abstract

Differences in the expression levels of aluminium (Al) tolerance genes are a known determinant of Al tolerance among plant varieties. We combined transcriptomic analysis of six Arabidopsis thaliana accessions with contrasting Al tolerance and a reverse genetic approach to identify Al-tolerance genes responsible for differences in Al tolerance between accession groups. Gene expression variation increased in the signal transduction process under Al stress and in growth-related processes in the absence of stress. Co-expression analysis and promoter single nucleotide polymorphism searching suggested that both trans-acting polymorphisms of Al signal transduction pathway and cis-acting polymorphisms in the promoter sequences caused the variations in gene expression associated with Al tolerance. Compared with the wild type, Al sensitivity increased in T-DNA knockout (KO) lines for five genes, including TARGET OF AVRB OPERATION1 (TAO1) and an unannotated gene (At5g22530). These were identified from 53 Al-inducible genes showing significantly higher expression in tolerant accessions than in sensitive accessions. These results indicate that the difference in transcriptional signalling is partly associated with the natural variation in Al tolerance in Arabidopsis. Our study also demonstrates the feasibility of comparative transcriptome analysis by using natural genetic variation for the identification of genes responsible for Al stress tolerance.

Genome-Wide Association Study and Genomic Prediction Elucidate the Distinct Genetic Architecture of Aluminum and Proton Tolerance in Arabidopsis thaliana

“…This suggests that protein processing in the ER is involved in Arabidopsis Al tolerance mechanisms. In fact, a gene encoding the ER-localized protein chaperon (BINDING PROTEIN3) was previously identified as one of the Al tolerant genes in Arabidopsis (Kusunoki et al, 2017). Expression level polymorphism of AtALMT1 and AtTRX1 due to cis-regulatory allelic variation was identified as one of the causes of Al tolerance variation detected by GWA mapping.…”

“…Expression level polymorphism is one of the mechanisms which causes phenotypic variation of Al tolerance among Arabidopsis accessions (Kusunoki et al, 2017). Using randomly chosen 25 accessions, we measured the expression level of four GWASdetected Al tolerance genes, AtALMT1, AtTRM28, AtTRX1, and AtSFR6, that showed more than 30% decrease of Al tolerance in the mutant compared to WT as shown in Figure 5, and analyzed the correlation between the ELP of tolerance genes and RRL Alassociated SNP (Figure 7).…”

“…Furthermore, integration of GP and co-expression gene network analysis could further improve the sensitivity and accuracy of the population genetic methods used for GWAS (Kobayashi et al, 2016;Kooke et al, 2016;Butardo et al, 2017). Novel and unidentified Al tolerance genes were detected previously using genome-wide expression level polymorphism [Expression level polymorphism (ELP); Delker and Quint, 2011] analyses, by comparing the transcriptomes of three Al tolerant and Al sensitive accessions (Kusunoki et al, 2017). This identified genes that had not previously been reported to relate to known Al tolerant mechanisms (e.g., Al extrusion and internal Al tolerant mechanisms), for example BINDING PROTEIN 3, that is linked to the quality control of proteins in endoplasmic reticulum.…”

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

“…The nutrient solution was renewed every 2 days. Subsequently, the seedlings were transferred to the Al stress solution (modified 2% MGRL without Pi, 10 μM AlCl 3 , pH 5.0) according to a previously described method (Kusunoki et al, 2017). After incubation for 9 hr under Al stress conditions, the roots of the seedlings were harvested and immediately frozen in liquid nitrogen.…”

Transcriptional Regulation of Aluminum-Tolerance Genes in Higher Plants: Clarifying the Underlying Molecular Mechanisms

“…Differences in the expression levels of Al-tolerance genes influence the extent of Al tolerance in several important crops such as wheat ( Sasaki et al, 2004 ), rice ( Yamaji et al, 2009 ), and sorghum ( Magalhaes et al, 2007 ). Additionally, an analysis of expression level polymorphisms among Arabidopsis thaliana accessions identified several novel genes that regulate Al tolerance ( Kusunoki et al, 2017 ). In contrast, the identification and characterization of transcription factors and regulatory proteins (e.g., protein kinases) revealed that the transcription of Al-tolerance genes is likely regulated by a very complex mechanism.…”