The Tomato Transcription Factor SlNAC063 Is Required for Aluminum Tolerance by Regulating SlAAE3-1 Expression

Abstract

Aluminum (Al) toxicity constitutes one of the major limiting factors of plant growth and development on acid soils, which comprises approximately 50% of potentially arable lands worldwide. When suffering Al toxicity, plants reprogram the transcription of genes, which activates physiological and metabolic pathways to deal with the toxicity. Here, we report the role of a NAM, ATAF1, 2 and CUC2 (NAC) transcription factor (TF) in tomato Al tolerance. Among 53 NAC TFs in tomatoes, SlNAC063 was most abundantly expressed in root apex and significantly induced by Al stress. Furthermore, the expression of SlNAC063 was not induced by other metals. Meanwhile, the SlNAC063 protein was localized at the nucleus and has transcriptional activation potentials in yeast. By constructing CRISPR/Cas9 knockout mutants, we found that slnac063 mutants displayed increased sensitivity to Al compared to wild-type plants. However, the mutants accumulated even less Al than wild-type (WT) plants, suggesting that internal tolerance mechanisms but not external exclusion mechanisms are implicated in SlNAC063-mediated Al tolerance in tomatoes. Further comparative RNA-sequencing analysis revealed that only 45 Al-responsive genes were positively regulated by SlNAC063, although the expression of thousands of genes (1,557 upregulated and 636 downregulated) was found to be affected in slnac063 mutants in the absence of Al stress. The kyoto encyclopedia of genes and genomes (KEGG) pathway analysis revealed that SlNAC063-mediated Al-responsive genes were enriched in “phenylpropanoid metabolism,” “fatty acid metabolism,” and “dicarboxylate metabolism,” indicating that SlNAC063 regulates metabolisms in response to Al stress. Quantitative real-time (RT)-PCR analysis showed that the expression of SlAAE3-1 was repressed by SlNAC063 in the absence of Al. However, the expression of SlAAE3-1 was dependent on SlNAC063 in the presence of Al stress. Taken together, our results demonstrate that a NAC TF SlNAC063 is involved in tomato Al tolerance by regulating the expression of genes involved in metabolism, and SlNAC063 is required for Al-induced expression of SlAAE3-1.

Oxalate in Plants: Metabolism, Function, Regulation, and Application

“…Oxalate is an antinutritional factor for both animals and human; therefore, manipulating the oxalate content via regulation of oxalate metabolism enzymes, especially reducing the oxalate content in edible parts in crops and pastures, will be of great interest in the future. Our recent finding that a tomato NAC transcription factor SlNAC063 negatively regulates SlAAE3-1 expression that participates in oxalate degradation to improve fruit quality and Al tolerance in tomato provides a new vision for genetic manipulation of oxalic acid metabolism in plants. , …”

Mining Candidate Genes Related to Heavy Metals in Mature Melon (Cucumis melo L.) Peel and Pulp Using WGCNA

“…In recent years, many genes involved in the heavy metal response have been identified and speculated in plants [ 51 , 52 , 53 ]. The expression of these genes plays an important role in the transport and enrichment of heavy metal ions in cells and the improvement of plant resistance.…”

“…The expression of the tomato NAC transcription factor SlNAC063 was upregulated by Al stress. In addition, the expression level of SlNAC063 induced by Al increased with increasing Al concentration and time [ 52 ]. SlNAC063 negatively regulates tomato aluminum tolerance by CRISPR/Cas9 gene editing technology [ 52 ].…”

“…In addition, the expression level of SlNAC063 induced by Al increased with increasing Al concentration and time [ 52 ]. SlNAC063 negatively regulates tomato aluminum tolerance by CRISPR/Cas9 gene editing technology [ 52 ]. The Arabidopsis thaliana WRKY33 gene can be induced to express by exogenous Cd stress, and the Cd accumulation in the overexpression line is lower than that of the wild type, indicating that WRKY33 can regulate the tolerance of Arabidopsis thaliana to Cd stress [ 55 ].…”

Combined de novo transcriptomic and physiological analyses reveal RyALS3-mediated aluminum tolerance in Rhododendron yunnanense Franch

“…In addition to genes encoding transporter protein, a transcription factor (TF) SENSITIVE TO PROTEON RHIZOTOXICITY1 (STOP1) has been demonstrated as a master TF that regulates the expression of many downstream Al-tolerance genes ( Sawaki et al, 2009 ). However, most research advances were achieved by studying crop plants such as wheat and rice and model plants such as Arabidopsis and tomato ( Kochian et al, 2015 ; Yang et al, 2019 ; Jin et al, 2021 , 2022 ; Chen et al, 2022 ). Al toxicity also occurs in forests because nearly 67% of acid soils are covered by forests and woodland ( Brunner and Sperisen, 2013 ).…”