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.
Highlights
We have previously demonstrated that there are 7 out of 93 tomato SlNAC genes regulated by Al stress
We further demonstrated that SlNAC063 is a master regulator of SlAAE3-2 transcription, but its regulation on SlAAE3-1 transcription is affected by Al stress
The SlNAC063 gene (Solyc07g063410) encodes a 356-aa protein with a typical NAC domain in its N terminus, which can be divided into five subdomains, namely A, B, C, D, and E (Ooka et al, 2003; Figure 1A)
Summary
Aluminum (Al) is the most abundant metal element in the earth’s crust and its solubility is determined by soil pH. Ionic Al is released into the soil solution, which is highly toxic to plant roots (Kochian, 1995). To cope with Al toxicity, plants have evolved sophisticated mechanisms at multiple levels (Kochian et al, 2015). Upon receiving Al toxic signal, a complicated signaling network might be triggered, which reprograms the expression of an array of Al-responsive genes (Liu et al, 2014). Based on the spatial location of these triggered processes, the implicated mechanisms could be assigned into either external exclusion mechanism or internal tolerance mechanism (Kochian et al, 2015). Among various external exclusion mechanisms, Al-induced organic acid anions secretion has been well-documented as a very important mechanism and widely adopted by many plants to chelate Al, forming non-toxic complexes (Yang et al, 2019; Chen et al, 2022). Internal tolerance mechanisms have been related to the complexation of Al and subsequent compartmentation once Al has entered into cells (Ma et al, 2001)
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