Involvement of phosphatidylinositol metabolism in aluminum-induced malate secretion in Arabidopsis

Abstract

To identify the upstream signaling of aluminum-induced malate secretion through aluminum-activated malate transporter 1 (AtALMT1), a pharmacological assay using inhibitors of human signal transduction pathways was performed. Early aluminum-induced transcription of AtALMT1 and other aluminum-responsive genes was significantly suppressed by phosphatidylinositol 4-kinase (PI4K) and phospholipase C (PLC) inhibitors, indicating that the PI4K–PLC metabolic pathway activates early aluminum signaling. Inhibitors of phosphatidylinositol 3-kinase (PI3K) and PI4K reduced aluminum-activated malate transport by AtALMT1, suggesting that both the PI3K and PI4K metabolic pathways regulate this process. These results were validated using T-DNA insertion mutants of PI4K and PI3K-RNAi lines. A human protein kinase inhibitor, putatively inhibiting homologous calcineurin B-like protein-interacting protein kinase and/or Ca-dependent protein kinase in Arabidopsis, suppressed late-phase aluminum-induced expression of AtALMT1, which was concomitant with the induction of an AtALMT1 repressor, WRKY46, and suppression of an AtALMT1 activator, Calmodulin-binding transcription activator 2 (CAMTA2). In addition, a human deubiquitinase inhibitor suppressed aluminum-activated malate transport, suggesting that deubiquitinases can regulate this process. We also found a reduction of aluminum-induced citrate secretion in tobacco by applying inhibitors of PI3K and PI4K. Taken together, our results indicated that phosphatidylinositol metabolism regulates organic acid secretion in plants under aluminum stress.

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 cellular phosphate levels regulated by AtPHO1 are triggered by the binding of inositol polyphosphate signaling molecules (Wild et al, 2016). Recently, we found that the phosphatidyl inositol metabolic pathway regulates the expression of AtMATE as well as AtALMT1 under Al stress (Wu et al, 2019). Indeed, LaMATE is highly expressed not only under Al stress, but also under phosphate deficiency conditions in the proteoid roots of white lupin (Lupinus albus) (Uhde-Stone et al, 2005).…”

“…Recently, we found that the PtdIns-4-kinase (PI4K) pathway regulated the AtSTOP1-regulating genes of AtALMT1, AtMATE, and ALS3 (Wu et al 2019). However, the mechanism of transcriptional regulation of AtMATE and its association with natural variation are mostly unknown.…”

Ca2+/Calmodulin Complex Triggers CAMTA Transcriptional Machinery Under Stress in Plants: Signaling Cascade and Molecular Regulation

“…In addition, even the transcriptome of CAMTA6 under control and salt stress condition revealed 1,020 upregulated and 1,467 downregulated salt-responsive genes in the wild type (Shkolnik et al, 2019). With regard to context, although CAMTA2 in plants has been less explored, studies highlight the regulation of AtALMT1 (aluminum-activated malate transporter 1) by CAMTA2 in association with WRKY46 (Tokizawa et al, 2015;Wu et al, 2019). Next, considering the involvement of CAMTAs in plant development, the role of CAMTA1 and CAMTA5 is also extended in pollen development.…”

“…Suppressor of SA biosynthesis-related gene transcripts A. thaliana Kim et al, 2013;Sun et al, 2020 Activator of AtALMT1 (metal toxicity) A. thaliana Tokizawa et al, 2015;Wu et al, 2019 Pipecolic acid biosynthesis and priming of immunity genes A. thaliana Kim et al, 2020 AtCAMTA3…”

Root Adaptation via Common Genetic Factors Conditioning Tolerance to Multiple Stresses for Crops Cultivated on Acidic Tropical Soils

“…Recently, Wu et al (2019) reported that blockade of phosphatidylinositol (PI) signaling, especially the Phosphatidylinositol 4-kinase (PI4K) and phospholipase C (PLC) pathways, leads to down-regulation of a number of Al-inducible genes, including ALMT1. PI and its derivatives are membrane lipids and conserved as signaling molecules among eukaryotes, and are involved in various important biological process such as membrane trafficking, root hair and pollen tube tip growth, and stress responses in plants (Meijer and Munnik, 2003;Thole and Nielsen, 2008;Ischebeck et al, 2010;Hou et al, 2016).…”