Dissection of Root Transcriptional Responses to Low pH, Aluminum Toxicity and Iron Excess Under Pi-Limiting Conditions in Arabidopsis Wild-Type and stop1 Seedlings

Abstract

Acidic soils constrain plant growth and development in natural and agricultural ecosystems because of the combination of multiple stress factors including high levels of Fe 3+ , toxic levels of Al 3+ , low phosphate (Pi) availability and proton rhizotoxicity. The transcription factor SENSITIVE TO PROTON RHIZOTOXICITY (STOP1) has been reported to underlie root adaptation to low pH, Al 3+ toxicity and low Pi availability by activating the expression of genes involved in organic acid exudation, regulation of pH homeostasis, Al 3+ detoxification and root architecture remodeling in Arabidopsis thaliana . However, the mechanisms by which STOP1 integrates these environmental signals to trigger adaptive responses to variable conditions in acidic soils remain to be unraveled. It is unknown whether STOP1 activates the expression of a single set of genes that enables root adaptation to acidic soils or multiple gene sets depending on the combination of different types of stress present in acidic soils. Previous transcriptomic studies of stop1 mutants and wild-type plants analyzed the effect of individual types of stress prevalent in acidic soils. An integrative study of the transcriptional regulation pathways that are activated by STOP1 under the combination of major stresses common in acidic soils is lacking. Using RNA-seq, we performed a transcriptional dissection of wild-type and stop1 root responses, individually or in combination, to toxic levels of Al 3+ , low Pi availability, low pH and Fe excess. We show that the level of STOP1 is post-transcriptionally and coordinately upregulated in the roots of seedlings exposed to single or combined stress factors. The accumulation of STOP1 correlates with the transcriptional activation of stress-specific and common gene sets that are activated in the roots of wild-type seedlings but not in stop1 . Our data indicate that perception of low Pi availability, low pH, Fe excess and Al toxicity converges at two levels via STOP1 signaling: post-translationally through the regulation of STOP1 turnover, and transcriptionally, via the activation of STOP1-dependent gene expression that enables the root to better adapt to abiotic stress factors present in acidic soils.

Titanium nanoparticles activate a transcriptional response in Arabidopsis that enhances tolerance to low phosphate, osmotic stress and pathogen infection

“…These genes include multiple upregulated genes in response to Ti encoding S, Boron (B), putative Silicon (Si) and amino acid transporters, that could play a role in enhancing nutrient uptake in response to Ti treatment ( Figure 5 ). We found that 31 of the so-called Pi-starvation responsive (PSR) genes ( Ojeda-Rivera et al., 2020 ) were upregulated DEGs in roots after 10 days of Ti treatment ( Supplementary Figure S5 ). PSR genes activated by Ti treatment included those encoding the purple acid phosphatases PAP1, and PAP2, which facilitate Pi uptake from organic molecules present in soil ( Figure 5A ).…”

Mass spectrometry‐based quantification and spatial localization of small organic acid exudates in plant roots under phosphorus deficiency and aluminum toxicity

“…Because in our experiments we used seedlings subjected to relatively short Al exposure times, the seedlings were very similar in size, thus normalization by plant gives a better outlook of the potential to exudate OAs under a specific type of stress. It was recently reported that low pH, which in turn interacts with other related stresses like P deficiency and Al and Fe toxicity in acid soils, contributes to STOP1 stabilization and ALMT1 transcriptional activation (Balzergue et al , 2017; Godon et al , 2019; Ojeda‐Rivera et al , 2020). Instead, the role of ALMT1 in roots of WT plants under P deficiency may be restricted to increase malate excretion to the root tip as a component of the meristematic exhaustion mechanism that triggers the root architecture modifications that characterize this nutritional stress (Gutiérrez‐Alanís et al , 2018).…”

Genome accessibility dynamics in response to phosphate limitation is controlled by the PHR1 family of transcription factors inArabidopsis

“…Analysis of GO enrichment and cluster analysis by biological process were performed using g:profiler ( 71 ). Heatmaps of differentially expressed genes were constructed following published bioinformatics methods ( 72 ).…”