Abstract
Root architecture responds to environmental stress. Stress-induced metabolic and nutritional changes affect the endogenous root development program. Transcriptional and translational changes realize the switch between stem cell proliferation and cell differentiation, lateral root or root hair formation and root functionality for stress acclimation. The current work explores the effects of stress combination of arsenic toxicity (As) and hypoxia (Hpx) on root development in Arabidopsis thaliana. As revealed previously, combined As and Hpx treatment leads to severe nutritional disorder evident from deregulation of root transcriptome and plant mineral contents. Both As and Hpx were identified to pose stress-specific constraints on root development that lead to unique root growth phenotype under their combination. Besides inhibition of root apical meristem (RAM) activity under all stresses, As induced lateral root growth while root hair density and lengths were strongly increased by Hpx and HpxAs-treatments.A dual stimulation of phosphate (Pi)-starvation response was observed for HpxAs-treated plant roots; however, the response under HpxAs aligned more with Hpx than As. Transcriptional evidence along with biochemical data suggests involvement of PHOSPHATE STARVATION RESPONSE 1; PHR1-dependent systemic signaling. Pi metabolism-related transcripts in close association with cellular iron homeostasis modulate root development under HpxAs. Early redox potential changes in meristematic cells, differential ROS accumulation in root hair zone cell layers and strong deregulation of NADPH oxidases, NADPH-dependent oxidoreductases and peroxidases signify a role of redox and ROS signaling in root architecture remodeling under HpxAs. Differential aquaporin expression suggests transmembrane ROS transport to regulate root hair induction and growth. Reorganization of energy metabolism through NO-dependent alternate oxidase, lactate fermentation, and phosphofructokinase seems crucial under HpxAs. TOR and SnRK-signaling network components were potentially involved in control of sustainable utilization of available energy reserves for root hair growth under combined stress as well as recovery on reaeration. Findings are discussed in context of combined stress-induced signaling in regulation of root development in contrast to As and Hpx alone.
Highlights
Root development is a dynamic and highly regulated process (Scheres et al, 2002; Hodge et al, 2009; Petricka et al, 2012)
Induction of root hairs (RHs) growth serves as an effective strategy to salvage deregulated nutrient uptake by increasing the total root surface area and in turn absorption capability (Gahoonia and Nielsen, 1998; Müller and Schmidt, 2004; Cui S. et al, 2018)
Multiple transcripts involved in root development were identified to be deregulated under HpxAs and potentially responsible for observed root hair growth phenotype
Summary
Root development is a dynamic and highly regulated process (Scheres et al, 2002; Hodge et al, 2009; Petricka et al, 2012). The developmental plasticity of root systems allows plants to establish a sustainable organ tailored to the prevailing environmental conditions. Fine-tuning of the plant root architecture is required upon stress exposure at any life stage. Molecular understanding of root development and underlying gene regulatory networks presently evolves using genomic and molecular biological approaches. Several transcription factors under control of nutrients, redox and reactive oxygen species (ROS) or hormones have been identified (Shin and Schachtman, 2004; Hodge et al, 2009; Ruiz Herrera et al, 2015)
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