Systemic proteomic rearrangements under combined hypoxia and arsenic stress drive metabolic shift towards re-aeration survival

Co-occurrence of hypoxia (Hpx) and arsenic (As) exposure is common in nature. Individual Hpx and As-responses in plants have been scrutinized, however only recent studies have revealed unique features of the combination (HpxAs). HpxAs exposure inflates cellular S-demand to offset the highly oxidised cytosolic glutathione redox potential along with required As(III)-sequestration. Further, a dual phosphate-starvation response is recognised in HpxAs. The present study focussed on systemic influence of these HpxAs-responses. HpxAs-exposed plants showed pronounced reduction in carbon assimilation (50%), ferredoxin oxidation (40%), but accumulation of H2O2, Cys and ascorbate (1.41, 2.88 and 2.88-fold, respectively) in leaves. A comprehensive proteomic and metabolomic analysis revealed a hypoxia-predominance in these systemic effects. Critically, despite lowered protein synthesis (rRNA levels), HpxAs-plants showed a selective increase in 935 proteins (322 specific to HpxAs). Their in depth analysis, besides accumulated ABA (4.37-fold) and cis-OPDA (22.2-fold) levels helped identify S- and P-homeostasis-dependent alterations as primary drivers of systemic acclimatization, and role of ROS, ABA and cis-OPDA/oxylipins in systemic signalling. The associated modulation of primary metabolism appears to aid HpxAs plants to endure the imminent re-aeration, thus induce early flowering and the completion of life cycle. This specific set of proteins regulates flowering in HpxAs-exposed Arabidopsis and requires further investigation to identify central regulatory elements.