Abstract
Oryza sativa L. is a worldwide food-crop frequently growing in cadmium (Cd)/arsenic (As) polluted soils, with its root-system as the first target of the pollutants. Root-system development involves the establishment of optimal indole-3-acetic acid (IAA) levels, also requiring the conversion of the IAA natural precursor indole-3-butyric acid (IBA) into IAA, causing nitric oxide (NO) formation. Nitric oxide is a stress-signaling molecule. In rice, a negative interaction of Cd or As with endogenous auxin has been demonstrated, as some NO protective effects. However, a synergism between the natural auxins (IAA and/or IBA) and NO was not yet determined and might be important for ameliorating rice metal(oid)-tolerance. With this aim, the stress caused by Cd/As toxicity in the root cells and the possible recovery by either NO or auxins (IAA/IBA) were evaluated after Cd or As (arsenate) exposure, combined or not with the NO-donor compound sodium-nitroprusside (SNP). Root fresh weight, membrane electrolyte leakage, and H2O2 production were also measured. Moreover, endogenous IAA/IBA contents, transcription-levels of OsYUCCA1 and OsASA2 IAA-biosynthetic-genes, and expression of the IAA-influx-carrier OsAUX1 and the IAA-responsive DR5::GUS construct were analyzed, and NO-epifluorescence levels were measured. Results showed that membrane injury by enhanced electrolyte leakage occurred under both pollutants and was reduced by the treatment with SNP only in Cd-presence. By contrast, no membrane injury was caused by either exogenous NO or IAA or IBA. Cd- and As-toxicity also resulted into a decreased root fresh weight, mitigated by the combination of each pollutant with either IAA or IBA. Cd and As decreased the endogenous NO-content, increased H2O2 formation, and altered auxin biosynthesis, levels and distribution in both adventitious (ARs) and mainly lateral roots (LRs). The SNP-formed NO counteracted the pollutants’ effects on auxin distribution/levels, reduced H2O2 formation in Cd-presence, and enhanced AUX1-expression, mainly in As-presence. Each exogenous auxin, but mainly IBA, combined with Cd or As at 10 µM, mitigated the pollutants’ effects by increasing LR-production and by increasing NO-content in the case of Cd. Altogether, results demonstrate that NO and auxin(s) work together in the rice root system to counteract the specific toxic-effects of each pollutant.
Highlights
Environmental soil pollution by toxic metal(oid)s is a grave threat to agricultural sustainability and food security, especially in developing and overpopulated countries
The results showed that the negative effects of Cd and As causing alterations in root nitric oxide (NO) levels and auxin biosynthesis, levels, distribution, and cellular damages were mitigated by the exogenous application of indole-3-butyric acid (IBA), indole-3-acetic acid (IAA), and the NO-donor SNP, demonstrating that NO and auxins work together to counteract the pollutants’ toxicity in the root system of rice
Cadmium and arsenic effects on membrane integrity are known as an expression of their toxicity at cellular level, with membrane injury usually resulting from altered antioxidant defence system
Summary
Environmental soil pollution by toxic metal(oid)s is a grave threat to agricultural sustainability and food security, especially in developing and overpopulated countries. Rice (Oryza sativa L.) is the staple food of an estimated 3.5 billion people worldwide and represents one of the main causes of toxic metal poisoning for humans (Abtahi et al, 2017). Inorganic arsenate [As(V)] is one of the most toxic and predominant As forms in aerobic environments and, in rice, is taken up by phosphate transporters, reduced to arsenite [As(III)] in the root cells, loaded into the xylem, and delivered to the grain through the phloem (Zhao et al, 2010). In addition to causing oxidative stress and lipid peroxidation, As(V) exerts its toxicity especially by replacing inorganic phosphate (Pi) in key biochemical reactions and cellular signaling (Garg and Singla, 2011; Finnegan and Chen, 2012)
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