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Ethylene Signaling Causing Tolerance of Arabidopsis thaliana Roots to Low pH Stress is Linked to Class III Peroxidase Activity

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Abstract

One irreversible consequence of acidic pH for roots is cell death. Growing evidence suggests the role of hormones and cell wall-related enzymes in response to acidic pH that could possibly avoid cell mortality. Here, we have investigated the role of ethylene and class III peroxidases (CIII Prxs) activity on sensitivity to further low pH treatment. Seedlings of Arabidopsis thaliana were pretreated with ethylene, at various concentrations for various times, and then exposed to low pH. In contrast to non-treated roots, roots pretreated with ethylene for 3 h became tolerant to subsequent low pH, with negligible cell mortality in meristematic (MZ), transition (TZ), and early elongation (EZ) zones. This effect of ethylene was time dependent since it was achieved only when seedlings were pre-incubated with ethylene for at least 3 h. This tolerance induced by ethylene was not observed in the gain-of-function mutation etr1-1 (insensitive to ethylene 1–1). Besides, it was prevented by salicylhydroxamic acid (SHAM) which is an inhibitor of CIII Prxs activity. In late EZ, the decrease in cell expansion due to low pH was dependent on both ethylene signaling and a SHAM-sensitive process. The responses mediated by ethylene signaling might involve CIII Prxs-dependent cell wall modifications, leading to tolerance to low pH and arrest in cell expansion during stress.

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Acknowledgements

We are thankful to CAPES for the support to J.P.G. through the Programa de Doutorado-Sanduíche no Exterior - Brazilian CAPES (Grant # 88881.135425/2016-01). Also, we thank the Paul Sabatier-Toulouse 3 University, CNRS, and the GBF laboratory for experimental support. Finally, we thank the FR AIB imaging platform in Auzeville-Tolosane, particularly Dr Alain Jauneau, Yves Martinez, and Aurélie Le Ru for their great help with microscopy. Finally, we thank the science editor and the anonymous reviewer for their time and a fruitful series of comments.

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JPG performed all experiments. JEL participated in the experiments examining cell expansion. CC designed a system for ethylene application and experimental trials. CD examined experiments regarding CIII Prx. LEPP contributed with suggestions for the project. JPG and VAV wrote the manuscript with major contributions of EJ and CC.

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Correspondence to Victor Alexandre Vitorello or Christian Chervin.

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The authors declare that the research was conducted in the absence of any conflict of interest.

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Graças, J.P., Lima, J.E., Peres, L.E.P. et al. Ethylene Signaling Causing Tolerance of Arabidopsis thaliana Roots to Low pH Stress is Linked to Class III Peroxidase Activity. J Plant Growth Regul 40, 116–125 (2021). https://doi.org/10.1007/s00344-019-10060-9

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  • DOI: https://doi.org/10.1007/s00344-019-10060-9

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