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Cell death induced by fumonisin B1 in two maize hybrids: correlation with oxidative status biomarkers and salicylic and jasmonic acids imbalances

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Abstract

Fungal and plant secondary metabolites modulate host-pathogen interactions. However, the participation of fumonisin B1 (FB1) in the Fusarium verticillioides-maize pathosystem is unclear. In this work, cell death and the reactive oxygen species-phytohormone imbalance interplay as well as their correlation with the FB1 phytotoxicity in two maize genotypes with contrasting resistance to Fusarium ear rot were studied. Resistant (RH) and susceptible hybrid (SH) maize seedlings, grown from uninoculated seeds irrigated with FB1 (1 and 20 μg/mL), were harvested at 7, 14 and 21 days after planting, and were examined for electrolyte leakage (aerial parts) and for oxidative stress biomarkers (aerial parts and roots). The salicylic/jasmonic acid levels associated with cytotoxicity were further explored in seedlings exposed 24 h to FB1 (1 μg/mL) in hydroponics, with and without pre-treatment with the antioxidant ascorbic acid (AA). Cell death increased in RH and SH watered with 1 and 20 μg/mL of mycotoxin, respectively. Both toxin concentrations were pro-oxidant, and the major perturbations were found in roots. The overall plant stress, estimated by an Integrated Biomarker Response index, was higher in plants treated with 20 μg/mL of FB1, while treatment with 1 μg/mL caused more stress in RH at 21 days. Different phytohormone changes were found in both hybrids: salicylic acid increases (prevented by AA) in RH, and jasmonic acid decreases in both germplasms (although prevented by AA pre-treatment only in SH). Cell death induced by FB1 was associated with different phytohormonal regulatory mechanisms in both maize genotypes, some of which were mediated by the redox status.

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Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Code availability

Not applicable.

Abbreviations

AA:

ascorbic acid

CAT:

catalase

dap:

days after planting

EL:

electrolyte leakage

FB1:

fumonisin B1

GPOX:

guaiacol peroxidase

JA:

jasmonic acid

MDA:

malondialdehyde

O2 •- :

superoxide radical anion

RH:

resistant hybrid

ROS:

reactive oxygen species

SA:

salicylic acid

SH:

susceptible hybrid

SOD:

superoxide dismutase

TBA:

thiobarbituric acid

TBARS:

thiobarbituric acid reactive substances

TCA:

trichloroacetic acid

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Acknowledgements

This study was funded by Secretaría de Ciencia y Tecnología (SECyT-UNC, grants 33620180101257CB and 34020190100081CB); Agencia Nacional de Promoción de la Investigación, el Desarrollo Tecnológico y la Innovación, Argentina (ANPCyT, grants PICT 2015-2810; PICT 2019-03229 and PICT 2019-04329); and Ministerio de Ciencia y Tecnología, Córdoba (MINCyT-Cba, grants PE-2019 Theca-free, and GRFT 2019). MGR holds fellowship from ANPCyT. SNOG and PAV hold fellowships from the National Research Council from Argentina (CONICET). MGT, VSM and LB are career investigators of the latter institution.

We thank Ms. Silvina A. Colla, Sworn Translator of English, for the linguistic revision of the manuscript. The content of this work is the sole responsibility of their authors and does not necessarily represent the official views of the organisms that funded this research.

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  1. Centro de Investigaciones en Bioquímica Clínica e Inmunología (CIBICI), UNC, CONICET, Departamento de Bioquímica Clínica, Facultad de Ciencias Químicas, Universidad Nacional de Córdoba, Haya de la Torre y Medina Allende, Ciudad Universitaria, X5000HUA, Córdoba, Argentina

    Santiago N. Otaiza-González, Verónica S. Mary, Silvina L. Arias, Lidwina Bertrand, Pilar A. Velez, María G. Rodriguez, Héctor R. Rubinstein & Martín G. Theumer

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  1. Santiago N. Otaiza-González
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Theumer M.G. conceived and designed research. Otaiza-González S.N. conducted experiments. Arias S.L, Mary V.S., Bertrand L., Velez P.A., Rodriguez M.G. y Rubinstein H.R. contributed to conduct experiments and analyse data. Otaiza-González S.N. and Theumer M.G. wrote the manuscript. All authors have read and approved the manuscript.

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Otaiza-González, S.N., Mary, V.S., Arias, S.L. et al. Cell death induced by fumonisin B1 in two maize hybrids: correlation with oxidative status biomarkers and salicylic and jasmonic acids imbalances. Eur J Plant Pathol 163, 203–221 (2022). https://doi.org/10.1007/s10658-022-02469-y

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