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Metabolomics by UHPLC-HRMS reveals the impact of heat stress on pathogen-elicited immunity in maize

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Abstract

Introduction

Studies investigating crop resistance to abiotic and biotic stress have largely focused on plant responses to singular forms of stress and individual biochemical pathways that only partially represent stress responses. Thus, combined abiotic and biotic stress treatments and the global assessment of their elicited metabolic expression remains largely unexplored. In this study, we employed targeted and untargeted metabolomics to investigate the molecular responses of maize (Zea mays) to abiotic, biotic, and combinatorial stress.

Objective

We compared the inducible metabolomes of heat-stressed (abiotic) and C. heterostrophus-infected (biotic) maize and examined the effects of heat stress on the ability of maize to defend itself against C. heterostrophus.

Methods

Ultra-high-performance liquid chromatography-high-resolution mass spectrometry was performed on plants grown under control conditions (28 °C), heat stress (38 °C), Cochliobolus heterostrophus infection, or combinatorial stress [heat (38 °C) + C. heterostrophus infection].

Results

Multivariate analyses revealed differential metabolite expression between heat stress, C. heterostrophus infection, and their respective controls. In combinatorial experiments, treatment with heat stress prior to fungal inoculation negatively impacted maize disease resistance against C. heterostrophus, and distinct metabolome separation between combinatorial stressed plants and the non-heat-stressed infected controls was observed. Targeted analysis revealed inducible primary and secondary metabolite responses to abiotic/biotic stress, and combinatorial experiments indicated that deficiency in the hydroxycinnamic acid, p-coumaric acid, may contribute to the heat-induced susceptibility of maize to C. heterostrophus.

Conclusion

These findings demonstrate that abiotic stress can predispose crops to more severe disease symptoms, underlining the increasing need to investigate defense chemistry in plants under combinatorial stress.

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Data availability

The datasets generated during and/or analyzed during the current study are available at the Metabolomics Workbench Repository (https://doi.org/10.21228/M8NT36).

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Acknowledgements

We thank Fred Quispe, Maritza Romero, Bevin Furguson, and Steve Willms for their technical support. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the USDA.

Funding

This research was funded by the United States Department of Agriculture (USDA) Agricultural Research Service (ARS) project 6036-11210-001-00D.

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  1. Casey A. Chamberlain

    Present address: Department of Chemistry, Washington University in St. Louis, St. Louis, MO, USA

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  1. Chemistry Research Unit, United States Department of Agriculture–Agricultural Research Service, Center for Medical, Agricultural, and Veterinary Entomology, Gainesville, FL, USA

    Shawn A. Christensen, E’lysse A. Santana, Hans T. Alborn, Anna K. Block & Casey A. Chamberlain

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Contributions

SAC and ES designed research; SAC, ES, CAC, and AKB performed research; CAC and HTA contributed analytical tools; SAC, ES, and CAC analyzed the data; SAC, ES, CAC, and AKB interpreted the data; and SAC, ES, and CAC wrote the paper.

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Correspondence to Shawn A. Christensen.

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11306_2020_1739_MOESM1_ESM.xlsx

Supplementary Table 1. Parameters for processing of metabolomics acquisition data using MZmine (Version 2.30). (XLSX 11 kb)

11306_2020_1739_MOESM2_ESM.xlsx

Supplementary Table 2. Significant metabolites identified in this study; all were detected in positive ion mode. (XLSX 11 kb)

11306_2020_1739_MOESM3_ESM.xlsx

Supplementary Table 3. Top significant identified and unidentified features from the four comparisons in this study, all were detected in positive ion mode. (XLSX 28 kb)

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Supplementary Table 4. Principal component analysis loadings values for heat stress (38ºC) vs. control (28ºC) (ref. Fig. 1). (XLSX 298 kb)

11306_2020_1739_MOESM5_ESM.xlsx

Supplementary Table 5. Principal component analysis loadings values for C. heterostrophus infection vs. control (ref. Fig. 2). (XLSX 332 kb)

11306_2020_1739_MOESM6_ESM.xlsx

Supplementary Table 6. Principal component analysis loadings values for heat stress (38ºC) vs. C. heterostrophus infection (ref. Fig. 3). (XLSX 288 kb)

11306_2020_1739_MOESM7_ESM.xlsx

Supplementary Table 7. Principal component analysis loadings values for C. heterostrophus infected maize leaf tissue under control (28ºC) or heat-stressed (38ºC) conditions (ref. Fig. 4). (XLSX 331 kb)

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Christensen, S.A., Santana, E.A., Alborn, H.T. et al. Metabolomics by UHPLC-HRMS reveals the impact of heat stress on pathogen-elicited immunity in maize. Metabolomics 17, 6 (2021). https://doi.org/10.1007/s11306-020-01739-2

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