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Regulation of defense responses via heat shock transcription factors in Cucumis sativus L. against Botrytis cinerea

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Abstract

Heat shock transcription factors (HSFs) regulate the responses of plants to heat stress, but their functions in heat-shock-induced resistance (HSIR) are poorly understood. Here, we investigated the functions of HSFs in the resistance induced by a heat shock treatment (HST; 50 °C for 20 s) against gray mold (Botrytis cinerea) in Cucumis sativus by measuring lesion area using image processing and quantitative gene expression analysis. The HST reduced the percentage of lesion area, consistent with the upregulation of peroxidase (POX) and pathogenesis-related (PR) 1.C1 genes at 24 and 48 h after treatment, respectively. Both genes were detected after the upregulation of the heat shock transcription factor A2 (HSFA2) and B2 (HSFB2 genes. Heat shock element (HSE) motifs were found upstream of POX, PR1.C1, POX73, and POX43, and they were upregulated at 24 h after the HST. A heat shock protein 90 (HSP90) inhibitor, geldanamycin (GDA), maintained the upregulation of the HSE-containing PR, thereby reducing gray mold lesions. The GDA treatment enhanced local resistance, whereas the HST induced systemic resistance. The combination of heat shock and GDA treatments induced HSE-containing PR expression and enhanced plant resistance against B. cinerea. The HSIR mechanism involves a pathway related to systemic acquired resistance (SAR). It also involves an HSF-mediated pathway that is associated with local resistance and concealed by the SAR. This study provides novel insights into the molecular mechanisms of HSIR and an alternative approach to activate defense responses against pathogens in cucumber plants.

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Funding

This research was supported by JSPS KAKENHI (Grant Number 17K07637).

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Conceptualization, investigation, validation, formal analysis, resources, data curation, writing—original draft, reviewing and editing, and visualization: ADK and TS; methodology: ADK, NAA, and TS; software: ADK and NAA; supervision: KY, ST, and TS; project administration and funding acquisition: TS.

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Correspondence to Tatsuo Sato.

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The authors declare they have no conflict of interest.

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This article does not contain any studies with human participants or animals performed by any of the authors.

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10327_2021_1041_MOESM1_ESM.tif

Supplementary file1 Supplementary Figure S1. Expression of a POX and b PR1.C1 after only the first leaves of the cucumber plants were subjected to heat shock treatment (partial HST) at 50 °C for 20 s. RNA was extracted from the first and second leaves 24 h after HST and subjected to quantitative PCR; gene expression was normalized using actin expression. Different letters above data for a specific time indicate a significant difference among treatments; bars are error bars (n = 6; Tukey’s test, p < 0.05) (TIF 575 KB)

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Kharisma, A.D., Arofatullah, N.A., Yamane, K. et al. Regulation of defense responses via heat shock transcription factors in Cucumis sativus L. against Botrytis cinerea. J Gen Plant Pathol 88, 17–28 (2022). https://doi.org/10.1007/s10327-021-01041-6

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  • DOI: https://doi.org/10.1007/s10327-021-01041-6

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