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HOS1 activates DNA repair systems to enhance plant thermotolerance

A Publisher Correction to this article was published on 21 December 2020

This article has been updated

Abstract

Plants possess an astonishing capability of effectively adapting to a wide range of temperatures, ranging from freezing to near-boiling temperatures1,2. Yet, heat is a critical obstacle to plant survival. The deleterious effects of heat shock on cell function include misfolding of cellular proteins, disruption of cytoskeletons and membranes, and disordering of RNA metabolism and genome integrity3,4,5. Plants stimulate diverse heat shock response pathways in response to abrupt temperature increases. While it is known that stressful high temperatures disturb genome integrity by causing nucleotide modifications and strand breakages or impeding DNA repair6, it is largely unexplored how plants cope with heat-induced DNA damages. Here, we demonstrated that high expression of osmotically reponsive genes 1 (HOS1) induces thermotolerance by activating DNA repair components. Thermotolerance and DNA repair capacity were substantially reduced in HOS1-deficient mutants, in which thermal induction of genes encoding DNA repair systems, such as the DNA helicase RECQ2, was markedly decreased. Notably, HOS1 proteins were thermostabilized in a heat shock factor A1/heat shock protein 90 (HSP90)-dependent manner. Our data indicate that the thermoresponsive HSP90–HOS1–RECQ2 module contributes to sustaining genome integrity during the acquisition of thermotolerance, providing a distinct molecular link between DNA repair and thermotolerance.

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Fig. 1: HOS1 is required for the acquisition of thermotolerance.
Fig. 2: DNA damage response is reduced in hos1-3 mutant at high temperatures.
Fig. 3: HOS1 mediates the thermal induction of RECQ2 gene during thermotolerance response.
Fig. 4: The HSFA1–HSP90–HOS1 module activates DNA repair response at high temperatures.

Data availability

The raw RNA-seq data generated during this study were deposited in the NCBI Sequence Read Archive (SRA) database under the accession code PRJNA658831. Source data are provided with this paper. The authors declare that any other supporting data are available from the corresponding author upon request.

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Acknowledgements

We thank Y.-Y. Charng for providing the hsfa1 QK mutant seeds and D. Somers for providing the HSP90-RNAi plants and the ABRC for Arabidopsis plant materials. The RECQ2 cDNA was kindly provided by H. Puchta (Karlsruhe Institute of Technology, Germany). We thank J.-H. Kim for subcloning the RECQ2 gene and S. Shim for statistical analysis. This work was supported by the Leaping Research (grant no. NRF-2018R1A2A1A19020840) Program provided by the National Research Foundation of Korea (NRF) and the Next-Generation BioGreen 21 Program (PJ013134) provided by the Rural Development Administration of Korea.

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Authors

Contributions

C.-M.P. conceived and designed the experiments. C.-M.P. prepared the manuscript with the contributions of S.-H.H. and Y.-J.P. S.-H.H. carried out thermotolerance assays and gene expression and biochemical assays. Y.-J.P. performed data analysis together with S.-H.H. S.-H.H. and Y.-J.P bred and maintained the plant materials. All authors approved the manuscript.

Corresponding author

Correspondence to Chung-Mo Park.

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The authors declare no competing interests.

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Peer review information Nature Plants thanks Chunzhao Zhao and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Fig. 1 Thermotolerance phenotypes of 35S:MYC-HOS1 transgenic plants.

Seven-day-old seedlings grown on ½ X Murashige and Skoog- agar (hereafter referred to as MS-agar) plates at 23 oC were exposed to 37 oC for 4 d. Heat-treated seedlings were allowed to recover at 23 oC for 5 d under constant light conditions before taking photograph (a). Chlorophyll contents were measured (b). Three measurements, each consisting of 15–20 seedlings, were statistically analysed. Error bars indicate standard error of the mean (s.e.m.). Different letters represent significant differences (P < 0.01) determined by one-way analysis of variance (ANOVA) with post hoc Tukey test. The circles indicate individual datapoints. Source data

Extended Data Fig. 2 Relative contents of chlorophylls in DNA damage response-related mutants.

Seven-day-old seedlings grown on MS-agar plates at 23 oC were exposed to 37 oC for 1.5 d. The heat-treated seedlings were allowed to recover at 23 oC for 5 d under constant light conditions before measuring chlorophyll contents. Biological triplicates, each consisting of 15–20 seedlings, were statistically analysed. a, Chlorophyll contents in DNA damage response-related mutants. The selected mutants are defective in genes that were predicted to be involved in the HOS1- mediated induction of thermotolerance from RNA sequencing analysis (refer to Fig. 2c). The upper side of each boxplot indicates median. Error bars indicate s.e.m. (one-sided t-test, *P < 0.01, difference from Col-0). The circles indicate individual datapoints. b, Thermotolerance phenotypes of wrnexo mutant. The RECQ2 protein physically interacts with WERNER SYNDROME-LIKE EXONUCLEASE (WRNexo), a 3'-5' exonuclease that participates in sustaining DNA integrity. Seven-day-old seedlings grown on MS-agar plates at 23 oC were exposed to 37 oC for 1.5 d and then allowed to recover at 23 oC for 10 d under constant light conditions. Biological triplicates, each consisting of 10 seedlings, were statistically analysed. Error bars indicate s.e.m. Different letters represent significant differences (P < 0.01) determined by one-way ANOVA with post hoc Tukey test. The circles indicate individual datapoints. Source data

Extended Data Fig. 3 HOS1 binding to RECQ2 promoter.

a, RECQ2 promoter sequences examined in chromatin immunoprecipitation (ChIP)-qPCR. The conserved G-box and GATA-box sequences were underlined in green and blue, respectively. b, Control data for ChIP–qPCR assays. The assays were performed under the assay conditions identical to those described in Fig. 3f. The measurements were statistically analysed, as described in Fig. 3f. Error bars indicate standard deviation from the mean (s.d.). The data with P1, P2, and P4 sequence elements were displayed. The circles indicate individual datapoints. Source data

Extended Data Fig. 4 Thermotolerance phenotypes of hos1-3 recq2 double mutant.

Seven-day-old seedlings grown on MS-agar plates at 23 oC were exposed to 37 oC for either 1 d (a) or 1.5 d (b) and then allowed to recover at 23 oC for 5 d under constant light conditions (left photographs). Chlorophyll contents were measured (right graphs). Biological triplicates, each consisting of 10 seedlings, were statistically analysed. Error bars indicate s.e.m. Different letters represent significant differences (P < 0.01) determined by one-way ANOVA with post hoc Tukey test. The circles indicate individual datapoints. Source data

Extended Data Fig. 5 Effects of mitomycin on thermotolerance.

a, Thermotolerance phenotypes of hos1-3 mutant in the presence of mitomycin (MMC). Seven-day-old seedlings grown on MS-agar plates at 23 oC were transferred to liquid MS cultures containing 10 μg/ml MMC, which is known to damage DNA molecules by inducing cross-linking of nucleotides, and exposed to 37 oC for 1 d. Heat-treated seedlings were allowed to recover at 23 oC for 5 d under constant light conditions (left photographs). Three measurements of chlorophyll contents, each consisting of 15–20 seedlings, were statistically analysed (right graph). Error bars indicate s.e.m. Different letters represent significant differences (P < 0.05) determined by two-way ANOVA with post hoc Fisher’s multiple comparison test. b, Thermotolerance phenotypes of recq2 mutant in the presence of MMC. Heat-treated seedlings were allowed to recover at 23 oC for 10 d under constant light conditions (left photographs). Chlorophyll contents were measured and statistically analysed (right graph), as described above. The circles indicate individual datapoints. Source data

Extended Data Fig. 6 Effects of radicicol on the thermal accumulation of HOS1 proteins and genomic integrity.

a, Effects of radicicol on the thermal accumulation of HOS1 proteins. Seven-day-old 35S:MYC-HOS1 transgenic seedlings grown on MS-agar plates at 23 oC were transferred to 37 oC and subjected to treatments with 10 μM radicicol, an antibiotic inhibitor of HSP90. The MYC-HOS1 proteins were immunologically detected using an anti-MYC antibody. TUB proteins were assayed in parallel for loading control. Brown arrows mark 112 kDa, and green arrows mark 50 kDa. d, day. Immunoblots were quantitated using the ImageJ software, and three quantitations were statistically analysed. The dotplots indicate median. Error bars indicate s.d. b, Comet assays in the presence of radicicol. Seedling growth, heat treatments, and comet assays were performed, as described in Fig. 2e. DNA breaks were quantitated by measuring the tail ratio of total fluorescence intensity in comet-shaped DNA spots. DNA spots of 8–12 were statistically analysed. Error bars indicate s.d. Different letters represent significant differences (P < 0.01) determined by one-way ANOVA with post hoc Tukey test. Source data

Extended Data Fig. 7 Thermotolerance phenotypes of HSP90- RNAi plants.

a, b, Thermotolerance phenotypes. Seven-day-old seedlings grown on MS-agar plates at 23 oC were exposed to 37 oC for 2 d. Heat-treated seedlings were allowed to recover at 23 oC for 5 d under constant light conditions before taking photograph (a). Chlorophyll contents were measured (b). Three measurements, each consisting of 15–20 seedlings, were statistically analysed using one-sided Student’s t-test (*P = 0.008, difference from Col-0). c, Transcription of RECQ2 gene. Seven-day-old seedlings grown on MS-agar plates at 23 oC were exposed to 37 oC for 2 d. Whole seedlings were used for total RNA preparation. Transcript levels were analysed by RT- qPCR. Biological triplicates, each consisting of 15 seedlings, were statistically analysed (one-sided t-test, *P = 0.0005, **P = 0.0007, difference from 23 oC). In b and c, the upper side of each boxplot indicates median. Error bars indicate s.e.m. The circles indicate individual datapoints. Source data

Extended Data Fig. 8 Thermotolerance phenotypes of hos1-3 mutant in the presence of radicicol.

Seven-day-old seedlings grown on MS-agar plates at 23 oC were transferred to liquid MS cultures containing 10 μM radicicol and exposed to 37 oC for 1 d. Heat-treated seedlings were allowed to recover at 23 oC for 5 d under constant light conditions. Three measurements of chlorophyll contents, each consisting of 15–20 seedlings, were statistically analysed. Error bars indicate s.e.m. Different letters represent significant differences (P < 0.05) determined by two-way ANOVA with post hoc Fisher’s multiple comparison test. The circles indicate individual datapoints. Source data

Extended Data Fig. 9 Thermotolerance phenotypes of hsfa1a/hsfa1b/hsfa1d/ hsfa1e quadruple knockout (hsfa1 QK) mutant.

a, b, Thermotolerance phenotypes. Seven-day-old hsfa1 QK mutant seedlings grown on MS-agar plates at 23 oC were exposed to 37 oC for 1 d. Heat-treated seedlings were allowed to recover at 23 oC for 5 d under constant light conditions before taking photograph (a). Chlorophyll contents were measured (b). Three measurements, each consisting of 15–20 seedlings, were statistically analysed using one-sided Student’s t-test (*P = 0.004, difference from Col-0). c, Transcription of RECQ2 gene. Seven-day-old seedlings grown on MS-agar plates at 23 oC were exposed to 37 oC for 1 d. Whole seedlings were used for total RNA preparation. Transcript levels were analysed by qRT–PCR. Biological triplicates, each consisting of 15 seedlings, were statistically analysed (one-sided t-test, *P = 0.0002, difference from 23 oC). In b and c, the upper side of each boxplot indicates median. Error bars indicate s.e.m. The circles indicate individual datapoints. Source data

Extended Data Fig. 10 Thermotolerance phenotypes of uvh6 mutant.

a, Transcription of ULTRAVIOLET HYPERSENSITIVE 6 (UVH6) gene in hos1-3 mutant at high temperatures. Seven-day-old seedlings grown on MS-agar plates at 23 oC were exposed to 37 oC for 1.5 d. Total RNA samples were extracted from whole seedlings. Transcript levels were analysed by qRT–PCR. Biological triplicates, each consisting of 15 seedlings, were statistically analysed using one-sided Student’s t-test (*P = 0.0019, **P = 0.0017, difference from 23 oC). The upper side of each boxplot indicates median. Error bars indicate s.e.m. The circles indicate individual datapoints. b, Thermotolerance phenotypes of uvh6 mutant. Seven-day-old UVH6-deficient uvh6 mutant grown on MS-agar plates at 23 oC were exposed to 37 oC for 1.5 d and then allowed to recover at 23 oC for 5 d under constant light conditions (left photographs). Chlorophyll contents were measured (right graph). Biological triplicates, each consisting of 10 seedlings, were statistically analysed (one-sided t-test, *P = 0.002, difference from Col-0). The upper side of each boxplot indicates median. Error bars indicate s.e.m. The circles indicate individual datapoints. Source data

Supplementary information

Supplementary Information

Supplementary Figs. 1–9.

Reporting Summary

Supplementary Table 1

Primers used. The PCR primers used were designed according to the National Center for Biotechnology Information (NCBI) Primer-BLAST software (https://www.ncbi.nlm.nih.gov/tools/primer-blast/) in a way that the calculated melting temperatures of the primers are in a temperature range of 50–65 °C. F, forward primer. R, reverse primer.

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Han, SH., Park, YJ. & Park, CM. HOS1 activates DNA repair systems to enhance plant thermotolerance. Nat. Plants 6, 1439–1446 (2020). https://doi.org/10.1038/s41477-020-00809-6

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