Increasing the resilience of plant immunity to a warming climate

doi:10.1038/s41586-022-04902-y

. 2022 Jul;607(7918):339-344.

doi: 10.1038/s41586-022-04902-y. Epub 2022 Jun 29.

Increasing the resilience of plant immunity to a warming climate

Jong Hum Kim^#^{1

2

3}, Christian Danve M Castroverde^#^{4

5

6}, Shuai Huang^{7

8

9}, Chao Li¹⁰, Richard Hilleary^{1

2

3}, Adam Seroka^{1

2

11

12}, Reza Sohrabi^{1

2

3

11}, Diana Medina-Yerena³, Bethany Huot^{1

11}, Jie Wang¹², Kinya Nomura^{1

2

3}, Sharon K Marr¹³, Mary C Wildermuth¹³, Tao Chen¹⁰, John D MacMicking^{7

8

9}, Sheng Yang He^{14

15

16

17

18}

Affiliations

¹ Department of Biology, Duke University, Durham, NC, USA.
² Howard Hughes Medical Institute, Duke University, Durham, NC, USA.
³ Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, MI, USA.
⁴ Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, MI, USA. dcastroverde@wlu.ca.
⁵ Plant Resilience Institute, Michigan State University, East Lansing, MI, USA. dcastroverde@wlu.ca.
⁶ Department of Biology, Wilfrid Laurier University, Waterloo, Ontario, Canada. dcastroverde@wlu.ca.
⁷ Howard Hughes Medical Institute, Yale University, West Haven, CT, USA.
⁸ Yale Systems Biology Institute, Yale University, West Haven, CT, USA.
⁹ Departments of Immunobiology and Microbial Pathogenesis, Yale University School of Medicine, New Haven, CT, USA.
¹⁰ State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University, Wuhan, China.
¹¹ Plant Resilience Institute, Michigan State University, East Lansing, MI, USA.
¹² Department of Plant Biology, Michigan State University, East Lansing, MI, USA.
¹³ Department of Plant and Microbial Biology, University of California Berkeley, Berkeley, CA, USA.
¹⁴ Department of Biology, Duke University, Durham, NC, USA. shengyang.he@duke.edu.
¹⁵ Howard Hughes Medical Institute, Duke University, Durham, NC, USA. shengyang.he@duke.edu.
¹⁶ Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, MI, USA. shengyang.he@duke.edu.
¹⁷ Plant Resilience Institute, Michigan State University, East Lansing, MI, USA. shengyang.he@duke.edu.
¹⁸ Department of Plant Biology, Michigan State University, East Lansing, MI, USA. shengyang.he@duke.edu.

^# Contributed equally.

PMID: 35768511
PMCID: PMC9279160
DOI: 10.1038/s41586-022-04902-y

Increasing the resilience of plant immunity to a warming climate

Jong Hum Kim et al. Nature. 2022 Jul.

. 2022 Jul;607(7918):339-344.

doi: 10.1038/s41586-022-04902-y. Epub 2022 Jun 29.

Authors

Affiliations

¹ Department of Biology, Duke University, Durham, NC, USA.
² Howard Hughes Medical Institute, Duke University, Durham, NC, USA.
³ Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, MI, USA.
⁴ Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, MI, USA. dcastroverde@wlu.ca.
⁵ Plant Resilience Institute, Michigan State University, East Lansing, MI, USA. dcastroverde@wlu.ca.
⁶ Department of Biology, Wilfrid Laurier University, Waterloo, Ontario, Canada. dcastroverde@wlu.ca.
⁷ Howard Hughes Medical Institute, Yale University, West Haven, CT, USA.
⁸ Yale Systems Biology Institute, Yale University, West Haven, CT, USA.
⁹ Departments of Immunobiology and Microbial Pathogenesis, Yale University School of Medicine, New Haven, CT, USA.
¹⁰ State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University, Wuhan, China.
¹¹ Plant Resilience Institute, Michigan State University, East Lansing, MI, USA.
¹² Department of Plant Biology, Michigan State University, East Lansing, MI, USA.
¹³ Department of Plant and Microbial Biology, University of California Berkeley, Berkeley, CA, USA.
¹⁴ Department of Biology, Duke University, Durham, NC, USA. shengyang.he@duke.edu.
¹⁵ Howard Hughes Medical Institute, Duke University, Durham, NC, USA. shengyang.he@duke.edu.
¹⁶ Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, MI, USA. shengyang.he@duke.edu.
¹⁷ Plant Resilience Institute, Michigan State University, East Lansing, MI, USA. shengyang.he@duke.edu.
¹⁸ Department of Plant Biology, Michigan State University, East Lansing, MI, USA. shengyang.he@duke.edu.

^# Contributed equally.

PMID: 35768511
PMCID: PMC9279160
DOI: 10.1038/s41586-022-04902-y

Abstract

Extreme weather conditions associated with climate change affect many aspects of plant and animal life, including the response to infectious diseases. Production of salicylic acid (SA), a central plant defence hormone^1-3, is particularly vulnerable to suppression by short periods of hot weather above the normal plant growth temperature range via an unknown mechanism^4-7. Here we show that suppression of SA production in Arabidopsis thaliana at 28 °C is independent of PHYTOCHROME B^8,9 (phyB) and EARLY FLOWERING 3¹⁰ (ELF3), which regulate thermo-responsive plant growth and development. Instead, we found that formation of GUANYLATE BINDING PROTEIN-LIKE 3 (GBPL3) defence-activated biomolecular condensates¹¹ (GDACs) was reduced at the higher growth temperature. The altered GDAC formation in vivo is linked to impaired recruitment of GBPL3 and SA-associated Mediator subunits to the promoters of CBP60g and SARD1, which encode master immune transcription factors. Unlike many other SA signalling components, including the SA receptor and biosynthetic genes, optimized CBP60g expression was sufficient to broadly restore SA production, basal immunity and effector-triggered immunity at the elevated growth temperature without significant growth trade-offs. CBP60g family transcription factors are widely conserved in plants¹². These results have implications for safeguarding the plant immune system as well as understanding the concept of the plant-pathogen-environment disease triangle and the emergence of new disease epidemics in a warming climate.

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Conflict of interest statement

The authors declare no competing interests.

Figures

**Fig. 1. Temperature vulnerability of *CBP60g* gene expression and the SA transcriptome.**
Leaves of 4- to 5-week-old *Arabidopsis* plants were syringe-infiltrated with mock (0.25 mM MgCl₂), *Pst* DC3000 (10⁶ colony forming units (CFU) per ml⁻¹ suspension) or BTH solution and then incubated at 23 °C or 28 °C. Hormone analysis, RNA sequencing (RNA-seq), and quantitative PCR with reverse transcription (RT–qPCR) were performed 24 h after treatment (that is, 1 day post-inoculation (dpi)). a, A schematic diagram of the experimental protocol. b,c, *ICS1* transcript (b) and SA (c) levels in mock- and *Pst* DC3000-infiltrated Col-0 plants at 1 dpi. FW, fresh weight. d,e, SA levels in mock- and *Pst* DC3000-inoculated Col-0 (d,e) and *35S::ICS1* (d) or *npr1*^S11D/S15D (e) plants at 1 dpi. f, Endogenous *CBP60g* transcript level of samples in b at 1 dpi. g, Top, schematic of the *GUS* reporter gene. Bottom, *GUS* reporter gene expression in mock-, *Pst* DC3000- and BTH-treated *pCBP60g::GUS* plants one day after treatment. h, Gene Ontology (GO) analysis of *Pst* DC3000-induced genes that are differentially regulated at elevated temperature and their overlap with the SARD1 and CBP60g ChIP–sequencing dataset. i, Representative RNA-seq reads after *Pst* DC3000 infection of defence-related CBP60g target genes for plants in h. TPM, transcripts per million mapped reads. Data in b–g,i are mean ± s.d. (n = 3 (c,g,i) or 4 (b,d–f) biological replicates) from one representative experiment analysed with two-way ANOVA with Tukey’s honest significant difference (HSD) for significance. Experiments were independently performed three times, except for i, with two experiments. Exact P-values for all comparisons are shown in the Source Data. Source data

**Fig. 2. Elevated temperature represses *CBP60g* promoter activity.**
Four- to five-week-old Col-0 and indicated transgenic plants were treated with mock (0.1% DMSO) or 100 µM BTH solution and then incubated at 23 °C and 28 °C. ChIP–qPCR and confocal imaging were performed in plants one day after treatment. a, ChIP–qPCR analyses of *NPR1pro::NPR1-YFP* using anti-GFP antibody and indicated primer sets. The position of the *CBP60g* primer sequence is shown in f. b, Confocal imaging of eGFP–GBPL3 in *35S::eGFP-GBPL3* infiltrated with mock (0.1% DMSO), 200 µM SA or 100 µM BTH solution at 23 °C or 28 °C 1 day after treatment. Scale bar, 10 μm. c–e, ChIP–qPCR analyses of *35S::eGFP-GBPL3* (c), *NPR1pro::NPR1-YFP* (d) and *MED16pro::MED16-flag* (e) plants using the indicated antibodies and primer sets. f, Schematic showing known regulators binding at the *CBP60g* locus. Temperature-susceptible (green) and temperature-resilient (orange) modules are indicated. Primer positions (P1 for promoter region and P2 for coding region) are indicated. For ChIP analyses, the *TA3* transposon was used as the negative control target locus in (a,c–e). A BTH-treated Col-0 sample incubated at 23 °C (c,e) was used as a negative control for immunoprecipitation. Results in (a,c–e) are mean ± s.d. of three independent experiments; two-way ANOVA with Tukey’s HSD. Images in b show one representative experiment (of four independent experiments); one-way ANOVA with Bartlett’s test. Exact P-values greater than 0.05 are shown in the Source Data. Source data

**Fig. 3. Restoration of SA accumulation and immunity at elevated temperature in *35S::CBP60g* plants.**
Wild-type Col-0 and *35S::CBP60g* plants were syringe-infiltrated with mock (0.25 mM MgCl₂) or *Pst* DC3000 (10⁶ CFU ml⁻¹) and incubated at 23 °C or 28 °C. a, SA levels in mock- and *Pst* DC3000-inoculated plants at 24 h (1 dpi). b, Images of leaves from *Pst* DC3000-inoculated plants at 3 dpi. c, In planta *Pst* DC3000 bacterial levels at 3 dpi. d,e, In planta *Pst* DC3000 (*avrPphB*) (d) or *Pst* DC3000 (*avrRps4*) (e) bacterial levels at 3 dpi. f, Heat map of RNA-seq reads for genes that are downregulated in Col-0 grown at 28 °C but fully or partially restored in *35S::CBP60g* grown under the same conditions. RPKM, reads per kilobase of transcript per million mapped reads. Data in a,c,e are mean ± s.d. (n = 4 biological replicates) of one representative experiment (out of three independent experiments) analysed by two-way ANOVA with Tukey’s HSD. Results in d are mean ± s.d. (n = 4 biological replicates except *35S::CBP60g* at 23 °C (n = 3 biological replicates)) of one representative experiment (out of three independent experiments) analysed by two-way ANOVA with Tukey’s HSD. Exact P-values for all comparisons are shown in the Source Data. Source data

**Fig. 4. Optimized *CBP60g* expression leads to temperature-resilient SA defences without growth or developmental trade-offs.**
Col-0, *35S::CBP60g* and *35S::uORFs*_TBF1-CBP60g plants were syringe-infiltrated with mock (0.25 mM MgCl₂) or *Pst* DC3000 solution (10⁶ CFU ml⁻¹) and then incubated at 23 °C and 28 °C. a, Foliar disease symptoms were evaluated at 3 dpi. b, In planta *Pst* DC3000 bacterial levels in samples in a at 3 dpi. c, SA levels in samples in a at 1 dpi. d, In planta *Pst* DC3000 (*avrPphB*) and *Pst* DC3000 (*avrRps4*) bacterial levels at 3 dpi. e, Fresh weight (left) at day 28 and flowering time (right) for the indicated plant genotypes. f, A working model of how elevated temperature targets the SA defence and immune network through *CBP60g* expression. At normal growth temperature, infection induces *CBP60g* gene expression. CBP60g regulates various defence genes, including those involved in SA accumulation (such as *ICS1, EDS1* and *PAD4*). At elevated temperature, recruitment of Mediator, GBPL3 and RNA Pol II to the *CBP60g* locus is impaired, leading to lower SA production and reduced immunity at elevated temperature. Data in b–d are mean ± s.d. (n = 3 biological replicates) from one representative experiment (out of three independent experiments) analysed by two-way ANOVA with Tukey’s HSD. Data in e are mean ± s.d. (n = 12 biological replicates) from one representative experiment (out of three independent experiments), analysed by one-way ANOVA with Bartlett’s test. Exact P-values greater than 0.05 are shown in the Source Data. Source data

**Extended Data Fig. 1. The SA pathway is downregulated at elevated temperatures in different plant species examined.**
**a–b**, SA levels in 4-week-old Col-0 plants at 24 h after treatment [i.e., 1 day post-inoculation (dpi)] with flg22 peptide treatment (a) or *Pst* DC3000(*avrRps4*) inoculation [1.0 x 10⁸ Colony Forming Units (CFU) mL⁻¹] (b) at 23 °C and 28 °C. **c–d**, Transcript levels of *BnaPR1* in leaves of 4-week-old rapeseed Westar plants infiltrated with mock (0.25 mM MgCl₂) or *Pst* DC3000 [1.0 x 10⁵ Colony Forming Units (CFU) mL⁻¹] (c) and *NtPR1* in leaves of 4-week-old tobacco plants infiltrated with mock (0.25 mM MgCl₂) or *Ps tabaci* 11528 [1.0 x 10⁶ Colony Forming Units (CFU) mL⁻¹] (d) at 24 h post-inoculation (1 dpi) at 23 °C and 28 °C. e, *BnaPR1* expression levels in leaves of 4-week-old rapeseed Westar plants 1 day after mock (0.1% DMSO) or 50 µM BTH treatment at 23 °C and 28 °C f, SA marker gene (*SlPR1b*) expression levels in 4-week-old Castlemart tomato plants 1 day after mock (0.1% DMSO) or 100 µM BTH treatment at 23 °C and 32 °C. g, SA marker gene (*OsPR1b*) expression levels in 5-week-old rice plants 1 day after mock (0.1% DMSO) or 200 µM BTH treatment at 28 °C and 35 °C. Results show the means ± S.D. [n = 3 (c, e–g) or 4 (a, b, d) biological replicates] from one representative experiment (of three independent experiments) analyzed with two-way ANOVA with Tukey’s HSD for significance. Exact P-values for all comparisons are detailed in the Source Data files Source data

Extended Data Fig. 2. Basal resistance to *Pst* DC3000 at control (23 °C) and elevated temperature (28–30 °C) in constitutively activated phyB and ELF3 thermosensor lines and in genetically activated SA biosynthetic and signalling mutants.
**a–f**, Symptom expression at 3 day post-inoculation (dpi) (a, d), *in planta Pst* DC3000 bacterial levels at 3 dpi (b, e) and SA levels of mock (0.25 mM MgCl₂)- and *Pst* DC3000-inoculated leaves [1.0 x 10⁶ Colony Forming Units (CFU) mL⁻¹] at 1 dpi (c, f) of Ler (a–c), Col-0 (d–f), *35S::PHYB*^Y276H (a–c), and *BdELF3-*OE (d–f). **g–j**, Symptom expression at 3 dpi (g, i) and *in planta Pst* DC3000 bacterial levels at 3 dpi (h, j) of Col-0 (g–j), *35S::ICS1* (g, h), and *npr1*^S11D/S15D (i, j). **k–p**, Symptom expression at 3 dpi (k,n), *in planta Pst* DC3000 bacterial levels at 3 dpi (l, o) and SA levels of mock- and *Pst* DC3000-inoculated leaves at 1 dpi (m, p) of Col-0 (k–p), *npr3/4* (k–m), and *35S::TGA1* (n–p). Results show the means ± S.D. [n = 4 (c, e, j, l, m, p) or n = 3 (h, o) biological replicates] from one representative experiment (of three independent experiments) analyzed with two-way ANOVA with Tukey’s HSD for significance. Results show the means ± S.D. [(b) n = 4 biological replicates except *35S::PHYB*^Y276H at 30 °C (n = 3 biological replicates), (f) n = 4 biological replicates except *BdELF3*-OE, *Pst* at 23 °C (n = 3 biological replicates)] from one representative experiment (of three independent experiments) analyzed with two-way ANOVA with Tukey’s HSD for significance. Exact P-values for all comparisons are detailed in the Source Data files Source data

**Extended Data Fig. 3. Effect of elevated temperature on transcript levels, protein levels and promoter recruitment of SA pathway regulators.**
**a–d**, Endogenous *EDS1* (a)*, PAD4* (b)*, WRKY75* (c), and *BSMT1* (d) transcript levels of samples in Fig. 1b at 24 h after treatment (1 dpi). e, *CBP60g* gene expression levels in Col-0 and *npr1*–6 plants at 24 h after *Pst* DC3000 inoculation [1.0 x 10⁶ Colony Forming Units (CFU) mL⁻¹] at 23 °C. f, ChIP-qPCR analysis of *35S::TGA1-4myc* using anti-myc antibody and primer sets indicated in Fig.2f. Binding of TGA1-myc to *CBP60g* locus is not affected by temperature in mock (0.1% DMSO)- or BTH-treated samples (P-value = 0.7903 and 0.9566, respectively). g, Immunoblot results of *35S::TGA1-myc* used for ChIP-qPCR analyses in (f). h, NPR1 immunoblot of *NPR1pro::NPR1-YFP* plant cytosolic and nuclear protein fractions 24 h after BTH treatment at 23 °C and 28 °C. Both NPR1 oligomers (high molecular weight) and monomers (low molecular weight) are indicated by arrowheads. Anti-UGPase immunoblot is shown as the cytoplasmic marker control. i, ChIP-qPCR results of *NPR1pro::NPR1-YFP* using anti-MED6 antibody and primer sets indicated in Fig.2f. j, Immunoblot result of *MED16pro::MED16-3flag* used for ChIP-qPCR analysis in Fig. 2e. k, Immunoblot results of *NPR1pro::NPR1-YFP* using anti-MED6 antibody used for ChIP-qPCR analyses in (i). l, ChIP-qPCR results of *35S::CDK8-myc* using anti-myc antibody and primer sets indicated. m, Immunoblot results of *35S::CDK8-myc* using anti-myc antibody used for ChIP-qPCR analyses in (l). For immunoblot (g, j, k, m), stained RuBisCO large subunits are shown as loading controls. Numbers in panels (g, h, j, k, m) indicate relative protein band signal intensities compared to the corresponding band denoted with a * symbol(s). For gel/blot source data, see Supplementary Fig. 1. For ChIP analyses, the *TA3* transposon was used as the negative control target locus. Primer positions (P1 for promoter region and P2 for coding region) are indicated in Fig. 2f. Antibody information is included in Supplementary Table 5. Result in (a–e) shows the means ± S.D. [n = 4 (a–d) or 3 (e) biological replicates] from one representative experiment [of three (a–d) or two (e) independent experiments] analyzed with two-way ANOVA with Tukey’s HSD for significance. Results in (g, h, j, k, m) show one representative experiment [of two (g, h) or three (j, k, m) independent experiments]. Results in (f, i, l) are the average ± S.D. [of three independent experiments (n = 3 experiments)], analyzed with two-way ANOVA with Tukey’s HSD for significance. Exact P-values for those comparisons that are greater than 0.05 are detailed in the Source Data files Source data

**Extended Data Fig. 4. Characterization of *35S::eGFP-GBPL3* and *GBPL3 OX* plants.**
a, *CBP60g* gene expression levels in Col-0, *gbpl3-3*, and *35S::eGFP-GBPL3* plants at 24 h (1 day) after mock (water) or 200 µM salicylic acid spray at 23 °C. b, Immunoblot results of *35S::eGFP-GBPL3* used for ChIP-qPCR analyses in Fig. 2c. Stained RuBisCO large subunits are shown as loading controls. Numbers in the panel indicate relative protein band signal intensities compared to the corresponding band denoted with a * symbol. c, Subcellular fractionation of *Arabidopsis* Col-0 leaf cells treated with mock (0.1% DMSO) or BTH for 24h at control (23 °C) or elevated temperature (28 °C). Actin and Histone H3 protein were used as markers of cytoplasmic and nuclear fractions, respectively. d, *In planta Pst* DC3000 [1.0 x 10⁶ Colony Forming Units (CFU) mL⁻¹] bacterial levels in Col-0, *GBPL3* OX #16 and *GBPL3* OX #20 plants at 3 dpi. e, *CBP60g* gene expression levels of Col-0 and *GBPL3* OX #20 plants at 24 h after mock (0.1% DMSO) or 100 µM BTH spray at 23 °C or 28 °C. f, Time lapse confocal microscopy of *Arabidopsis* mesophyll cell expressing eGFP-GBPL3 after transfer to 28 °C from 23 °C or to 23 °C from 28 °C. Scale bar, 10 µm. g, Prediction of intrinsically disordered region in AtMED15 (Threshold score: 0.5). h, Confocal microscopy of *Nicotiana tabacum* mesophyll cells transiently expressing eGFP-GBPL3 and mRFP-MED15 at 23 °C and 28 °C. Six to seven weeks old *N. tabacum* leaves were infiltrated with *Agrobacterium* harbouring *35S::eGFP-GBPL3* or *35S::mRFP-MED15-flag*. After incubation for 3 days at control temperature, the plants were treated with 100 µM BTH solution and shifted to 23 °C or 28 °C. After 1 day, mesophyll cells were visualized by confocal microscopy. Scale bar, 10 µm. Results in (a, d, e) show the means ± S.D. [(a) n = 4, (d) n = 4 except GBPL3 OX 16 at 23 °C (n = 3 biological replicates), or (e) n = 3 biological replicates] from one representative experiment (of two independent experiments), analyzed with two-way ANOVA with Tukey’s HSD for significance. Results in (b, left panel of c) show one representative experiment (of three independent experiments). Result in (right panel of c) shows the means ± S.D. (of three independent experiments) analyzed with one-way ANOVA with Bartlett’s test for significance. Results in (f, h) show one representative experiment (of two independent experiments). Exact P-values for all comparisons are detailed in the Source Data files Source data

**Extended Data Fig. 5. Characterization of *35S::CBP60g* 16 and *cbp60g-1* plants.**
a, *CBP60g* transcript levels in 4-week old *35S::CBP60g* at 23 °C or 28 °C 1 day after mock (0.25 mM MgCl₂) treatment or *Pst* DC3000 infection [1.0 x 10⁶ Colony Forming Units (CFU) mL⁻¹]. **b–d**, SA levels at 1 dpi (b), symptom expression at 3 dpi (c) and *in planta Pst* DC3000 [1.0 x 10⁶ Colony Forming Units (CFU) mL⁻¹] bacterial levels at 3 dpi (d) of Col-0 and *35S::CBP60g* 16 plants. **e–g**, bacterial levels in Col-0 and *cbp60g-1* plants inoculated with *Pst* DC3000 (e), *Pst* DC3000 (*avrPphB*) (f), and *Pst* DC3000 (*avrRps4*) (g) at 3 dpi. h, *ICS1* gene expression levels in *Pst* DC3000 *ΔhrcC-*infected Col-0 and *35S:CBP60g* plants [1.0 x 10⁸ Colony Forming Units (CFU) mL⁻¹] at 12- and 24-h post-inoculation (hpi). i, SA levels in *Pst* DC3000 *ΔhrcC-*infected Col-0 and *35S:CBP60g* plants (1.0 x 10⁸ Colony Forming Units (CFU) mL⁻¹) at 24 h post-inoculation. **j–k**, *In planta Pst* DC3000 (*avrPphB*) (j), and (*avrRps4*) (k) bacterial levels of Col-0 and *35S::CBP60g* 16 plants at 3 dpi. l, *ICS1, EDS1* and *PAD4* gene expression levels of Col-0 and *35S::CBP60g* plants 1 day after mock (0.25 mM MgCl₂)- and *Pst* DC3000-infiltration [1.0 x 10⁶ Colony Forming Units (CFU) mL⁻¹]. Results show the means ± S.D. [n = 3 (a, f, g, h) or 4 (b, d, i) biological replicates] from one representative experiment [of two (a, h, i) or three (b, d, f, g) independent experiments] analyzed with two-way ANOVA with Tukey’s HSD for significance. Results in (e) show the means ± S.D. [n = 4 biological replicates except Col-0 at 23 °C (n = 3 biological replicates)] from one representative experiments (of three independent experiments) analyzed with two-way ANOVA with Tukey’s HSD for significance. Results in (j) show the means ± S.D. [n = 4 (Col-0) or 3 (*35S::CBP60g* 16) biological replicates] from one representative experiments (of three independent experiments) analyzed with two-way ANOVA with Tukey’s HSD for significance. Results in (k) show the means ± S.D. [n = 4 biological replicates except *35S::CBP60g* 16 at 23 °C (n = 3 biological replicates)] from one representative experiments (of three independent experiments) analyzed with two-way ANOVA with Tukey’s HSD for significance. Exact P-values for those comparisons that are greater than 0.05 are detailed in the Source Data files Source data

**Extended Data Fig. 6. Characterization of *35S::SARD1* plants.**
**a–c**, SA levels at 24 h (a), symptom expression at day 3 (b), *in planta* bacterial levels at day 3 (c) post-inoculation with mock (0.25 mM MgCl₂) or *Pst* DC3000 solution [1.0 x 10⁶ Colony Forming Units (CFU) mL⁻¹]. d, *SARD1* gene expression levels in 4-week-old plants of Col-0 and *35S::SARD1*. e, Appearance of 4.5-week-old Col-0 and *35S::SARD1* plants (lines b1 and b2) grown at 23 °C were infiltrated with 1 x 10⁶ CFU mL⁻¹ *Pst* DC3000 and further incubated at 28 °C for 3 days. Results in (a) show the means ± S.D. [n = 6 (Col-0, 23 °C mock and Col-0, 23 °C *Pst*), 7 (Col-0, 28 °C mock and Col-0, 28 °C *Pst*), 8 (all *35S::SARD1* b1 line data), 7 (*35S::SARD1* b2 line, 23 °C mock), 8 (*35S::SARD1* b2 line, 23 °C *Pst*), 8 (*35S::SARD1* b2 line, 28 °C mock), or 7 (*35S::SARD1* b2 line, 28 °C *Pst*) biological replicates from two independent experiments] analyzed with two-way ANOVA with Tukey’s HSD for significance. Results in (c) show the means ± S.D. [n = 3 (Col-0 at 23 °C), 4 (Col-0 at 28 °C), 3 (*35S::SARD1* b1 at 23 °C), 4 (*35S::SARD1* b1 at 28 °C), or 3 (*35S::SARD1* b2 at 23 °C and 28 °C) biological replicates] from one representative experiments (of four independent experiments) analyzed with two-way ANOVA with Tukey’s HSD for significance. Results in (d) show the means ± S.D. (n = 3 biological replicates) from one representative experiments (of two independent experiments) analyzed with one-way ANOVA with Bartlett’s test for significance. Result in (e) shows one representative experiment of four independent experiments. Exact P-values for those comparisons that are greater than 0.05 are detailed in the Source Data files Source data

**Extended Data Fig. 7. *BnaICS* and *BnaPR1* transcript levels in transgenic rapeseed plants expressing *AtCBP60g-myc*.**
a, A schematic diagram of experimental flow using *Agrobacterium*-mediated transient expression system. b, Transcript levels of *BnaICS1* and myc-tagged transgenes (*mRFP-myc* or *AtCBP60g-myc*) in mock (0.25 mM MgCl₂)- or *Pst* DC3000-infiltrated [1.0 x 10⁵ Colony Forming Units (CFU) mL⁻¹] rapeseed leaves at 1 dpi. Leaves were pre-infiltrated with *Agrobacterium* suspension 3 days before mock or *Pst* DC3000 treatment. Results in (b) are the means ± S.D. (n = 4 biological replicates from two independent experiments). Statistical analysis was performed using two-way ANOVA with Tukey’s HSD. The experiment was repeated four times with similar results. c, Transcript levels of *BnaICS1*, *BnaPR1* and *AtCBP60g-myc* in mock- or *Pst* DC3000-infiltrated [1.0 x 10⁵ Colony Forming Units (CFU) mL⁻¹] wild-type and two independent *35S::AtCBP60g-myc* transgenic rapeseed leaves. *AtCBP60g* transcript level in each leaf sample was quantified (bottom row). No *AtCBP60g* transcript was detected in Westar samples as control, whereas *AtCBP60g* transcript was detected in each *35S::AtCBP60g-myc* sample. Data in (c) are the means S.E.M. (n = 4 biological replicates). The experiment was repeated twice. Statistical analysis was performed using two-way ANOVA with Tukey’s HSD. n.a., not applicable. Exact P-values for those comparisons that are greater than 0.05 are detailed in the Source Data files Source data

**Extended Data Fig. 8. *Pst* DC3000 bacterial population levels in *Arabidopsis* Col-0 and the *ics1* mutant.**
**a–b**, *In planta Pst* [1.0 x 10⁶ Colony Forming Units (CFU) mL⁻¹] bacterial levels in Col-0 and *ics1* (i.e., *sid2-2*) plants at 23 °C and 30 °C at 1 (a) and 3 (b) dpi. Data are the means ± S.D. (n = 4 biological replicates). The experiment was repeated three times. Statistical analysis was performed using two-way ANOVA with Tukey’s HSD. Exact P-values for all comparisons are detailed in the Source Data files Source data

**Extended Data Fig. 9. SA accumulation and basal immunity to *Pst* DC3000 at elevated temperature in plants altered in positive and negative SA regulators.**
**a–e**, SA levels at 1 dpi (left panels), symptom expression at 3 dpi (middle panels) and *in planta Pst* DC3000 bacterial levels at 3 dpi (right panels) of Col-0 (a–e) and *35S::EDS1* (a)*, 35S::PAD4* (b), *35S::WRKY75* (c), *bsmt1* (d) and *camta2/3* plants (e) [1.0 x 10⁶ Colony Forming Units (CFU) mL⁻¹]. Results show the means ± S.D. [n = 4 (a, b) biological replicates] from one representative experiment (of three independent experiments) analyzed with two-way ANOVA with Tukey’s HSD for significance. Results in (c) show the means ± S.D. [left panel: n = 4 biological replicates except *35S::WRKY75, Pst* at 23 °C (n = 3 biological replicates); right panel: n = 3 biological replicates except *35S::WRKY75* at 23 °C (n = 4 biological replicates)] from one representative experiment (of three independent experiments) analyzed with two-way ANOVA with Tukey’s HSD for significance. Results in (d) show the means ± S.D. [left panel: n = 4 biological replicates; right panel: n = 4 biological replicates except *bsmt1*, *Pst* at 28 °C (n = 3 biological replicates)] from one representative experiment (of three independent experiments) analyzed with two-way ANOVA with Tukey’s HSD for significance. Results in (e) show the means ± S.D. [left panel: n = 4 biological replicates except Col-0, *Pst* at 23 °C (n = 3 biological replicates); right panel: n = 4 biological replicates] from one representative experiment (of three independent experiments) analyzed with two-way ANOVA with Tukey’s HSD for significance. Exact P-values for all comparisons are detailed in the Source Data files Source data

**Extended Data Fig. 10. Characterization of *35S::ICS1*, *35S::CBP60g* and *uORF-CBP60g* plants.**
a, Appearance of 6-week-old Col-0, *35S::ICS1*, *35S::CBP60g* and *uORFs-CBP60g* plants. b, Quantification of fresh weights of 6-week-old Col-0, *35S::ICS1*, *35S::CBP60g*. c, Flowering time phenotypes of Col-0 and *35S::CBP60g* plants. d, *CBP60g* transcript levels in 4-week old Col-0, and *35S::uORFs-CBP60g* plants measured by RT-qPCR. Results in (b) show the means ± S.D. [n = 15 (Col-0, *35S::CBP60g*), n = 16 (*35S::ICS1*) biological replicates] from one representative experiment (of two independent experiments) analyzed with one-way ANOVA with Bartlett’s test for significance. Results in (c) show the means ± S.D. (n = 4 biological replicates) from one representative experiment (of two independent experiments) with two-tailed Student’s t-test. Results in (d) show the means ± S.D. (n = 4 biological replicates of two independent experiments) analyzed with one-way ANOVA with Bartlett’s test for significance. Exact P-values for all comparisons are detailed in the Source Data files Source data

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References

1. Glazebrook J. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 2005;43:205–227. - PubMed
1. Fu ZQ, Dong X. Systemic acquired resistance: turning local infection into global defense. Annu. Rev. Plant Biol. 2013;64:839–863. - PubMed
1. Peng Y, Yang J, Li X, Zhang Y. Salicylic acid: biosynthesis and signaling. Annu. Rev. Plant Biol. 2021;72:761–791. - PubMed
1. Castroverde CDM, Dina D. Temperature regulation of plant hormone signaling during stress and development. J. Exp. Bot. 2021;72:7436–7458. - PubMed
1. Velásquez AC, Castroverde CDM, He SY. Plant–pathogen warfare under changing climate conditions. Curr. Biol. 2018;28:R619–R634. - PMC - PubMed

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[1] Glazebrook J. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 2005;43:205–227. - PubMed

[2] Glazebrook J. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 2005;43:205–227. - PubMed

[3] Fu ZQ, Dong X. Systemic acquired resistance: turning local infection into global defense. Annu. Rev. Plant Biol. 2013;64:839–863. - PubMed

[4] Fu ZQ, Dong X. Systemic acquired resistance: turning local infection into global defense. Annu. Rev. Plant Biol. 2013;64:839–863. - PubMed

[5] Peng Y, Yang J, Li X, Zhang Y. Salicylic acid: biosynthesis and signaling. Annu. Rev. Plant Biol. 2021;72:761–791. - PubMed

[6] Peng Y, Yang J, Li X, Zhang Y. Salicylic acid: biosynthesis and signaling. Annu. Rev. Plant Biol. 2021;72:761–791. - PubMed

[7] Castroverde CDM, Dina D. Temperature regulation of plant hormone signaling during stress and development. J. Exp. Bot. 2021;72:7436–7458. - PubMed

[8] Castroverde CDM, Dina D. Temperature regulation of plant hormone signaling during stress and development. J. Exp. Bot. 2021;72:7436–7458. - PubMed

[9] Velásquez AC, Castroverde CDM, He SY. Plant–pathogen warfare under changing climate conditions. Curr. Biol. 2018;28:R619–R634. - PMC - PubMed

[10] Velásquez AC, Castroverde CDM, He SY. Plant–pathogen warfare under changing climate conditions. Curr. Biol. 2018;28:R619–R634. - PMC - PubMed

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Increasing the resilience of plant immunity to a warming climate

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