Next-generation Systemic Acquired Resistance

Overview

Journal Plant Physiol

Specialty Physiology

Date 2011 Dec 8

PMID 22147520

Citations 234

Authors

Estrella Luna

Toby J A Bruce

Michael R Roberts

Victor Flors

Jurriaan Ton

Affiliations

Soon will be listed here.

Abstract

Systemic acquired resistance (SAR) is a plant immune response to pathogen attack. Recent evidence suggests that plant immunity involves regulation by chromatin remodeling and DNA methylation. We investigated whether SAR can be inherited epigenetically following disease pressure by Pseudomonas syringae pv tomato DC3000 (PstDC3000). Compared to progeny from control-treated Arabidopsis (Arabidopsis thaliana; C(1)), progeny from PstDC3000-inoculated Arabidopsis (P(1)) were primed to activate salicylic acid (SA)-inducible defense genes and were more resistant to the (hemi)biotrophic pathogens Hyaloperonospora arabidopsidis and PstDC3000. This transgenerational SAR was sustained over one stress-free generation, indicating an epigenetic basis of the phenomenon. Furthermore, P(1) progeny displayed reduced responsiveness of jasmonic acid (JA)-inducible genes and enhanced susceptibility to the necrotrophic fungus Alternaria brassicicola. This shift in SA- and JA-dependent gene responsiveness was not associated with changes in corresponding hormone levels. Instead, chromatin immunoprecipitation analyses revealed that SA-inducible promoters of PATHOGENESIS-RELATED GENE1, WRKY6, and WRKY53 in P(1) plants are enriched with acetylated histone H3 at lysine 9, a chromatin mark associated with a permissive state of transcription. Conversely, the JA-inducible promoter of PLANT DEFENSIN1.2 showed increased H3 triple methylation at lysine 27, a mark related to repressed gene transcription. P(1) progeny from the defense regulatory mutant non expressor of PR1 (npr1)-1 failed to develop transgenerational defense phenotypes, demonstrating a critical role for NPR1 in expression of transgenerational SAR. Furthermore, the drm1drm2cmt3 mutant that is affected in non-CpG DNA methylation mimicked the transgenerational SAR phenotype. Since PstDC3000 induces DNA hypomethylation in Arabidopsis, our results suggest that transgenerational SAR is transmitted by hypomethylated genes that direct priming of SA-dependent defenses in the following generations.

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References

Cedar H, Bergman Y . Linking DNA methylation and histone modification: patterns and paradigms. Nat Rev Genet. 2009; 10(5):295-304. DOI: 10.1038/nrg2540. View

Chanda B, Xia Y, Mandal M, Yu K, Sekine K, Gao Q . Glycerol-3-phosphate is a critical mobile inducer of systemic immunity in plants. Nat Genet. 2011; 43(5):421-7. DOI: 10.1038/ng.798. View

Liu P, von Dahl C, Park S, Klessig D . Interconnection between methyl salicylate and lipid-based long-distance signaling during the development of systemic acquired resistance in Arabidopsis and tobacco. Plant Physiol. 2011; 155(4):1762-8. PMC: 3091099. DOI: 10.1104/pp.110.171694. View

Czechowski T, Bari R, Stitt M, Scheible W, Udvardi M . Real-time RT-PCR profiling of over 1400 Arabidopsis transcription factors: unprecedented sensitivity reveals novel root- and shoot-specific genes. Plant J. 2004; 38(2):366-79. DOI: 10.1111/j.1365-313X.2004.02051.x. View

Vlot A, Klessig D, Park S . Systemic acquired resistance: the elusive signal(s). Curr Opin Plant Biol. 2008; 11(4):436-42. DOI: 10.1016/j.pbi.2008.05.003. View

Kalisz S, Purugganan M . Epialleles via DNA methylation: consequences for plant evolution. Trends Ecol Evol. 2006; 19(6):309-14. DOI: 10.1016/j.tree.2004.03.034. View

Vaucheret H . Post-transcriptional small RNA pathways in plants: mechanisms and regulations. Genes Dev. 2006; 20(7):759-71. DOI: 10.1101/gad.1410506. View

March-Diaz R, Garcia-Dominguez M, Lozano-Juste J, Leon J, Florencio F, Reyes J . Histone H2A.Z and homologues of components of the SWR1 complex are required to control immunity in Arabidopsis. Plant J. 2007; 53(3):475-87. DOI: 10.1111/j.1365-313X.2007.03361.x. View

Liu P, von Dahl C, Klessig D . The extent to which methyl salicylate is required for signaling systemic acquired resistance is dependent on exposure to light after infection. Plant Physiol. 2011; 157(4):2216-26. PMC: 3327180. DOI: 10.1104/pp.111.187773. View

10.

van den Burg H, Takken F . Does chromatin remodeling mark systemic acquired resistance?. Trends Plant Sci. 2009; 14(5):286-94. DOI: 10.1016/j.tplants.2009.02.003. View

11.

Yi H, Richards E . Gene duplication and hypermutation of the pathogen Resistance gene SNC1 in the Arabidopsis bal variant. Genetics. 2009; 183(4):1227-34. PMC: 2787416. DOI: 10.1534/genetics.109.105569. View

12.

Stokes T, Kunkel B, Richards E . Epigenetic variation in Arabidopsis disease resistance. Genes Dev. 2002; 16(2):171-82. PMC: 155322. DOI: 10.1101/gad.952102. View

13.

Zhang X, Clarenz O, Cokus S, Bernatavichute Y, Pellegrini M, Goodrich J . Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis. PLoS Biol. 2007; 5(5):e129. PMC: 1852588. DOI: 10.1371/journal.pbio.0050129. View

14.

Attaran E, Zeier T, Griebel T, Zeier J . Methyl salicylate production and jasmonate signaling are not essential for systemic acquired resistance in Arabidopsis. Plant Cell. 2009; 21(3):954-71. PMC: 2671706. DOI: 10.1105/tpc.108.063164. View

15.

Spoel S, Johnson J, Dong X . Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proc Natl Acad Sci U S A. 2007; 104(47):18842-7. PMC: 2141864. DOI: 10.1073/pnas.0708139104. View

16.

Truman W, Bennett M, Turnbull C, Grant M . Arabidopsis auxin mutants are compromised in systemic acquired resistance and exhibit aberrant accumulation of various indolic compounds. Plant Physiol. 2010; 152(3):1562-73. PMC: 2832264. DOI: 10.1104/pp.109.152173. View

17.

Ahmad S, Gordon-Weeks R, Pickett J, Ton J . Natural variation in priming of basal resistance: from evolutionary origin to agricultural exploitation. Mol Plant Pathol. 2010; 11(6):817-27. PMC: 6640509. DOI: 10.1111/j.1364-3703.2010.00645.x. View

18.

Koornneef A, Rindermann K, Gatz C, Pieterse C . Histone modifications do not play a major role in salicylate-mediated suppression of jasmonate-induced PDF1.2 gene expression. Commun Integr Biol. 2009; 1(2):143-5. PMC: 2686002. DOI: 10.4161/cib.1.2.6997. View

19.

Haring M, Offermann S, Danker T, Horst I, Peterhansel C, Stam M . Chromatin immunoprecipitation: optimization, quantitative analysis and data normalization. Plant Methods. 2007; 3:11. PMC: 2077865. DOI: 10.1186/1746-4811-3-11. View

20.

Li J, Brader G, Kariola T, Palva E . WRKY70 modulates the selection of signaling pathways in plant defense. Plant J. 2006; 46(3):477-91. DOI: 10.1111/j.1365-313X.2006.02712.x. View