A Regulon Conserved in Monocot and Dicot Plants Defines a Functional Module in Antifungal Plant Immunity

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2010 Nov 25

PMID 21098265

Citations 52

Authors

Matt Humphry

Pawel Bednarek

Birgit Kemmerling

Serry Koh

Monica Stein

Ulrike Gobel

Kurt Stuber

Mariola Pislewska-Bednarek

Ann Loraine

Paul Schulze-Lefert

Shauna Somerville

Ralph Panstruga

Affiliations

Soon will be listed here.

Abstract

At least two components that modulate plant resistance against the fungal powdery mildew disease are ancient and have been conserved since the time of the monocot-dicot split (≈ 200 Mya). These components are the seven transmembrane domain containing MLO/MLO2 protein and the syntaxin ROR2/PEN1, which act antagonistically and have been identified in the monocot barley (Hordeum vulgare) and the dicot Arabidopsis thaliana, respectively. Additionally, syntaxin-interacting N-ethylmaleimide sensitive factor adaptor protein receptor proteins (VAMP721/722 and SNAP33/34) as well as a myrosinase (PEN2) and an ABC transporter (PEN3) contribute to antifungal resistance in both barley and/or Arabidopsis. Here, we show that these genetically defined defense components share a similar set of coexpressed genes in the two plant species, comprising a statistically significant overrepresentation of gene products involved in regulation of transcription, posttranslational modification, and signaling. Most of the coexpressed Arabidopsis genes possess a common cis-regulatory element that may dictate their coordinated expression. We exploited gene coexpression to uncover numerous components in Arabidopsis involved in antifungal defense. Together, our data provide evidence for an evolutionarily conserved regulon composed of core components and clade/species-specific innovations that functions as a module in plant innate immunity.

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References

Luo F, Yang Y, Chen C, Chang R, Zhou J, Scheuermann R . Modular organization of protein interaction networks. Bioinformatics. 2006; 23(2):207-14. DOI: 10.1093/bioinformatics/btl562. View

Douchkov D, Nowara D, Zierold U, Schweizer P . A high-throughput gene-silencing system for the functional assessment of defense-related genes in barley epidermal cells. Mol Plant Microbe Interact. 2005; 18(8):755-61. DOI: 10.1094/MPMI-18-0755. View

Yun B, Atkinson H, Gaborit C, Greenland A, Read N, Pallas J . Loss of actin cytoskeletal function and EDS1 activity, in combination, severely compromises non-host resistance in Arabidopsis against wheat powdery mildew. Plant J. 2003; 34(6):768-77. DOI: 10.1046/j.1365-313x.2003.01773.x. View

Krattinger S, Lagudah E, Spielmeyer W, Singh R, Huerta-Espino J, McFadden H . A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science. 2009; 323(5919):1360-3. DOI: 10.1126/science.1166453. View

Wang D, Weaver N, Kesarwani M, Dong X . Induction of protein secretory pathway is required for systemic acquired resistance. Science. 2005; 308(5724):1036-40. DOI: 10.1126/science.1108791. View

Gigolashvili T, Berger B, Mock H, Muller C, Weisshaar B, Flugge U . The transcription factor HIG1/MYB51 regulates indolic glucosinolate biosynthesis in Arabidopsis thaliana. Plant J. 2007; 50(5):886-901. DOI: 10.1111/j.1365-313X.2007.03099.x. View

Wei H, Persson S, Mehta T, Srinivasasainagendra V, Chen L, Page G . Transcriptional coordination of the metabolic network in Arabidopsis. Plant Physiol. 2006; 142(2):762-74. PMC: 1586052. DOI: 10.1104/pp.106.080358. View

Kumar J, Huckelhoven R, Beckhove U, Nagarajan S, Kogel K . A Compromised Mlo Pathway Affects the Response of Barley to the Necrotrophic Fungus Bipolaris sorokiniana (Teleomorph: Cochliobolus sativus) and Its Toxins. Phytopathology. 2008; 91(2):127-33. DOI: 10.1094/PHYTO.2001.91.2.127. View

Bednarek P, Pislewska-Bednarek M, Svatos A, Schneider B, Doubsky J, Mansurova M . A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science. 2008; 323(5910):101-6. DOI: 10.1126/science.1163732. View

10.

Xu J, Li Y, Wang Y, Liu H, Lei L, Yang H . Activation of MAPK kinase 9 induces ethylene and camalexin biosynthesis and enhances sensitivity to salt stress in Arabidopsis. J Biol Chem. 2008; 283(40):26996-7006. DOI: 10.1074/jbc.M801392200. View

11.

Srinivasasainagendra V, Page G, Mehta T, Coulibaly I, Loraine A . CressExpress: a tool for large-scale mining of expression data from Arabidopsis. Plant Physiol. 2008; 147(3):1004-16. PMC: 2442548. DOI: 10.1104/pp.107.115535. View

12.

Ehlting J, Provart N, Werck-Reichhart D . Functional annotation of the Arabidopsis P450 superfamily based on large-scale co-expression analysis. Biochem Soc Trans. 2006; 34(Pt 6):1192-8. DOI: 10.1042/BST0341192. View

13.

Persson S, Wei H, Milne J, Page G, Somerville C . Identification of genes required for cellulose synthesis by regression analysis of public microarray data sets. Proc Natl Acad Sci U S A. 2005; 102(24):8633-8. PMC: 1142401. DOI: 10.1073/pnas.0503392102. View

14.

Heath M . Nonhost resistance and nonspecific plant defenses. Curr Opin Plant Biol. 2000; 3(4):315-9. DOI: 10.1016/s1369-5266(00)00087-x. View

15.

Bergmann S, Ihmels J, Barkai N . Similarities and differences in genome-wide expression data of six organisms. PLoS Biol. 2004; 2(1):E9. PMC: 300882. DOI: 10.1371/journal.pbio.0020009. View

16.

Aoki K, Ogata Y, Shibata D . Approaches for extracting practical information from gene co-expression networks in plant biology. Plant Cell Physiol. 2007; 48(3):381-90. DOI: 10.1093/pcp/pcm013. View

17.

Bak S, Tax F, Feldmann K, Galbraith D, Feyereisen R . CYP83B1, a cytochrome P450 at the metabolic branch point in auxin and indole glucosinolate biosynthesis in Arabidopsis. Plant Cell. 2001; 13(1):101-11. PMC: 102201. DOI: 10.1105/tpc.13.1.101. View

18.

Consonni C, Humphry M, Hartmann H, Livaja M, Durner J, Westphal L . Conserved requirement for a plant host cell protein in powdery mildew pathogenesis. Nat Genet. 2006; 38(6):716-20. DOI: 10.1038/ng1806. View

19.

Hirai M, Sugiyama K, Sawada Y, Tohge T, Obayashi T, Suzuki A . Omics-based identification of Arabidopsis Myb transcription factors regulating aliphatic glucosinolate biosynthesis. Proc Natl Acad Sci U S A. 2007; 104(15):6478-83. PMC: 1849962. DOI: 10.1073/pnas.0611629104. View

20.

Collins N, Thordal-Christensen H, Lipka V, Bau S, Kombrink E, Qiu J . SNARE-protein-mediated disease resistance at the plant cell wall. Nature. 2003; 425(6961):973-7. DOI: 10.1038/nature02076. View