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Science 333 (6042): 596-601

Copyright © 2011 by the American Association for the Advancement of Science

Independently Evolved Virulence Effectors Converge onto Hubs in a Plant Immune System Network

M. Shahid Mukhtar,1,*,{dagger} Anne-Ruxandra Carvunis,2,3,4,* Matija Dreze,2,3,5,* Petra Epple,1,* Jens Steinbrenner,6 Jonathan Moore,7 Murat Tasan,8 Mary Galli,9 Tong Hao,2,3 Marc T. Nishimura,1 Samuel J. Pevzner,2,3,10,11 Susan E. Donovan,6,{ddagger} Lila Ghamsari,2,3 Balaji Santhanam,2,3 Viviana Romero,2,3 Matthew M. Poulin,2,3 Fana Gebreab,2,3 Bryan J. Gutierrez,2,3 Stanley Tam,2,3 Dario Monachello,12 Mike Boxem,13 Christopher J. Harbort,1,§ Nathan McDonald,1 Lantian Gai,9 Huaming Chen,9 Yijian He,1 European Union Effectoromics Consortium, Jean Vandenhaute,5 Frederick P. Roth,2,14,|| David E. Hill,2,3 Joseph R. Ecker,9,15 Marc Vidal,2,3,¶ Jim Beynon,6,7,¶ Pascal Braun,2,3,¶ Jeffery L. Dangl1,16,17,18,¶

Abstract: Plants generate effective responses to infection by recognizing both conserved and variable pathogen-encoded molecules. Pathogens deploy virulence effector proteins into host cells, where they interact physically with host proteins to modulate defense. We generated an interaction network of plant-pathogen effectors from two pathogens spanning the eukaryote-eubacteria divergence, three classes of Arabidopsis immune system proteins, and ~8000 other Arabidopsis proteins. We noted convergence of effectors onto highly interconnected host proteins and indirect, rather than direct, connections between effectors and plant immune receptors. We demonstrated plant immune system functions for 15 of 17 tested host proteins that interact with effectors from both pathogens. Thus, pathogens from different kingdoms deploy independently evolved virulence proteins that interact with a limited set of highly connected cellular hubs to facilitate their diverse life-cycle strategies.

1 Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA.
2 Center for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana-Farber Cancer Institute, Boston, MA 02215, USA.
3 Department of Genetics, Harvard Medical School, Boston, MA 02115, USA.
4 Computational and Mathematical Biology Group, TIMC-IMAG, CNRS UMR5525 and Université de Grenoble, Faculté de Médecine, 38706 La Tronche cedex, France.
5 Unité de Recherche en Biologie Moléculaire, Facultés Universitaires Notre-Dame de la Paix, 5000 Namur, Wallonia-Brussels Federation, Belgium.
6 School of Life Sciences, University of Warwick, Wellesbourne, Warwick, CV35 9EF, UK.
7 Warwick Systems Biology Centre, Coventry House, University of Warwick, Coventry, CV4 7AL, UK.
8 Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA 02115, USA.
9 Genomic Analysis Laboratory, The Salk Institute for Biological Studies, La Jolla, CA 92037, USA.
10 Biomedical Engineering Department, Boston University, Boston, MA 02215, USA.
11 Boston University School of Medicine, Boston, MA 02118, USA.
12 Unité Mixte de Recherche en Génomique Végétale (URGV), UMR, Institut National de la Recherche Agronomique (INRA), Université d’Evry–Val d'Essonne—European Research Laboratory (UEVE–ERL), CNRS, 91057 Evry Cedex, France.
13 Utrecht University, 3584 CH Utrecht, Netherlands.
14 Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA 02115, USA.
15 Plant Biology Laboratory, Salk Institute for Biological Studies, La Jolla, CA 92037, USA.
16 Curriculum in Genetics and Molecular Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA.
17 Carolina Center for Genome Science, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA.
18 Department of Microbiology and Immunology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA.

* These authors contributed equally to this project.

{dagger} Present address: Department of Biology, CH106, University of Alabama at Birmingham, 1300 University Boulevard, Birmingham, AL 35294, USA.

{ddagger} Present address: ADAS Boxworth Research Centre, Boxworth, Cambridgeshire CB23 4NN, UK.

§ Present address: Max Planck Institute for Infection Biology, Chariteplatz 1, 10117 Berlin, Germany.

||Present address: Donnelly Centre for Cellular and Biomolecular Research, University of Toronto, Toronto, Ontario M5S3E1, Canada, and Samuel Lunenfeld Research Institute, Mt. Sinai Hospital, Toronto, Ontario M5G1X5, Canada.

To whom correspondence should be addressed. E-mails: dangl{at}email.unc.edu (J.L.D.); pascal_braun{at}dfci.harvard.edu (P.B.); jim.beynon{at}warwick.ac.uk (J.B.); marc_vidal{at}dfci.harvard.edu (M.V.)

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