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Seminars in Cell & Developmental Biology 20 (2009) 1015–1016 Contents lists available at ScienceDirect Seminars in Cell & Developmental Biology journal homepage: www.elsevier.com/locate/semcdb Editorial Systems biology of plant–pathogen interactions Plant–pathogen interactions, besides their obvious importance for agriculture and economy, represent a very useful conceptual and experimental tool for dissection of many basic biological sys- tems of the host cells and organisms. For example, plant interactions with viruses and bacteria have been instrumental in studies of such diverse and fundamental cellular processes as cell–cell recogni- tion [1], intercellular transport [2–6], macromolecular transport across membranes [7,8], nuclear and intranuclear transport [6,9,10], chromatin targeting [11], DNA repair and integration [12,13], pro- grammed cell death [14,15], RNA silencing [14,16–18], and many more. This is possible mainly because pathogens most often insin- uate into and adapt the host cellular pathways for their own needs. This Special Edition presents eight reviews that focus on eight aspects of interactions between plant pathogens and different bio- logical systems of the host. Each article is contributed by leaders in their respective fields. We begin the issue with the story of how pathogens are specifically recognized by the plant resistance (R) system, with a focus on the nucleotide-binding domain leucine- rich repeat (NB-LRR) class of R proteins. Another plant innate system for recognition of the invading pathogen, termed pathogen- associated molecular pattern (PAMP)-triggered immunity (PTI), is reviewed next, focusing on pattern recognition receptors (PRRs) and illuminating similarities between plant and animal innate immune systems which most likely have arisen by converging evo- lution. The following review describes another major response system of the host, RNA silencing; a special emphasis is made on the strat- egy of plant viruses to disable this defense by producing their own factors that act as RNA silencing suppressors. The programmed cell death (PCD) system of plant cells and its involvement in the response to viral infection is discussed in the next article, that proposes that the PCD signals may originate from the chloroplast, which itself may be consumed by autophagy. The autophagosomal degradation story is followed by the article focusing on the major proteolytic degradation system of the cell, the ubiquitin/26S protea- some, and its involvement in interactions with diverse pathogens; an emphasis is made on how some pathogens can subvert this nor- mally defensive system to facilitate their infection. Taking aim at the host defenses is the subject of the next review article, which focuses on bacterial effector proteins that translocate into the host cell and suppress diverse host cellular systems. The issue closes with two articles that focus on plant cell walls and on intercellular connections, the plasmodesmata, that span cell walls and plasma membranes. The first review discusses the defen- sive aspect of the cell wall, describing how it represents not only a physical battier for invading pathogens, but also a sophisticated anti-pathogen system that deploys an array of inhibitors targeting cell wall-degrading enzymes secreted by the pathogen. The final manuscript of the issue focuses on plasmodesmata as gateways for viruses, allowing them to move between cells in circiumvention of the cell wall barriers; for this movement, plant viruses have evolved specialized cell-to-cell movement proteins (MPs), and this paper proposes a molecular mechanism by which MPs increase plasmod- esmal permeability and traffic, together with the viral genomes, between cells. We would like to thank all our colleagues who elected to share their knowledge and ideas in this Special Edition. We hope that the readers will find the reviews not only interesting, but also stimu- lating and useful for their own research in diverse areas of plant biology and microbiology. References [1] von Bodman SB, Bauer WD, Coplin DL. Quorum sensing in plant–pathogenic bacteria. Annu Rev Phytopathol 2003;41:455–82. [2] Hofmann C, Sambade A, Heinlein M. Plasmodesmata and intercellular transport of viral RNA. Biochem Soc Trans 2007;35:142–5. [3] Lucas WJ, Lee JY. Plasmodesmata as a supracellular control network in plants. Nat Rev Mol Cell Biol 2004;5:712–26. [4] Pennazio S, Roggero P, Conti M. Plasmodesmata and plant viruses. A centenary story. New Microbiol 1999;22:389–404. [5] Nelson RS, Citovsky V. Plant viruses: invaders of cells and pirates of cellular pathways. Plant Physiol 2005;138:1809–14. [6] Tzfira T, Rhee Y, Chen MH, Citovsky V. Nucleic acid transport in plant–microbe interactions: the molecules that walk through the walls. Annu Rev Microbiol 2000;54:187–219. [7] Christie PJ, Atmakuri K, Krishnamoorthy V, Jakubowski S, Cascales E. Biogene- sis, architecture, and function of bacterial type IV secretion systems. Annu Rev Microbiol 2005;59:451–85. [8] Backert S, Meyer TF. Type IV secretion systems and their effectors in bacterial pathogenesis. Curr Opin Microbiol 2006;9:207–17. [9] Krichevsky A, Kozlovsky SV, Gafni Y, Citovsky V. Nuclear import and export of plant viral proteins and genomes. Mol Plant Pathol 2006;7:131–46. [10] Tzfira T, Citovsky V. Partners-in-infection: host proteins involved in the transformation of plant cells by Agrobacterium. Trends Cell Biol 2002;12: 121–9. [11] Citovsky V, Kozlovsky SV, Lacroix B, Zaltsman A, Dafni M, Vyas S, et al. Biologi- cal systems of the host cell involved in Agrobacterium infection. Cell Microbiol 2007;9:9–20. [12] Tzfira T, Li J, Lacroix B, Citovsky V. Agrobacterium T-DNA integration: molecules and models. Trends Genet 2004;20:375–83. [13] Tinland B. The integration of T-DNA into plant genomes. Trends Plant Sci 1996;1:178–84. [14] Soosaar JL, Burch-Smith TM, Dinesh-Kumar SP. Mechanisms of plant resistance to viruses. Nat Rev Microbiol 2005;3:789–98. [15] Patel S, Caplan J, Dinesh-Kumar SP. Autophagy in the control of programmed cell death. Curr Opin Plant Biol 2006;9:391–6. [16] Voinnet O. RNA silencing as a plant immune system against viruses. Trends Genet 2001;17:449–59. [17] Eamens A, Wang MB, Smith NA, Waterhouse PM. RNA silencing in plants: yes- terday, today, and tomorrow. Plant Physiol 2008;147:456–68. [18] Voinnet O. Induction and suppression of RNA silencing: insights from viral infections. Nat Rev Genet 2005;6:206–20. 1084-9521/$ – see front matter © 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.semcdb.2009.05.011

Systems biology of plant–pathogen interactions

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Page 1: Systems biology of plant–pathogen interactions

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Seminars in Cell & Developmental Biology 20 (2009) 1015–1016

Contents lists available at ScienceDirect

Seminars in Cell & Developmental Biology

journa l homepage: www.e lsev ier .com/ locate /semcdb

ditorial

ystems biology of plant–pathogen interactions

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[15] Patel S, Caplan J, Dinesh-Kumar SP. Autophagy in the control of programmedcell death. Curr Opin Plant Biol 2006;9:391–6.

Plant–pathogen interactions, besides their obvious importanceor agriculture and economy, represent a very useful conceptualnd experimental tool for dissection of many basic biological sys-ems of the host cells and organisms. For example, plant interactionsith viruses and bacteria have been instrumental in studies of such

iverse and fundamental cellular processes as cell–cell recogni-ion [1], intercellular transport [2–6], macromolecular transportcross membranes [7,8], nuclear and intranuclear transport [6,9,10],hromatin targeting [11], DNA repair and integration [12,13], pro-rammed cell death [14,15], RNA silencing [14,16–18], and manyore. This is possible mainly because pathogens most often insin-

ate into and adapt the host cellular pathways for their own needs.his Special Edition presents eight reviews that focus on eightspects of interactions between plant pathogens and different bio-ogical systems of the host. Each article is contributed by leadersn their respective fields. We begin the issue with the story of howathogens are specifically recognized by the plant resistance (R)ystem, with a focus on the nucleotide-binding domain leucine-ich repeat (NB-LRR) class of R proteins. Another plant innateystem for recognition of the invading pathogen, termed pathogen-ssociated molecular pattern (PAMP)-triggered immunity (PTI), iseviewed next, focusing on pattern recognition receptors (PRRs)nd illuminating similarities between plant and animal innatemmune systems which most likely have arisen by converging evo-ution.

The following review describes another major response systemf the host, RNA silencing; a special emphasis is made on the strat-gy of plant viruses to disable this defense by producing their ownactors that act as RNA silencing suppressors. The programmedell death (PCD) system of plant cells and its involvement in theesponse to viral infection is discussed in the next article, thatroposes that the PCD signals may originate from the chloroplast,hich itself may be consumed by autophagy. The autophagosomal

egradation story is followed by the article focusing on the majorroteolytic degradation system of the cell, the ubiquitin/26S protea-ome, and its involvement in interactions with diverse pathogens;n emphasis is made on how some pathogens can subvert this nor-ally defensive system to facilitate their infection. Taking aim at

he host defenses is the subject of the next review article, whichocuses on bacterial effector proteins that translocate into the hostell and suppress diverse host cellular systems.

The issue closes with two articles that focus on plant cell walls

nd on intercellular connections, the plasmodesmata, that span cellalls and plasma membranes. The first review discusses the defen-

ive aspect of the cell wall, describing how it represents not onlyphysical battier for invading pathogens, but also a sophisticated

nti-pathogen system that deploys an array of inhibitors targeting

[

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084-9521/$ – see front matter © 2009 Elsevier Ltd. All rights reserved.oi:10.1016/j.semcdb.2009.05.011

cell wall-degrading enzymes secreted by the pathogen. The finalmanuscript of the issue focuses on plasmodesmata as gateways forviruses, allowing them to move between cells in circiumvention ofthe cell wall barriers; for this movement, plant viruses have evolvedspecialized cell-to-cell movement proteins (MPs), and this paperproposes a molecular mechanism by which MPs increase plasmod-esmal permeability and traffic, together with the viral genomes,between cells.

We would like to thank all our colleagues who elected to sharetheir knowledge and ideas in this Special Edition. We hope that thereaders will find the reviews not only interesting, but also stimu-lating and useful for their own research in diverse areas of plantbiology and microbiology.

References

[1] von Bodman SB, Bauer WD, Coplin DL. Quorum sensing in plant–pathogenicbacteria. Annu Rev Phytopathol 2003;41:455–82.

[2] Hofmann C, Sambade A, Heinlein M. Plasmodesmata and intercellular transportof viral RNA. Biochem Soc Trans 2007;35:142–5.

[3] Lucas WJ, Lee JY. Plasmodesmata as a supracellular control network in plants.Nat Rev Mol Cell Biol 2004;5:712–26.

[4] Pennazio S, Roggero P, Conti M. Plasmodesmata and plant viruses. A centenarystory. New Microbiol 1999;22:389–404.

[5] Nelson RS, Citovsky V. Plant viruses: invaders of cells and pirates of cellularpathways. Plant Physiol 2005;138:1809–14.

[6] Tzfira T, Rhee Y, Chen MH, Citovsky V. Nucleic acid transport in plant–microbeinteractions: the molecules that walk through the walls. Annu Rev Microbiol2000;54:187–219.

[7] Christie PJ, Atmakuri K, Krishnamoorthy V, Jakubowski S, Cascales E. Biogene-sis, architecture, and function of bacterial type IV secretion systems. Annu RevMicrobiol 2005;59:451–85.

[8] Backert S, Meyer TF. Type IV secretion systems and their effectors in bacterialpathogenesis. Curr Opin Microbiol 2006;9:207–17.

[9] Krichevsky A, Kozlovsky SV, Gafni Y, Citovsky V. Nuclear import and export ofplant viral proteins and genomes. Mol Plant Pathol 2006;7:131–46.

10] Tzfira T, Citovsky V. Partners-in-infection: host proteins involved in thetransformation of plant cells by Agrobacterium. Trends Cell Biol 2002;12:121–9.

11] Citovsky V, Kozlovsky SV, Lacroix B, Zaltsman A, Dafni M, Vyas S, et al. Biologi-cal systems of the host cell involved in Agrobacterium infection. Cell Microbiol2007;9:9–20.

12] Tzfira T, Li J, Lacroix B, Citovsky V. Agrobacterium T-DNA integration: moleculesand models. Trends Genet 2004;20:375–83.

13] Tinland B. The integration of T-DNA into plant genomes. Trends Plant Sci1996;1:178–84.

14] Soosaar JL, Burch-Smith TM, Dinesh-Kumar SP. Mechanisms of plant resistanceto viruses. Nat Rev Microbiol 2005;3:789–98.

16] Voinnet O. RNA silencing as a plant immune system against viruses. TrendsGenet 2001;17:449–59.

17] Eamens A, Wang MB, Smith NA, Waterhouse PM. RNA silencing in plants: yes-terday, today, and tomorrow. Plant Physiol 2008;147:456–68.

18] Voinnet O. Induction and suppression of RNA silencing: insights from viralinfections. Nat Rev Genet 2005;6:206–20.

Page 2: Systems biology of plant–pathogen interactions

1 lopme

fax: +1 631 632 8575.E-mail address: [email protected]

(V. Citovsky)

016 Editorial / Seminars in Cell & Deve

Tzvi TzfiraDepartment of Molecular, Cellular and

Developmental Biology, The University of Michigan,Ann Arbor, MI 48109, United States

Vitaly Citovsky ∗

Department of Biochemistry and Cell Biology, StateUniversity of New York, Stony Brook,

NY 11794-5215, United States

ntal Biology 20 (2009) 1015–1016

∗ Corresponding author. Tel.: +1 631 632 9534;

Available online 6 June 2009