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Molecular Biology of Plant-Pathogen Interactions

How microbial pathogens cause diseases in higher eukaryotes is a major unresolved question in biology.  Our research is focused on the interaction between Arabidopsis thaliana and Pseudomonas syringae. In this model interaction, both the host and the pathogen are genetically and genomically amenable, making it a fascinating system for dissecting the molecular details of bacterial virulence, host defense, and host-pathogen co-evolution. The ability of P. syringae to cause disease in susceptible plants or to elicit the hypersensitive response (HR, a rapid plant cell death response) in resistant plants is dependent on the bacterial type III secretion apparatus. Bacteria use this apparatus to inject a battery of virulence proteins (type III effector proteins) directly into the plant cell interior to affect plant physiology, leading to disease or triggering resistance.

Figure 1. Disease symptoms (necrotic lesions surrounded by chlorosis) caused by the phytobacterium Pseudomonas syringae pv. tomato (Pst) strain DC3000 on inoculated leaves of a susceptible Arabidopsis thaliana Col-0 plant. Green leaves were not inoculated. [Photo by R. Thilmony]

We are currently pursuing four lines of research: (1) We investigate host proteins and pathways targeted by P. syringae virulence proteins. (2) We study the role of stomate-based defense and counter-defense in host-P. syringae interactions. (3) We explore novel strategies to produce disease-resistant plants, based on our basic understanding of the Arabidopsis-P. syringae interaction. (4) We study the type III protein secretion apparatus. Our research is driven by scientific questions.   All available and proper technologies are used to solve specific questions. This lab provides a supportive environment for students and postdocs to gain experience in molecular biology, genetics, cell biology, and biochemistry, with a specialization in plant-microbe interactions.

Host targets of P. syringae type III effector proteins

What do P. syringae type III effector proteins do inside the Arabidopsis cell? What host proteins and pathways are targeted by these bacterial proteins?  Answering these questions is fundamental to our understanding of host-pathogen interactions.  This is an interesting new area in the field of molecular plant-pathogen inter­actions. Our recent studies suggest that a major function of P. syringae effector proteins is suppression of host innate immune response. Using transgenics, global gene profiling, protein structure, and yeast two-hybrid protein trap methods, we are elucidating the molecular mechanisms by which some of these effector proteins suppress host defense.

Stomate-based defense against bacterial invasion into host tissue

Biotechnology

Bacterial type III protein secretion mechanism

Selected Publications

Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling.  Nature 448:661-665 Abstract

Melotto M, Underwood W, Koczan J, Nomura K, He SY (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126:969-980. Abstract

Nomura K, DebRoy S, Lee YH, Pumplin N, Jones, He SY (2006) A bacterial virulence protein suppresses host innate immunity to cause plant disease. Science 313:220-223 Abstract

Thilmony R, Underwood W, He SY (2006) Genome-wide transcriptional analysis of the Arabidopsis thaliana interaction with the plant pathogen Pseudomonas syringae pv. tomato DC3000 and the human pathogen Escherichia coli O157:H7. Plant J 46:34-53 Abstract

Lee YH, Kolade OO, Nomura K, Arvidson, DN, He SY (2005) Use of dominant-negative HrpA mutants to dissect Hrp pilus assembly and type III secretion in Pseudomonas syringae pv. tomato. J Biol Chem 280:21409-21417 Abstract

Nomura K, He SY (2005) Powerful screens for bacterial virulence proteins. Proc Natl Acad Sci USA 102:3527-3528 Paper

DebRoy S, Thilmony R, Kwack YB, Nomura K, He SY (2004) A family of conserved bacterial effectors inhibits salicylic acid-mediated basal immunity and promotes disease necrosis in Arabidopsis. Proc Natl Acad Sci USA 101:9927-9932 Abstract

Hauck P, Thilmony R, He SY (2003) A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants. Proc Natl Acad Sci USA 100:8577-8582 Abstract

Kang L, Li J, Zhao T, Xiao F, Tang X, Thilmony R, He SY, Zhou JM (2003) Interplay of the Arabidopsis nonhost resistance gene NHO1 with bacterial virulence. Proc Natl Acad Sci USA 100:3519-24 Abstract

Jin Q.-L., He SY (2001) Role of the Hrp pilus in type III secretion in Pseudomonas syringae. Science 294: 2556-2558 Paper

Wei W, Plovanich-Jones A, Deng W-L, Jin, Q-L, Collmer A, Huang, H-C, He, SY (2000) The gene coding for the structural protein of the Hrp pilus is required for type III secretion of Hrp and Avr proteins in Pseudomonas syringae pv. tomato. Proc Natl Acad Sci USA 97:2247-2252 Abstract

Roine E, Wei W, Yuan J, Nurmiaho-Lassila E, Kalkkinen N, Romantschuk M, He SY (1997) Hrp pilus: An  hrp-dependent bacterial surface appendage produced by Pseudomonas syringae pv. tomato DC3000.  Proc Natl Acad Sci USA 94: 3459-3464 Paper

Gopalan S, Bauer D, Alfano J, Loniello A, He SY, Collmer A (1996) Expression of the Pseudomonas syringae avirulence protein AvrB in plant cells alleviates its dependence on the hypersensitive response and pathogenicity (Hrp) secretion system in eliciting genotype-specific hypersensitive cell death. Plant Cell 8: 1095-1105(Suresh Gopalan is from SYH’s lab) Abstract

He SY, Huang HC, Collmer A (1993) Pseudomonas syringae pv. syringae harpin_Pss: a protein that is secreted via the Hrp pathway and elicits the hypersensitive response in plants. Cell 73: 1255-1266 Abstract

Wei Z-M, Laby JR, Zumoff CH, Bauer DW, He SY, Collmer A, Beer SV (1992) Harpin, elicitor of the hypersensitive response produced by the plant pathogen Erwinia amylovora. Science 257: 85-88 Abstract

He SY, Lindeberg M, Chatterjee AK, Collmer A (1991) Cloned out genes from Erwinia chrysanthemi EC16 enable Escherichia coli strains to selectively secrete a diverse family of heterologous proteins to its milieu. Proc Natl Acad Sci USA 88: 1079-1083 Abstract

Selected Review Articles

Underwood W, Melotto M, He SY (2007) Role of plant stomata in bacterial invasion. Cell Microbiol 9:1621-1629 Abstract

Osbourn A, He SY (2006) Biotic interactions: Towards a unifying and balanced view. Curr Opin Plant Biol 9:347-350. Abstract

Nomura K, Melotto M, He SY (2005) Suppression of host defense in compatible plant-Pseudomonas syringae interactions. Curr Opin Plant Biol 8(4):361-368 Abstract

He SY Nomura K, Whittam T (2004) Type III secretion in mammalian and plant pathogens. Biochim Biophys Acta 1694:181-206 (a special review issue on protein secretion pathway in bacteria). Abstract

He SY, Jin Q (2003) The Hrp pilus: learning from flagella. Curr Opin Microbiol 6:15-19 Abstract

Jin Q-L, Thilmony R, Zwiesler-Vollick J, He SY (2003) Type III secretion in Pseudomonas syringae. Microbes Infect 5:301-310 Abstract

Katagiri F, Thilmony R, He SY (2002) The Arabidopsis thaliana-Pseudomonas syringae Interaction, The Arabidopsis Book, eds. C.R. Somerville and E.M. Meyerowitz, American Society of Plant Biologists, Rockville, MD, DOI 10.1199-tab.0039 Abstract

Patents

“Pseudomonas syringae pv. syringae HrpZ gene,” 1997, CRF D-1425, with Alan Collmer and Hsiou-chen Huang

“Elicitor of the hypersensitive response in plants,” 1998, CRF D-1172A, with Steve Beer et al.  This patent has led to the development of the disease control product “MESSENGER^TM” sold by Eden Bioscience Corp.

“Broad-spectrum disease resistance conferred by expression of the Pseudomonas syringae hrmA gene in plants,” 2001, US 6342654 B1, with Qing Shun Li, Songhai Shen and Arthur Hunt.

Teaching

He Lab Website