Gregory Martin

Scientist, Boyce Schulze Downey Chair

Office/Lab: Room 327/326

Contact: gbm7@cornell.edu / 607-254-1208

Affiliations:

Professor in Cornell University’s Department of Plant Pathology and Plant-Microbe Biology

Graduate Field: Plant Pathology, Plant Biology

Curriculum Vitae (PDF; 368 KB)

Research Summary

The Martin laboratory studies the molecular basis of bacterial pathogenesis, plant disease susceptibility, and plant immunity. Most of our research focuses on bacterial speck disease which is caused by the infection of tomato leaves with the bacterial pathogen Pseudomonas syringae pv. tomato. This is an economically important disease that can decrease both the yield and quality of tomato fruits. It also serves as an excellent model system for understanding plant-pathogen biology because much is known about the molecular biology of this pathosystem and many genomics resources are available for both tomato and P. s. pv. tomato.

Symptoms of bacterial speck disease of tomato caused by the bacterial pathogen Pseudomonas syringae pv. tomato

In the tomato-Pseudomonas interaction, the virulence proteins AvrPto and AvrPtoB are delivered into the plant cell by the bacterial type III secretion system. Both proteins then act to suppress host basal defenses and thereby promote plant disease susceptibility. Some tomato genotypes express the Pto gene which encodes a protein kinase that detects the presence of AvrPto and AvrPtoB and confers resistance to bacterial speck disease. This resistance is activated by the physical interaction of the Pto kinase with AvrPto or AvrPtoB and also by the interaction of Pto with Prf, a protein containing a nucleotide-binding site and a region of leucine-rich repeats
(i.e., an NB-LRR protein).

This early recognition event activates a complex series of signaling events that leads ultimately to host defense responses, including transcriptional reprogramming and localized host cell death, that restrict growth of the pathogen. We have found recently that a C-terminal domain of AvrPtoB encodes an E3 ubiquitin ligase that, in certain tomato genotypes, can interfere with activation of this host resistance response. Thus, some bacterial virulence proteins appear to have evolved to suppress both basal and resistance-gene mediated host defenses and plants have, in turn, evolved to interfere with both of these activities.

To further understand the molecular basis of bacterial virulence, plant immunity, and susceptibility in this pathosystem we are using various experimental approaches including: genomics, biochemistry, cell biology, molecular biology, forward and reverse genetics, and structural biology. Our long term goal is to use the knowledge we gain about plant-pathogen interactions to engineer plants for increased resistance to diseases and thereby lessen the need for synthetic chemical inputs.

Publications

View Publications

Munkvold, K. and G. B. Martin. 2009. Advances in experimental methods for the elucidation of Pseudomonas syringae effector function with a focus on AvrPtoB. Molecular Plant Pathology, doi 10: 1111/j.1365-313X.2009.04028.x.
Chakravarthy, S., Velasquez, A.C., and Martin, G.B. 2009. Assay for pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI) in plants. Journal of Visualized Experiments 31: doi: 10.3791/1442
Dong, J., Xiao, F., Fan, F., Gu, L., Cang, H., Martin, G.B., and Chai, J. 2009. Crystal structure of the complex between Pseudomonas effector AvrPtoB and the tomato Pto kinase reveals both a shared and a unique interface compared with AvrPto-Pto. Plant Cell 21: 1846-1859
Kvitko, B. H., A. C. Velásquez, C.-F. Wei, A. B. Russell, G. B. Martin, D. J. Schneider and A. Collmer. 2009. Deletions in the repertoire of Pseudomonas syringae pv. tomato DC3000 type III secretion effector genes reveal functional overlap among effectors. PLoS Pathogens 5: e1000388
Yeam, I., Nguyen, H.P., and Martin, G.B. 2009. Phosphorylation of Pseudomonas syringae effector AvrPto is required for an FLS2/BAK1-independent virulence activity and recognition by tobacco. Plant Journal : in press
Velásquez A.C., Chakravarthy S., Martin G.B. 2009. Virus-induced gene silencing (VIGS) in Nicotiana benthamiana and tomato. Journal of Visualized Experiments 28: doi: 10.3791/1292
Kim, J.G., Li, X., Roden, J.A., Taylor, K.W., Aakre, C.D., Su, B., Lalonde, S., Kirik, A., Chen, Y., Baranage, G., McLane, H., Martin, G.B., and Mudgett, M.B. 2009. Xanthomonas type III secretion effector XopN suppresses PAMP-triggered immunity and interacts with a tomato atypical receptor-like kinase and TFT1. Plant Cell 21: 1305-1323
Almeida, N. F., S. Yan, M. Lindeberg, D. J. Studholme, D. J. Schneider, B. Condon, H. Liu, C. J. Viana, A. Warren, C. Evans, E. Kemen, D. MacLean, A. Angot, G. B. Martin, J. D. Jones, A. Collmer, J. C. Setubal and B. A. Vinatzer. 2008. A draft genome sequence of Pseudomonas syringae pv. tomato T1 reveals a type III effector repertoire significantly divergent from that of Pseudomonas syringae pv. tomato DC3000. Molecular Plant-Microbe Interactions 22: 52-62
Shan L., P. He, J. Li, A. Heese, S. Peck, T. Nürnberger, G. B. Martin and J. Sheen. 2008. Bacterial effectors target BAK1 to disrupt MAMP receptor signaling complexes and impede plant innate immunity. Cell Host-Microbe 4: 17-27
Martin, G. B. 2008. Use of tomato as a model system to understand the molecular basis of plant disease resistance. Report of the Tomato Genetics Cooperative 58: 6-10
Wei, C. F., B. H. Kvitko, R. Shimizu, E. Crabill, J. R. Alfano, N. C. Lin, G. B. Martin, H. C. Huang, A. Collmer. 2007. A Pseudomonas syringae pv. tomato DC3000 mutant lacking the type III effector HopQ1-1 is able to cause disease in the model plant Nicotiana benthamiana. Plant Journal 51: 32-46
Rosebrock, T. R., L. Zeng, J. J. Brady, R. B. Abramovitch, F. Xiao, and G. B. Martin. 2007. A bacterial E3 ubiquitin ligase targets a host protein kinase to disrupt plant immunity. Nature 448: 370-374
Moeder, W., O. del Pozo, D. A. Navarre, G. B. Martin and D. F. Klessig. 2007. Aconitase plays a role in regulating resistance to oxidative stress and cell death in Arabidopsis and Nicotiana benthamiana. Plant Molecular Biology 63: 273-287
Gabriels, S. H. E. J., J. H. Vossen, A. M. Abd-El-Haliem, G. C. M. van den Berg, S. K. Ekengren, G. B. Martin, P. J. G. M. de Wit and M. H. A. J. Joosten. 2007. An NB-LRR protein required for HR signaling mediated by both extra- and intracellular resistance proteins. Plant Journal 50: 14-28
Oh, C.-S., G. B. Martin, and S. V. Beer. 2007. DspA/E, a type III effector of Erwinia amylovora, is required for early rapid growth in Nicotiana benthamiana and causes NbSGT1-dependent cell death. Molecular Plant Pathology 8: 255-265
Anand, A. Z. , Vaghchhipawala, C.-M. Ryu, L. Kang, K. Wang, O. del-Pozo, G. B. Martin and K. S. Mysore. 2007. Identification of genes involved in Agrobacterium-mediated plant transformation by using virus-induced gene silencing as a functional genomics tool. Molecular Plant-Microbe Interactions. 20: 41-52
Xiao, F., P. Giavalisco, and G. B. Martin . 2007. Pseudomonas syringae type III effector AvrPtoB is phosphorylated in plant cells on serine 258 promoting its virulence activity. Journal of Biological Chemistry 282: 30737-30744
Lin, N.-C. and G. B. Martin, . 2007. Pto/Prf-mediated recognition of AvrPto and AvrPtoB restricts the ability of diverse Pseudomonas syringae pathovars to infect tomato. Molecular Plant-Microbe Interactions 20: 806-815
Xiao, F., P. He, R. B. Abramovitch, J. E. Dawson, L. K. Nicholson, J. Sheen, and G. B. Martin. 2007. The N-terminal region of Pseudomonas type III effector AvrPtoB elicits Pto-dependent immunity and has two distinct virulence determinants. Plant Journal 52: 595-614
Janjusevic, R., R. B. Abramovitch, G. B. Martin, C. E. Stebbins. 2006. A Bacterial Inhibitor of Host Programmed Cell Death Defenses Is an E3 Ubiquitin Ligase. Science 311(5758): 222-226
Devarenne, T. P., S. K. Ekengren, K. F. Pedley, G. B. Martin. 2006. Adi3 is a Pdk1-interacting AGC Kinase that Negatively Regulates Plant Cell Death. EMBO Journal 25: 255-265
Abramovitch, R. B., J. C. Anderson, G. B. Martin. 2006. Bacterial elicitation and evasion of plant innate immunity. Nature Reviews Molecular Cell Biology 7(8): 601-611
Lin, N. C., R. B. Abramovitch, Y. J. Kim, G. B. Martin. 2006. Diverse AvrPtoB Homologs from Several Pseudomonas syringae Pathovars Elicit Pto-Dependent Resistance and Have Similar Virulence Activities. Applied and Environmental Microbiology 72(1): 702-712
Anderson, J. C., P. E. Pascuzzi, F. Xiao, G. Sessa, G. B. Martin. 2006. Host-Mediated Phosphorylation of Type III Effector AvrPto Promotes Pseudomonas Virulence and Avirulence in Tomato. Plant Cell 18(2): 502-514
Abramovitch, R. B., R. Janjusevic, C. E. Stebbins, G. B. Martin. 2006. Type III Effector AvrPtoB Requires Intrinsic E3 Ubiquitin Ligase to Suppress Plant Cell Death and Immunity. Proceedings of the National Academy of Sciences, USA 103: 2851-2856
Cohn, J. R., G. B. Martin. 2005. Pseudomonas syringae pv. tomato Type III Effectors AvrPto and AvrPtoB Promote Ethylene-dependent Cell Death in Tomato. The Plant Journal 44(1): 139-154
Pedley, K. F., G. B. Martin. 2005. Role of Mitogen-activated Protein Kinases in Plant Immunity. Current Opinion in Plant Biology 8: 541-547
Alba, R., P. Payton, Z. Fei, R. McQuinn, P. Debbie, G. B. Martin, S. D. Tanksley, J. J. Giovannoni. 2005. Transcriptome and Selected Metabolite Analysis Reveal Multiple Points of Ethylene Control During Tomato Fruit Development. Plant Cell 17(11): 2954-2965
Burch-Smith, T. M., J. C. Anderson, G. B. Martin, S. P. Dinesh-Kumar. 2004. Applications and advantages of virus-induced gene silencing for gene function studies in plants. The Plant Journal 39(5): 734-746
del Pozo, O., K. F. Pedley, G. B. Martin. 2004. MAPKKKα is a Positive Regulator of Cell Death Associated with both Plant Immunity and Disease. EMBO Journal 23: 3072-3082
Abramovitch, R. B., Y. J. Kim, S. R. Chen, M. B. Dickman, G. B. Martin. 2003. Pseudomonas Type III Effector AvrPtoB Induces Plant Disease Susceptibility by Inhibition of Host Programmed Cell Death. EMBO Journal 22(1): 60-69
Pedley, K. F., G. B. Martin. 2003. Molecular Basis of Pto-mediated Resistance to Bacterial Speck Disease in Tomato. Annual Review of Phytopathology 41: 215-243
Martin, G. B., A. J. Bogdanove, G. Sessa. 2003. Understanding the Functions of Plant Disease Resistance Proteins. Annual Review of Plant Biology 54: 23-61
Mysore, K., O. Crasta, R. Tuori, O. Folkerts, P. Swirsky, G. B. Martin. 2002. Comprehensive transcript profiling of Pto-mediated disease resistance in tomato leaves reveals both Prf-dependent and -independent gene expression during Pseudomonas infection. The Plant Journal 32: 299-315
Kim, Y.-J., N.-C. Lin, G. B. Martin. 2002. Two highly distinct Pseudomonas effector proteins interact with the Pto kinase and activate plant immunity. Cell 109: 589-598
Riely, B., G. B. Martin. 2001. Ancient origin of pathogen recognition specificity conferred by the tomato disease resistance gene Pto. Proceedings of the National Academy of Sciences, USA 98: 2059-2064
Sessa, G., M. D’Ascenzo, G. B. Martin. 2000. Thr38 and Ser198 are Pto Autophosphorylation Sites Required for the AvrPto-Pto-mediated Hypersensitive Response. EMBO Journal 19(10): 2257-2269
Frederick, R., R. L. Thilmony, G. Sessa, G. B. Martin. 1998. Recognition Specificity for the Bacterial Avirulence Protein AvrPto is Determined by Thr-204 in the Activation Loop of the Tomato Pto Kinase. Molecular Cell 2(2): 241-245
Zhou, J., X. Tang, G. B. Martin. 1997. The Pto Kinase Conferring Resistance to Tomato Bacterial Speck Disease Interacts with Proteins that Bind a cis-element of Pathogenesis-related Genes. EMBO Journal 16: 3207-3218
Tang, X., R. Frederick, D. Halterman, J. Zhou, G. B. Martin. 1996. Initiation of Plant Disease Resistance by Physical Interaction of AvrPto and Pto Kinase. Science 274(5295): 2060-2063
Zhou, J., Y.-T. Loh, G. B. Martin. 1995. The Pto kinase conferring resistance to bacterial speck disease in tomato physically interacts with and phosphorylates a second kinase, Pti1. Cell 83: 925-935
Martin, G. B., S. H. Brommonschenkel, J. Chunwongse, A. Frary, M. W. Ganal, R. Spivey, T. Wu, E. D. Earle, S. D. Tanksley. 1993. Map-based Cloning of a Protein Kinase Gene Conferring Disease Resistance in Tomato. Science 262(5138): 1432-1436