Boyce Thompson Institute for Plant Research
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Gregory Martin

Gregory Martin
Gregory Martin
Professor
Office/Lab: 327/326
gbm7@cornell.edu
Office: 607-254-1208
Lab: 607-220-9610

Curriculum Vitae
Google Scholar
ResearchID
ORCID #0000-0003-0044-
6830

Research Summary

Research Summary

How do bacteria infect plants and how do plants defend themselves from such attacks?

The Martin laboratory studies the molecular basis of bacterial infection processes and the plant immune system. The research focuses on 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 system for studying the mechanisms that underlie plant-pathogen interactions and how they have evolved. Many experimental resources including an increasing number of genome sequences are available for both tomato and P. s. pv. tomato. Current work relies on diverse experimental approaches involving methods derived from the fields of biochemistry, bioinformatics, cell biology, forward and reverse genetics, genomics, molecular biology, plant breeding, plant pathology, and structural biology.

Gregory Martin

In the tomato-Pseudomonas interaction, the plant responds rapidly to a potential infection by detecting certain conserved molecules expressed by the pathogen. At this stage the pathogen uses a specialized secretion system to deliver virulence proteins, such as AvrPto and AvrPtoB, into the plant cell. These proteins suppress early host defenses and thereby promote disease susceptibility. Some tomato varieties express a resistance gene, Pto, which encodes a protein that detects the presence of AvrPto or AvrPtoB and activates a second strong immune system that halts the progression of bacterial speck disease.

The Martin lab is currently studying many aspects of the molecular mechanisms that underlie the bacterial infection process and the plant response to infection. One project takes advantage of the genetic natural variation present in wild relatives of tomato to identify new genes that contribute to plant immunity. These genes provide insights into the plant immune system and also can be bred into new tomato varieties to enhance disease resistance. A second project relies on next-generation sequencing methods to identify tomato genes whose expression increases during the interaction with P. s. pv. tomato. The expression of these genes is then reduced by using virus-induced gene silencing to test whether they make a demonstrable contribution to immunity. A third project uses photo-crosslinking and other novel biochemical methods to isolate plant proteins that play a direct role in recognizing the conserved bacterial molecules that activate the early plant immune system.

The long-term goal in this research is to use the knowledge gained about the molecular basis of plant-pathogen interactions to develop plants with increased natural resistance to diseases. Such plants would require fewer applications of pesticides producing economic and environmental benefits while providing food for consumers with less pesticide residue.

Selected Publications

Selected Publications

All papers on PubMed

Bombarely, A., Rosli, H.G., Vrebalov, J., Moffett, P., Mueller, L.A. and Martin, G.B. 2012. A draft genome sequence of Nicotiana benthamiana to enhance molecular plant-microbe biology research. Molecular plant-microbe interactions 25: 1523-1530

Avila, J., Gregory, O.G., Su, D.Y., Deeter, T.A., Chen, S.X., Silva-Sanchez, C., Xu, S.L., Martin, G.B. and Devarenne, T.P. 2012. The beta-subunit of the SnRK1 complex is phosphorylated by the plant cell death suppressor Adi3. Plant Physiology 159: 1277-1290

Du, X.R., Miao, M., Ma, X.R., Liu, Y.S., Kuhl, J.C., Martin, G.B. and Xiao, F.M.. 2012. Plant programmed cell death caused by an autoactive form of Prf is suppressed by co-expression of the Prf LRR domain.. Molecular Plant 5: 1058-1067

Lee, J., Teitzel, G.M., Munkvold, K., del Pozo, O., Martin, G.B., Michelmore, R.W. and Greenberg, J.T. 2012. Type III secretion and effectors shape the survival and growth pattern of Pseudomonas syringae on leaf surfaces. Plant Physiology 158: 1803-1818

Martin, G. 2012. Suppression and Activation of the Plant Immune System by Pseudomonas syringae Effectors AvrPto and AvrPtoB. In Effectors in Plant-Microbe Interactions: Wiley-Blackwell 0: pp. 121-154

Velsquez, A.C. and Martin, G.B. 2012. Molecular Mechanisms Involved in the Interaction Between Tomato and Pseudomonas syringae pv. tomato. In Molecular Plant Immunity: Wiley-Blackwell 0: pp. 187-209

Zeng, L., Velasquez, A.C., Munkvold, K.R., Zhang, J. and Martin, G.B. 2012. A tomato LysM receptor-like kinase promotes immunity and its kinase activity is inhibited by AvrPtoB. The Plant journal : for cell and molecular biology 69: 92-103

Zeng L., A. C. Velasquez, K. R. Munkvold, J. Zhang, and G. B. Martin. 2011. A tomato LysM receptor-like kinase promotes immunity and its kinase activity is inhibited by AvrPtoB. Plant Journal 69: 92-103
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Oh, C.S. and Martin, G.B. 2011. Tomato 14-3-3 protein TFT7 interacts with a MAP kinase kinase to regulate immunity-associated programmed cell death mediated by diverse disease resistance proteins. J Biol Chem 286: 14129-14136
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Oh, C.S. and Martin, G.B. 2011. Effector-triggered immunity mediated by the Pto kinase. Trends Plant Sci 16: 132-140
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Cunnac, S., Chakravarthy, S., Kvitko, B.H., Russell, A.B., Martin, G.B. and Collmer, A. 2011. Genetic disassembly and combinatorial reassembly identify a minimal functional repertoire of type III effectors in Pseudomonas syringae. Proc Natl Acad Sci U S A 108: 2975-2980
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Cheng, W., Munkvold, K.R., Gao, H., Mathieu, J., Schwizer, S., Wang, S., Yan, Y.B., Wang, J., Martin, G.B. and Chai, J. 2011. Structural analysis of Pseudomonas syringae AvrPtoB bound to host BAK1 reveals two similar kinase-interacting domains in a type III effector. Cell Host Microbe 10: 616-626
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Nguyen, H.P., Yeam, I., Angot, A. and Martin, G.B. 2010. Two virulence determinants of type III effector AvrPto are functionally conserved in diverse Pseudomonas syringae pathovars. New Phytol 187: 969-982
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Nguyen, H.P., Chakravarthy, S., Velasquez, A.C., McLane, H.L., Zeng, L., Nakayashiki, H., Park, D.H., Collmer, A. and Martin, G.B. 2010. Methods to study PAMP-triggered immunity using tomato and Nicotiana benthamiana. Mol Plant Microbe Interact 23: 991-999
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Kang, H.G., Oh, C.S., Sato, M., Katagiri, F., Glazebrook, J., Takahashi, H., Kachroo, P., Martin, G.B. and Klessig, D.F. 2010. Endosome-associated CRT1 functions early in resistance gene-mediated defense signaling in Arabidopsis and tobacco. Plant Cell 22: 918-936

Chakravarthy, S., Velasquez, A.C., Ekengren, S.K., Collmer, A. and Martin, G.B. 2010. Identification of Nicotiana benthamiana genes involved in pathogen-associated molecular pattern-triggered immunity. Mol Plant Microbe Interact 23: 715-726
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Kelley, B.S., Lee, S.J., Damasceno, C.M.B., Chakravarthy, S., Kim, B.D., Martin, G.B. and Rose, J.K.C. 2010. A secreted effector protein (SNE1) from Phytophthora infestans is a broadly acting suppressor of programmed cell death. Plant Journal 62: 357-366
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Oh, C.S., Pedley , K.F. and Martin, G.B. 2010. Tomato 14-3-3 protein 7 positively regulates immunity-associated programmed cell death by enhancing protein abundance and signaling ability of MAPKKK {alpha}. Plant Cell 22: 260-272
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Yeam, I., Nguyen, H.P. and Martin, G.B. 2010. Phosphorylation of the Pseudomonas syringae effector AvrPto is required for FLS2/BAK1-independent virulence activity and recognition by tobacco. Plant Journal 61: 16-24
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Velasquez, A.C., Chakravarthy, S. and Martin, G.B. 2009. Virus-induced gene silencing (VIGS) in Nicotiana benthamiana and tomato. J Vis Exp 0:
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Chakravarthy, S., Velasquez, A.C. and Martin, G.B. 2009. Assay for pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI) in plants. J Vis Exp 0:
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Kvitko, B.H., Park, D.H., Velasquez, A.C., Wei, C.F., Russell, A.B., Martin, G.B., Schneider, D.J. and Collmer, A. 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
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Dong, J., Xiao, F.M., Fan, F.X., Gu, L.C., Cang, H.X., Martin, G.B. and Chai, J.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
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Shan, L.B., He, P., Li, J.M., Heese, A., Peck, S.C., Nurnberger, T., Martin, G.B. and Sheen, J. 2008. Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity. Cell Host & Microbe 4: 17-27
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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
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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: 222-226
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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: 502-514
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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
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Abramovitch, R. B., J. C. Anderson, G. B. Martin. 2006. Bacterial elicitation and evasion of plant innate immunity. Nature Reviews Molecular Cell Biology 7: 601-611
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He, P., L. Shan, N.-C. Lin, G. B. Martin, B. Kemmerling, T. Nurnberger, J. Sheen. 2006. Specific bacterial suppressors of MAMP signaling upstream of MAPKKK in Arabidopsis innate immunity. Cell 125: 563-575
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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
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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
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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
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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: 60-69
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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
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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
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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: 2257-2269
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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: 241-245
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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: 2060-2063
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Zhou, J., Y. T. Loh, G. B. Martin. 1995. The Tomato Gene Pti1 Encodes a Serine/threonine Kinase That is Phosphorylated by Pto and is Involved in the Hypersensitive Response. Cell 83: 925-935
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Martin, G. B., A. Frary, T. Wu, S. Brommonschenkel, J. Chunwongse, E. D. Earle, S. D. Tanksley. 1994. A Member of the Tomato Pto Gene Family Confers Sensitivity to Fenthion Resulting in Rapid Cell Death. Plant Cell 6: 1543-1552
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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: 1432-1436
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Features

Features

How do bacteria overcome a plant’s disease defense system?

feature released -2008

How do bacteria overcome a plant’s disease defense system?There’s an arms race underway in the plant world in which plants and disease-causing bacteria are continually evolving ways to outsmart each other. Plants have developed a defense system that enables them to resist disease, but some pathogens have evolved survival methods that undermine this system. Understanding the details of this race for dominance could lead to crop plants with more effective, natural resistance to disease.

Gregory Martin’s laboratory studies a bacterium called Pseudomonas syringae, which causes bacterial speck disease of tomatoes. When P. syringae invades a tomato plant, it injects a disease-promoting protein called AvrPtoB into the plant cells. However, the plant is ready and waiting with the protein Fen,which was recently discovered by Martin’s team. Fen recognizes AvrPtoB and, in doing so, activates the plant’s defense system.

Fighting back, P. syringae has cleverly engineeredAvrPtoB to act as a tomato E3 ligase, a protein that tags other proteins to be destroyed. When AvrPtoB binds the Fen protein, Fen is tagged and the plant’s own system takes Fen to the cell’s “garbage bin” before Fen can activate the plant’s defenses. This eliminates the plant’s ability to resist speck disease and ensures the survival of the bacterium.

In further studies,Martin’s laboratory found that the Fen gene is present in many wild species of tomatoes suggesting it is an ancient plant defense strategy. But if the bacterial protein AvrPtoB is so effective at destroying the Fen protein,why would the Fen gene be so prevalent? Martin answers that there are some strains of P. syringae that produce a version of AvrPtoB that cannot destroy Fen, and, therefore, cannot turn off the plant’s defense system. Consequently, he reasons that the bacteria have only recently evolved the version of AvrPtoB that can sabotage the plant’s defenses.

Martin’s work helps to explain how the plant/pathogen arms race works at the molecular level and sheds new light on how disease-resistant plants can suddenly become susceptible again. Understanding the strategies pathogens use to overcome plant defenses against disease may lead to crops that have more effective, longer lasting resistance – an advance that could lead to more productive varieties and less dependence on pesticides.

Stealthy Attackers.

feature released -2007

Stealthy Attackers.Millions of years of evolution have equipped viruses, bacteria, and other attackers with clever ways to slip past a plant’s defenses. One strategy Greg Martin’s lab has studied recently is molecular mimicry: evolving proteins that mimic plant proteins and can alter the plant’s physiology for the benefit of a pathogen.

Martin’s lab recently found two instances of this mimicry. In the first case, graduate student Jeff Anderson was looking for ways in which infection by the bacteria Pseudomonas syringae affects tomato cells. Specifically, he wanted to find whether the Pseudomonas protein AvrPto, which makes the bacteria more virulent, influences phosphorylation of host proteins, since attaching or taking away a phosphate group is a common way to change protein function.

He discovered instead that AvrPto itself gets phosphorylated by a host protein, and not by chance: a phosphate group is added at a specific amino acid. Mutating AvrPto so that it cannot be phosphorylated reduces the ability of AvrPto to promote plant disease. This observation suggests that a host enzyme specifically recognizes AvrPto and adds the phosphate. For that to happen, AvrPto likely mimics a host protein the enzyme normally acts on.

In a second case of molecular mimicry, graduate student Rob Abramovitch was looking for tomato proteins that interact with AvrPtoB, another Pseudomonas virulence protein. He came up with ubiquitin, a small protein plant cells commonly use to mark unneeded proteins for degradation.

Why would AvrPtoB bind to ubiquitin? Part of the answer came when Abramovitch found that AvrPtoB acts as a ubiquitin ligase, a host enzyme that attaches ubiquitin to host proteins. A collaborator on the project showed that the three-dimensional crystal structure of AvrPtoB looks like a typical host ubiquitin ligase. Martin and Abramovitch speculate that AvrPtoB makes plants more susceptible to disease by attaching ubiquitin to plant proteins involved in defense responses, thus tagging them for demolition.

The Molecular Arms Race.

feature released -2007

The Molecular Arms Race.In the battles between plants and the microbes that prey on them, victory goes to the organisms with the most effective genes. Gregory Martin’s lab studies tomato plants and disease-causing Pseudomonas syringae bacteria to seek the answer to a seemingly simple question: What makes a plant vulnerable to infection? The answer to that question could affect not only agriculture, but also human health.

One type of Pseudomonas causes bacterial speck disease in susceptible tomatoes, while different strains of the bacteria can infect other plants, and one even causes antibiotic-resistant infections in people with compromised immune systems. Martin helped sequence the speck-causing bacteria’s genome last year, information that sped up his search for genes that enable Pseudomonas to skirt tomatoes’ resistance.

Martin’s lab explored techniques for fleshing out the functions of tomato genes involved in the plant’s arms race with Pseudomonas. Using virus-induced gene silencing, for example, the Martin lab found signaling molecules in tomato that determine its response to Pseudomonas exposure. Resistant plants quickly corral and kill off infected cells, causing brown spots of dead cells to appear on the leaves. But susceptible plants also display specks, as Pseudomonas kills infected cells to spread further. Martin recently showed that the same molecular switch sets off both the defensive and disease-induced cell death, though through different channels. He suggests that this switch could be changed to make crops more resistant.

The lab has identified surprising similarities between immune systems in tomatoes and animals, indicating that in some cases, plants could be used to model human response to disease.

Lab Members

Current Lab Members

Jay Worley
Jay Worley
PostDoc
Office/Lab: 323 / 326
jnw29@cornell.edu
Office: 607-220-9610
Lab:
Patrick Boyle
Patrick Boyle
Postdoc
Office/Lab: 319/316
pcb56@cornell.edu
Office:
Lab: 607 220 9610
Diane Dunham
Diane Dunham
Laboratory Manager
Office/Lab: 323
dmd248@cornell.edu
Office:
Lab: 607 220 9610
Sarah Hind
Sarah Hind
Postdoc
Office/Lab: 325/318
srh226@cornell.edu
Office:
Lab: 607 220 9610
Christine Kraus
Christine Kraus
Graduate Student
Office/Lab: 325/316
cmk253@cornell.edu
Office:
Lab: 607 220 9610
Marina Pombo
Marina Pombo
Postdoc
Office/Lab: 323/318
map383@cornell.edu
Office:
Lab: 607 220 9610
Paige Reeves
Paige Reeves
Greenhouse/Research Assistant
Office/Lab: 319/316
plr58@cornell.edu
Office:
Lab: 607 220 9610
Hernan Rosli
Hernan Rosli
Postdoc
Office/Lab: 321/316
hgr28@cornell.edu
Office:
Lab: 607 220 9610
Simon Schwizer
Simon Schwizer
Grad Student
Office/Lab: 319/318
ss968@cornell.edu
Office:
Lab: 607 220 9610
Zhilong Bao
Zhilong Bao
Postdoc
Office/Lab: 321/318
zb36@cornell.edu
Office: 607-220-9610
Lab:

Undergraduate Lab Members

Emma Rosenthal
Emma Rosenthal
Brandon Maziuk
Brandon Maziuk
Tess Posekany
Tess Posekany
Ruth Anne
Ruth-Anne Langan