Gregory Martin

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.

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 or they are mutated using CRISPR/Cas9 to test whether they make a demonstrable contribution to immunity. A third project uses photo-crosslinking and other biochemical methods to characterize 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

Google Scholar profile and publications.

• Zhang, N., C. Hecht, X. Sun, Z. Fei, and G.B. Martin (2022). Loss of function of the bHLH transcription factor Nrd1 in tomato enhances resistance to Pseudomonas syringae. Plant Physiology 
• Powell, A.F., A. Feder, J. Li, M.H.-W Schmidt, L. Courtney, S. Alseekh, E.M. Jobson, A. Vogel, Y. Xu, D. Lyon, K. Dumschott, M. McHale, R. Sulpice, K. Bao, R. Lal, A. Duhan, A. Hallab, A.K. Denton, M.E. Bolger, A.R. Fernie, S.R. Hind, L.A. Mueller, G.B. Martin, Z. Fei, C. Martin, J.J. Giovannoni, S.R. Strickler, B. Usadel (2022). A Solanum lycopersicoides reference genome facilitates insights into tomato specialized metabolism and immunity. Plant Journal 110:1791-1810.
• Wang, L., H.B. Kaya, N. Zhang, R. Rai, M.R. Willmann, S.C.D. Carpenter, A.C. Read, F. Martin, Z. Fei, J.E. Leach, G.B. Martin and A.J. Bogdanove (2020). Spelling changes and fluorescent tagging with prime editing vectors for plants. Frontiers in Genome Editing 
• Mazo-Molina, C., S. Mainiero, B. J. Haefner, R. Bednarek, J. Zhang, A. Feder, K. Shi, S. R. Strickler and G. B. Martin (2020). Ptr1 evolved convergently with RPS2 and Mr5 to mediate recognition of AvrRpt2 in diverse solanaceous species. Plant Journal 103:1433-1445.
• Roberts, R., A.E. Liu, L. Wan, A. M. Geiger, S. R. Hind, H. G. Rosli and G. B. Martin (2020). Molecular characterization of differences between the tomato immune receptors Fls3 and Fls2. Plant Physiology 183:1825-1837.
• Zhang, N., H. M. Roberts, J. Van Eck and G. B. Martin (2020). Generation and molecular characterization of CRISPR/Cas9-induced mutations in 63 immunity-associated genes in tomato reveals specificity and a range of gene modifications. Frontiers in Plant Science 11:1-13.
• Zhang, N., M. A. Pombo, H. G. Rosli and G. B. Martin (2020). Tomato wall-associated kinase SlWak1 acts in an Fls2- and Fls3-dependent manner to promote apoplastic immune responses to Pseudomonas syringae. Plant Physiology 183:1869-1882.
• Eckshtain‐Levi, N., M. Lindeberg, G. E. Vallad and G. B. Martin (2019). The tomato Pto gene confers resistance to Pseudomonas floridensis, an emergent plant pathogen with just nine type III effectors. Plant Pathology 68:977-984.
• Mazo-Molina, C., S. Mainiero, S. R. Hind, C. M. Kraus, M. Vachev, F. Maviane-Macia, M. Lindeberg, S.Saha, S. R. Strickler, A. Feder, J. J. Giovannoni, C. D. Smart, N. Peeters and G. B. Martin (2019). The Ptr1 locus of Solanum lycopersicoides confers resistance to race 1 strains of Pseudomonas syringae pv. tomato and Ralstonia pseudosolanacearum by recognizing the type III effectors AvrRpt2 and RipBN. Molecular Plant-Microbe Interactions 32: 949-960.
• Roberts, R., S. Mainiero, A. F. Powell, A. E. Liu, K. Shi, S. R. Hind, S. R. Strickler, A. Collmer and G. B. Martin (2019). Natural variation for unusual host responses and flagellin-mediated immunity against Pseudomonas syringae in genetically diverse tomato accessions. New Phytologist 223:447-461.
• Roberts, R., S. R. Hind, K. F. Pedley, B. A. Diner, M. J. Szarzanowicz, D. Luciano-Rosario, B. B. Majhi, G. Popov, G. Sessa, C.-S. Oh and G. B. Martin (2019). Mai1 protein acts between host recognition of pathogen effectors and MAPK signaling. Molecular Plant-Microbe Interactions 32:1496-1507.
• Zheng, Y., N. Zhang, G. B. Martin and Z. Fei (2019). Plant Genome Editing Database (PGED): A call for submission of information about genome-edited plant mutants. Molecular Plant 12:127-129.
• Jacobs, T. B., N. Zhang, D. Patel and G. B. Martin (2017). Generation of a collection of mutant tomato lines using pooled CRISPR libraries. Plant Physiology 174:2023-2037.
• Schwizer, S., C. M. Kraus, D. M. Dunham, Y. Zheng, N. Fernandez-Pozo, M. A. Pombo, Z. Fei, S. Chakravarthy and G. B. Martin (2017). The tomato kinase Pti1 contributes to production of reactive oxygen species in response to two flagellin-derived peptides and promotes resistance to Pseudomonas syringae infection. Molecular Plant-Microbe Interactions 30:725-738.
• Hind S. R., S. R. Strickler, P. C. Boyle, D. M. Dunham, Z. Bao, I. M. O'Doherty, J. A. Baccile, J. S. Hoki, E. G. Viox, C. R. Clarke, B. A. Vinatzer, F. C. Schroeder and G. B. Martin (2016). Tomato receptor FLAGELLIN-SENSING 3 binds flgII-28 and activates the plant immune system. Nature Plants 2:16128.
• Kraus C. M., K. R. Munkvold and G. B. Martin (2016). Natural variation in tomato reveals differences in the recognition of AvrPto and AvrPtoB effectors from Pseudomonas syringae. Molecular Plant 9:639-49.
• Wei, H. L., Chakravarthy, S., Mathieu, J., Helmann, T., Stodghill, P., Swingle, B., Martin, G. B., & Collmer, A. (2015). Pseudomonas syringae pv. tomato DC3000 Type III secretion effector polymutants reveal an interplay between HopAD1 and AvrPtoB. Cell Host & Microbe. 17:752-762.
• Mathieu, J., Schwizer, S., & Martin, G. B. (2014). Pto kinase binds two domains of AvrPtoB and its proximity to the effector E3 ligase determines if it evades degradation and activates plant immunity. PLoS Pathogens. 10:e1004227.
• Pombo, M. A., Zheng, Y., Fernandez-Pozo, N., Dunham, D. M., Fei, Z., & Martin, G. B. (2014). Transcriptomic analysis reveals tomato genes whose expression is induced specifically during effector-triggered immunity and identifies the Epk1 protein kinase which is required for the host response to three bacterial effector proteins. Genome Biology. 15:492.
• Rosli, H. G., Zheng, Y., Pombo, M. A., Zhong, S., Bombarely, A., Zhangjun, Z., Collmer, A., & Martin, G. B. (2013). Transcriptomics-based screen for genes induced by flagellin and repressed by pathogen effectors identifies a cell wall-associated kinase involved in plant immunity. Genome Biology. 14:R139.
• Bombarely, A., Rosli, H. G., Vrebalov, J., Moffett, P., Mueller, L. A., & 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.
• Cunnac, S., Chakravarthy, S., Kvitko, B. H., Russell, A. B., Martin, G. B., & Collmer, A. (2011). Genetic disassembly and combinatorial reassembly identify a minimal functional repertoire of type III effectors in Pseudomonas syringae pv. tomato DC3000. PNAS: Proceedings of the National Academy of Sciences of the United States of America. 108:2975-2980.
• Oh, C., Pedley, K., & Martin, G. B. (2010). Tomato 14-3-3 protein 7 (TFT7) positively regulates immunity-associated programmed cell death by enhancing protein abundance and signaling ability of MAPKKKα. The Plant Cell. 22:260-272.
• Shan, L., He, P., Li, J., Heese, A., Peck, S., Numberger, T., Martin, G. B., & Sheen, J. (2008). Bacterial effectors target BAK1 to disrupt MAMP receptor signaling complexes and impede plant innate immunity. Cell Host & Microbe. 4:17-27.
• Rosebrock, T. R., Zeng, L., Brady, J. J., Abramovitch, R. B., Xiao, F., & Martin, G. B. (2007). A bacterial E3 ubiquitin ligase targets a host protein kinase to disrupt plant immunity. Nature. 448:370-374.

Presentations and Activities

• U.S. Patent Application No. 16/916,757: ‘Enhanced disease resistance in plants. Inventors: G. B. Martin, A. Feder, S. Mainiero, S. Hind, and D. C. Mazo-Molina. Filed June 30, 2020 by the Boyce Thompson Institute for Plant Research, Ithaca, NY.
• U.S. Patent No. 10557145: ‘FlgII-28 sensitivity 3 (FLS3) protein and methods of use’. Inventors: G. B. Martin, S. Hind, and S. Strickler. Issued February 11, 2020 to the Boyce Thompson Institute, Ithaca, NY.