Adam Bahrami

Research Interests

I am interested in the ecology, evolution and molecular biology of three-way interactions among plants, microbial pathogens and insect herbivores. Using a three-way model established in the Pierce and Ausubel Labs comprised of the plant Arabidopsis thaliana, the plant-pathogen Pseudomonas syringae and the generalist herbivore Trichoplusia ni (cabbage looper), I am examining how the plant immune system copes with simultaneous and/or sequential attack by pathogens and herbivores.

Perhaps not surprisingly, infection of Arabidopsis with P. syringae alters the plant’s ability to subsequently defend itself against T. ni caterpillars (Cui et al. 2002). What is surprising, however, is that simple genetic changes in P. syringae reversed the bacterium’s effect on plant defense against insects. Whereas a P. syringae strain evading a host resistance response (a so-called 'virulent' pathogen) induces plant susceptibility to subsequent herbivory by T. ni, an isogenic P. syringae strain carrying an avr gene, which rapidly induces systemic pathogen resistance in the plant, induces cross-resistance to subsequent herbivory. These data do not support a conventional model of “trade-offs” in plant defense responses to pathogens and herbivores and, therefore, require a more detailed dissection of the network regulating the plant immune system.

Subsequent work confirmed the importance of the plant hormones salicylic acid (SA), inducing resistance to pathogens such as P. syringae, and jasmonic acid (JA), inducing resistance to herbivores (Cui et al. 2002, Cui, Bahrami et al. 2005). Further, a previously identified, mutually antagonistic interaction between the SA and JA pathways was shown to be acting in our model. However, the interactions described in the previous paragraph cannot be explained by SA/JA antagonism, because an avr expressing pathogen, which most significantly upregulates SA, would be expected to induce susceptibility to subsequent herbivory (via SA/JA antagonism) and not resistance, as was observed. Conversely, virulent pathogens that do not elicit a strong SA-dependent host response would not be expected to induce susceptibility to herbivory, which was observed. Clearly other, as-yet unidentified pathways must regulate the plant defense response.

Recent work identified another novel pathogen-manipulated defense pathway, this time involving P. syringae’s ability to cause systemic induced susceptibility, which we termed SIS, to subsequent P. syringae infection in the same plant (Cui, Bahrami et al. 2005). The identification of SIS represents another departure from conventional models of pathogen-induced resistance, because previous work had shown that prior infection of Arabidopsis with P. syringae leads to either systemic acquired resistance (SAR) in the case of an avr-carrying strain, or no effect in the case of an unrecognized virulent strain, but never susceptibility. We demonstrated that P. syringae causes SIS by producing coronatine (COR), a structural and functional mimic of JA. The ability of COR to induce SIS required an intact JA signaling pathway in the plant, confirming that COR acts through the JA pathway. P. syringae has apparently evolved the ability to produce COR to upregulate JA signaling, which in turn, downregulates SA-dependent resistance responses. Interestingly, SAR is more strongly induced by P. syringae lacking the ability to produce COR.

Because virulent P. syringae can induce host plant susceptibility to subsequent infection by P. syringae, we aimed to determine whether COR was also responsible for the observed induction of susceptibility to herbivory by T. ni. We found, however, that, consistent with its role as a JA mimic, COR induces systemic host resistance to T. ni (Cui, Bahrami et al. 2005). This experiment highlights the multi-faceted complexity of P. syringae manipulation of plant defense systems in that the pathogen simultaneously induces resistance to T. ni via the production of coronatine and susceptibility to T. ni via an as-yet uncharacterized mechanism.

Current work using a combination of genetic, genomic and ecological experiments aims to identify the mechanisms by which avr-expressing strains of P. syringae induce resistance to T. ni and virulent strains induce susceptibility to T. ni. Taken together, our experiments expose a previously unknown, complex interplay between plants and their natural enemies. This work should provide a springboard to examine complex multi-way interactions among plants, pathogens and herbivores in field settings.

Lab publications relevant to this project:

Cui J,* Bahrami AK,* Pringle EG, Hernandez-Guzman G, Bender C, Pierce NE & Ausubel FM. (2005). Pseudomonas syringae manipulates systemic plant defenses against pathogens and herbivores. Proceedings of the National Academy of Sciences 102(5): 1791-1796. pdf
(*equal contribution)

Cui J, Jander G, Racki L, Pierce NE & Ausubel FM. (2002). Signals involved in Arabidopsis resistance to Trichoplusia ni caterpillars induced virulent and avirulent strains of phytopathogen Pseudomonas syringae. Plant Physiology 129: 551-564. pdf

Jander G, Cui J, Nhan E, Pierce NE & Ausubel FM. (2001). The TASTY locus on chromosome 1 of Arabidopsis thaliana affects feeding of the insect herbivore, Trichoplusia ni. Plant Physiology 126: 890-898. pdf

Education

2001-present PhD program in the Department of Organismic & Evolutionary Biology, Harvard University.

1995-1999 BS in Conservation & Resource Studies (High Honors), University of California, Berkeley. Self-designed emphasis: chemical and fungal ecology.

Previous Research

1999-2001 Research Assistant in the laboratory of Dr. Anita Sil (University of California, San Francisco) studying the pathogenesis of the fungus Histoplasma capsulatum. Genetic and genomic tools, including a conditional promoter construct and a random shotgun DNA microarray, were developed to understand how the fungus evades being controlled inside the animal immune system (human and mouse).

1996-1999 Undergraduate Researcher in the laboratory of Dr. Ignacio Chapela (University of California, Berkeley) studying the chemically-mediated attraction of insects to a wood-decomposing fungus in a California woodland ecosystem. Novel insect traps baited with fungal biomass were designed and deployed in the field to assess the diversity of insects attracted to volatile chemical signals emanating from the fungus.

Honors thesis: "Selective chemically-mediated insect attraction to the fungus Stereum hirsutum (Stereaceae: Aphyllophorales) in a woodland ecosystem."

Publications

Gebhart D*, Bahrami AK* & Sil A. (2006). Identification of a copper-inducible promoter for use in ectopic expression in the fungal pathogen Histoplasma capsulatum. Eukaryotic Cell. 5(6): 935-944.

(*equal contribution) [PDF]

Cui J,* Bahrami AK,* Pringle EG, Hernandez-Guzman G, Bender C, Pierce NE & Ausubel FM. (2005). Pseudomonas syringae manipulates systemic plant defenses against pathogens and herbivores. Proceedings of the National Academy of Sciences 102(5): 1791-1796. [PDF]
(*equal contribution)

Hwang L, Hocking-Murray D, Bahrami AK, Andersson M, Rine J, Sil A. (2003) Identifying phase-specific genes in the fungal pathogen Histoplasma capsulatum using a genomic shotgun microarray. Molecular Biology of the Cell 14(6): 2314-2326. [PDF]

Before	After

Adam jamming with Simon Chan in California, December 2004. Instruments: Martin Ukelele and Brazilian fiddle (rabeca) by Mane' Pitunga from Ferreiros, Pernambuco. Photo credit: Christie Young (copyright 2004).