R Genes Help Unravel Signaling Paths

For this article, Steve Bunk interviewed Tina Romeis, postdoctoral researcher, Sainsbury Laboratory, John Innes Center, Norwich, UK. Data from the Web of Science (ISI, Philadelphia) show that Hot Papers are cited 50 to 100 times more often than the average paper of the same type and age. T. Romeis, P. Piedras, S. Zhang, D.F. Klessig, H. Hirt, J.D.G. Jones, "Rapid Avr9- and Cf-9-dependent activation of MAP kinases in tobacco cell cultures and leaves: convergence of resistance gene, elicitor, wound, and salicylate responses," Plant Cell, 11:273-88, February, 1999. (Cited in 94 papers) Compared to what's known of how mammals respond to potential harm, the defense mechanisms of plants remain largely mysterious. "The signaling cascade from receptor through to transcription factor is just not available in plants," notes Tina Romeis, this paper's lead author. Even so, she adds, "It appears that only a limited number of pathways are available for the plant to react to the environment." Disease resistance, or R genes, are key players studied by postdoctoral researcher Romeis and colleagues, led by senior author Jonathan D.G. Jones, whose lab is part of the Sainsbury Laboratory, John Innes Center, Norwich, UK. R gene products are thought to either act as receptors or belong to receptor complexes for matching proteins, which are encoded by avirulence (avr) genes in the pathogen. Courtesy of Tina RomeisTina Romeis For example, the tomato plant's Cf-9 gene is named after the leaf mold fungus Cladosporium fulvum. When a peptide encoded by the pathogenic gene Avr9 infects a Cf-9 plant, an intracellular signaling cascade begins for plant defense. But plants also must guard against so-called nonspecific elicitors, which are molecules from fungi, viruses, or bacteria that don't fit into specific Avr/R pairings. Other environmental stresses, such as wounds and drought, also exist. For this paper, researchers asked the key question: Are signaling pathways for a plant's defense against various enemies separate, or do they merge? In transgenic tobacco plants and cultures expressing the Cf-9 tomato gene product, the researchers identified two proteins that quickly became activated after exposure to Avr9 and to other stressors, such as tiny leaf cuts or treatment with salicylic acid. Both proteins proved to be mitogen-activated protein (MAP) kinases that had been previously characterized in tobacco. MAP kinases participate in signaling cascades to defend against Avr/R-specific and nonspecific elicitors. The paper was "the first to show that these kinases were involved in all these responses," Romeis notes. "The question then was, how, despite converging signaling pathways and shared MAP kinase signaling components, is a wound response different from a pathogen response?" says Romeis. The paper established that plant defense is a complex network. Future research will require an integrated approach to understanding the function of R genes. The Jones team's current work involves various methods of searching for mutations that affect R gene function. Romeis nominates two papers from other groups as important recent contributions to the plant MAP kinase signaling field. The first showed that one MAP kinase in the mustard plant Arabidopsis thaliana actually represses resistance to pathogens.1 The second demonstrated that a MAP kinase-activated cascade can induce cell death in tobacco, a form of disease resistance.2 "What the field lacks," she concludes, "is reverse genetics of signaling components, combined with a detailed subsequent biochemical analysis." The Jones lab has contributed to this goal by spearheading development of a process to isolate insertional mutants in Arabidopsis using reverse genetics screens.3 Steve Bunk (sbunk@the-scientist.com) is a contributing editor for The Scientist. References 1. M. Peterson et al., "Arabidopsis MAP kinase 4 negatively regulates systemic acquired resistance," Cell, 103:1111-20, Dec. 22, 2000. 2. K.Y. Yang et al., "Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco," Proceedings of the National Academy of Sciences USA, 98:741-6, Jan. 16, 2001. 3. A.F. Tissier et al., "Multiple independent defective suppressor-mutator transposon insertions in Arabidopsis: a tool for functional genomics," Plant Cell, 11:1841-52, 1999.

R Genes Help Unravel Signaling Paths

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