The Past Is Present: Coevolution of Viruses and Host Resistance Within Geographic Centers of Plant Diversity

Understanding the coevolutionary history of plants, pathogens, and disease resistance is vital for plant pathology. Here, I review Francis O. Holmes's work with tobacco mosaic virus (TMV) framed by the foundational work of Nikolai Vavilov on the geographic centers of origin of plants and crop wild relatives (CWRs) and T. Harper Goodspeed's taxonomy of the genus Nicotiana. Holmes developed a hypothesis that the origin of host resistance to viruses was due to coevolution of both at a geographic center. In the 1950s, Holmes proved that genetic resistance to TMV, especially dominant R-genes, was centered in South America for Nicotiana and other solanaceous plants, including Capsicum, potato, and tomato. One seeming exception was eggplant (Solanum melongena). Not until the acceptance of plate tectonics in the 1960s and recent advances in evolutionary taxonomy did it become evident that northeast Africa was the home of eggplant CWRs, far from Holmes's geographic center for TMV-R-gene coevolution. Unbeknownst to most plant pathologists, Holmes's ideas predated those of H.H. Flor, including experimental proof of the gene-for-gene interaction, identification of R-genes, and deployment of dominant host genes to protect crop plants from virus-associated yield losses.