Parallels in Intercellular Communication in Oomycete and Fungal Pathogens of Plants and Humans

Abstract

Sexual reproduction is one of the most fascinating evolutionary outcomes in nature. Sexual development is paradoxical, conferring both benefits and costs, which makes sex an attractive subject in evolutionary biology. In pathogenic microbes, sexual development generates progeny with diverse genetic repertoires and can contribute to create more virulent genotypes. Sexual reproduction is ubiquitous in eukaryotic organisms, from single-celled yeasts to humans. Mating systems are highly adapted in each group and vary from species to species, which results in extremely diverse sexual modes throughout nature. However, in some cases, quite divergent groups share similar mechanisms. This review describes a similarity in pheromone synthesis routes in two group of microbial pathogens of historic importance that are evolutionarily quite distinct: zygomycete pathogenic fungi that belong to the kingdom Fungi in the opisthokonts clade, and Phytophthora oomycete species that belong to the stramenopile supergroup [1] (Figure 1). Figure 1 Eukaryotic tree of life (adapted from Baldauf, Science, 2003 [1], with her permission). Historical Aspects of the Two Evolutionarily Distinct Pathogenic Molds: Mucoralean Fungi and Phytophthora Mucorales of the fungal Zygomycota and Phytophthora in the oomycetes have historical significance. One of the Mucor species belonging to the Mucoralean order was the first microbe ever observed in detail by the human eye via Robert Hooke's microscope. Hooke described the microscopic structures of this mold in his book Micrographia [2]. In addition, the first description of sexual development in fungi was of a Mucoralean species nearly two hundred years ago [3]. Several fungal species in the Mucoralean order are the causal agents of mucormycosis, a deadly fungal infection. These species include Rhizopus spp., Mucor spp., Rhizomucor spp., Absidia spp., Cunninghemella spp., and others [4]. Mucormycosis is an emerging, serious fungal infection with high mortality rates. A recent mucormycosis outbreak occurred in victims of the tornadoes in Joplin, Missouri, United States. Oomycetes such as Phytophthora spp. were previously considered members of the fungal kingdom. However, more recent molecular analyses revealed oomycetes are not true fungi but instead divergent stramenopiles that are more closely related to the diatoms and brown alga, with only one known human pathogen in the group: Blastocystis hominis [5]. Phytophthora spp are known as notorious plant destroyers. Phytophthora infestans exemplifies this threat; it was the first species described in the genus and left a path of devastation in its wake on potato crops in the US, Ireland, and Europe in the 19th century [6]. Movement of infected potato tubers led to the potato famine epidemics of the 19th century, which resulted in widespread human hunger, disease, and ultimately the death of 2 million people in Ireland. The pathogen is still a threat to food security in the developing world.