From appressorium to transpressorium—Defining the morphogenetic basis of host cell invasion by the rice blast fungus

ntroductionTo cause disease, many fungal pathogens develop specialised structures to rupture the tough outer layers of their plant or animal hosts.These infection cells, called appressoria, have been extensively studied in many fungal species [1].However, once inside host tissue, pathogens must also invade new cells and traverse host cell junctions.How they do this has received much less attention, but recent evidence from the rice blast fungus suggests that cell invasion within a host plant may also require the development of a specialised infection structure.Here, we compare the developmental biology of invasive growth during different stages of plant infection by the rice blast fungus.We identify the remarkable parallels between the biology of appressorium development and cell-to-cell movement.Finally, we evaluate evidence suggesting that a specialised infection cell-the transpressorium-is necessary for invasive growth. How does the rice blast fungus puncture an intact leaf?Rice blast disease is one of the world's most important crop diseases, each year destroying enough rice to feed 60 million people [2].Given that rice is the staple food for almost 3.7 billion of the world's population-many of them in low-income countries-blast disease represents a clear and present danger to global food security.The blast fungus Magnaporthe oryzae can, however, infect more than 50 different grass species, including other major cereals such as barley, oats, finger millet, and wheat.Significant outbreaks of wheat blast have occurred in Brazil, Bangladesh [3,4], and, most recently, in Zambia [5]-now threatening wheat production on 3 continents.Understanding the biology of blast diseases is therefore important if new disease control strategies are to be developed.To gain entry to a plant, M. oryzae uses a dome-shaped, melanin-pigmented appressorium [1].A conidium germinates on the leaf surface to form a polarised germ tube, which differentiates into an appressorium within 4 to 6 hours.There are 3 important prerequisites for appressorium morphogenesis.First of all, a hard hydrophobic surface [6] must be recognised by M. oryzae, which requires the Pmk1 mAU : PleasenotethatMAPhasbeendefinedasmitogen À activatedpr itogen-activated protein kinase (MAU : Pleasenotethattheabbrevi APK) signalling pathway.Upstream sensory proteins trigger a phosphorylation cascade that involves Mst11 (mitogen-activated protein kinase kinase kinase, MAU : PleasenotethatMAPKKKhasbeendefinedasmito APKKK), Mst7 (mitogen-activated protein kinase kinase, MAU : PleasenotethatMAPKKhasbeendefinedasmitogen À activatedproteinkinasekinase APKK), and Pmk1 (MAPK).In the absence of Pmk1, the fungus is unable to form an appressorium, and, therefore, incapable of causing disease [7].The second prerequisite is that the germinating cell of the 3-celled conidium must undergo mitosis.An S phase checkpoint is necessary for the initiation of appressorium development, and the nucleus must then pass through G2-M to enable appressorium maturation to progress [8].Finally, the