Regulation of Appressorium Development in Pathogenic Fungi

Available online at www.sciencedirect.com ScienceDirect Regulation of appressorium development in pathogenic fungi Lauren S Ryder and Nicholas J Talbot Many plant pathogenic fungi have the capacity to breach the specialised structures called appressoria [4,5]. These cells intact cuticles of their plant hosts using specialised infection can take various forms — either single-celled structures, or cells called appressoria. These cells exert physical force to compound appressoria composed of numerous cells, which rupture the plant surface, or deploy enzymes in a focused way can collectivelyformstructuresknownasinfection cushions to digest the cuticle and plant cell wall. They also provide the [6]. In many cases appressoria are simple terminal swellings means by which focal secretion of effectors occurs at the point at the tips of germ tubes that emerge from spores on the leaf of plant infection. Development of appressoria is linked to re- surface [7], whereas in other species such as the rice blast modelling of the actin cytoskeleton, mediated by septin fungus, Magnaporthe oryzae and the anthracnose disease- GTPases, and rapid cell wall differentiation. These processes causing Colletotrichum species, appressoria are melanin-pig- are regulated by perception of plant cell surface components, mented, septate structures that initially form at the tips of and starvation stress, but also linked to cell cycle checkpoints germ tubes, but then differentiate into dome-shaped fully that control the overall progression of infection-related differentiated infection structures [7] (see Figure 1). development. Address In this review, we compare and evaluate recent studies School of Biosciences, University of Exeter, Stocker Road, Exeter EX4 that have investigated the biology of appressorium de- 4QD, United Kingdom velopment in plant pathogenic fungi. Many of the studies focus on model plant pathogenic species, such as the rice Corresponding author: Talbot, Nicholas J ([email protected]) blast fungus M. oryzae and the corn smut fungus Ustilago maydis [8]. These two species are diverse — M. oryzae is an ascomycete and U. maydis a basidiomycete. However, Current Opinion in Plant Biology 2015, 26:8–13 there are some common themes emerging from studies of This review comes from a themed issue on Biotic interactions both of these species, and indeed among other appresso- Edited by Uta Paszkowski and D Barry Scott rium-forming fungi. There is, for example, an emerging picture of a highly orchestrated developmental process requiring perception of physical and chemical cues from the plant leaf surface, coupled with control of both http://dx.doi.org/10.1016/j.pbi.2015.05.013 nuclear and cell division. Targeting such fundamental 1369-5266/# 2015 Published by Elsevier Ltd. morphogenetic processes may therefore be important in terms of developing the next generation of anti-penetrant fungicides, or targeting plant-based methods to control some of the most important cereal diseases [3,4]. Introduction Early appressorium development Plant pathogenic fungi cause many of the world’s most Early appressorium development occurs soon after a spore devastating crop diseases and each year significant ex- lands on the surface of its host. In the rice blast fungus M. penditure is required to combat plant diseases and there- oryzae a three-celled conidium germinates within an hour by ensure food security [1,2]. The problem is even more of attaching itself to the leaf surface which it does by means pressing in the developing world, where the high cost of of an adhesive, specially adapted to adhere tightly to the fungicides means that disease outbreaks have serious hydrophobic, waxy leaf cuticle [4]. Upon hydration and consequences; farmers frequently face economic ruin surface contact, the spore rapidly germinates and sends out and the societal and economic impact of plant diseases a germ tube, normally emerging from the tapering end of is significant. It has been estimated that up to 30% of the the three-celled conidium. The germ tube extends for 10– global harvest is lost each year to plant disease and 15 mm before flattening at its tip, hooking, and beginning therefore identifying durable solutions to plant diseases to differentiate into the unicellular appressorium. Control is likely to be one of the most important means by which of initiation of appressorium development is based on plant productivity can be increased in a sustainable way perception of hydrophobicity (the surface needs to have [2,3]. water contact angles of greater than 90 degrees, typical of plastic surfaces such as Teflon) and surface hardness [3]. In Many plant pathogenic fungi have evolved the capacity to addition, the fungus is able to respond to wax monomers breach the intact cuticles of their plant hosts by elaborating such as 1,16-hexadecanediol, which are powerful inducers Current Opinion in Plant Biology 2015, 26:8–13 www.sciencedirect.com Appressorium development Ryder and Talbot 9 Figure 1 (a) (b) Guy11/Sep5 Δnox1/Sep5 Δnox2/Sep5 ΔnoxR /Sep5 (c) Guy11/gelsolin Δnox1/gelsolin Δnox2/gelsolin ΔnoxR/gelsolin Current Opinion in Plant Biology Photomicrographs showing appressorium development by the rice blast fungus Magnaporthe oryzae. Conidia were inoculated onto hydrophobic glass coverslips and incubated in a moist chamber at 26 8C for 8 hours. (a) Bright field, epifluorescence and merged images to show localization of the Sep5-GFP septin gene fusion in a hetero-oligomeric ring at the base of the appressorium. The septin ring is necessary for re-modelling F- actin to the appressorium pore [29]. Bar = 10 mm. (b) Septin localization to the appressorium pore is dependent on regulated synthesis of ROS by the Nox2 NADPH oxidase and its regulatory NoxR sub-unit. Sep5-GFP localization in a Dnox1, Dnox2 and DnoxR mutant. (c) Nox2-dependent localization of the actin-binding protein gelsolin. Gelsolin-GFP localization in a Dnox1, Dnox2 and DnoxR mutant. See [32 ] for details. Bar for (b) and (c) = 5 mm. of appressorium development at the leaf surface [3]. How- at the neck of the appressorium, which differentiates the ever, in addition to the perception of physical cues, cell cell from the rest of the pre-penetration structures [11]. cycle control is pivotal to development appressoria [9]. Autophagy is then stimulated within the conidium, such Each compartment of the three-celled conidium contains a that all of the intracellular contents of the three-celled single nucleus and the cell from which the germ tube spore are degraded before being trafficked to the incipi- emerges undergoes a single round of nuclear division, ent appressorium [9]. The culmination of this process is before appressorium development [9]. Entry of this conid- turgor generation within the appressorium of up to 6– ial nucleus into DNA replication (S-phase) is necessary for 8 MPa, which is sufficient to breach the underlying rice initiation of appressorium development [10] and inhibiting cuticle [4,12]. Blocking autophagy by targeted mutation DNA replication, either with hydroxyurea or by generation of any of the 16 genetic components of the non-selective of a temperature-sensitive nim1 mutant, which undergoes macroautophagy pathway is sufficient to render the aberrant mitosis in the absence of DNA replication, fungus non-pathogenic [13]. Interestingly, cell cycle completely prevents the ability of germ tubes to differen- control of appressorium development is likely to be a tiate at their tips [10]. Subsequently, appressorium matu- conserved process [10]. In U. maydis, for example, cell ration and melanisation is controlled by entry of the cycle arrest is necessary for an infective filament of the nucleus into G2 and mitosis. Only if mitosis occurs does fungus to be able to penetrate plant tissue [14 ]. U. the appressorium become fully functional. At this point maydis undergoes a self-/non-self-recognition process on cytokinesis occurs and a contractile actomyosin ring forms the corn leaf surface in which two monokaryotic sporidia www.sciencedirect.com Current Opinion in Plant Biology 2015, 26:8–13 10 Biotic interactions fuse to form an infectious dikaryotic filament [8]. This pathway also appears to regulate microconidia formation forms an appressorium, which is necessary to breach the by M. oryzae, because Pmk1 and Mst12 mutants show corn leaf surface [14 ,15]. Recent evidence suggests reduced microconidia production while Mcm1 is essen- that cell cycle arrest is required for plant infection. The tial for their development. Microconidia may represent cell cycle arrest results by cooperation of at least two an alternative means of propagation by the pathogen to distinct underlying mechanisms, one of these involves facilitate rapid spread within plant tissue [24 ]. activation of the DNA damage response cascade, and the other relies on transcriptional regulation of a gene called The Pmk1 pathway is widely conserved in other plant HSL1, which encodes a protein kinase that modulates pathogenic fungi and is likely to be required for infection- the G2 to M transition [14 ,15]. Thus, the control of related morphogenesis, although the diversity of these nuclear division and its coordination with morphogene- processes in different plant pathogens and the absence of sis at the leaf surface appear to be processes which are systemic comparative analysis, has precluded detailed fundamental to penetration of the cuticle by diverse analysis [8]. plant pathogens [8]. Appressorium formation also relies on perception of physical and biochemical

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