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25 Oomycete Diseases 25 Oomycete Diseases Katherine J. Hayden,1* Giles E.St.J. Hardy2 and Matteo Garbelotto1 1University of California, Berkeley, California, USA; 2Murdoch University, Murdoch, Western Australia 25.1 Pathogens, Significance in part by the extreme generalist Phytophthora and Distribution cinnamomi Rands (Crandall et al., 1945; Anagnostakis, 1995). P. cinnamomi is notori- The most important oomycete forest patho- ous for the massive mortality it has caused gens comprise two genera: Pythium and the in jarrah (Eucalyptus marginata Donn ex Sm.) formidable genus Phytophthora, whose name forests in Western Australia, where it was appropriately means ‘plant destroyer’. Pythium first observed in the 1920s (Podger, 1972). spp. cause seed and root rots and damping- P. cinnamomi causes root disease in agricultural off diseases that thwart seedling establish- and forest systems worldwide with varying ment, and have been implicated in helping degrees of virulence, but as Phytophthora to drive forest diversity patterns through dieback it has been seen to kill 50–75% of increased disease pressures on seedlings clos- the species in sites in Western Australia, in est to their mother tree (Janzen, 1970; Connell, some cases leaving every tree and much of 1971). In contrast, Phytophthora spp. can cause the understorey dead (Weste, 2003). Shearer disease at every life stage of forest trees, from et al. (2004) estimate that of the 5710 described root to crown, and from trunk cankers to plant species in the South West Botanical foliar blights (Erwin and Ribeiro, 1996). They Province of Western Australia, approximately are remarkably flexible and effective patho- 2300 species are susceptible, of which 800 of gens with an unusual genetic architecture these are highly susceptible. that may favour the rapid evolution of patho- More recently, the trunk canker caused genicity (Jiang et al., 2008; Raffaele et al., 2010; by Phytophthora ramorum Werres, De Cock & Seidl et al., 2011). Outbreaks of disease caused Man in’t Veld has caused a devastating die-off by Phytophthora spp. (especially when they of oaks (Quercus spp.) and tanoak (Lithocarpus have been introduced to new systems) have densiflorus (Hook. & Arn.) Rehder) in western been documented with dramatic, and some- North America (Rizzo and Garbelotto, 2003), times disastrous, effects since the mid 1800s. spreading from a relatively minor foliar blight European and North American chestnuts of ornamentals in nurseries to a fatal scourge (Castanea spp.) began dramatic declines in US wildlands and UK gardens. In contrast from chestnut ink disease, a root rot caused to P. cinnamomi, which is a root pathogen * E-mail: [email protected] 518 ©CAB International 2013. Infectious Forest Diseases (eds P. Gonthier and G. Nicolotti) GGonthier_Ch25.inddonthier_Ch25.indd 551818 22/4/2013/4/2013 11:21:19:21:19 PPMM Oomycete Diseases 519 transmitted by soil and water, infection by strong evidence that P. cinnamomi is unable to and transmission of P. ramorum occur prima- survive saprophytically in the absence of host rily above ground. While the two species plants. In dry conditions, it persists in the have much in common, e.g. extremely broad hardpan layer, where deep lateral roots may host ranges and disastrous consequen ces be in contact with free water even when the of introduction on native ecosystems, their surface soil is dry (Shea et al., 1983; Kinal et al., contrasting modes of transmission span the 1993; Shearer et al., 2010). It favours warmer range for oomycete pathogens. Here, we treat temperatures than most Phytophthora spp., these two species and the extensive literature but has a wide range of conducive tempera- surrounding them as case studies for oomyc- tures, facilitating its worldwide distribution. ete diseases and their management. P. ramorum is the cause of sudden oak A great many more species of Phytophthora death trunk canker, ramorum blight and die- have an impact on forest systems, and new back, and is distributed in nurseries in the species are discovered almost yearly. Most of western USA, western Canada and through- these are likely to have been established for out Europe. It is present in gardens in the UK some time (even if they are relatively recent and wildlands in the USA. Diseases caused introductions), but have only just noticed by P. ramorum emerged in the mid 1990s as because of increased sampling and new foliar and twig blight of nursery ornamentals molecular tools (Jung et al., 2002, 2011; Hansen in Europe (Werres et al., 2001), and as fatal et al., 2003; Balci et al., 2008; Burgess et al., canker disease of oaks and tanoaks in a 300 km 2009; Scott et al., 2009). Others are entirely stretch of the California coast (Rizzo et al., new, however, notably a novel Phytophthora 2002). The twig and foliar blight infects species complex that has begun to decimate hosts in nearly every plant family, and is the alders (Alnus spp.) in Europe (Brasier et al., primary source of inoculum even in the US 1995, 1999). In addition to the more detailed epidemic (Garbelotto et al., 2002). The canker descriptions of P. cinnamomi and P. ramorum, form in true oaks has not been documented to we briefly describe a selection of those spe- contribute to pathogen spread, but tanoaks cies currently known to have the greatest are distinctly susceptible to both the sporulat- impacts on forest systems. For a more com- ing foliar and twig disease and the fatal plete description of the biology and disease canker (Davidson et al., 2008). The disease has control of older Phytophthora spp., refer to been responsible for the deaths of hundreds Erwin and Ribeiro (1996). of thousands, if not millions of oaks and P. cinnamomi has a worldwide distribu- tanoaks (Plate 30), the near extirpation in tion, and is the cause of Phytophthora root tanoak in some parts of its range, and millions and collar rot (synonyms: ink disease of of US dollars incurred in costs due to quaran- hardwoods, Phytophthora dieback, littleleaf tine and the monitoring of nurseries. disease of pines, stripe canker of cinnamon). Pythium spp. (e.g. P. debaryanum R. Hesse, P. cinnamomi was confirmed as a cause of P. irregulare Buisman, P. ultimum Trow) are ink disease, along with P. cambivora (Petri) distributed worldwide, are root pathogens Buisman in Europe, in the early 1900s (Day, and a major cause of seed rots and damping- 1938), and as the cause of ‘jarrah dieback’ in off diseases. These diseases are a major cause 1965 (Podger et al., 1965; Podger, 1972). The of seedling mortality, and have long been pathogen causes root rots on a huge number thought to help drive diversity in tropical for- of species (Hardham, 2005). Disease severity ests through density-dependent mortality ranges from asymptomatic to fatal, depend- (Augspurger, 1984; Bell et al., 2006). They have ing on the host and environmental conditions, also been documented in temperate systems with among the worst observed in the jarrah (Packer and Clay, 2000, 2003). See Gilbert ‘graveyards’ of Western Australia. It has been (2002) for a review of the role and limitations documented to live saprophytically, and to of pathogens as natural enemies in driving persist in moist soil for as long as 6 years forest diversity, as proposed by Janzen (1970) (Zentmyer and Mircetich, 1966). However, and Connell (1971). Put simply, the Janzen– the work of McCarren et al. (2005) provides Connell hypothesis posits density-dependent GGonthier_Ch25.inddonthier_Ch25.indd 551919 22/4/2013/4/2013 11:21:19:21:19 PPMM 520 K.J. Hayden et al. feedback, wherein the highest density of Phytophthora cactorum (Lebert & Cohn) seeds and their pathogens or other natural J. Schröt. is globally distributed and causes enemies will both occur close to a parent tree. disease on a wide range of species, from forest Seeds may have to travel some distance to trees to ornamentals. It has been associated escape their enemies, thus helping to drive with canker diseases on maple (Acer spp.) forest diversity. (Caroselli and Howard, 1939; Erwin and For forest managers, seed rots and Ribeiro, 1996), beech (Jung et al., 2006), horse damping-off diseases are a hindrance to re- chestnut (Aesculus hippocastanum L.) (Brasier seeding efforts, and may inspire the use of and Strouts, 1976) and white poplar (Populus nursery-grown seedlings rather than starting alba L.) (Cerny et al., 2008), and with declining new trees from seed, bringing with them the oaks in Europe (Jung et al., 1996); it has long potential to spread nursery diseases into been associated with root rots of conifers. wildlands. Pythium spp. have been impli- Phytophthora cambivora has a world- cated in the decline of spruce (Picea spp.) and wide distribution and, as already noted, is beech (Fagus spp.) in Bavaria (Nechwatal and co-implicated with P. cinnamomi as the cause Osswald, 2001), the decline of Spanish oaks of ink disease of chestnut in Europe, both in (Romero et al., 2007), and as contributing its historic form, dating to before 1800 (Day, to growth reductions of Scots pine (Pinus 1938; Crandall et al., 1945), and in its recent sylvestis L.) in Scotland, especially when resurgence (Vettraino et al., 2001, 2005). The mixed with P. cinnamomi or Fusarium spp. infection spreads from roots into the collar (Chavarriaga et al., 2007). Features of the of the tree, and frequently causes death within P. ultimum genome sequence are consistent 2 years. The disease may also move more with its status as a necrotroph and generalist slowly, and cause the slow decline of the pathogen of seedlings; it lacks cutinases to crown, followed by death within several break down plant cuticles, lacks xylanase to years (Day, 1938). Ink disease is characterized digest complex polysaccharides, and does by a black exudate from a lesion that spreads not have the RXLR effectors (effector pro- upwards from the soil.
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