Phytophthora

Phytophthora ramorum and P. kernoviae; the most serious threat yet to the UK's native forests and historic gardens.

Mathew Elliot, Uni St Andrews and Science & Advice for Scottish Agriculture

A number of particularly severe plant diseases have been introduced into forests and gardens over the past century including such well known examples as chestnut blight (Cryphonectria parasitica) and Dutch elm disease (Ophiostoma spp.) (Anagnostakis, 1987; Hubbes, 1999).

The latest serious threat to cause alarm in the UK are two recently discovered, potentially devastating fungal-like plant pathogens, Phytophthora ramorum (so called Sudden Oak Death) (Rizzo, et. al., 2002) and P. kernoviae (Brasier, et. al., 2005). These unpredictable and destructive Phytophthora species affect forest tree species as well as ornamental trees and shrubs causing leaf necrosis, wilting, shoot tip die-back and bleeding cankers on infected tree trunks and ultimately the death of a wide range of plant species. The host species that are susceptible to infection cover a much wider range of species in the UK compared to other affected countries. As of August 2010, there were 149 host species listed for P. ramorum globally and almost half of these (71) were found in the UK; P. kernoviae is currently very much a British problem as all but one of the known 37 hosts were found here (FERA, 2010). The most important host species for both of these pathogens in the UK is itself an invasive weed species, Rhododendron ponticum (Sheppard, et. al., 2006).

The genus Phytophthora (Greek for 'plant destroyer') belongs to the class of organisms known as oomycetes. The most important developmental stage of oomycetes, which sets them apart from true fungi, and also allows oomycete diseases to become epidemics, is the formation of zoospores (Walker & Van West, 2007). Zoospores are asexual motile spores consisting of single nucleated wall-less cells which have two flagella that allow them to swim (Judelson & Blanco, 2005), an adaptation that makes them highly dependent on water.

It is the sporulation of zoospores on to surrounding plants that drives Phytophthora epidemics at such an alarming rate. Zoospores that are released from multinucleated sporangia land on leaves and stems of surrounding plants through air or in rain splashes, then germinate (Walker & Van West, 2007). Depending on the species, a variable number of zoospores are formed within the sporangia and are released during a period of low temperature (below 12 - 15oC) through the sporangial apex. At temperatures above approximately 15oC the sporangia germinate directly on the leaves by producing a germ tube (Hardham, 2007).

Due to the dependency on water shown by Phytophthora, the climatic conditions in certain parts of the UK have proved particularly conducive to infection and spread. Gardens, parkland and the wider environment in Cornwall have been severely affected and it is here that P. kernoviae was first discovered, hence its name (Kernow is Cornish for Cornwall) (Brasier, et. al., 2005). The first infected larch plantations were also discovered in south west England (Webber, et. al., 2010). The wetter west of Scotland also appears to provide ideal conditions for the spread of these pathogens and this is where the majority of Scottish garden and parkland infections have been found (Schlenzig, 2008).

The origin of both pathogens remains an enigma. It is thought that P. ramorum may have originated from somewhere in Asia, and was transported around the world on collected ornamental plants. Asia is a centre of diversity for many of the known hosts of P. ramorum (Vannini, et. al., 2009) and plant collectors have been bringing plants back from Asia for at least 150 years. More specifically, Yunnan Province in northern China has been suggested as the possible origin for P. ramorum due to the abundance of hosts and favourable climate (Goheen, et. al., 2006).

The origin of P. kernoviae is also unknown but it has been suggested that it too may have originated from Asia, however, it has been found in native and exotic forests in New Zealand (in soil samples) from several regions on North Island (Ramsfeld, et. al., 2007). Historical records also show that P. kernoviae has been recorded in New Zealand since the 1950s (as Phytophthora sp.) (MAFBNZ, 2008), and the only diseased plants found in New Zealand are Annona cherimola (Ramsfeld, et. al., 2007) which is the only host known outside of the UK. These theories remain speculative as P. ramorum and P. kernoviae have not yet been found in natural environments in these regions.

The direct and indirect effects of such pathogens on the structure of natural plant communities are of increasing interest, particularly the reduction of mature tree populations by the direct influence of exotic pathogens (Dobson & Crawley, 1994). The resulting effects on relative abundance of the species involved within the wider plant community are discernible for many years after the initial disease outbreak has passed. This is particularly the case for P. ramorum and P. kernoviae as it is not yet known how long these organisms can survive in the soil in the absence of a host, thus new plant recruitment is severely affected as seedlings become infected and die before maturity. Further to this, given the trade-off between disease resistance and other fitness components, the competitive abilities of genotypes are altered during epidemics which may affect the genetic composition of populations (Alexander & Holt, 1998).

Concern about the impact of exotic plant pathogens in the wider UK environment has recently significantly increased after the discovery of infected plants in both heathland environments and commercial plantations. In 2008 P. kernoviae was discovered infecting wild heathland plants of blaeberry (Vaccinium myrtillus) in a Scottish woodland and Cornish heathland (FERA, 2009b), whilst P. ramorum was found on the same species in Staffordshire (FERA, 2009a). These infections have important implications for heathland biodiversity.

More recently, forest plantations have also been found to be infected with P. ramorum on Larix kaempferi (Japanese larch) (Brasier & Webber, 2010). As of July 2010, P. ramorum has been found in 68 larch plantations in England (Webber, et. al., 2010) and has also been found infecting this host in Wales and Northern Ireland. The main concern with larch infection, apart from the commercial implications, is that many other species have been infected as a result of growing in close proximity to the infected trees, the foliage of which is providing a platform for P. ramorum to sporulate heavily onto surrounding plants. The other species infected include Fagus sylvatica, Nothofagus obliqua, Castanea sativa, Betula pendula, Rhododendron ponticum, Tsuga heterophylla and Pseudotsuga menziesii (Webber, et. al., 2010).

The nursery trade throughout the world has had an important role both in the spread of pathogens from wherever they may originate, and in the spread of plant species on which the pathogens depend. This has certainly been the case in spreading P. ramorum but in contrast P. kernoviae has been found on very few occasions in nurseries. In the UK, the horticultural plant market is based on >73 000 plants species and cultivars, to which the native flora (~1500 species) make a negligible contribution (Perrings, et. al., 2005). Globally, this trade has been a major source of invasive species. In one infamous example of pathogen spread from the US in 2004, millions of Camellia plants infected with P. ramorum were shipped from west coast America to the east, involving 1200 nurseries in 39 states increasing fears of endangering the oak resource in the eastern United States (Stokstad, 2004). Studies using microsatellite markers have also shown frequent migration between Oregon, California and Washington state nurseries (Goss, et. al., 2009).

Given these problems, and that they are newly discovered, managing the spread of P. ramorum and P. kernoviae is very challenging. There are three management levels to consider: the individual plant, the landscape (or forest stand), and the regional to international scale (Rizzo, et. al., 2002), and each level poses its own set of challenges. A number of actions have been attempted in the past to control exotic pathogen invasions including widespread clear-cutting which was ultimately unsuccessful at stopping chestnut blight (Cryphonectria parasitica) across the north-eastern United States in the early 1900s (Anagnostakis, 1987), and the large scale removal of host material which was attempted for the control of white pine blister rust (Cronartium ribicola) (Kinloch, 2003).

Prior to the findings of P. ramorum and P. kernoviae in plantations and heathland, management had already proved very difficult in historic gardens such as Botanic Gardens and National Trust properties. Generally speaking, the nursery trade was more used to dealing with pests and diseases, along with the associated plant health measures involved, whereas historic gardens had not been as widely involved until the Phytophthora outbreaks, and DEFRA had no experience with dealing with the historic garden sector in this context (Tomlinson, et. al., 2009). The initial bad communication and slow realisation of the problem, the large number and variety of hosts in close proximity, a long tradition of plant collecting and plant swapping and, in some gardens, apathy towards the adoption of new hygienic horticultural techniques has certainly had a detrimental effect on some historic gardens that will persist into the future.

Sanitation programs have also been tried against a number of pathogens including Dutch elm disease (Ophiostoma ulmi, O. novo-ulmi) in North America and Europe, Phytophthora cinnamomi in Australia, and P. lateralis in Oregon and California (Cannon, et. al., 1977; Hansen, et. al., 2000; Hardy, et. al., 2001). Fungicides were also applied widely against P. cinnamomi in Australia to try to reduce the spread (Hardy, et. al., 2001). The success of these programs was very variable with some effective control on one hand, and continued tree mortality on the other.

Within the public garden setting, management has particular considerations and problems, such as the potential inadvertent spread of pathogens by visitors and staff. Management of infected plants in these gardens in the UK have so far focused on the eradication of infected plants upon their discovery (Tomlinson, et. al., 2009). The problem with eradicating the infected plants as soon as they are discovered is that this action reduces the opportunities for studying these pathogens in this particular ecosystem. The removal of R. ponticum from gardens and parks has started and this is an important measure to reduce hosts and therefore sources of inoculum.

Our understanding of the spread of infection within public gardens and from one garden to another is very limited. These aspects are critical if these pathogens are going to be managed successfully as the movement of people through public gardens could be spreading infection both within the garden and from one garden to another. Before effective management techniques can be developed, more research is needed into the epidemiology of these two Phytophthora species to increase our understanding of how they are spread.

References:

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