Abstract
The oomycete genus Phytophthora contains a large number of plant pathogens that cause significant damage to natural and agricultural systems. Until recently species have been distinguished using a limited set of morphological characters. The development of DNA-based technologies has revealed much broader and more complex diversity than previously recognised, and has led to the recent description of many new species. This review looks at the underlying mechanisms for the generation of diversity within the genus. The intercontinental movement and transplantation of infected plant material partially explains the appearance of new species in unexpected places. However, it is also likely that novel species arise as a result of the hybridisation and rapid evolution of introduced species under episodic selection pressures. Hybrid progeny may possess equal or greater virulence than parent species, thereby posing an increasing risk to our natural environment and agricultural production systems. These discoveries amplify the threats posed by the introduction of plant pathogens into new environments, and expose a crucial weakness in current evidence-based biosecurity regimes. Further work is required to identify hybrids, anticipate and understand the occurrence of hybridisation, and to implement appropriate quarantine and risk management measures.
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Introduction
The genus Phytophthora contains plant pathogens that cause significant damage to both agricultural and natural systems. DNA and RNA sequencing technologies have been used to describe new species responsible for recent ecologically and economically damaging disease outbreaks (Tyler et al. 2006; Haas et al. 2009; Runge et al. 2011; Grunwald et al. 2012; Yang et al. 2014). Consequently, about 70 of the 120 or so currently described species of Phytophthora have been added since 2000 (Fig. 1) (Érsek and Ribeiro 2010; Runge et al. 2011; Yang et al. 2014), and Brasier (2009) predicts there may be up to 600 extant species.
While new technologies have uncovered previously unrecognised diversity in situ, trade in infected plants has been linked to new confrontations in exotic environments (Brasier 2008; Davison et al. 2006; Fry et al. 1993; Grunwald et al. 2012; Ristaino 2002; Scott et al. 2013). Otherwise benign species have been shown to evolve rapidly when exposed to selective pressures in new environments, a phenomenon termed “episodic selection” (Brasier 1995). This selection, together with the potential for hybridisation of introduced and indigenous species, can lead to the rapid emergence of new or modified species.
The emergence of new Phytophthora species has very serious implications for biosecurity and risk management (Scott et al. 2013). In Australia for example, Phytophthora dieback has always been attributed to P. cinnamomi, however recent surveys of waterways in Western Australia, and soils in the Gondwana Rainforests of Eastern Australia, have identified the presence of numerous known and unknown Phytophthora species (Burgess et al. 2009; Daniel et al. unpublished; Huberli et al. 2013). This review will argue that, as well as new technologies that distinguish existing but morphologically similar species, the emergence of new Phytophthora species can be linked to globalisation and international plant trade, resulting in episodic selection, hybridisation and the rapid evolution of novel species, some with extended host ranges.
Identifying Phytophthora species
Traditionally, fungal and oomycete species have been identified on a limited set of morphological characters that may be homoplastic, and may vary with environmental conditions (Cooke and Duncan 1997; Cooke et al. 2000; Förster et al. 2000; Burgess et al. 2009). Consequently, morphology alone is now considered to be an unreliable indicator of identity and phylogenetic relationships (Burgess et al. 2009; Jung and Burgess 2009; Jung et al. 2011; Villa et al. 2006). Cooke et al. (2000) used rRNA Internal Transcribed Spacer (ITS) sequences to construct a 10-clade phylogeny that has since been supported by further DNA analyses (Blair et al. 2008; Runge et al. 2011; Yang et al. 2014). These molecular approaches have been vital in revealing the evolution and natural phylogeny of the genus.
Episodic selection as a force driving rapid evolution
The increased volume of world trade in plants has led to an increase in the spread of plant pathogens (Brasier 2008; Scott et al. 2013). Poor hygiene in nurseries, the use of systemic fungicides that suppress disease symptoms without eradicating the pathogen (Linderman and Davis 2006), and the use of recycled irrigation water may have further contributed to an increase in the regional and global spread of plant pathogens (Brasier et al. 2003; Huberli et al. 2013; Scott et al. 2013). The impact of these exotic plant pathogens may also be intensified due to habitat disturbance, climate change and pollution (Scott et al. 2013).
Within their natural distributions the coevolution of plants and their associated microbial pathogens has resulted in an evolutionary arms race that tends to dampen the severity of epiphytotics (Kaschani and Van der Hoorn 2011). Because the “founder effect” initially limits the genetic diversity of an introduced species, the lonely intruder may fail to survive and establish (Facon et al. 2006; Mayr 1942). Alternatively, the naïve host species may be at a disadvantage, not having co-evolved with the pathogen, and the invasion of a new environment may release the pathogen from environmental and host constraints, precipitating disastrous environmental damage and crop losses (Facon et al. 2006).
Consequently, the most destructive genotypes of the pathogen establish dominant founder populations. This is a particular issue if the virulent new pathogen is introduced into monocultures of an agricultural crop, where plants lack genetic diversity and tend to be bred for yield and robustness against current, rather than exotic, pathogens. There are countless examples of exotic plant pathogens causing disease epidemics throughout history, including the Irish Potato Famine in the mid-19th century (Ristaino 2002), the coffee rust epidemics in Ceylon (1870s) and Brazil (1970s) (Arneson 2011), the two Dutch elm disease pandemics in the 20th century (Heybroek 1993), Phytophthora dieback in Australia in the last 50 years (Podger 1968), and stripe rust of wheat in Australasia in the 1980s (Wellings and McIntosh 1990).
Under certain circumstances episodic selection of founder populations can lead to the rapid selection and evolution of introduced organisms (Brasier 1995; Man in’t Veld et al. 2007). Alternatively, episodic selection pressures such as geographic transposition, exposure to a new host, a new climate or different competition can lead to recombination and the generation of better adapted genotypes (Fig. 2) (Brasier 1995; Facon et al. 2006; Ahmed et al. 2012). In the case of exotic Phytophthora pathogens, episodic selection has already resulted in the emergence of more virulent strains and species that appear better equipped to target indigenous hosts (Bertier et al. 2013; Bonants et al. 2000; Goss et al. 2011).
How geographic transposition generates novel genotypes
The transport of Phytophthora isolates can lead to the emergence of novel genotypes and species through both sexual reproduction and hybridisation events, posing another serious risk to ecosystems and agrosystems. Typically, the introduction of isolates from a single mating type of a heterothallic species establishes clonal founder populations (Peters et al. 2014). However further introductions of infected plant material increase the probability of sexual reproduction through the introduction of compatible mating types (Drenth et al. 1994; Fry et al. 1993; Peters et al. 2014).
Sexual recombination generates genetic diversity, which, when followed by episodic selection pressures, inevitably results in progeny with enhanced fitness, virulence and host range (Drenth and Goodwin 1999; Wuethrich 1998). These “Red Queens” out-compete existing genotypes within the population, and pose real threats to ecosystems and agriculture around the world (Clay and Kover 1996).
Sexual reproduction in most heterothallic Phytophthora populations is apparently rare, even when both mating types are present, and clonal populations dominate (Linde et al. 1997). There is little evidence of sexual reproduction occurring amongst populations of P. cinnamomi in Australia or South Africa (Dobrowolski et al. 2003; Linde et al. 1997), P. palmivora and P. capcisi in the tropics (Drenth and Guest 2013; Truong et al. 2010) and P. nicotianae in the US (Parkunan et al. 2010).
However following the introduction of compatible mating types of P. infestans, recombinant strains quickly replaced previously established strains across much of the Northern Hemisphere (Cooke and Andersson 2013; Drenth et al. 1994; Gavino et al. 2000; Goodwin et al. 1998). In Poland the identification of a novel A2 isolate of P. infestans in 1989 was followed by sexual recombination, and by 1991, novel genotypes dominated the pathogen population (Sujkowski 1994). In North America, the introduction of the A2 mating type in the 1990s resulted in the proliferation of clonal lineages of the novel recombinants US-8, US-11, US-22, US-23 and US-24, believed to have resulted from crosses between US-6 and US-7 (Gavino et al. 2000; Halterman and Gevens 2013; Peters et al. 2014).
Hybridisation
Hybridisation may present an even more immediate and dangerous route to the emergence of new, virulent strains of Phytophthora (Brasier 2000). Phytophthora hybrids have been identified in clades 1, 6, 7 and 8 (Bertier et al. 2013; Bonants et al. 2000; Brasier et al. 2004; Goss et al. 2011; Nirenberg et al. 2009) and as identification techniques continue to improve, these numbers are predicted to increase (Érsek and Man in’t Veld 2013).
While hybridisation is known to occur naturally in populations of Fungi and Oomycota, the chances of it occurring increase following the removal of geographic barriers because previously allopatric species often lack the genetic barriers to mating found in co-occurring species (Brasier 1995; Brasier 2000). Indeed, all the Phytophthora hybrids identified to date have been the offspring of an exotic and a native species (Érsek and Man in’t Veld 2013). In addition to heterothallic species it has also been experimentally shown that homothallic species can outbreed to produce new virulence combinations (Whisson et al. 1994) and that hybridisation can occur between different homothallic species (May et al. 2003).
Hybrids can emerge sexually (Goodwin and Fry 1994), or through mitotic or parasexual recombination (Drenth and Goodwin 1999; Érsek et al. 1995). Successful fusion depends on a number of environmental and genetic factors, including the ability of the introduced taxon to compete in the new environment, the amount of niche contact between parent taxa and finally, their vegetative or sexual compatibility (Fig. 2) (Brasier 1995). Once hybrids form, further diversity may be generated from back-crosses with one or both parents, or as the result of subsequent recombination events and chromosome losses (Fig. 2) (Érsek and Man in’t Veld 2013).
Hybrid progeny can range from being marginally different to the parent species, or they can be entirely new species with a genome that is a combination of both parents (Fig. 2) (Brasier 1991; Donahoo and Lamour 2008). The offspring that possess a combination of chromosomal material from both parent species, sometimes in allopolyploid form, sometimes hybridised in diploid form, are of the greatest interest because of their potential to adapt to new environments and hosts compared to clonally produced offspring (Text Box 1) (Fig. 3). Often a range of genomic strains may result from one set of parents, as is the case with Phytophthora alni, where we see a “swarm” of allopolyploid genotypes (Ioos et al. 2006). Unlike the nuclear DNA, the mitochondrion is uni-parentally inherited in Phytophthora (Érsek and Man in’t Veld 2013; Whittaker et al. 1991). Therefore, while mtDNA cannot be used to identify hybrids, it can be used to identify at least one of the parent species (Man in’t Veld et al. 1998).
Pathogenicity
The genus Phytophthora has proven a challenging group of pathogens to control because of its ability to overcome host resistance (Haas et al. 2009; Bertier et al. 2013). It appears that hybridisation and the often-associated state of polyploidy may enhance pathogenicity (Text Box 1) (de Cock and Lévesque 2004; Jung and Burgess 2009; Rea et al. 2010; Sansome 1977; Sansome and Brasier 1974; Sansome et al. 1991; Win-Tin and DickDick 1975). Because human interventions increase the chances of hybridisation we can anticipate the emergence of novel plant pathogens.
There are many examples of enhanced virulence in hybrid plant pathogens. Often hybrid species are adapted to the combined geographic and host ranges of their parent species. For example, when crosses were made between poplar species Populus deltoides and Populus trichocarpa in the 1980s for commercial purposes, their associated rust pathogens Melampsora medusae and M. occidentalis also appeared to have hybridised (Newcombe et al. 2000). These hybrid pathogens attack both parental species as well as the hybrid. Furthermore, introgression may extend the host ranges of each parental species (Brasier 2001).
Indeed, another risk associated with hybrids is that they can act as genetic bridges between the two previously geographically isolated parental populations, allowing the transfer of virulence genes (Newcombe et al. 2000; Brasier 2001). The two Dutch elm disease pathogens Ophiostoma ulmi and O. novo-ulmi appear to have formed transient hybrids at the epidemic fronts that transferred biologically useful loci from O. ulmi to the more virulent O. novo-ulmi (Brasier et al. 1998).
Finally, hybrids may possess novel virulence. Hybrids of Phytophthora cambivora, a pathogen of hardwoods, with P. fragariae, a pathogen of strawberry and raspberry, acquired virulence on alder, a host that neither of the presumptive parents are able to attack (Érsek et al. 1995; Brasier et al. 1999). Similarly, hybrids of P. hedraiandra and P. cactorum colonise species beyond the host range of either parent (Man in’t Veld et al. 2007).
Recently, the genetic mechanism behind the adaptability and virulence of Phytophthora has been partially unveiled. Like many plant pathogens, Phytophthora species secrete effectors that modify host plant physiology to facilitate colonisation (Haas et al. 2009; Whisson et al. 2007). Both Crinkler (CRN) cytoplasmic effectors and RxLR effector proteins are considered to be major determinants of host specificity and virulence in Phytophthora (Bertier et al. 2013). The genes controlling the relevant effectors are contained in highly variable, gene-sparse and repetition-rich regions of the genome (Haas et al. 2009). This allows homologous recombination between effector gene regions to occur without a high risk of lethality (Bertier et al. 2013). This process is likely to have led to the diversity and abundance of RxLR and CRN genes observed in Phytophthora species (Haas et al. 2009). These dynamic and expanded effector repertoires may enable the pathogenic adaptability of the genus (Vercauteren et al. 2011; Bertier et al. 2013).
Evolutionary implications
Hybridisation and allopolyploidy enable adaptation and speciation and are considered important forces in the evolution of Angiosperm plants, as well as in the evolution, speciation and pathogenicity of Phytophthora (Bertier et al. 2013). Recent analysis showing the presence of many small duplicated blocks of two or three consecutive genes indicates that an ancient whole genome duplication (WGD) created a polyploid ancestor that evolved into P. infestans, P. sojae and P. ramorum (Martens and Van de Peer 2010). Many of the duplicated genes were related to pathogenicity and infection, which suggests that the WGD contributed to the pathogenicity of the genus (Martens and Van de Peer 2010).
Further, evidence suggests newly developed hybrids continue to evolve rapidly (Goss et al. 2011). Evolving strains have now been identified in at least three Phytophthora species (P. alni subsp. alni, P. nicotianae × P. cactorum and P. hedraiandra × P. cactorum) (Man in’t Veld et al. 2007; Érsek and Man in’t Veld 2013). This continuing evolution occurs through intercrossing, introgression, mitotic chromosomal rearrangements and chromosome loss (Érsek and Man in’t Veld 2013). With their short life cycles, the rapid evolution of Phytophthora pathogens gives them a competitive advantage in the evolutionary arms race over their relatively slower evolving hosts, and biosecurity protocols (Clay and Kover 1996; Wuethrich 1998; Érsek and Man in’t Veld 2013).
Future directions
This review highlights the pressing need to improve our capacity to identify and describe Phytophthora hybrids, and exposes a serious flaw in current biosecurity protocols. Due to their rarity, atypical phenotypes and limited number of robust morphological characters, Phytophthora species are often difficult to distinguish (Brasier et al. 1999; Érsek and Man in’t Veld 2013). For example, while P. multivora was only recently described in Western Australia using ITS sequencing, it was found to be abundant in historical collections where it had been mistaken for the phenotypically similar P. citricola (Scott et al. 2009). Phytophthora multivora was found to be the second-most widespread Phytophthora species in Western Australia after P. cinnamomi, and at many sites it is P. multivora rather than P. cinnamomi that causes tree mortality. This finding has significant implications for controlling the spread of Phytophthora dieback.
Although molecular techniques provide better resolution for distinguishing hybrids and species, they are not always reliable. ITS-based techniques, for example, may homogenise hybrid rDNA arrays (Brasier et al. 1999; Bertier et al. 2013). Therefore to confidently distinguish species and hybrids it is necessary to analyse several independent loci in conjunction with morphological and physiological assessments (Man in’t Veld et al. 2007).
Additionally, following identification, there remains the issue of how to taxonomically name and define hybrids or hybrid complexes for legal and biosecurity purposes (Brasier et al. 1999). As more hybrids are described it becomes increasingly important to improve detection methods and develop consistent rules for nomenclature.
There is also much to be learnt regarding the rapid evolution and hybridisation of introduced Phytophthora species and other pathogens. For instance, a better understanding of the factors leading to hybridization, regulating virulence and host range in hybrid progeny and an understanding of how novel traits arise in hybrid progeny is required. For example, many examples of hybridisation appear to have occurred in water, either following heavy flooding or in hydroponic systems (Érsek and Man in’t Veld 2013). Such research will lead to better risk assessment and management of novel pathogen species.
Novel Phytophthora species and hybrids pose a serious biosecurity threat as trade in plant material inevitably increases. Biosecurity and control protocols focus on the risks posed by known, rather than unknown pathogens (Brasier 2008; Scott et al. 2009). Yet, the examples of P. ramorum and P. cinnamomi, amongst others, show that species that are benign in their centre of origin can become destructive in new environments as the result of episodic selection, hybridisation or perhaps through becoming part of a novel disease complex (Brasier 2008). Even when pathogens are known as minor pathogens in certain parts of the world the occurrence of hybridization among endemic and exotic species may produce hybrid species with novel pathogenicity and virulence characteristics as has been shown for the Phytophthora on alder (Brasier and Kirk 2001; Érsek et al. 1995). These organisms are difficult to detect in their native environments because native hosts show few or no symptoms of disease, and so are overlooked during the risk analysis processes. The current biosecurity system and their current basis for risk assessment must therefore be revised to consider the potential for benign microbes to cause damage when introduced to different environments.
Conclusion
The emergence of new, highly virulent Phytophthora species in unexpected places, whether they are undescribed or previously known, has fundamental implications for current biosecurity and control practices. There is now a strong body of evidence to suggest that exotic species have the capacity to evolve rapidly, sometimes via hybridisation, and that this process can lead to enhanced pathogenicity and virulence (Brasier 1995; Newcombe et al. 2000; Brasier 2000). Although hybridisation has probably always been an important evolutionary force for Phytophthora, the probability that it will happen increases as more infected and uninfected plants are traded and planted outside their natural geographic range, and new diseases may arise as a result. This review highlights the importance of continued monitoring of natural and anthropomorphised systems in order to identify novel Phytophthora species, their ecological role and if applicable, their pathogenicity. Assessment of risk and assessment of impacts due to introductions of exotic Phytophthora species and the consequences of hybridisations needs to be taken in consideration by Biosecurity agencies if they desire to make sound decisions based on established principles of invasion biology.
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Acknowledgments
We thank Professor André Drenth for his insightful and constructive discussions and comments.
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Novel pathogenic Phytophthora species are emerging as the result of the rapid evolution of introduced species, and pose an increasing biosecurity risk.
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Callaghan, S., Guest, D. Globalisation, the founder effect, hybrid Phytophthora species and rapid evolution: new headaches for biosecurity. Australasian Plant Pathol. 44, 255–262 (2015). https://doi.org/10.1007/s13313-015-0348-5
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DOI: https://doi.org/10.1007/s13313-015-0348-5