Research review. Rust fungi and global change. Review. Summary. Introduction

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1 Review Rust fungi and global change Author for correspondence: Stephan Helfer Tel: Stephan Helfer Royal Botanic Garden Edinburgh, 20A Inverleith Row, Edinburgh EH3 5LR, UK Received: 24 July 2013 Accepted: 28 September 2013 doi: /nph Key words: biogeography, fungal conservation, global change, pathogens, Pucciniales (rust fungi). Summary Rust fungi are important components of ecological communities and in ecosystem function. Their unique life strategies as biotrophic pathogens with complicated life cycles could make them vulnerable to global environmental change. While there are gaps in our knowledge, especially in natural plant rust systems, this review of the exposure of rust fungi to global change parameters revealed that some host rust relationships would decline under predicted environmental change scenarios, whereas others would either remain unchanged or become more prevalent. Notably, some graminicolous rusts are negatively affected by higher temperatures and increased concentrations of atmospheric CO 2. An increase of atmospheric O 3 appears to favour rust diseases on trees but not those on grasses. Combined effects of CO 2 and O 3 are intermediary. The most important global drivers for the geographical and host plant range expansion and prevalence of rusts, however, are global plant trade, host plant genetic homogenization and the regular occurrence of conducive environmental conditions, especially the availability of moisture. However, while rusts thrive in high-humidity environments, they can also survive in desert habitats, and as a group their environmental tolerance is large, with no conclusive change in their overall prevalence predictable to date. Introduction Rust fungi (Uredinales or Pucciniales) are a globally distributed order of obligate parasitic fungi occurring on vascular plants. With c species (Toome & Aime, 2013), they constitute a component of global biodiversity. As biotrophic plant parasites they are believed to be crucial as drivers for community dynamics and diversification through co-evolution with their host plants (Gilbert, 2002). They strongly influence vegetation composition and plant community structure when they occur in epidemics (Dobson & Crawley, 1994). By reducing the photosynthetic potential of their hosts and by diverting and metabolizing photosynthesate in their own biomass, they reduce the carbon sequestration of their host plant communities. In energy plantations, for example, dry matter yield losses in excess of 40% have been recorded following rust infections (Dawson et al., 2005). Despite their potential ecosystem importance, the effect of global change on rust fungi has so far not been considered in detail (Desprez-Loustau et al., 2007b). Within climate change parameters, temperature, humidity and leaf wetness are important in rust establishment on host plants, and solar radiation and air turbulence are significant variables for the dispersal of propagules. The Intergovernmental Panel on Climate Change (IPCC) has published reports on recent climate variability and produced climate projections on indices, based on contrasting scenarios (IPCC, 2007). Abiotic as well as biotic factors have been considered, and changes in the incidence and severity of pests and diseases of humans, animals and plants are monitored (Tegart et al., 1990; Luck et al., 2011) and have been modelled for future decades (IPCC, 2007). Data on pathogen interactions indicate significant impacts of global change on human wellbeing through the negative effects of plant diseases and pests. While some projections predict increases in crop pathogen range as a consequence of extreme events (Rosenzweig et al., 2001), others focus on increased pathogen reproduction and survival as a consequence of more favourable general climatic conditions (IPCC, 2007; Hicke et al., 2012). Rust fungi, while having been included in impact models for crop plants (Mitchell et al., 2003; Luck et al., 2011), and as pathogens, have not been considered as distinct elements in global change scenarios. The aim of this review is to fill this gap in the present state of 770

2 New Phytologist Review 771 knowledge, by focussing on rust fungi as a case study plantpathogen system. Evidence obtained since the middle of last century suggests that reported threats to plant health as a result of new disease outbreaks have been increasing (Fletcher et al., 2010; Black, 2013). Google Scholar search hits for new reports on plant disease number 512 for the 30 yr from 1961 to 1990 and more than three times as many (1670) in the 22 yr from 1991 to Rust fungi feature in at least six and 39 of these reports, respectively, representing a ninefold annual increase. While these metrics are problematic as only papers in English were considered, the trend appeared to be the same when the search was restricted to Anglophone regions such as the USA, India or the UK. Many of these new occurrences are attributable to introductions through the movement of infected plants, rather than to natural extension of the range because of climate change. Occasionally they represent pathogen organisms new to science. However, preliminary data suggest an additional role for climate change in the provision of new suitable climate space for disease incidence, leading to range extension (Desprez-Loustau et al., 2007a), as well as facilitated natural dispersal of plant pathogens, possibly through the occurrence of extreme weather events (Rosenzweig et al., 2001; Fletcher et al., 2010). This review first introduces the biology of rusts and their relevance in provisioning ecosystem services, before providing an overview of the impact of human-induced global change on these fungi. This introductory section is followed by evidence relating different aspects of global change to the biology of rusts, providing a platform with which to understand how these plant pathogens both respond to the drivers of anthropogenic change and are themselves an important feedback in regulating the structure of natural ecosystems and influencing their functioning. Rust fungi The rust fungi (Uredinales or Pucciniales) are an order in the highly diverse phylum of Basidiomycota, which includes the well-known mushrooms and bracket fungi and encompasses some described species (Kirk et al., 2008). Rusts are obligate biotrophic and exclusively pathogenic fungi on vascular plants, including ferns, gymnosperms and most families of angiosperms. They are present in all terrestrial ecosystems containing plants. Their exploitation of living host plant tissues is known to result in extensive damage to agricultural and forestry crops (see e.g. Park & Wellings, 2012) as well as causing recurrent low to medium levels of disease in native plant populations (Dinoor & Eshed, 1984; Burdon et al., 2006). Rust fungi are globally represented in c. 166 genera and 14 families (Kirk et al., 2008). The majority of species occur in the genera Puccinia and Uromyces, for which over 5000 and 1500 taxon names are listed, respectively, in Index Fungorum (2013). Recent results of molecular analyses of rust DNA confirm that these two genera are polyphyletic, a fact that was already suspected by Tulasne (1854) (Maier et al., 2003, 2007; Van der Merwe et al., 2007), and further research is needed to elucidate the natural relationships within the rust fungi (Aime, 2006). Many rust species exhibit complicated life cycles (see Fig. 1) with variable host plant specificity (Anikster, 1989). As actively growing rusts cannot n IV R! 2n survive unfavourable conditions on dead plant tissue, resting teliospores are normally produced at the end of the growing season and numerous rusts have annual life cycles. A common feature in many rusts is a heteroecious life cycle, requiring two exclusive and unrelated host plant taxa for their completion, as illustrated in the well-documented example of wheat stem rust on species of Berberis (barberry) and Triticum (wheat). This life cycle can comprise up to five spore stages (Cummins & Hirastuka, 2003) as shown in Fig. 1. As well as being of general biological and ecological importance, this survival strategy poses interesting questions in the gene regulation and transcriptomics of virulence genes which confer access to the host plants carbon and nutrient resources. Heteroecious rust fungi are incapable of infecting the alternate host during parts of the life cycle, while possessing all the genetic information to do so (Feau et al., 2007). Notwithstanding ecological constraints imposed by the requirement for two sympatric host species, the success of the rust life strategy is evidenced by the common occurrence of rusts in natural ecosystems and occasional catastrophic losses among crop plants in agricultural settings. In cereals, reduction in crop production attributable to rust fungi can amount to an estimated 75% in some areas (Rapilly, 1979; Eversmeyer & Kramer, 2000), and losses to legume crops can often be as much as 50% in developing economies, where fungicidal control is not normally available (Tissera & Ayres, 1986). Global change Basidia (meiospores) K! Telia (resting) III 0 Spermogonia (spermatia) Aecia (dikaryon) Uredinia (repeating) n+n I Fig. 1 Typical life cycle of rust fungi: for heteroecious macrocyclic rusts, stages 0 and I are on the aecial host, and stages II and III on the telial host; stage IV develops on germination of teliospores. Meiosis (reduction division, R!), producing haploid (n) spores follows immediately after the fusion of nuclei (karyogamy, K!; 2n) in germinating teliospores; plasmogamy (P!), leading to dikaryotic (n+n) cells, follows after the transfer of spermatia to compatible receptive hyphae in the spermogonia. Autoecious rusts remain on only one host throughout; hemicyclic rusts omit stages 0 and I; demicyclic rusts omit stage II; microcyclic rusts omit stages I and II; endocyclic rusts produce stage III (telia) morphologically resembling stage I and omit stage II. Anthropogenic climate change and global warming are by-products of many human activities to have caused significant alterations of the ecology of the earth; together with other human impacts, these long-term effects may be considered as anthropogenic global change (Sala et al., 2000). Land use changes through P! II

3 772 Review New Phytologist agriculture and plantation forestry have caused natural habitat loss and impacted on the distribution of plants world-wide (Walker & Steffen, 1996). The associated use of agrochemicals, especially fertilizers, herbicides and pesticides, has affected nutrient availability and survival of plants, animals and fungi, both in humandominated environments and in contiguous natural landscapes through secondary deposition (Wolters et al., 2000). Agrochemical drift and pollution have changed the chemistry of water, air and soils, shifting the compositional structure of ecosystems in adaptation to new resource limitations (Johnson et al., 2013). Elevated concentrations of CO 2 and O 3 have direct effects on plants, associated arthropods and microbes (Lindroth, 2010; Bissett et al., 2013). Urbanization, transport and infrastructure developments, mining and other land use changes have further impacted on vulnerable habitats (Harris et al., 2009; Benıtez-Lopez et al., 2010). Notably, road building has led to fragmentation of habitats and provided channels of incursion for invasive species (Chornesky et al., 2005). Furthermore, international trade, including the cultivation of exotic species in gardens and parks, and worldwide travel have led to the establishment of invasive alien species as weeds, pests and pathogens (Pysek et al., 2011) as well as the introduction of plant disease vectors (Johannesen et al., 2012). Climate change adds a further dimension to this matrix of impacts: while some organisms may be able to acclimate or adapt in situ to these pressures, others will become increasingly rare and may suffer regional or global extinction (Brown & Hovmøller, 2002). Climate change effects on rusts are discussed later. The concept of disease escape Rust species are limited in their distributions by their host plant ranges. However, it has been suggested for some plant species that large areas of their range may have remained free from rust infection until the recent past as a result of disease escape phenomena (Agrios, 2005). Plant diseases are only possible when susceptible host plants, virulent pathogens and conducive environmental conditions are coincident at the same time (Barrett et al., 2009; Garrett et al., 2009). Where disease escape has currently been maintained because of unfavourable environmental conditions, climate change is now a relevant factor which may be instrumental in the widening or narrowing of the range of rust fungi. In other instances the transport of susceptible host plants and virulent rusts, for example by the unintentional introduction of diseased plants into a hitherto disease-free host plant range, has caused extensive new disease epidemics. Examples include the continued spread of coffee rust (Hemileia vastatrix) in coffee (Coffea sp.) plantations world-wide (McCook, 2006), and the white pine blister rust (Cronartium ribicola) which has been epidemic in the native ranges of North American white pines (Pinus sp.) for almost a century (Kim et al., 2010). This review discusses the role of various factors which control the biogeography, distribution and ecological impact of rusts, and which must be considered in managing rust diseases during a period of global change. Table 1 shows examples of changes to rust fungi that have occurred as a consequence of current global change and that are expected for future change scenarios. These factors are divided into: (1) host constraints; (2) rust host co-evolution; (3) dispersal; and (4) abiotic variables, including climate. Host constraints Rusts distributions are limited by the availability of a normally relatively small natural range of host plant species, whose distribution is governed by various ecological factors. Dramatic host range expansion potentials have been reported for alfalfa rust caused by Uromyces striatus (Skinner & Stuteville, 1995) and the rust of South American Myrtaceae Puccinia psidii (Carnegie & Lidbetter, 2012; Morin et al., 2012; Kriticos et al., 2013). In the first example, 141 (out of 345) taxa from 11 genera of legumes (out of 27 genera) were found to be susceptible to single uredinial isolates (clones) of the rust on first encounter (these plants had not co-evolved with the pathogen) (Skinner & Stuteville, 1995). The second example revealed the susceptibility of 129 species in 33 genera of Myrtaceae in Australia to a rust native to Brazil and Central America (Kriticos et al., 2013). These range expansions are facilitated by human-caused dispersal of plants and pathogens. Interestingly, in the case of P. psidii, the rust had recently been considered as a potential biocontrol agent against an invasive tree in Florida (Rayachhetry et al., 2001). The natural distribution and frequency of plants are determined by variables of abiotic (climatic, edaphic), community (symbionts, competitors, predators) and autogenic factors (diversity, plasticity, dispersal mechanisms, adaptive evolution). Climate change clearly presents a major factor for future plant distributions, and bioclimatic envelope models have been used to predict these (Pearson et al., 2002). Questions have been raised about the usefulness of bioclimatic envelope models for single-species modelling for local-scale distributions (Davis et al., 1998), an important concern in the modelling of future host ranges for heteroecious rusts. However, Pearson et al. (2002) contended that climatic envelope models are appropriate at larger spatial scales (regional to global) and edaphic and biotic factors play more important roles at the higher resolution local scales ( m) (Seem, 2004). It is significant that coarsegrained model projections for shifts in distribution are consistent with observed trends: a vegetation altitude shift of 65 m was observed by Kelly & Goulden (2008) in California over a 30-yr period and similar range shifts have been documented for plants in Europe (Lenoir et al., 2008; Wipf et al., 2013). Range shifts of this magnitude and speed have been heralded as strong indicators of possible future biodiversity loss for high montane species (Engler et al., 2011; Dullinger et al., 2012). However, these trends are difficult to generalize and down-slope shifts have also been observed. These have been explained by biotic competition changes rather than increasing temperatures (Lenoir et al., 2010), illustrating the complexity of ecological interactions. Several studies have applied bioclimatic modelling to interacting organisms, for example, butterflies with their host plant range (Schweiger et al., 2012), incorporating interactions in species distribution models (SDMs) (Wisz et al., 2013), thereby indicating that models to examine the distribution of rust host plants may also have merit. This approach may be limited in practice, as there are few rust fungi whose distribution is adequately documented. Most rust

4 New Phytologist Review 773 Table 1 Examples of potential changes to the impact of rust fungi as a result of global change Change parameter Potential change Examples of affected rust taxa References Climate warming Increased pathogen survival Puccinia graminis on Pfender & Vollmer (1999) cereals and grasses Phakopsora pachyrhizi on soybean crops Park et al. (2008) Restricted pathogen survival Puccinia striiformis on cereals Roelfs et al. (1992); Garrett et al. (2006) Uropyxis petalostemonis on white clover Worapong et al. (2009) Higher humidity Increased disease incidence Hemileia vastatrix on coffee Cressey (2013) Extreme weather Enhanced air borne spore dispersal Many species Zambino (2010); Nascimento et al. (2012); Brown (1997) Water dispersal Chrysomyxa weirii Crane et al. (2000) Spread of alien Increased geographical range Puccinia hieracii McKenzie (1998) plants or rusts Phragmidium ivesiae Savile (1976) Increased host range Puccinia psidii Morin et al. (2012) Cronartium ribicola See Farr & Rossman (2013) Genetic recombination and somatic hybridization Melampsora, Cronartium and Puccinia Park & Wellings (2012); Desprez-Loustau et al. (2007b) Increased CO 2 Increased/restricted pathogen fitness Graminicolous rusts Bencze et al. (2013); Tiedemann & Firsching (2000) Unchanged pathogen fitness Poplar rusts Karnosky et al. (2002) Increased O 3 Increased pathogen fitness Poplar rusts Karnosky et al. (2002) Decreased rust fitness Wheat rusts Tiedemann & Firsching (2000) distributional data records are extracted from herbarium collections (GBIF, 2013). The most frequently recorded species are, unsurprisingly, rusts of crop plants (Farr & Rossman, 2013). There are, however, endemic rust species on island archipelagos such as Hawaii (Gardner, 1994) and New Zealand (McKenzie, 1998) which, because of the limited distribution of their host plants, may provide opportunities for testing bioclimatic models. Furthermore, species such as Uredo puawhananga G.T.S. Baylis have since spread to introduced alien plants and are potentially invasive aliens elsewhere. They may provide opportunities to compare a species realized bioclimatic niche in its native host range with its potential spread in new environments and via host range expansion (McKenzie, 1998). The spread of white pine blister rust Cronartium ribicola across the North American native range of five needle pines demonstrates that a pathogen may by far exceed previous expectations based on its native host range (Newcombe & Dugan, 2010). Fungal aggressiveness as expressed by the speed and success of fungal reproduction at a cost to host plant fitness is a major factor in the invasiveness of rust fungi, as shown in the soybean rust caused by Phakopsora pachyrhizi (Rossman, 2009). Furthermore, it has been demonstrated that relatively harmless endophytes or mildly parasitic fungi may become aggressive pests when host plants suffer from other biotic or abiotic stresses such as those potentially caused by climate change (Manter et al., 2005). Conversely, it is possible that climate change effects may increase plant resistance to rust fungi, especially when these are limited by their moisture and temperature requirements. In crop diseases, such increased plant resistance has been shown in the wheat yellow rust system (Chakraborty et al., 2011; Luck et al., 2011). Host rust co-evolution and specificity As with other biotrophic pathogens and pests, rust fungi are presumed to have co-evolved with their host plants (Thompson & Burdon, 1992; Giraud et al., 2008). The following forces are at play: the parasite makes use of the host plant s resources, causing a fitness cost to the plant; the host plant then advances a defence system against the pathogen; irrespective of the nature of this defence (either constitutive or induced), there is a cost to the plant, and a balance between the fitness costs of parasitism and defence ensues (Barrett et al., 2009). Furthermore, pathogenicity, as well as providing access to resistant hosts, can carry costs to pathogens, superfluous virulence being detrimental to their fitness (Laine & Barres, 2013). Heteroecious rust fungi exemplify plant parasites specialized in sympatric ecological relationships with two unrelated host plant species and normally exerting pressures on both, proportional to the negative impact of each stage; similar parasitisms are known from animal pathology (Otranto & Traversa, 2003; Arora, 2012). This co-evolution is on-going and new rust host relationships arise frequently (Qi et al., 2011), especially where major gene host plant resistance has been identified, exploited and introduced at large scales in agricultural crops. Flor (1942) famously described the gene-for-gene relationships of Linum (flax) and its rust Melampsora lini. Nevertheless, host specificity still represents a barrier to rust range expansion, and background levels of plant diversity normally contain rust infection (Roscher et al., 2007). Pronounced host specificity is therefore a limiting factor, especially considering the dependence of heteroecious rusts on the timely occurrence of three critical elements: (1) the presence of two unrelated and susceptible host species within proximity; (2) the successful mechanisms for spore dispersal between the host plants at the appropriate time in the respective life cycles of both rust and hosts; and (3) the prevalence of favourable environmental conditions during both infection periods. Mechanisms of co-evolution and host specificity are a key area in the response of rusts to global change, and have strong relevance to biological homogenization of floras and the erosion of biodiversity. As Newcombe & Dugan (2010) report, the problem with plant

5 774 Review New Phytologist (and pathogen) introductions is not a new one. From the beginning of agriculture c yr ago, plants have been moved into new habitats, selected for beneficial traits and thus restricted in their natural diversity. The range and movement of plants was initially local and along well-known trade routes (Farrington & Urry, 1985). It has increased strongly since the first global circumnavigations in the 16th Century and the rate and speed of plant movement have again increased dramatically in the last century with modern transport developments (Stukenbrock & McDonald, 2008). The internet and global free trade have brought another step change to the movement of plants and plant products during the past two decades (Meissner et al., 2009). Within the context of floristic change, rusts with narrow host ranges are clearly less prone to be invasive compared with those that exhibit a wide range of hosts (Carnegie & Lidbetter, 2012). However, this is not the case where the hosts are common, susceptible and of low genetic diversity, as in many crop plant species. For instance, the coffee rust Hemileia vastatrix is of relatively low importance in its natural range in Ethiopia. This is probably because of the low rainfall in this part of Africa (McCook, 2006) in addition to established natural resistance in the host. When faced with a densely growing cultivated host of low genetic diversity in a moist and warm climate, the rust spreads explosively, however, and has rendered coffee cultivation uneconomical in several regions of the world (Ridley, 2011). The reproductive success of this rust fungus has in turn led to nonspecific hyperparasitism by another fungus, the dual entomoand mycopathogenic species Lecanicillium lecanii, aided by invertebrate vectors (Vandermeer et al., 2009). There are indications that the evolution of new pathogenicity traits in a number of agricultural pathogens has accelerated in the recent past (Stukenbrock & McDonald, 2008). Where the fungus exhibits a wide host range, the possibility of invasion of new territories and host species can lead to serious concerns. Puccinia psidii is a native rust of guava (Psidium guajava) in South America, causing only minor damage to the original native host (Coutinho et al., 1998). Introductions of Australian Eucalyptus trees into its native range have provided the pathogen with the opportunity to spread to other members of the Myrtaceae, where it now poses a considerable risk to many host plant species in their native ranges, for which susceptibility has been established in trials (Glen et al., 2007). Puccinia psidii has since been accidentally introduced to Australia and shown to be of major plant health concern, with 107 new host species in Australia (Carnegie & Lidbetter, 2012). As rust fungi and similar pathogens have short generation times spanning weeks or months, combined with vast numbers of propagules (Helfer, 1986; Newton et al., 1999; Pringle & Taylor, 2002), their adaptive and evolutionary potential is relatively great, when faced with rapid environmental change. Many host plants, in contrast, have generation times of several months (herbaceous plants) to many years (trees) and reproduce far less numerously, giving them fewer opportunities for adaptation or evolution and resulting in loss of overall fitness. Fast anthropogenic dispersals of rusts and similar pathogens to new hosts and territories, combined with rapid climate change, are therefore expected to lead to repeated disease outbreaks and possibly host extinctions, as shown in the global amphibian chytridiomycosis crisis (Kilpatrick et al., 2010). Dispersal It has been shown that host plant range acts as a strong environmental filter in the distribution of rust fungi. However, a second key mechanism explaining microorganism biogeography is spore dispersal (Fr ohlich-nowoisky et al., 2012). Heteroecious rust fungi disperse between the alternate hosts by means of basidiospores (from telial hosts to aecial host) and aeciospores (from aecial host to telial host) (Cummins & Hirastuka, 2003). Dispersal between individuals of the telial hosts is normally effected by urediniospores in repeated short succession generations (see Fig. 1). There is not normally infectivity between aecial hosts, and spermogonia function as sexual organs in the exchange of spermatia between mating types. During the first part of the life cycle, the delicate hyaline basidiospores of rust fungi are normally wind dispersed. They are produced on germinated teliospores located either in the tissue of the host plant or dispersed independently from the tissue and are actively discharged into the air stream. Basidiospores are of a similar size to small water droplets (10 20 lm diameter). High humidity and a narrow temperature range are necessary for the spores to survive. These spores normally have a dispersal range of c. 300 m (Kinloch, 2003) but can be carried much further on occasional turbulent moist airstreams at night (up to 8 km according to Van Arsdel, 1967; Zambino, 2010). Spermatia are produced in spermogonia in the tissue of the aecial host plant. They are again small, hyaline and vulnerable to desiccation and UV damage. Not having infectious potential, they are the sexual spores, leading to the dikaryotization of the rust mycelium. Spermatia are normally insect-dispersed (Roy, 1994). In the Puccinia arrhenatheri Berberis vulgaris pathosystem, Naef et al. (2002) observed Diptera from 11 different families as main spermogonium visitors, with Hymenoptera (mainly ants) and spider species also involved. Considering this diversity, it is unlikely that environmental change (short of the catastrophic decline of arthropods generally) would affect this outcrossing mechanism of rust fungi. Aeciospores, produced in the aecial host tissue, by contrast are larger, often thick-walled and more resistant to environmental challenges. Their size, however, often in excess of 25 lm, has been reported to limit their dispersal to a few tens of metres (Barnes et al., 2005), depending on both vegetation characteristics and climate, with small numbers of aeciospores travelling > 400 m from the aecial host. The extreme dispersal of 720 km for Cronartium ribicola, attributed to Mielke (1943) by Kinloch et al. (1998) has been arrived at by deduction, and not experiment. However, viable aeciospores and urediniospores have been intercepted in air currents at heights exceeding 300 and 2000 m, respectively, altitudes at which long-distance dispersal in high winds is possible. In some special adaptations, insects are the carriers of spores, as some rusts induce their hosts to produce pseudo-flowers which mimic the flower scent in order to attract insect vectors (Roy, 1994; Kaiser, 2006). Urediniospores are the repeating spores on the telial host. They are produced in vast numbers and represent the spore stage with the highest dispersal potential, generally being considered as the agents

6 New Phytologist Review 775 of rust epidemics in many crop plants (Nascimento et al., 2012). Spore sizes are c lm diameter and many species have urediniospores with thickened cell walls and fine spines, promoting long-distance dispersal in air currents (Brown, 1997; Wang et al., 2010) and by attaching themselves to animals or other moving objects (vehicles, tools or luggage). In optimal conditions, these spores can travel for thousands of kilometres, as has been shown in the spread of new virulent wheat rusts within Europe (Hovmøller et al., 2002) and soybean rust from Asia to Africa, to South America and finally to North America, with potentially devastating consequences for soya production (Isard et al., 2005). However, this longdistance dispersal is only successful if the appropriate host plants are available at the destination, and most global dispersal events are at least partly caused by human actions (crop plants of narrow genetic base, movement of infected plants, or movement of inoculum on clothes/vehicles/tools) (Gregory et al., 2009; Ono, 2012). The dispersal potential of the final, teliospore stage of rusts is limited by the fact that many species produce sessile teliospores and also that teliospores are commonly the largest spores with reduced wind dispersal potential. Teliospores are normally thick-walled, long-lived, often dark-coloured and relatively resistant to desiccation and UV radiation (Brown, 1997). However, teliospores can be dispersed in detached host plant tissues (grass stems or leaves of tree hosts), and storm dispersal is possible. Additionally, water dispersal has been observed in rust teliospores of Chrysomyxa weirii (Crane et al., 2000). Abiotic variables There is no clear indication that rusts have expanded their host ranges as a result of climatic factors alone; however, their incidence and epidemic severity are correlated with relative humidity and leaf surface moisture. Optimal temperature requirements of rusts are variable between species, and it can be expected that warming temperatures will have an effect on the distribution of species (Luck et al., 2011) in two opposing settings. While milder winter temperatures, on the one hand, appear to be the main factor explaining rust survival for a number of warm temperate host rust relationships, high summer temperatures, on the other hand, may be restricting the infection potential in other host rust pathosystems. As rust infection is also dependent on a range of other climatic factors including relative humidity and leaf wetness during critical periods in the infection process, a spectrum of outcomes can be anticipated from projected climate change scenarios, keeping in mind, however, that many rust species occur in desert environments (Zhuang, 1989). For instance, current epidemic levels of coffee rust caused by Hemileia vastatrix in the Neotropics have partially been attributed to climate change (Cressey, 2013). Temperature The majority of data about plant disease and climate are relevant to agricultural crop plants (Evans et al., 2010; Roos et al., 2011). It is generally believed that warmer climates will lead to higher disease incidence (Evans et al., 2008), although this effect may be compensated for in high latitudes and high-altitude areas by increased primary production of the host plant. Elevated concentrations of CO 2 are also believed to significantly increase plant primary production (Ainsworth & Long, 2005) and, finally, the physiological effect of climate change on host plants may play an important role. Rusts that may increase in their incidence through global warming include the stem rust of tall fescue (Festuca arundinacea) and perennial ryegrass (Lolium perenne) Puccinia graminis subsp. graminicola, as it does not survive winter temperatures below 13 C (Pfender & Vollmer, 1999); milder winter temperatures may therefore extend the spatial-temporal range of this disease. Similarly, the rust Phakopsora pachyrhizi of soya beans (Glycine max) appears to maintain the ability to cause infection even following extended winter conditions in the main soybean production areas of the USA (Park et al., 2008), a fact that is of serious concerns to soybean producers. Currently this rust is of lesser importance in more northern areas of soybean production and needs to reinvade these areas annually. Warmer winters could change this situation, giving the pathogen an earlier start. As world production of soybeans was 261 million metric tonnes in 2011, with the USA producing some 32%, followed by Brazil with 29% (FAO, 2013), this threat is of huge economic and social concern. Conversely, some rusts, such as the yellow rusts of cereals, are impeded in their infection potential by higher temperatures (Roelfs et al., 1992; Garrett et al., 2006), possibly leading to a decline of their threat to crops in currently cool temperate climates. The recent emergence of new races in North America with increased aggressiveness and greater tolerance for higher temperatures may, however, compensate for any decrease in yellow rust incidence as a consequence of future climate warming, and demonstrates how the aggressiveness of rust pathogens can adapt to environmental change (Milus et al., 2009). Furthermore, the infective potential of the systemic rust on native American prairie white clover (Dalea candida) Uropyxis petalostemonis drops sharply at temperatures > 25 C (Worapong et al., 2009), reducing the risk of summer infection and shifting the main epidemic to cooler areas and to an earlier infection period in the spring. Many rusts are dependent on high humidity during the initial infection, and climate change-related shifts in humidity levels will affect rust development (Dixon et al., 2010). Thus, while entirely dependent on the presence and the resistance behaviour of compatible host plants, there is evidence that rusts may nevertheless be directly subject to effects of climate change, especially changes in rainfall and relative humidity patterns and climate warming (Nagarajan & Joshi, 1985; Del Ponte et al., 2006; Garrett et al., 2006). In crop plants such as soybean or wheat, this may be connected more to disease severity than to overall occurrence or distribution (West et al., 2012). A higher probability of extreme storm events is likely to increase aeciospore and urediniospore dispersal and the dispersal of plant debris carrying all manner of plant pathogens, including spores of rusts (Anderson et al., 2004; Hodson et al., 2011; Singh et al., 2011). CO 2,O 3 and other atmospheric gases An increase in atmospheric CO 2 has been shown to have a slightly negative effect on cereal rusts (Tiedemann & Firsching, 2000), while elevated O 3 concentrations had a strongly negative effect on cereal

7 776 Review New Phytologist rusts compared with a strongly positive effect on leaf rust of poplar (Populus sp.), caused by Melampsora medusae (Percy et al., 2002; Ghini et al., 2008). As O 3 has deleterious effects on many plants directly, compounding effects are likely. There is no information on the effects of SO 2 or nitrous oxides on rusts; however, it is well known that SO 2 is detrimental to fungi and lichens (Saunders, 1966) and negative effects on rust fungi can be expected. Hybridization in rust fungi As discussed in the section on Host rust co-evolution and specificity, the evolution of rust fungi is subject to the normal processes of mutation and selection in the form of host plant defence mechanisms, other biotic agents and the abiotic environment. This process can be aided by rust somatic recombination and sexual hybridization, as demonstrated in hybrid cereal rusts (Park & Wellings, 2012) and poplar rust fungi (Spiers & Hopcroft, 1994). Global change is projected here to increase the rusts ability to generate new virulence combinations: (1) host plant homogenization leads to greater numbers of susceptible individuals, allowing higher numbers of recombinants to be produced (Park & Wellings, 2012); and (2) the bringing together of hitherto separate rust genotypes through global movement of pathogens provides the opportunity for novel hybrid species to be generated. While many of these new recombinations are expected to be less aggressive than their parent strains, occasional more highly adapted strains are likely to emerge and, given the availability of susceptible host plants, may cause unprecedented epidemics (Kerr & Keane, 1997). It is suggested that the current high number of cereal rust species, compared with their host plant diversity, is a result in part of such processes having happened in the past (Park & Wellings, 2012). Threats to rusts A major component of this review has addressed the response of rusts to global change, where these are perceived as plant pests. However, within their natural range, rusts constitute important components of ecosystem structure and function. Plant diversity and community structure are a direct result of feedbacks from the biotic and abiotic environment (Mordecai, 2011; Bever et al., 2012). As biotic antagonists, rust fungi play an important role in the evolution of diversity of their hosts. The negative feedback (selective disadvantage) from parasitism on a homogenous host population is stronger than the cost of diversification (Jarosz & Davelos, 1995), leading to host plant diversification in the presence of pathogens. This in turn can have an influence on the ecosystem functioning of the host species and their populations. There is an argument that healthy ecosystems are rich in parasitic organisms, including rusts (Hudson et al., 2006). Conversely, diverse plant communities are less conducive than homogenous ones to epidemic proliferation of individual pathogens. In biotrophic pathogens with complicated life cycles and multiple interactions, such as the rust fungi, more complex mechanisms of co-evolution can be expected (Newcombe & Dugan, 2010; Schenk et al., 2012). For instance, white pine blister rust, caused by Cronartium ribicola, is dependent on the close geographical proximity of two ecologically similar yet nonidentical host plant ranges: those of five needle pines (Pinus subgenus Strobus, the alternate hosts) and those of gooseberries and their relatives (Ribes spp., the principal hosts) (Stephan & Hyun, 1983; Kaitera & Hiltunen, 2012). Where diversification and evolution of host plant resistance in combination with abiotic factors have resulted in a threat to the survival of the pathogen, conservation issues may ensue, and many locally rare rust species have been reported (Helfer, 1993). Further research is required into the conservation needs of rust fungi on a local, regional and global scale. There are currently no rusts on the red data list of endangered species, published by the International Union for Conservation of Nature (IUCN, 2013) and few are listed on regional and national lists (Foitzik, 1996; Handtke & Otto, 1999; Evans et al., 2006). However, highly specialized rusts of rare and endangered plant species are very likely endangered themselves and should therefore be afforded some form of protection (Helfer, 1993). Recently, the conservation needs of rust and smut fungi have been recognized by the IUCN in establishing a Species Survival Commission Rusts and Smuts Specialist Group (Denchev, 2011). However, as parasites, rust fungi often find themselves on the wrong side of the conservation debate where common and destructive epidemic species have been targeted for control measures (IUCN, 2010). Biological factors relating to threat or invasiveness Host ranges, diversities and densities Species of rust fungi are reputed to have narrow host ranges (Savile, 1979). This trait has been used by some mycologists to employ host plant identity as part of rust species definition (G aumann, 1959) and has been exploited in their use as biological control agents (Ellison et al., 2008). However, recent evidence has shown that host ranges are by no means fixed, and dramatic range expansions have been observed among certain species (Skinner & Stuteville, 1995; Morin et al., 2012). This can lead to unpredictable invasions, as has been seen in white pine blister rust in North America, Asia and Europe (Kim et al., 2010; Kaitera et al., 2012) and the rust of Myrtaceae Puccinia psidii in South and Central America, Southern Africa and Australia, as discussed in the section Host constraints. Aggressiveness As shown in the section Host constraints, host resistance to rust infection can be dependent on climatic variables (Nagarajan & Joshi, 1985). It is also widely believed that pathogen virulence is dependent on temperature (Roelfs et al., 1992; Evans et al., 2008). However, as this dependence is linked to the host pathogen interaction, with climate changes potentially resulting in conflicting disease outcomes, it is to be expected that climate change will lead to changes in rust species distributions rather than overall disease incidence. Critical factors are host and pathogen co-occurrence, conducive environmental conditions and the potential exchange and recombination of virulence genes between rusts of different origin, as discussed by Sendall et al. (2006) for the sunflower Puccinia helianthi pathosystem.

8 New Phytologist Review 777 Biological antagonists Rusts are commonly infected by hyperparasitic fungi (Farr & Rossman, 2013). However, there are only a few studies showing the effects of these (Kiss, 2001; Newcombe et al., 2001; Moricca et al., 2005). Other antagonists (viruses or bacteria) may equally play a role in rust ecology (Moricca & Ragazzi, 2008). The influence of global change on biological antagonists is still unclear. Conclusions from work to date While some rusts, especially crop pathogens, have been studied extensively, the rust species of native or naturalized vegetation are not well understood. Those that are relatively well known do not appear to behave in a generally predictable manner under any of the commonly projected climate change parameters. However, the following overarching conditions appear to favour rust fungi: the availability of high humidity for several hours favours rust infection; host plant uniformity favours rust epidemics; high nutrient availability favours rust incidence through the availability of soft host tissue; furthermore, the global movement of plants and their rusts provides a basis for pathogen range expansion, genetic recombination and the evolution of new host rust relationships and is considered here as the variable with the greatest impact on rust fungi globally. Uncertainties and outstanding questions As has been discussed, there are many uncertainties when predicting the future for rust fungi. Global change may bring unprecedented climatic challenges and opportunities for this group of organisms, while rises in CO 2,O 3 and other atmospheric gases affect host plants and parasites in different ways. Range shifts for individual species are likely but it is currently uncertain which species will benefit and which will lose out. Research trends and proposals Focused research into plant rust interactions in climate change scenarios should be intensified and extended to noncrop plants, in order to gain a better understanding of the effects of climate change variables on rust fungi and downstream ecosystem function and services. Range expansion experiments, as carried out for P. psidii on Myrtaceae (Morin et al., 2012), could be applied to other rusts and putative host plant families, an approach that has been employed on a limited scale since Klebahn s original studies of heteroecious rusts (Klebahn, 1904). Acknowledgements This work was funded by the Scottish Government s Rural and Environment Science and Analytical Services Division. I gratefully acknowledge the assistance given by numerous authors in providing access to their work. I am also thankful to Prof. D. S. 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