Evolution and Adaptation of Forest and Crop Pathogens in the Anthropocene
- Pauline Hessenauer1
- Nicolas Feau2
- Upinder Gill3
- Benjamin Schwessinger4
- Gurcharn S. Brar5 †
- Richard C. Hamelin1 2 †
- 1Faculty of Forestry, Geography and Geomatics, Laval University, Quebec City, QC, G1V 0A6 Canada
- 2Faculty of Forestry, The University of British Columbia, Vancouver, BC, V6T 1Z4 Canada
- 3College of Agriculture, Food Systems, and Natural Resources, North Dakota State University, Fargo, ND 58102, U.S.A.
- 4Research School of Biology, Australian National University, Acton, ACT 2601 Australia
- 5Faculty of Land and Food Systems, The University of British Columbia, Vancouver, BC, V6T 1Z4 Canada
Anthropocene marks the era when human activity is making a significant impact on earth, its ecological and biogeographical systems. The domestication and intensification of agricultural and forest production systems have had a large impact on plant and tree health. Some pathogens benefitted from these human activities and have evolved and adapted in response to the expansion of crop and forest systems, resulting in global outbreaks. Global pathogen genomics data including population genomics and high-quality reference assemblies are crucial for understanding the evolution and adaptation of pathogens. Crops and forest trees have remarkably different characteristics, such as reproductive time and the level of domestication. They also have different production systems for disease management with more intensive management in crops than forest trees. By comparing and contrasting results from pathogen population genomic studies done on widely different agricultural and forest production systems, we can improve our understanding of pathogen evolution and adaptation to different selection pressures. We find that in spite of these differences, similar processes such as hybridization, host jumps, selection, specialization, and clonal expansion are shaping the pathogen populations in both crops and forest trees. We propose some solutions to reduce these impacts and lower the probability of global pathogen outbreaks so that we can envision better management strategies to sustain global food production as well as ecosystem services.
In the age of the Anthropocene, human activities have caused deep global changes (Zalasiewicz et al. 2008). The transformation of the world ecosystems during this period has had a serious impact on biodiversity and important consequences on natural resources (Hobbs et al. 2006). The domestication of plants and animals, the intensification of agriculture, and deforestation are among the most important anthropogenic drivers of these changes.
Domestication of annual plants.
Plant domestication (Box 1), the accelerated evolutionary process operating under human selection (Harlan 1992), has transformed the course of human history. Nearly 70% of the calories consumed by humans are supplied by only 15 domesticated crops (Ross-Ibarra et al. 2007). Agriculture began more than 50,000 years ago although the domestication of today’s major crops (wheat, barley, oat, rice, maize, etc.) occurred within the last 10,000 years (Brown 2018; Brown et al. 2009). Plants with the favorable traits have been preferentially selected and multiplied for thousands of generations, gradually shaping genetic variation in local populations and isolating domesticated from wild populations. Over time, artificial selection and the restriction of gene flow caused domesticated populations to diverge genetically and phenotypically from the wild ancestral populations (Olsen and Wendel 2013; Zeder et al. 2006). The outcome of this process differs according to the degree of domestication, resulting in a continuum of plant populations that ranges from exploited wild plants to cultivated human-dependent crops.
BOX 1. Glossary
Agroforestry: A land-using system where long-lived perennials are planted in combination with herbaceous plants, taking advantage of the ecological interactions existing between species with different life history traits.
Cost of domestication: The evolutionary burden caused by domesticating a wild species and subsequent breeding; these effects include small effective population size, inbreeding and strong selection on domestication genes that will result in an increase of deleterious mutations, imposing a genetic load to the domesticated population.
Cost of pestification: By analogy to the cost of domestication, adaptation of a new pathogen lineage to a domesticated plant species impose some evolutionary effects such as reduction in population effective size, strong selection on “pestification” genes and sometimes absence of sexual recombination that will lead to the accumulation of deleterious mutations.
Crop: A plant that is grown in managed plantations, often originating following a process of domestication and improvement and is harvested for commercial or subsistence purposes.
Domestication: An accelerated evolutionary process operating under human selection. In its most simple form, plants with the most interesting traits have been selected and multiplied via seeds or propagules over multiple generations, gradually shaping genetic variation in local populations and isolating the domesticated population from external gene flow.
Domesticated species: A species is domesticated when it has been selected and reproductively isolated for a period of time long enough to cause genetic divergence from its wild relative.
Domestication syndrome: The set of traits selected by humans during domestication that differentiates modern crops from their wild progenitors.
Domesticated pathogen: A pathogen is domesticated when it coevolves with its main host which is under “domestication” process.
Natural forest, seminatural forest and plantation: Terms describing a gradient of management practices where trees grow and disperse naturally with limited to inexistent human intervention (natural forest) to highly managed systems where tree species and diversity is controlled and trees are planted artificially (plantation).
Plant breeding: Human-associated/preferential selection and propagation of genotypes with desirable traits.
A crop is a plant that usually resulted from a long process of domestication and genetic improvement. Crops are grown and harvested for commercial or subsistence purposes. Their yields have increased dramatically, particularly during the 20th century, by exploiting their genetic potential and improving their management by capitalizing on the use of fertilizers in monoculture systems and minimizing competition from weeds, insect-pests, and pathogens with the intensive use of agrochemicals (Miflin 2000).
Domestication of long-lived perennials.
In contrast, the domestication of long-living woody perennials, including fruit trees, started only during the last few centuries (Campbell et al. 2003; Gaut et al. 2015; Harfouche et al. 2012; Miller and Gross 2011; Sederoff et al. 2009; Zohary and Hopf 2000). While some fruit tree cultivars are almost undomesticated and indistinguishable from their wild relatives (e.g., cacao trees) (Efombagn et al. 2009), others have been bred and selected for hundreds of years, producing many different cultivars, such as apple trees (Cornille et al. 2014). Horticultural traits in these trees have been selected and then fixed by human-mediated methods such as vegetative propagation with cuttings and grafting, leading to a gradual genetic isolation of selected cultivars from the original populations.
Domestication is also recent for forest trees used for lumber, pulp, and wood products in part because of their long reproductive cycle and the easily accessible timber in primary natural forests (Food and Agriculture Organization [FAO] 2020). As a result, most planted forests are composed of nondomesticated trees that are characterized by high genetic diversity, age, species heterogeneity, and long time scales. There is a wide diversity of forested landscapes, reflecting different degrees of anthropogenization. In the past half century, the increasing demand for fiber and wood products has led to a strong expansion of tree plantations, representing now three percent of forest area worldwide (FAO 2020). In the southern hemisphere highly-productive monoculture plantations of eucalyptus, acacia, and pine account for most of the wood supply (Paquette and Messier 2010). Tree planting as a mean to fix carbon and reduce greenhouse gases is creating further demand to increase forest acreage, with countries such as China, India, the United States, and Canada proposing plans to plant trillions of trees.
Therefore, long-lived perennials comprise a mixture of highly domesticated and intensively managed plantations and forest stands as well as highly heterogeneous undomesticated forests. This provides a striking contrast with the genetically homogeneous, annual, and highly managed crops.
Exploring pathogen evolution along the domestication gradient.
Crops and forest trees are affected by diseases caused by pathogens that are sometimes phylogenetically closely related. Because of the contrasts highlighted in the previous sections, we expect different impacts on pathogen populations. However, there is a gradient along the domestication and management continuum (Fig. 1). Forest trees occurring in natural forests such as oaks and chestnuts are less domesticated and managed than the pines and poplars grown in intensive plantations. Fruit trees are woody long-lived perennials and their genetic domestication is mostly recent; yet they are intensely managed, in a way very similar to crops, with frequent human interventions to increase pest and disease protection and increase yield.
Exploring how these different production systems impact pathogen population evolution and adaptation might help the community of crop and forest pathologists, geneticists, breeders, and conservationists better understand and manage diseases. In this review, we synthesize the current knowledge on the impact of domestication and management of crop and forest production systems on evolving pathosystems. In particular, we focus on the development of global genomics data such as worldwide populations genomes and the accessibility to high quality reference assemblies for understanding the evolution and adaptation of pathogens and to answer hypothesis-driven questions. A summary of the main pathogens of annual and perennial plants pathogens discussed/mentioned in this review is presented in Table 1.
AGRICULTURE AND FOREST ECOSYSTEMS IN THE AGE OF THE ANTHROPOCENE
Impact of domestication on agriculture and forest ecosystems.
Ecosystem design and subsequent plant domestication have both, to some extent, been carried out in very linear ways. Wild and genetically diverse plant resources were selected into phenotypically and genetically homogeneous cultivars while complex and diversified ecosystems were simplified into monocultural and/or uniform plantations. The term “domestication syndrome” was described by Karl Hammer in 1984 as the set of traits that humans selected during domestication and differentiates modern crops from their wild progenitors (Box 1) (Olsen and Wendel 2013). The domestication syndrome may evolve over a period ranging from few to thousands of generations as desirable traits are selected and become fixed within the crop population (Meyer et al. 2012).
Comparative features of wild versus domesticated annual plants.
Annual crop plants were the first to be domesticated from their wild ancestors. In annual crop plants, the domestication syndrome traits include loss of seed shattering, decreased seed dormancy, seed size, and seed number (Zohary and Hopf 2000). Originally, small numbers of progenitor genotypes were selected by early farmers for traits usually related to overall yield, harvesting, and edibility. Some of those annual crops are self-pollinated such as annual herbaceous crops. The strong human-made selection process, often combined with inbreeding and sometimes selfing (e.g., rice) (Kovach et al. 2007), causes genetic bottlenecks of varying degrees that result in reduction of the level of genetic variation (Olsen and Gross 2008), generating in some cases a “cost of domestication” (Box 1) due to the accumulation of deleterious mutation in the domesticated population (Lu et al. 2006; Moyers et al. 2018). Domesticated Poaceae such as maize, wheat, oats, and barley lost one third of the nucleotide diversity relative to their wild progenitors (Buckler et al. 2001). Genome resequencing of cultivated and wild rice indicated that the average nucleotide diversity in cultivated rice varieties was 25% lower than in their wild counterparts, suggesting reduction in effective population sizes during domestication bottlenecks (Xu et al. 2012). The reduction of genetic diversity has been even more drastic in wheat which is dominated by intensive selection of a handful of loci (Hao et al. 2017; Liu et al. 2019). In wheat, selective sweeps around the genes controlling flowering time and phenology are evident (Cavanagh et al. 2013). Similarly, intensive selection of reduced height and photoperiod insensitivity genes resulted in semidwarf “Green Revolution” cultivars, which replaced all old cultivars in south Asia (Borlaug 2007; Cavanagh et al. 2013). In addition to this reduction in genetic diversity, there is an intrinsic genetic homogenization since fields are often planted to a single variety.
Comparative features of wild versus domesticated long-lived perennials.
Natural forests have built-in diversity with different tree and plant species and different age classes. Because of their long-lived nature, forest trees maintain genetic variation for decades which slows the erosion of diversity by drift. Trees often carry a heavy genetic load of deleterious recessive alleles (Boshier et al. 2000) despite rather large effective population sizes covering extensive geographic areas and largely outcrossing mating systems. In most plant species, there is a positive relationship between population size, genetic diversity, and fitness (Leimu et al. 2006). Taken together, these life-history traits promote the maintenance of abundant levels of genetic variation in most forest tree populations compared with annual plants (Hamrick and Godt 1996), which in theory should help adaptation to changing environmental conditions but also pathogen resistance.
Tree life-history traits and biological features, multiple geographical origins, and ongoing crop-wild gene flow, contribute to mild domestication bottlenecks. For example, perennial fruit crops such as apple and olive trees have on average retained 90 to 95% of the neutral genetic variation found in wild populations (Fig. 1A), even for those supposedly under domestication since a long time (e.g., 10,000 to 5,000 years ago for the European hazelnut, Corylus avellana; Helmstetter et al. 2020). For some recently domesticated perennial fruit crops, this slight reduction in genetic diversity was more likely due to selective propagation in a cultivated setting, rather than to many generations of selective breeding (Miller and Gross 2011). Impact of domestication on forest trees is usually mild, too. Only a slight decrease in genetic diversity was observed following the first steps of the domestication process (i.e., phenotypic selection and tree improvement cycles) of western hemlock (Wellman et al. 2003), interior hybrid spruce (Stoehr and El-Kassaby 1997), and Douglas fir (El-Kassaby and Ritland 1996) in British Columbia, Canada. Likewise, no difference in gene diversity was found between natural and managed populations of Picea glauca and Pinus banksiana (Godt et al. 2001). Lessons have been learned from the domestication experiences with annual crops and subsequent loss in genetic variation, and most forest tree breeding programs have ensured that selected populations were large enough to capture a maximum of genetic diversity and allelic richness (Harfouche et al. 2012; Ingvarsson and Dahlberg 2019).
In forestry, genetic and genomic techniques combined with conventional breeding is accelerating tree domestication (Boerjan 2005; Campbell et al. 2003; Sederoff et al. 2009). It is still unclear which genetic and genomic changes might become associated with tree domestication (Boerjan 2005; Sederoff et al. 2009). Forest tree species are in various stages of domestication depending on the degree of selection exerted (Boerjan 2005; Neale 2007). For example, cottonwoods (poplars of the botanical section Populus) are among the most advanced forest trees on the domestication gradient. They have emerged as extremely versatile trees with natural attributes favorable to their domestication: ease of vegetative propagation, rapid growth, relatively short juvenile phase, and interspecific compatibility that allows breeding hybrids with broad adaptability, improved growth, and acceptable levels of disease resistance. This has contributed to the recognition of poplars as a model for tree domestication (Boerjan 2005; Bradshaw et al. 2000; Taylor 2002). In contrast, most deciduous and conifer tree species are long-lived perennials with lengthy juvenile phases, high levels of genetic diversity, extensive outcrossing, widespread natural hybridization, and weak population structure. Despite limited among-population structure, natural tree populations are usually locally adapted.
The domestication gradient of annuals and long-lived perennials.
“Plant domestication” (Box 1) can be seen as a gradient correlated with different features such as the time (reported as a number of years the breeding process started or a number of breeding generations), the level of genetic isolation to the wild population of origin or the proportion of natural diversity retained in the end of the domestication process. Due to differences in the time the domestication process started and in their life traits and biological features, annual plants and long-lived perennials are positioned differently along this gradient (Fig. 1B). At one end of the gradient are annual plants that have received intensive human-selection pressures starting thousands of years ago while at the other end of the spectrum are the wild counterparts of these crops, conifers, and deciduous forest trees that remain “untouched” (with the exception of management with the plantation of particular genotypes or provenances of interest; see section on “Management of crops and forests”). Between these two extreme points, long-lived perennials are scattered. Although perennial fruit crops do not have the biological features of annual plants to facilitate the domestication process (see above) they have received much more attention than forest trees in the history of plant domestication. Therefore, they can be placed at an intermediate level on the domestication gradient. Then, forest tree species tend to be rather close to the second end of the gradient, in various stages of domestication depending on the degree of selection exertable and exerted (Boerjan 2005; Neale 2007). As mentioned above, cottonwoods (poplars of the botanical section Populus) are among the most advanced species in the domestication process of forest trees. Eucalyptus trees have similar features, making them of particular interest for breeding and domestication, too. In contrast, most conifer and deciduous tree species are long-lived perennials with lengthy juvenile phases, high levels of genetic diversity, extensive outcrossing, widespread natural hybridization, and weak population structure, which are hardly compatible with the requirement of the domestication process.
Management of crops and forests.
In addition to the reduction in genetic diversity associated with domestication, there has been a drastic reduction in plant diversity as only a handful of cultivated crop species dominate the arable land globally; for example, maize, wheat, soybean, and cotton are grown over two third of the total arable land in the United States (Margosian et al. 2009). This combination of low genetic and species diversity has invariably been accompanied by increases in pest and disease problems. Hence, human management has become an essential part of production of crops and trees in monoculture conditions (Fuller et al. 2010). In these conditions, pathogens are mostly controlled by crop and land management and genetic selection for certain disease resistance traits. Similarly, as a part of management, pesticides and fungicides have increased crop productivity and are required for maintaining the high quality of the produce; they have become an integral part of modern agricultural ecosystems (Ishii and Holloman 2015). These intensive management approaches are not sustainable in the long term, in part because of the intense selection pressure on the pathogen population to become resistant to fungicides or evolve to overcome resistance (Storkey et al. 2019).
Most modern crop cultivars carry one or few major resistance genes for each of the locally important diseases. Relying on single genes for resistance exposes the crop to a major risk as pathogens can easily evolve to overcome a single resistance gene (Brar et al. 2019). Reduction in the selection pressure can be achieved by breeders by sequential release of resistance genes or gene pyramiding which is the combination of multiple resistance genes in the same crop cultivars. Overall crop management practices combined with human selection has led to a dramatic reduction in crop diversity at multiple levels.
By contrast, forests are managed quite differently from most crops and vary dramatically with the type of forest. Overall, use of pesticides is rare and usually only applied to combat invasive species. Human intervention in forest management usually involves silvicultural approaches such as species and provenance selection for planting, spacing, thinning or pruning. These management approaches can be conducive to disease outbreaks. For example, root pathogens such as Heterobasidion spp. and Armillaria spp. take advantage of the logging or thinning practices to invade the root systems and spread from tree to tree. Genetic resistance is often present in natural populations, but its exploitation, via breeding, is rare because of the long breeding cycle unlike agricultural crops (Goheen and Goheen 1990). Even breeding horticultural woody perennial crops is faster and easier than breeding forest trees. Some of the best-documented cases of resistance breeding in trees are against rusts (poplar rust [caused by Melampsora spp.], fusiform rust [caused by Cronartium quercuum f. sp. fusiforme], and white pine blister rust [caused by Cronartium ribicola]) (Jorge et al. 2005; Sniezko et al. 2014). Deployment of resistance using a single gene approach similar to crop breeding has also resulted in selection of pathogen populations capable of overcoming resistance.
There are many different ways in which associated activities throughout tree management practices may influence genetic diversity of trees (reviewed in Ratnam et al. 2014). Stand or landscape genetic variation can be altered by planting seedlings, thinning, selective harvesting, or through deployment of material from tree improvement programs. Forest fragmentation, which inevitably follows clear-cut harvesting, is expected to have an impact on genetic diversity and population structure of trees by affecting a magnitude of evolutionary processes, such as genetic drift, gene flow, and selection. However, studies investigating the effect of harvesting and regeneration on genetic diversity reported mixed results (Ratnam et al. 2014). The extent of genetic erosion depends on the management system applied, stand structure, as well as species’ distribution and demography, biological attributes, and ecology.
Forest plantations have been seen as a way to reduce pressure on natural forests while answering the increasing demand for wood products and providing multiple ecosystem services (Paquette and Messier 2010). While the implementation of industrial large-scale and monocultures of fast growing and exotic species has been the gold standard, there is a growing interest in accelerating development of mixed-species plantations and agroforestry systems (Liu et al. 2018a; Payn et al. 2015). Agroforestry is the integration of some tree species with crop plants on the same piece of land. Agroforestry then bridges the gap between crop ecosystems and forest ecosystems and increases resilience of crop plant species to environmental changes by increasing ecological services (Dainese et al. 2019; Hajjar et al. 2008).
PLANTS VERSUS PATHOGENS: THE CONSEQUENCES OF CROP DOMESTICATION AND MANAGEMENT
In natural ecosystems, the antagonistic interaction between host plants and their pathogens drives a coevolutionary arms race of reciprocal adaptations. This coevolutionary process shapes genetic variation in both plants and pathogens (Brown and Tellier 2011), sometimes resulting in mirrored genetic structures (Barrett et al. 2008; Feurtey et al. 2016; Hartmann et al. 2020). One of the main consequences of domestication is the “artificial” evolution (through breeding) of the plant, and the absence of “natural” response to pathogen pressure. In turn, plant domestication and management have increased the selection pressure on pathogens. Domestication, combined with globalization, facilitates the rapid dispersal of pathogens and provides new ecological niches leading to the emergence of a succession of specialized pathogens. This process is a major shift in the coevolutionary dynamics found in natural ecosystems between hosts and pathogens, resulting in significant changes in the structure of pathogen populations and in some instances in the genome architecture (Giraud et al. 2010; Lebarbenchon et al. 2008; Möller and Stukenbrock 2017; Stukenbrock and McDonald 2008).
An implicit hypothesis is that the accelerated genetic selection in crops results in strong directional selection in the pathogen population leading to the rapid emergence of specialized populations that can exploit the niche more effectively. The hypothesis, originally proposed for human pathogens (Pearce-Duvet 2006), has now been widely tested for crop pathogens. In the last 20 years, the comparison of several natural and agricultural systems on the basis of host specificities, phylogenetics, and estimates of divergence time supported the hypothesis that the divergence of new crop pathogens and specialized lineages from their wild ancestors was coincident with the development of domesticated crops (Couch et al. 2005; Stukenbrock and McDonald 2008; Stukenbrock et al. 2007; Zaffarano et al. 2008; however, see also Munkacsi et al. 2007).
There is little evidence that pathogens of domesticated crops often exhibit rates of adaptive substitutions different from their close wild relatives or populations on wild host plants (e.g., Zymoseptoria tritici [syn. Mycosphaerella graminicola]) (Brunner et al. 2009; Grandaubert et al. 2019; Stukenbrock et al. 2011). Yet, specific adaptation signatures vary and depend on several factors, including level of specialization and pathogen genetics and biology. These signatures are often linked to intrinsic genomic, reproduction, and infection features present before the domestication event. Coevolutionary host-tracking, in which the pathogens follow their host along the domestication course, and the emergence of new pathogen lineages, sometimes clonal, through host jump, hybridization, and positive directional selection constitute the main mechanisms underlying the rapid emergence of specialized populations. However, the combination of some of these features may have a reverse effect. Small effective population sizes, strong directional selection on few candidate genes and absence of sexual recombination in pathogen populations specializing on domesticated plants may induce a genetic load (i.e., a cost of pestification by analogy to the cost of domestication; Box 1) resulting from the accumulation of deleterious mutations (Feurtey et al. 2020a; Gladieux et al. 2018a; see Stukenbrock et al. 2011 for a counter-example in a sexual lineage).
Where the grass is greener: Emergence of new species following host jump, selection, and specialization.
The emergence of plant pathogens in agroecosystems has been extensively described using genetic markers (see Stukenbrock and McDonald 2008 for a review). Genome sequencing and population genomics are now shedding new lights on this process. Evolutionary processes related to the emergence of novel pathogen species via host range expansion and host jumps are becoming easier to track by analyzing whole genomes. Such events have shaped the diversification of powdery mildew pathogens. Although there is only one species of powdery mildew on grass, Blumeria graminis, different formae speciales are defined by the host they infect. Genome sequencing of B. graminis f. sp. hordei (Spanu et al. 2010) revealed that B. graminis f. sp. hordei and B. graminis f. sp. tritici diverged about 6 million years ago (MYA) from B. graminis f. sp. tritici, after the divergence of their hosts (barley and wheat, respectively) (Middleton et al. 2014; Wicker et al. 2013). The formae speciales secalis and tritici diverged more recently between 0.25 and 0.16 MYA, while the divergence between their hosts (rye and wheat, respectively) was estimated at 4 MYA. Host jump events and recent horizontal gene flow were also identified as processes that shaped current diverged lineages (Menardo et al. 2017).
Evolutionary processes related to domestication of the host can be tracked in a similar way. The evolution of the wheat leaf blotch pathogen Z. tritici follows a pattern of host-tracking in response to wheat domestication. The pathogen invaded the wheat-growing regions of the world together with its host Triticum aestivum and Triticum durum (Stukenbrock et al. 2007, 2012a). Z. tritici differentiated from its sister species Z. pseudotritici (S1) and Z. ardabiliae (S2) in the fertile crescent likely during wheat domestication and is currently a major invasive pathogen of wheat globally (Stukenbrock and Dutheil 2018; Stukenbrock et al. 2011). Genome sequencing and comparison revealed collinearity and high conservation of genomic, transcriptomic and epigenomic signatures of genome architecture (Feurtey et al. 2020b). High gene content variability both within and between species, mainly limited to the accessory chromosomes indicates compartmentalization that allows purifying selection to retain a functional core genome and relaxed selection on the accessory genome.
Fast and furious: Shifting gears and speeding up evolution.
Some pathogens of domesticated crops have undergone a shift to speed up evolution. The increased evolutionary capacity of Z. tritici compared with its sister species is driven by recombination, and transposable elements (TE) variation, high nucleotide diversity, and extensive structural variation (Badet et al. 2020; Oggenfuss et al. 2020; Plissonneau et al. 2018). In comparison, Z. pseudotritici, which infects naturally occurring grass species in Iran (Stukenbrock et al. 2012a, b), shows significantly less variation along its genome with only a limited number of haplotype groups. Alternatively, the difference in population effective size with Z. pseudotritici could explain the higher evolutionary potential for Z. tritici.
The high level of diversity in Z. tritici is driven by intrinsic factors such as high recombination rates and loss of part of its DNA methylation machinery which leads to relaxation of TE expression and hence likely enhanced TE mobility that might lead to higher mutation rates due to transpositions (Grandaubert et al. 2019; Möller et al. 2020). Differentiation of Z. tritici likely is driven by positive selection on secreted proteins. Indeed, effector candidates display twice the rate of adaptive substitution when compared with other genes and Z. tritici effectors have high levels of presence-absence polymorphism. Phenotypic characterization of some of the effector candidates with the largest signal for positive selection confirmed that these genes contribute to wheat infection by Z. tritici. The elevated rates of positive selection in Z. tritici at the genome level can be interpreted as increased adaptive evolution (Poppe et al. 2015). It will be important to discover the biochemical mechanisms that enable this increased adaptive evolution in Z. tritici for which loss of de novo DNA methylation might represent one example. Adaptive substitutions in DNA repair machinery genes are another set of prime candidates causing these phenotypes (Hartmann et al. 2020).
Evolutionary fast-track and host range expansion.
Interspecific hybridization plays a major role in natural ecosystems and can provide an evolutionary fast-track in filamentous pathogens (Brasier 2001; Milgroom et al. 2014; Park and Wellings 2012; Stukenbrock 2016). From a theoretical point of view, allopatric species are more likely to have a permeable reproductive barrier, thus allowing the emergence of hybrid individuals (Giraud et al. 2008; Le Gac and Giraud 2008). Pure F1 hybrids are rarely found in the wild because they often exhibit intermediate phenotypes that have a reduced fitness compared with their parents, or they can suffer from incompatibilities between parental alleles and repeated backcrossing with the parental species can lead to the transfer of adaptive traits between species and thereby be a mechanism that speeds up adaptive evolution (Depotter et al. 2016; Feurtey and Stukenbrock 2018; Gladieux et al. 2011; Stukenbrock 2016).
Hybridization played a role in the emergence of B. graminis f. sp. triticale on triticale (× Triticosecale), an artificial human-made hexaploid crop species from a cross between wheat (Triticum) and rye (Secale) (Menardo et al. 2016). Triticale was resistant to B. graminis when first introduced commercially in the 1960s, until it was attacked by B. graminis f. sp. triticale in 2001. The whole-genome sequencing of isolates of B. graminis from four formae speciales revealed that B. graminis f. sp. triticale is a hybrid between B. graminis f. sp. tritici and B. graminis f. sp. secalis (Menardo et al. 2017) that is estimated to have originated from at least two independent hybridization events after the introduction of triticale as a commercial crop in the 1960s (Menardo et al. 2016). A portion of the Z. tritici genome has also been recently introgressed from its sister species and interspecies hybridization appears to be common between Zymoseptoria spp. (Feurtey et al. 2019, 2020b).
Interspecific hybridization can also expand host range (Vlaardingerbroek et al. 2016). The wilt disease of crucifer crops caused by Verticillium longisporum, regroups taxa originating from at least three hybridization events between V. dahliae and undescribed Verticillium parental species (Depotter et al. 2017; Inderbitzin et al. 2011). The parental species V. dahliae is the causal agent of a vascular wilt disease on more than 200 host species, including many economically important crops. This fungus is a notorious example of an asexual plant pathogen with a high genome plasticity mediated by mechanisms different from meiotic recombination, such as horizontal gene transfer (Shi-Kunne et al. 2019), transposon activity and large‐scale genomic rearrangements (de Jonge et al. 2013; Faino et al. 2016). In contrast to V. dahliae and other Verticillium species, V. longisporum is not a haploid organism but rather an allodiploid hybrid (Depotter et al. 2017; Inderbitzin et al. 2011). Fixation of the MAT1-1 idiomorph in V. longisporum suggested that sexual recombination without separation of homologous chromosomes was not the mechanism at the origin of this new species; instead, hyphal fusion followed by karyogamy was a more likely scenario to explain the creation of a stable, diploid nucleus (Inderbitzin et al. 2011). Allodiploid hybridization in V. longisporum expanded the host range of the pathogen in the family Brassicaceae, compared with the parental species V. dahliae that does not colonize these plants (Novakazi et al. 2015). In addition, the three separate hybridization events have affected the pathogenicity of the different V. longisporum clonal lineages. The most widespread lineage and main causal agent of Verticillium stem striping on oilseed rape, A1/D1 is often found on multiple brassicaceous hosts, whereas lineage A1/D2 is specialized to horseradish (Depotter et al. 2017; Inderbitzin et al. 2011). Analysis of the genome structure and content of V. longisporum supported the allodiploid hybrid origin of this pathogen and identified a higher gene content than in V. dahliae, including many secreted proteins and carbohydrate active enzyme (CAZy) encoding genes of the glycoside hydrolase group (Fogelqvist et al. 2018). In a context of accentuated global exchange and climate change, as more species distribution overlap, such events of interspecific hybridization leading to an increased pathogenicity could become a major challenge in crops disease management.
The battle of the clones.
Some crop pathogens appear to consist almost entirely of globally distributed asexual lineages. Monocultures, i.e., cultivation of genetically homogeneous crop variety, has added an additional layer of selection pressure favoring the spread of lineages with high fitness that can cause devastating epidemics. The most notorious example are the wheat rusts, with their ability to track their host by evolving rapidly new lineages. These rusts are heteroecious, requiring infection of an alternate ‘sexual’ host to complete their life-cycle; sexual recombination can lead to high diversity in the wheat yellow (stripe) rust pathogen Puccinia striiformis f. sp. tritici in the Himalayan region, where the alternate host occurs, and provides the advantage of a quick turnaround of races (Ali et al. 2014; Hovmøller et al. 2016). However, where the alternate host is absent or scarce due to its natural distribution or eradication programs, the fungus is restricted to asexual propagation with lineage diversification usually arising by mutation.
Global populations of Puccinia triticina and Puccinia striiformis f. sp. tritici are composed of clonal lineages that maintain high levels of heterozygosity, due to their dikaryotic nature (Ali et al. 2014; Brar et al. 2018a; Fellers et al. 2020; Hovmøller et al. 2016; Kolmer et al. 2019; Lei et al. 2017). Population shifts can be attributed to mutations and selection within clonal lineages, and/or to the emergence of new exotic lineages (Hubbard et al. 2015). Some clonal lineages have different adaptive traits such as warm‐temperature growth or the production of telia (Brar et al. 2018a). An emergent population of Puccinia striiformis f. sp. tritici virulent on previously resistant wheat varieties suggests a rapid lineage turnover following host genotype replacement facilitated by long distance migration (Hubbard et al. 2015).
Even in the absence of sexual reproduction, there are mechanisms that ensure diversity in asexual lineages. Long-term asexual evolution appears to drive genome expansion via TE activity and leads to increased heterozygosity. The genomes of recent sexual isolates of Puccinia striiformis f. sp. tritici are smaller and less heterozygous compared with long-term asexual lineages (Schwessinger et al. 2020). Presence/absence polymorphism in Puccinia striiformis f. sp. tritici gene content is not driven by effector candidates in general. Instead, other genes of unknown functions appear to be specific to sexual isolates and these genes might be linked to infection of barberry during the sexual cycle as it has been shown that long-term asexual lineages are compromised in entering the sexual cycle with potential specific selection against it (Schwessinger et al. 2020).
In asexual lineages, the exchange of genetic material via hyphal fusion can constitute an adaptive mechanism that can rapidly generate new traits (Feurtey and Stukenbrock 2018). Somatic genetic exchange between individuals coinfecting the same host has been experimentally demonstrated (Lei et al. 2017; Park and Wellings 2012). The most important example of somatic hybridization was provided by the Ug99 strain of P. graminis f. sp. tritici that emerged following cultivation of wheat cultivars carrying resistance gene Sr31 (Basnet et al. 2015). The haplotype-phased genomes of races Ug99 and Pgt21 collected in Uganda and Australia share one haploid nucleus with no trace of recombination or chromosome reassortment, a clear indication of somatic hybridization (Li et al. 2019). Ug99 has spread clonally through Africa and the Middle East causing devastating epidemics and is a significant threat to global wheat production (Basnet et al. 2015). Even though somatic hybridization in dikaryotic Uredinales is demonstrated in laboratory, the cases of natural occurrence are rare which indicates that either the survival of resulting somatic hybrids is rare or the capacity (using molecular or phenotypic tools) to identify somatic hybrids is limited (Park and Wellings 2012).
Even though genetic diversity in clonal populations of many pathogens such as Puccinia striiformis may be lower but the pathogen populations can be very large and census population size can be an important factor in adaptation of the pathogen to their host (Barton 2010). In large clonal populations, random genetic drift must be negligible if the census population size is large. It is the selective sweeps and bottlenecks that limit the diversity in the population. Nevertheless, such clonal populations still have strong evolutionary potential despite their low genetic diversity.
Contacts between pathogens species from wild and domesticated crop plants.
Genetic exchanges between domesticated and wild species can impact disease outbreaks or result in the emergence of new pathogens (Gladieux et al. 2018a; Stukenbrock et al. 2012a). In agroecosystems, wild crop relatives or related wild/cultivated species can serve as sources of new pathogens. The apple tree pathogen Venturia inaequalis from the agricultural population evolved a higher virulence on both wild and domesticated trees. Secondary contact between this pathogen and wild apple trees would result in an invasion of this pathogen and potential introgression in the wild type pathogen (Feurtey et al. 2020a).
One of the recent examples of host jump is of Magnaporthe oryzae (Pyricularia oryzae), the wheat blast pathogen that was reported in South America (Cruz and Valent 2017) and then in Bangladesh, causing substantial losses (Islam et al. 2016). Phylogenomic analyses revealed that this outbreak was most likely caused by a wheat-infecting strain from South America (Islam et al. 2016). The wheat-infecting lineage of Magnaporthe oryzae is believed to have emerged from ‘Lolium’ and ‘Avena’ pathotypes (Couch et al. 2005; Farman et al. 2017; Inoue et al. 2017) and coexists with multiple host-specialized and genetically divergent lineages that infect other cereals and grasses (Chiapello et al. 2015; Islam et al. 2016; Yoshida et al. 2016). The rice infecting lineage of Magnaporthe oryzae is highly differentiated, a likely consequence of the host jump from Setaria 2,500 to 7,500 years ago after rice domestication (Gladieux et al. 2018a; Latorre et al. 2020). Host selection could have been important in the emergence of the wheat blast pathogen. Two avirulence genes of Magnaporthe oryzae, PWT3 and PWT4, were implicated in host specificity and avirulence on wheat cultivars carrying Rwt3 and Rwt4 genes (Inoue et al. 2017). Widespread cultivation of Rwt3 wheat cultivars in Brazil could have allowed the Lolium pathotypes of Magnaporthe oryzae containing PWT3 to establish in that country (Cruz and Valent 2017). However, recent population genomic analyses could not determine whether the wheat blast pathogen in Brazil had single or multiple origins (Ceresini et al. 2018). Genome-wide analysis of an extensive collection of the blast fungus confirmed that Magnaporthe oryzae consists of an assemblage of differentiated lineages associated with particular host genera (Gladieux et al. 2018b). This pattern of genetic isolation could be neutralized by the capacity of distinct lineages to colonize common cereals and wild grasses and weeds, increasing the chance for occasional gene flow between isolates from different lineages with overlapping host ranges (Gladieux et al. 2018b).
NOT SO SLOW, AFTER ALL: LONGER GENERATION TIME IN TREES DOES NOT RHYME WITH SLOWER FOREST PATHOGEN EVOLUTION
Trees have a longer reproductive cycle, are longer-lived and are less advanced on the domestication gradient than crop pathogens. Intuitively, we could expect the selective pressure imposed by tree domestication to be milder compared with crops with longer histories of domestication, with resulting differences in pathogen population structure and genome architecture. The consequence of tree domestication on populations of forest pathogens is much less documented largely due to the fact that most of the forest tree species are still in domestication infancy. Some woody trees such as coffee and apple have wild relatives but have been domesticated for thousands of years. Others, such as conifers from the northern hemisphere, are essentially undomesticated. Yet, similar evolutionary mechanisms appear to shape populations of tree and crop pathogens. The expansion of clonal lineages and the emergence of novel lineages following hybridization and host jump are also clearly important in the evolution of forest pathogens.
The return of the clones: When forest trees are threatened too.
Similar to crop pathogens, perennial trees can be threatened by clonal populations and lineages of pathogens. Trade of germplasm, genetic material and plant and forest products has resulted in some of the most dramatic introduction of exotic pathogens in naive environments. The introductions of the chestnut blight in North America and Europe and the white pine blister rust in North America are among the most striking examples of entire ecosystem and landscape level changes induced by invasive pathogens. Despite the effect of genetic drift and inbreeding caused by severe genetic bottleneck and clonality, invasive pathogens are still successful at occupying their new environment. This intriguing aspect often described as “the genetic paradox of invasiveness” has been discussed in multiple publications (Allendorf and Lundquist 2003; Gladieux et al. 2015; Sax and Brown 2000; Tsutsui et al. 2000). The phenotypic plasticity and the adaptability required for these clonal populations to be competitive and succeed on a new host and a new environment can be explained by mechanisms similar to those described in the previous section for crop pathogens (The battle of the clones).
The causal agent of chestnut blight, Cryphonectria parasitica, is native to eastern Asia and was introduced in North America where it devastated the native tree species Castanea dentata and later in Europe where it attacks the European sweet chestnut Castanea sativa (Dutech et al. 2012). In southern and southeastern Europe, the invasive population of this fungal pathogen is dominated by one single asexual lineage (identified as S12) consisting nearly exclusively of a single mating type. Genome sequence analyses showed that this lineage was already preadapted to success across the European niches as it likely arose from a bridgehead (sensu Bertelsmeier et al. 2018; Lombaert et al. 2010) pool of genotypes that were previously established in Europe through multiple introductions from North America (Stauber et al. 2020). Additional evolutionary forces such as cryptic sex purging deleterious mutations, transposon activity (Stauber et al. 2020) and epigenetic modifications (Vuković et al. 2019) keep diversifying this clonal lineage, underpinning the hypothesis of adaptation to its niche and rapid success of its expansion on sweet chestnut in Europe.
The oomycete Phytophthora ramorum, responsible for sudden oak death in the United States, sudden larch death in Europe and ramorum blight of trees and ornamental shrubs in North America and Europe, is probably one of the most successful invasive forest pathogens, with the ability to infect more than 150 different woody perennial host species (Grünwald et al. 2019). To date, four reproductively isolated lineages, presumably asexual and comprised of one single mating type are spreading in Europe and North America. Despite their supposed asexuality the four lineages exhibit substantial amounts of intralineage phenotypic and genotypic variation. At a small geographical scale (e.g., in the western United States), local environmental conditions and the presence of sporulating hosts seem to be the driver of outbreak development and expansion of new clonal genotypes (Peterson et al. 2015; Yuzon et al. 2020); a similar scenario has been proposed to explain the local dispersal of clonal lineages of the needle pathogen of Douglas fir Phytophthora pluvialis in the western United States and New Zealand (Brar et al. 2018b; Tabima et al. 2021). Nonsexual mechanisms of genotypic diversification can explain the intralineage variability and the resulting potential of generating new genotypes adapted to local conditions, even in the absence of sexual reproduction. Structural variation such as aneuploidy and copy number variation were observed within each Phytophthora ramorum lineage (Dale et al. 2019; Kasuga et al. 2016). In particular, by sequencing multiple genomes of each Phytophthora ramorum lineage, Dale et al. (2019) showed that mitotic recombination likely associated with transposon activity generated runs of homozygosity (ROH) affecting hundreds of genes simultaneously and generating nonsynonymous changes in about 17.0% of the Phytophthora ramorum proteome. Although some slight differences in fitness were observed between the Phytophthora ramorum isolates with and without ROH, additional testing of different hosts under different conditions is required to obtain a comprehensive picture of the effect of these changes on the pathogen phenotype (Dale et al. 2019; Grünwald et al. 2019). Similarly, a high ROH incidence was observed in the triploid hybrid Phytophthora × alni, the causal agent of alder decline in Europe. High ROH incidence in this triploid hybrid has been interpreted as a mechanism promoting genome stabilization (by reducing heterozygosity) and clonal diversification and response to stress such as winter temperature and soil acidity (Mizeriene et al. 2021).
The rise of the hybrids.
Interspecific hybridization and host jumps have been widely described in forest pathogens and is thought to provide a fast-track to evolution (Brasier 2000). In Dutch elm disease pathogens, interspecific hybridization with Ophiostoma ulmi has allowed the acquisition of a missing mating type in O. novo-ulmi, the more virulent species (Paoletti, Buck, and Brasier 2006). The introgression of this gene in O. novo-ulmi facilitated adaptation of this invasive species by enabling sexual reproduction in the population, thus allowing recombination and genetic shuffling. In addition, adaptive genes involved in growth at high temperature and in virulence were introgressed from O. ulmi to O. novo-ulmi (Hessenauer et al. 2020). In the basidiomycete species complex Heterobasidion annosum, the introduction of the North American taxon in Italy was linked to U.S. military activity during World War II (Gonthier et al. 2004). This exotic taxon hybridized with the local infertile European taxon, impacting the evolutionary trajectory of this organism in Europe (Gonthier et al. 2007). It resulted in massive introgression from the native to the introduced species, representing 5 to 45% of the genome content in admixed individuals (Gonthier and Garbelotto 2011). While these introgressed regions seem to occur randomly and not driven by selection, such an increase in genetic diversity could be a key factor for evolving adaptive alleles (Gonthier and Garbelotto 2011).
The coffee tree, Coffea arabica, is a domesticated tree species that resulted from the hybridization of the diploid species Coffea canephora and Coffea eugenioides about 10,000 years ago (Cenci et al. 2012). It accounts for about 60% of the world’s coffee production. Domestication of arabica coffee in Yemen, followed by intensive cultivation and spread to Asia, America, and Africa resulted in several severe genetic bottleneck narrowing drastically the genetic diversity of this tree crop. It is highly susceptible to the coffee leaf rust caused by the obligate biotrophic fungus Hemileia vastatrix (Talhinhas et al. 2017). The global coffee rust population comprises three distinct lineages, including the domesticated Hemileia vastatrix lineage (“C3” group) that emerged and specialized on tetraploid hosts during Coffea arabica domestication process via an host jump from diploid coffee hosts (Silva et al. 2018). Episodes of introgression between this lineage and those specialized on diploid hosts raise the possibility that virulence factors may be quickly exchanged between groups and increase the risk of emergence of new hypervirulent strains.
Rapid tracking of slow-moving trees.
There is a seemingly unbalanced advantage in the evolutionary arms-race of trees and their pathogens. Trees have long generation times and are expected to adapt slowly to biotic and abiotic changes. By comparison, their pathogens have a shorter generation time, providing a systematic advantage in the evolutionary race with their host. This has been particularly well documented for the domestication of the cultivated apple, Malus domestica in central Asia 4,500 years ago from the wild apple Malus sieversii and the apple scab pathogen, Venturia inaequalis (Gladieux et al. 2010). Venturia inaequalis is subdivided in a wild population representing a relic of the ancestral population and a current derived agricultural-type population that was disseminated westward by host-tracking of cultivated apple trees and introgressed the wild-type populations after having diverged in strict isolation during apple tree domestication (Feurtey et al. 2020a). This secondary contact caused by the introduction of domesticated apple trees in Central Asia about 100 years ago has led to the recent invasion of the agricultural-type population in the wild Malus sieversii forest and to the emergence of hybrids. The agricultural Venturia inaequalis population and the hybrids display greater virulence on wild apple trees than its own endemic wild-type population, facilitating invasion of Malus sieversii trees.
Increased virulence on the wild host was likely inherited during tracking of apple tree domestication. The agricultural Venturia inaequalis population has probably accumulated multiple alleles such as a truncated small secreted protein recognized by domesticated apple trees selected for resistance to apple scab (Cornille et al. 2012). This pattern is consistent with the concept known as “pestification” (Feurtey et al. 2020a; Saleh et al. 2014), under which selection by humans of more resistant plants unwittingly leads pathogens to accumulate virulence traits and to cause more severe symptoms. In spite of the long reproductive cycle, the domestication and deployment of homogeneously resistant cultivars is imposing selection pressures that are comparable to those described in annual crops.
Eucalyptus, poplars, and pines are among the most advanced trees on the domestication gradient in woody perennials. Yet, these trees grown for fiber and wood have been domesticated for less than a century, compared with thousands of years for most crops. However, the global deployment of fast-growing clones and interspecific hybrids carrying resistance genes in quasi-monoclonal stands over several decades has imposed a strong selection pressure on pathogen populations. One of the best examples is the European poplar leaf rust pathogen, Melampsora larici-populina, that undergoes demographic fluctuations consistent with a history of rapid adaptation of the pathogen in response to the deployment of resistance genes in the cultivated poplars. Rapid fixation of the Melampsora larici-populina virulence factor corresponding to a widely deployed resistance gene (R7) in poplar cultivars has resulted in the emergence of a unique, homogeneous and virulent rust genetic group that replaced the initial population in the North of France where the sexual host is absent (Persoons et al. 2017). By contrast, the more diverse Melampsora larici-populina population in Southern France, where the sexual host, larch, is present, was at equilibrium on the wild poplar Populus nigra (Xhaard et al. 2011, 2012).
Perhaps the proximity of natural populations of both pathogens and hosts in a forestry context can serve as a buffer to restore diversity. The bottleneck signature in the Melampsora larici-populina populations on cultivated resistant poplars was erased rapidly and genetic diversity was gradually increased over time. This contrasts with the usual pattern of host tracking associated with a reduction in diversity away from the center of domestication of the host plant (e.g., wheat yellow rust and apple scab; Ali et al. 2014; Gladieux et al. 2008). The presence of naturally occurring sexual populations in relatively close proximity could explain the rapid increase in genetic diversity (Persoons et al. 2017).
Increasing forest productivity: A tree pathogen paradise.
The rapid intensification of forestry is likewise having an impact on the evolutionary and demographic history of pathogens that have a long coevolution history with their host trees. The combination long-lived host with low diversity often deployed in clonal plantations could create ideal conditions for disease outbreaks. However, while the impact of forest management practices on genetic diversity and structure of forest trees is particularly well documented (Ratnam et al. 2014), their consequences on tree-pathogen populations remain poorly documented. Most significant examples available are those related to the impact of industrial large-scale plantations and monocultures (e.g., European poplar leaf rust Melampsora larici-populina described above). Indeed, the plantation of monospecific (or in some cases monoclonal) forests represents an extreme case on the spectrum of forest management practices (Fig. 1B). The increase of such a forest system in the last 50 years has provided favorable conditions for the build-up and spread of local pathogen populations (Labbé et al. 2015; Sakalidis et al. 2016; Tabima et al. 2020; Xhaard et al. 2011).
Two striking examples are Dothistroma septosporum and Armillaria ostoyae with the domestication and expansion of pine (Pinus spp.) cultivation. At least three isolated genetic lineages of the Dothistroma needle blight (DNB) pathogen D. septosporum emerged following the introduction and establishment of commercial plantations of the Monterey pine, Pinus radiata, in the Southern Hemisphere (Barnes et al. 2014; Bradshaw et al. 2019). Each of these genetically isolated DNB lineage arose from a highly diverse genetic pool in the endemic area of DNB in the Northern Hemisphere and have a clonal structure consistent with a scenario of recent introduction of a few founder individuals and high adaptation potential to their host (Bradshaw et al. 2019). In Southwestern France, the large monospecific plantation of maritime pines (Pinus pinaster) in the Landes de Gascogne during the nineteenth and twentieth centuries favored the expansion of the native root and butt-rot pathogen Armillaria ostoyae. The best fitting models using genome-wide single nucleotide polymorphism (SNP) and microsatellite markers are consistent with the recent and intensive pine plantation accelerating the rapid spread and success of the root pathogen (Dutech et al. 2016; Labbé et al. 2017).
Tree genetic improvement programs are still at the stage where they are capitalizing on the range-wide capture of trait variation of valuable tree species by establishing tree provenances and progeny trials (Koskela et al. 2014). However, transfer of germplasm and genetic material have increased the risk of emergence and spread of diseases (Koskela et al. 2014). There have been a significant number of documented examples of introduction of exotic pathogens of trees while transferring reproductive material (Liebhold et al. 2012). Introduction and intensive plantation of new host species may also provide an opportunity for the rapid emergence of modified pathogen populations and new diseases. The intensification of poplar cultivation in North America resulted in the emergence of a new disease with the rapid change of an innocuous foliar pathogen into a destructive and epidemic canker pathogen (Bier 1939; Thompson 1941). The ascomycete fungus Sphaerulina musiva, previously known as a necrotic leaf-spot pathogen on the native eastern cottonwood Populus deltoides (Bier 1939; Thompson 1941), adapted to infect and colonize poplar woody tissues as a result of horizontal transfer of genes from prokaryotes and fungi associated with wood decay (Dhillon et al. 2015). The pathogen population structure shows a strong association between multiple pathogen introductions and dissemination, creating genetic admixture, and poplar culture (Sakalidis et al. 2016; Tabima et al. 2020).
BRAVE NEW WORLD: NEW SOLUTIONS TO TACKLE THE RISKS ASSOCIATED WITH A CHANGING ENVIRONMENT
In several of the examples aforementioned the selective pressures exerted on pathogen populations by host domestication are intensified by secondary threats arising from anthropogenic activities. The risk and impact of factors related to the acceleration of anthropogenic activity on the diversity and evolution of plant pathogen populations has been extensively documented and discussed (Corredor‐Moreno and Saunders 2020; Desprez-Loustau et al. 2007; Fisher et al. 2012; Hamelin and Roe 2020; Stukenbrock et al. 2011). In theory, the impact of threats such as the introduction of invasive alien exotic species and global climate change on domesticated crops and natural systems should be highly variable and will depend on factors associated with the host and pathogen affected.
One of the challenges when an invasive alien pathogen is introduced is that the host has either not coevolved with the pathogen, and therefore resistance genes are at extremely low frequency or absent, or in the case of domesticated species, resistance has been integrated during traditional breeding cycles of the crop species or the host is simply not bred for resistance to that alien pathogen (Zhan et al. 2015). The introduction of sugarcane rust in the Americas and wheat stripe rust in Australia are some examples (Purdy et al. 1985). Introduction of invasive alien forest pathogens have caused irreversible damages and changes at the landscape level largely due to the absence of any resistance in the hosts (Loo 2008). Natural forests are more heterogeneous and diverse, suggesting a high potential for resilience to biotic stresses. However, the effect of exotic pathogen introductions seems to be strongly dependent upon pathogen biological traits and host ecological features (Lovett et al. 2006).
The new domestication toolbox to counter pathogens in a changing environment.
It is becoming clear that anthropogenic changes to the planet have to be countered with novel innovative approaches to reduce the threats on global food security and environment (Fones et al. 2020). Minimizing the effect of the changing environment on pathogens on crops and trees and mitigating their risk is becoming an urgent task as rapid increase in the global population is accelerating the need for increased agricultural production. New technologies are available to answer this need. While traditional breeding has increased yield or resistance to pests and pathogens, it remains a slow process, in particular for species with long reproductive cycles, that is unlikely to keep pace with the predicted demand. The new domestication toolbox comprises the recent advances in management practices, new sources of genetic diversity, genomics and biotechnology applied to breeding. This is broadening the possibilities of crop and tree growth and resilience optimization to find the right balance between productivity and sustainability in a changing environment. The lessons learned with the impact of plant domestication and management on crop and forest pathogen populations should guide the usage of this toolbox.
From plants to landscapes, diversity is the key.
The anthropogenic impacts on crops and trees result in homogenization and reduction in species and genetic diversity. The future of sustainable crop and tree protection relies on increasing plant cropping and forest systems and landscape diversity (Hajjar et al. 2008; Storkey et al. 2019). The intuitive idea of a positive association between landscape complexity and pest control has developed into an agroecological paradigm (Chaplin-Kramer et al. 2011; Gurr et al. 2003). Species richness had a positive effect on both pollination and pest control and a negative effect of landscape simplification on these ecological services (Dainese et al. 2019; Karp et al. 2018; for conflicting view see Dainese et al. 2019). At the genetic level, increasing diversity by planting crop cultivars with different resistance genes or gene stacks can reduce or prevent pathogen attacks (Mundt 2002). Ultimately, a sustainable future for agroecosystems and forestry could lie in the combination of different techniques and technologies improving the plants as well as informed management practices increasing diversity thus promoting ecological services.
Forests can range from unexploited ecosystems with minimal human impact such as old-growth, the late stage of forest development characterized by climax communities and large trees (Franklin 1981), to planted forests and fragmented habitats with different levels of forest management practices for wood production and agroforestry ecosystems where trees are managed as perennial production systems around or among crops or pastureland. Agroforestry is a direct response to a need for more diverse and sustainable agroecosystems; this system provides direct benefits such as carbon sequestration (Banerjee et al. 2016) and can help reduce the loss of biodiversity and ecosystem services (food, wood, and fiber) from intensive agricultural systems (Santos et al. 2019). In addition, the increase of diversity in agroforestry systems (higher genetic diversity, mixed planting, enhanced species richness) increases yields and pollinators and provides better weed and pest suppression (Isbell et al. 2017).
Modern breeding strategies: Searching for new resistance and adapting to the changes.
One-way plant breeders have found to mitigate the pest and pathogen problems is the generation of durable and broad-spectrum disease resistant crop cultivars. Sequencing technologies coupled with the availability of annotated crop genomes have significantly increased the pace with which disease resistance genes are selected or cloned (Keller et al. 2018). So far, modern breeding practices have exploited a very limited fraction of the crop diversity (Wang et al. 2017). There are still many possible sources of diversity available, e.g., wild relatives, landraces, and exotic germplasm accessions, that can be incorporated in breeding strategies and converted in long-term genetic gain (Dempewolf et al. 2014; Wang et al. 2017). They provide a promising basis to transit toward efficient crop breeding that will combine productivity and resilience to biotic and abiotic stresses.
Screening sources of diversity for pathogen resistance and adaptive traits.
Identification of resistance and adaptive traits in different sources of diversity remains a challenge. Advanced high-throughput genomics, phenomics and biotechnology tools can be used to identify markers associated with important traits such as drought tolerance in maize seedlings (Wang et al. 2016), deep-sowing tolerance in rice (Zhao et al. 2018) or seedling heat tolerance in winter wheat (Maulana et al. 2018). The use of whole-genome prediction models incorporating identified and characterized resistance genes can be effectively applied to select for quantitative disease resistance (Poland and Rutkoski 2016). This approach has been tested for a variety of crop and tree fungal diseases such as Fusarium head blight of wheat and barley (Mirdita et al. 2015; Sallam et al. 2015), stripe and stem rust of wheat (Ornella et al. 2012), cassava anthracnose (Ly et al. 2013) and chestnut blight of American chestnut (Westbrook et al. 2019) with variable success.
Hardwood trees have large genomes, coming from multiple whole-genome duplication events and the presence of abundant repeated elements. Since the first assembly of the Populus trichocarpa genome in 2006, a growing number of association studies have emerged in a variety of wooden plant species such as poplar (Populus trichocarpa and Populus deltoides) (Chhetri et al. 2019; Fahrenkrog et al. 2017; McKown et al. 2014), lodgepole pine (Parchman et al. 2012) or white spruce (Lamara et al. 2018), identifying loci associated with a wide range of phenotypic traits. The number of forest tree breeding programs that are now including durable resistance (or tolerance) to pests and pathogens has drastically increased. In Norway spruce, a genome-wide association study discovered candidate SNPs associated with larger necrotic lesions from Heterobasidion parviporum (Mukrimin et al. 2018). This study, and similar ones (Liu et al. 2018b; Resende et al. 2017; Vázquez-Lobo et al. 2017) provide information on the genetic architecture of traits and the identification of valuable markers involved in development, morphology, resistance to pathogens, or to harsh environmental conditions. One drawback of these approaches, however, is the lack of functional validation of promising candidate genes, due to the biological features particular to long-lived trees.
Engineering and editing the genomes of crops and trees to increase resistance to diseases.
The availability of genetic engineering tools such as transgenic expression of host/pathogen genes, RNA interference (RNAi) in agroecosystems could present rapid approaches to improve disease resistance in crops. With better understanding of host−microbe interactions, these tools can be effectively used to develop durable disease resistance (Schweizer 2019). RNAi-based biopesticides are based on topical application of double-stranded RNAs (dsRNAs) complementary to pathogen genes and can induce gene silencing in a specific pest (Fletcher et al. 2020). Use of dsRNA-based silencing has been reported with variable success for various plant fungal pathogens (Fletcher et al. 2020; Gill et al. 2018; Höfle et al. 2020; Hu et al. 2020). This method also offers perspectives in forestry with promising results in insect pest management as tested with the devastating mountain pine beetle (Kyre et al. 2020) and emerald ash borer (Leelesh and Rieske 2020). Beside the apparent effectiveness of this technology, the commercial use of dsRNA based biopesticides could be restrained by excessive cost and lack of effective delivery methods on a commercial scale, especially in forest plantations.
The success of genetically modified crops lies in finding target genes for genetic manipulation. Multiple disease resistance genes (pleiotropic genes) such as Lr34 (in wheat) have great potential. Lr34 encodes an ATP‐binding cassette transporter and confers resistance to stem rust, stripe rust, leaf rust, and powdery mildew of wheat. In addition to wheat, Lr34 is also effective against biotrophic pathogens of rice, barley, sorghum, and maize when expressed transgenically (Sucher et al. 2017). Transgenic crops carrying single or multiple R genes may put strong selection pressure on the pathogen and increase chances of disease epidemics in monocultures. However, how transgenic crops impact natural plant pathogen populations has not been well studied yet.
Genome editing (GE) utilizes mechanisms discovered in nature to change specific nucleotides within the plant genome. Over the last decade, the use of targeted genome editing technologies such as CRISPR/Cas9 has exploded in a variety of organisms. GE is a powerful tool for crop improvement and has already been widely used to modify plant immunity and increase pathogen resistance (Andolfo et al. 2016). For instance, mildew resistant plants have been generated by manipulating host susceptibility genes in wheat (Wang et al. 2014) and resistance to Magnaporthe oryzae was generated by modifying the ethylene pathway in rice (Liu et al. 2012). Although GE using CRISPR/Cas9 has become a viable approach to knock-out genes in fruit trees, such as citrus, apple, grape, cassava, coffee, and kiwifruit, site-specific gene targeting or allele replacement remains a major challenge in tree species (Bewg et al. 2018). The use of CRISPR/Cas9 in forestry and in forest pathology is in its infancy, yet offers great potential for disease control (Dort et al. 2020). In poplar, CRISPR-based gene editing has successfully been used to knock-out 4CL genes, associated with lignin and flavonoid biosynthesis (Zhou et al. 2015).
Combining tree genetic improvement with adaptation to climate.
Historically, foresters have taken the “local is best” approach to selecting reforestation seed sources. Tree breeding programs usually apply the same approach by operating within breeding zones. Climate fluctuations are starting to disrupt historical local adaptation and tree populations are simultaneously challenged to withstand the consequences of novel climates and unable to adapt or migrate rapidly enough to remain locally adapted (Aitken et al. 2008). Many current tree improvement programs are trying now to incorporate assisted gene flow to match reforestation with climates expected in the future. Tree improvement programs in Alberta and British Columbia (Canada) are designing climate-based seed transfer systems to mitigate adaptive discordance between tree genotype and climate (Gray et al. 2011; O’Neill and Ukrainetz 2008). Such an approach also necessitates a deep knowledge of genetic variation in climatically adaptive traits in breeding populations but also, genetic structure and pathogenicity profiles of present and future pathogen populations.
Epidemic outbreaks of the endemic pathogen Swiss needle cast, a foliar disease of Douglas fir caused by Nothophaeocryptopus gaeumannii have steadily increased in severity since the 1980s in response to rising winter temperatures, spring/summer precipitations, and changes in forestry practices (Agne et al. 2018; Mildrexler et al. 2019; Ritóková et al. 2016). Similarly, extensive tree mortality caused by DNB on lodgepole pine have been associated with key environmental factors that directly affected the life cycle components and biological traits of the pathogen, leading to recent increases in disease incidence and severity (Woods et al. 2005; Welsh et al. 2009). A population genomics study (Capron et al. 2021) identified four distinct DNB genetic lineages that diverged at the end of the last glacial maximum before recolonization of lodge lodgepole pine in western North America. A unique genetic lineage is present in the areas most affected by the climate-driven outbreak. This knowledge on the DNB population structure will inform future movements of planting material and assisted gene flow practices, preventing some secondary contact between genetically isolated DNB lineages that could result in new epidemics.
The planet’s ecosystems have been changing during the Anthropocene, with a global homogenization of plant species and genetic make-up and an intensification of production. This is a recipe for promoting the emergence of plant diseases or the adaptation and specialization of novel pathogens. In spite of the remarkably different characteristics of crop plants and forest trees, we find that similar processes such as hybridization, host jumps, selection, specialization, and clonal expansion are shaping the populations of pathogen of both crops and forest trees, in particular in cases where trees have been domesticated and are grown in managed plantations. Genomic tools to monitor pathogen populations can help identify lineages with increased virulence, different geographic origin or mating types or other adaptive traits (Hamelin and Roe 2020; Weldon et al. 2021). In some cases, this will directly influence disease management, for example to eradicate a lineage of Phytophthora ramorum and prevent potential mixing of different mating types (Grünwald et al. 2019). Genomics also provides the most promising solutions to discover and clone resistance genes or to develop biopesticides to rapidly address plant health issues. We propose that integrating these monitoring and management tools will lower the probability of global pathogen outbreaks so that we can envision better management strategies to sustain global food production as well as ecosystem services.
The author(s) declare no conflict of interest.
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First and second authors contributed equally to this work.
The author(s) declare no conflict of interest.