Effects of phytopathogens on plant community dynamics: A review

Acta Ecologica Sinica 35 (2015) 177–183

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Effects of phytopathogens on plant community dynamics: A review Tao Chen, Zhibiao Nan ⁎ The State Key Laboratory of Grassland Agro-ecosystems, College of Pastoral Agricultural Science and Technology, Lanzhou University Lanzhou 730020, China

a r t i c l e

i n f o

Article history: Received 9 April 2014 Received in revised form 13 January 2015 Accepted 15 February 2015 Keywords: Plant pathogens Plant communities Plant diversity Coexistence Janzen–Connell hypothesis Plant–soil feedbacks

a b s t r a c t The impacts of phytopathogens on agricultural systems, disease controls and economic losses caused by the pathogens are internationally important research subjects. Recently, increasing evidence has shown that phytopathogens play a critical role in mediating competitions among their host plant species. According to Chesson's coexistence framework, niche differences (i.e., species differences in resource use, host-specific pathogen loads, and other ecosystem processes) are more associated with intra-specific limitation than with interspecific limitation. However, fitness differences (i.e., variations in competition abilities among plant species) can determine the dominance of plant species. An increase in niche differences tends to promote the coexistence of plant species, whereas an increase in fitness differences tends to exclude competing species. In this review, two types of pathogen mechanisms that could affect plant communities are discussed based on the coexistence framework. Type I is the density-dependent pathogen mechanism, in which disease occurrence in a community is related to the density of host species. In this mechanism, disease transmission increases niche differences as a host species becomes common, and/or reduces niche differences as a host species becomes rare. Type II is the density-independent pathogen mechanism, in which disease transmission does not depend on host plant density. This mechanism mainly focuses on fitness differences. When competitively dominant host plants are more susceptible to pathogens, pathogens can reduce fitness differences among species and thereby improve plant diversity. Alternatively, if the competing species are more resistant than other species to pathogens, fitness differences are prone to be increased. The Janzen–Connell effect (JC effect) and plant–soil feedback theory are characterized by Type I phytopathogen mechanism and are discussed here in details. The JC hypothesis has been mostly applied to forest ecosystems, whereas the plant–soil feedback theory has been applied more widely in several ecosystems. The JC hypothesis assumes that seeds/seedlings around the mother plant are most susceptible to host-specific pathogens. Since seed/seedling mortality caused by pathogens is related to plant density, the JC effect is an example of negative density dependence. The plant–soil feedback theory illustrates the interactions between plants and soil. Plants can alter soil properties through the input of organic matter and chemicals, and provide habitats and nutrients for soil organisms, which in turn can affect plant performance. This feedback can be either negative or positive, depending on whether it leads to a net reduction or an enhancement of plant growth when comparing the plant species cultured in soil conditioned by the plant to that in mixed soil. This review summarizes phytopathogen effects on plant diversity, plant invasion, community succession, and addresses some future research challenges. Several research goals are highlighted; for instance, studies of pathogens with multiple hosts and host plants with multiple pathogens are necessary for a better understanding of the role of phytopathogens in plant community dynamics. Research on the interactions of plant pathogen with soil legacy (priority) could provide new insights into the influences of phytopathogen on plant communities during climate change. In addition, a combination of theoretical modeling and field studies would be an effective way to examine the function of phytopathogens in plant community dynamics. © 2015 Published by Elsevier B.V.

1. Introduction In agricultural ecosystems, plant pathogens not only negatively affect seedling survival and growth, but also reduce crop production and quality, which results in a great economic loss [1–2]. Until now most ⁎ Corresponding author. E-mail address: [email protected] (Z. Nan).

http://dx.doi.org/10.1016/j.chnaes.2015.09.003 1872-2032/© 2015 Published by Elsevier B.V.

of the work on plant pathogens has been focused on how to control and lower disease occurrences, while the function of pathogens in natural ecosystems has not been thoroughly investigated. Plant pathogens can transmit horizontally via vectors such as soil, water and insects, as well as vertically via mother plants [3]. Some pathogens are specific for certain plant species, while others that are nonspecific have a broad range of hosts. Hence, plant pathogens may play different roles among species within a community [4–5]. In this paper,

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we summarized the available mechanisms by which plant pathogens affect species composition and community dynamics, reviewed recent research developments in this area, and discussed the possible directions for future research. 2. General roles of plant pathogens in plant communities The interactions between plants and pathogens can promote or exclude species coexistence. Plant pathogens can influence community stabilities when their impact on plant growth relies on host relative abundance [6]. For example, host-specific pathogens increase as their preferred host becomes abundant in a community, thus limit further growth of the host, which is beneficial to the stabilization of the community [7–8]. When the impact of pathogens on communities does not depend on host abundance, it often alters fitness differences among plant species and indirectly affects species coexistence [6]. For instance, some pathogens that have a broad range of hosts can transmit among a variety of plant species. When the infection of these pathogens on rare species exceeds that on dominant species, it will lead to the further growth of highly competitive species, and cause the increase of fitness differences that might destabilize the whole community [9]. 3. Mechanisms of plant pathogen effects on plant communities In a community, plant species have niche differences that promote coexistence and fitness differences, which exclude coexistence. Niche differences should overrule fitness differences, if plant species coexist persistently in an ecosystem. This is referred to as Chesson's coexistence framework [10] (Fig. 1). Here we synthesized the major theories on how pathogens influence plant communities based on this framework. The theories include density-dependent mechanism that affects niche differences of plant species, and density-independent mechanism that affects fitness differences (Table 1). 3.1. The Janzen–Connell hypothesis Janzen (1970) and Connell (1971) hypothesized that specific enemies can maintain rainforest diversity by controlling the density of dominant species. That is, specific enemies such as predators or pathogens can effectively infect hosts and limit their further growth as host abundance increases in the community. In tropical ecosystems, seed dispersal from seed rains leads to a high seed density near the mother plant, which makes the seeds more susceptible to specific enemies and causes high seed and/or seedling mortality. This phenomenon is called the Janzen–Connell effect (JC effect). The JC effect is also known as negative density dependence (NDD), as the effect is associated with density of a population and the population was negatively mediated by the enemies.[11–12].

Table 1 Mechanisms by which pathogens affect plant community dynamics. Mechanisms

Plant community

A) Density-dependent pathogens a) Stabilization: disease transmission increases as a species becomes common. Janzen–Connell hypothesis grasslands [16];forests [7,13,44–45]; Negative plant–soil feedbacks grasslands [47–50];fields [24,51];forests [52,53]; Density-dependent attack grasslands [54]; forests [55] Density-dependent cost of infection fields [32,56,57] Disease response to host diversity grasslands [58,59]; fields [60–62] b) Destabilization: disease transmission increases as a species becomes rare. Pathogen spillover grasslands [9]; forests [33,63] Positive plant–soil feedbacks grasslands [26,34] B) Density-independent pathogens a) Reduced fitness differences: competitively dominant species experience the greatest cost during pathogen infections. Equalizing trade-offs grasslands [37,38,64]; forests [65,66]; fields [67] Enemy release of invading plants forests [39] Agriculture and biocontrol fields [40,68] b) Fitness hierarchy reversal/increased fitness differences: susceptible hosts face extreme fitness costs. Pathogen-driven succession deserts [69–71]; forests; fields [72] Highly virulent epidemics forests [42] Note: Modified from Mordecai [6].

To prove the JC effect, ecologists have paid much attention studying the role of pathogens in influencing species diversity. They hypothesized that pathogen accumulation near mother plants can reduce the survival and growth of conspecific seedlings owing to a high seed density, and consequently provide space for plant species with the same resource requirements [13–14]. For example, Augspurger [15] monitored the seed germination and seedling survival of a winddispersed tree Platypodium elegans on Barro Colorado Island, Panama for one year, and found that both the incidence and the rate of seedling damping-off caused by fungal pathogens were negatively correlated with the distance from the parental tree. Bell et al. [8] in the Chiquibul Forest Reserve near the Las Cuevas Research Station also examined the relationship between the seedling survival rate of tropical forest plant Sebastiana longicuspis and the plant population density. Their finding was that seedling survival was three times higher at low density in the non-fungicide-treated plots, whereas it was unaffected by density in the fungicide-treated plots, suggesting that the application of fungicides may kill soil pathogens and increase seedling survival. Though the JC effect was proposed for tropical forest systems, it has also been applied to other ecosystems such as grassland [16] and ocean systems [17]. For instance, Petermann et al. [16] conducted a controlled greenhouse experiment with 24 species planted in soil from field monocultures, which revealed the JC effect on plant dynamics in the European temperate grasslands. The results showed that the reduction of biomass in monoculture was due to the build-up of soil pathogens, which indicated that the JC effect might play a critical role in driving plant diversity in temperate ecosystems. 3.2. Plant–soil feedbacks

Fig. 1. The theoretical framework describing how interactions of plants with pathogens influence plant community dynamics [10]. The figure is adapted and substantially modified by Mordecai [6]. The x-axis measures the strength of stabilization or destabilization, and the y-axis measures the fitness differences between species.

Plants can alter soil properties through the input of organic matter and chemicals, which in turn affect plant performance. This process is referred to as plant–soil feedbacks (PSFs) [18–20]. There is increasing evidence that soil pathogens have an important function in the process

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of PSFs either by directly infecting plants or indirectly by altering soil properties [21–23]. For example, Mills and Bever [24] found that Pythium fungi isolated from the roots of Danthonia spicata and Panicum sphaerocarpon was more pathogenic to the two hosts than to the other two species, Anthoxanthum odoratum and Plantago lanceolata, suggesting that the accumulation of species-specific soil pathogens could account for the previous observation of negative feedbacks on plant growth. Plant–soil feedbacks can be positive by improving plant growth, or negative by restraining growth [18] (Fig. 2). Most studies on positive PSFs focused on soil mutualists such as AM fungi and N-fixing bacteria that can promote the plant uptake of soil nutrients [25]. The function of soil pathogens during the process of positive PSFs was rarely studied. However, Batten et al. [26] found that soil conditioned by Aegilops triuncialis exhibited negative effects on the native plant Lasthenia californica by delaying the flowering date and decreasing the aboveground biomass. The results indicate that invasion-induced changes in soil microbial communities may contribute to a positive feedback that increased the chance of successful invasion by Aegilops triuncialis. By contrast, the role of pathogens in negative feedbacks to plants has been extensively studied. A negative feedback is that the increase of plant abundance leads to the build-up of specific pathogens, which in turn limits the further expansion of this plant in the community, and therefore provides space for other inferior species and maintains species diversity [27] For example, Reinhart [28] investigated the direction of PSFs in different types of grasslands in Northern Great Plains Steppe ecoregion of North America. He found that negative PSFs were present from rare to dominant species and predominated across the three types of grasslands, suggesting that negative PSFs have a great potential to drive species coexistence in grasslands. 3.3. Other mechanisms on plant pathogens promoting system stability In addition to JC effects and negative PSFs, other pathogen-mediated mechanisms can also explain species coexistence. These mechanisms include density-dependent cost of infection (DDCF) [29] and disease response to host diversity [30]. One good example of DDCF is the promotion of vegetative growth by increasing the cost of sexual reproduction [31]. For instance, a castrating endophyte infection benefits the growth of Agrostis at low density, but problems arise at high density due to the reduced seed production [32]. The theory of disease response to host diversity is widely used in agriculture [6]. An example of this theory is that increasing crop species can reduce the occurrence of diseases. 3.4. Mechanisms on plant pathogens destabilizing systems Apart from promoting species coexistence, pathogens can also exclude species in communities, resulting in the destabilization of ecosystems [33–34]. This principle contains two important mechanisms: positive PSFs that has been discussed above, and pathogen spillover that we will address as follows.

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In the pathogen spillover mechanism, some plant species that are highly resistant to specific pathogens can be regarded as pathogen reservoirs. When the abundance of hosts in a community increases, pathogen reservoirs accumulate and the performance of less competitive species is impaired, resulting in the dominance of host plants in the community [9]. For example, Cobb et al. [35] studied the function of Phytophthora ramorum, a shared exotic pathogen, in the competition of canopy trees in California coastal redwood forests. The results showed that the inoculation of P. ramorum on California bay laurel (Umbellularia californica) had a great impact on the mortality of a competing species, tanoak (Lithocarpus densiflorus). Beckstead et al. [36] also found that an invasive annual weed cheatgrass (Bromus tectorum) acted as a reservoir for Pyrenophora semeniperda, a multiple-host fungal seed pathogen, and had appreciable influences on the co-occurring native grasses. 3.5. Effects of plant pathogens on fitness differences Pathogens can also influence the composition and dynamics of communities by altering fitness differences regardless of host abundance. Pathogens may decrease fitness differences via infecting highly competitive species, or increase fitness differences through infecting inferior species [6]. Mechanisms relating to lower fitness differences consist of equalizing trade-offs, [37–38] enemy release of invading plants, [39] and agriculture and biocontrol, [40] while mechanisms associated with increased fitness differences include pathogen-driven succession [41] and highly virulent epidemics [42] (Table 1). To date, most of the work on fitness differences emphasizes how to promote species coexistence by reducing the competitive abilities of dominant species, and how to benefit invaders by lowering the performance of native species. For example, Borer et al. [43] found that the prevalence of Barley yellow dwarf viruses reduced the dominance of California's native species and contributed to the invasion of European annual grasses. However, the evidence of above mechanisms affecting community dynamics is still lacking. 4. Impacts of plant pathogens on species diversity, biological invasion, and community succession Both JC effects and PSFs aim to explain the role of pathogens in plant communities, and thus the two mechanisms share some similar features. The JC effect is related to host density, while a negative PSF is associated with host abundance. In a typical example, Pack and Clay [46] in the temperate forests of North America found that seedlings close to their parents were more susceptible to Pythium fungi. The possible explanations are that the intensity of Pythium fungi was higher near the parent trees due to a high seed density (a JC effect), or that the build-up of Pythium close to the parents reduced the survival of seedlings to maintain species diversity in the community (a negative PSF). Besides the similarities, JC effects and PSFs differ in specific research areas. The JC effect puts emphasis on how pathogens affect species diversity and productivity in forests, while PSFs involve pathogen effects on community dynamics, [46] succession, [73] and invasion [74] and could be applied to a wider range of ecosystems (forests, grasslands and agricultural ecosystems, etc.). 4.1. Janzen–Connell hypothesis studies

Fig. 2. Illustration of the interaction mechanisms between soil pathogens and plants. The arrows and circles indicate the direction of beneficial and detrimental effects, respectively. The thickness of the lines indicates the relative strength of these effects (Modified from Bever, [27]).

The JC effect was firstly proposed for tropical forest ecosystems, and therefore most of the work has been done with tropical trees [75]. This is possibly because sufficient rainfall and suitable temperature proliferate soil pathogens, which in turn bring about a greater impact on tropical forests [76]. However, the study of Hille Ris Lambers et al. [7] in temperate deciduous forests of North Carolina argues that JC effects are more prevalent at tropical latitudes. They reported that the

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proportion of species affected by soil pathogens in temperate forests is equivalent to that in tropical forests. Although the effects of pathogens on plants seem not to be limited in forests, the application of JC effects to other ecosystems is rare, except few research conducted in grasslands [16]. A possible reason is that other ecosystems such as grasslands may not be as significant as forest ecosystems in maintaining the global climate, which led researchers to conduct more investigations on forests than on grasslands. Another more important reason might be that the belowground roots of various species intersect with each other in grasslands, making it difficult to determine the effects of soil pathogens on a particular species at the population level. Therefore, future work on JC effects in grasslands should be conducted at the community level.

[82] reported that in the Western Ghats of India, the arrival of an extensively destructive tropical weed, Chromolaena odorata, resulted in a dramatic rise of generalist soil borne fungi, Fusarium semitectum, and created a negative feedback for native plant species. However, a study by Nijjer et al. [83] in Big Thicket National Preserve (BTNP) in east Texas, USA, found that a stronger negative PSF exhibited on the invasive plant species Sapium sebiferum than on native species, indicating that soil pathogens may act as an inhibitor to limit the further expansion of invasive species when they occur in high abundance. The failure of exotic plants introduced to a new habitat is probably due to the change of PSFs during the invasion process [84]. For example, Diez et al. [85] found that the direction of PSF for 12 exotic plants was negatively correlated with the invasion time.

4.2. Interactions between pathogens and plant diversity

4.4. Community succession driven by PSFs

Ecologists have done a lot of work to determine the role of fungal pathogens and insect herbivores in structuring plant diversity [13–14]. For example, Bagchi et al. [45] performed a field experiment in Chiquibul Forest Reserve, Belize to test whether the JC effect has a community-wide role in maintaining tropical forest diversity. Experimental plots were treated with fungicides and insecticides, respectively, and seedling emergence and survival in these plots were observed. The results showed that seedling establishment was negatively density dependent (NDD) and species diversity was maintained at a high level in the untreated plots, whereas the effects of NDD were barely observed in the fungicide-treated plots and seedling species diversity dropped greatly. By contrast, the insecticide application did not alter species diversity, though it greatly increased seedling recruitment and caused a marked shift in species composition. This is the first field study explicitly demonstrating that fungal pathogens are more important than insects in determining niche differences and species diversity.[77] Pathogens affect species diversity, which in turn affects the intensity of pathogens. The loss of plant diversity can either increase or decrease the occurrence of disease on a theoretical basis, but most studies showed that it increased disease transmission [78]. For example, Schnitzer et al. [58] studied the effects of soil pathogens on plant productivity by combining an analytical model and a series of field experiments, and found that plant disease decreased with increased diversity and the productivity was increased by 500%. A similar study was done by Maron et al. [59] in western Montana grasslands, where the effects of soil pathogens on plant productivity was assessed by fungicide application. The results showed that the aboveground biomass was positively correlated to plant diversity in the untreated plots, whereas this relationship did not exist in the fungicide-treated plots. Fungicide application increased the plant production by 141% in the low-diversity plot and only by 33% in the high-diversity plot, indicating that soil pathogen intensity was inversely proportional to plant diversity.

By far, the role of PSFs in community succession has been extensively studied worldwide [41,86]. The direction of PSFs varies at different successional stages [87]. In the early successional stage, positive PSFs dominate across the community [88]. Since the original soil is short of nutrients, soil mutualists such as AM fungi and N-fixing bacteria may promote the uptake of soil nutrients by plants, thereby a positive PSF is displayed [89]. With the increase of plant abundance, specific soil pathogens start to cause negative PSFs by reducing the competitive ability of the early species and promoting the growth of the late species [90]. A typical example of this negative PSF is the succession of a foredune grass Ammophila arenaria, which performed very well in mobile dunes as it could escape from soil pathogens. However, the grass degenerated in stable dunes, probably because the exposure of the roots to soil pathogens created negative PSFs. In addition, primary successional species in abandoned fields are more susceptible to soil pathogens than secondary successional species [73]. The early succession contributes to the establishment of soil biota that can boost the development of a community and lead to a secondary succession [91]. Kardol et al. [87] held the opinion that the early stage of secondary succession is associated with negative PSFs, which accelerates the turnover of plant species, whereas the late stage of secondary succession is associated with positive PSFs, which is beneficial to community stability. With the development of succession, both plant species and soil biota change constantly, making the effects of PSFs on community dynamics in later stages unclear. Hou [92] investigated the survival of seed and/or seedlings by applying fungicides in plots with different grazing intensities in western China. The results indicate that livestock grazing had an impact on soil pathogens. However, further research is needed to address the combined effects of grazing and soil pathogens in community.

4.3. Explanations for biological invasions

The research in plant pathogens affecting community composition and dynamics is an important branch of species coexistence study. Nevertheless, most of the work was based on a specific plant species with a specialized pathogen. How pathogens with multiple hosts and host plants with multiple pathogens interact with each other still remain unclear. For example, the JC effects were extensively studied on the survival of conspecific plant seedlings exposed to a high density of soil specific pathogens, but the influences of pathogens on neighboring species were not well studied [26]. The study of PSFs is usually performed by comparing the growth of a plant species in soil conditioned by its own (home) and that in soil conditioned by a mixture of other plants (foreign). Plants can change soil properties as well as the composition of soil microorganisms. The differences in soil chemical compositions may also result in a difference in plant growth; therefore, the effects of soil pathogens could be overestimated in some cases [20]. In addition, the variance of experimental designs and data analysis can either amplify or diminish the

There are several explanations for the success of plant invasions. One explanation is that the new community is lacking in specific pathogens for invaders, which suffer from a negative feedback by soil pathogens in their original community [79]. For example, Klironomos [74] performed an experiment investigating the role of soil microbes in PSFs with five native and five invasive plant species. He found that when grown in monoculture, the native species suffered more seriously from specific fungal pathogens than the invasive species. Further studies revealed that it was caused by the lack of specific fungal pathogens when invasive plants entered the new habitat, rather than by a positive PSF resulted from AMF [80]. The second explanation for invasion success is that even though exotic plant species introduced to a new habitat may experience a negative PSF originated from soil pathogens, the degree of feedback is far less than that to the native species [81]. For instance, Mangla et al.

5. Future challenges

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effect of pathogens on plant growth [93]. Furthermore, soil legacies generated by field plants could be long-standing, even though the soil has been sterilized [94]. As for the first problem, we can separate the effects caused by soil chemicals through measuring the chemical contents of the soil. The second and the third problems cannot be solved at present; hence new approaches or novel technologies are required for future research.

5.1. Explanation for soil legacies and priority effects The influences of a plant species on soil can exist for a period of time, even though the species has disappeared completely from the community. This is referred to as soil legacies [95]. Correspondingly, the first arrival species in a community can suppress the growth of the late arrival species, which is coined as priority effects [96]. Both soil legacies and priority effects have great impacts on species diversity and productivity [97]. Grman and Suding [98] believed that priority effects are associated with plant competition, as the first-coming species occupy space and utilize resources and suppress the growth of the second-coming plants. Van de Voorde et al. [99] found that the growth of the early successional Jacobaea vulgaris was inhibited by its own-conditioned soil, and also by half of the co-occurring plants, suggesting that the performance of early successional plants can be decreased directly by the legacy effects of conspecifics, as well as indirectly by that of co-occurring plants. These studies imply that soil legacies and priority effects could exert great influences on the composition and succession of communities; however, the mechanisms of the two effects remain unclear. They may be caused by the combined effects of soil abiotic and biotic properties, soil microorganism activities, and plant competitions. We believe that soil pathogens play a key role in soil legacies and priority effects, but the hypothesis needs to be tested in future studies.

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5.4. Application of theoretical models Although conducting field experiments is the ideal way to test ecological hypotheses, these experiments are usually difficult to manipulate in the field. For example, it seems impossible to design field experiments for long term or for endangered species. In these cases, the problems could be solved effectively by theoretical modeling [106]. For example, Petermann et al. [16] investigated the effects of plant pathogens on European grassland communities using a combination of field experiments and parameterized models, and found that negative PSFs played a key role in maintaining plant traits. In addition, Borer et al. [43], who used a model with field-estimated parameters, found that the dominance of California's perennial grasslands was decreased by the infection of Barley and cereal yellow dwarf viruses, which was result of the invasion of exotic annual grasses. So far, the application of modeling is confined to the population level. Therefore, it would be more useful to the pathogen function study in ecology, if modeling is extended to a community or an ecosystem level [6]. 5.5. Further studies on multiple-hosts and multiple-pathogens Theoretical models inferred that community stabilization occurs when disease transmission within species exceeds that across species, and the converse causes community destabilization, where highly competitive species exclude the inferior species [107–109]. A similar inference is that two plant species sharing the same pathogen exclude each other, although they can coexist with the pathogen when stand alone [107]. Since these inferences are waiting to be verified, additional studies on pathogens with multiple hosts, and host plants with multiple pathogens are necessary for a better understanding of the role of phytopathogens in plant community dynamics. Acknowledgements

5.2. Plant pathogens responding to climate change Climate change can directly or indirectly influence the activities of soil microorganisms [100]. For example, the rise of temperature can directly activate most soil pathogens, and promote the decomposition of organic matter, which in turn can indirectly stimulate the activities of soil pathogens [101]. Recent studies showed that soil microorganisms have significant function in an ecosystem in response to climate change. For instance, De Vries et al. [102] found that the extensively-managed grassland soil with fungal-based food web was more adaptable to drought than the intensively-managed wheat soil with bacterial-based food web. At present, studies probing the behaviors of soil pathogens in response to climate change are still lacking.

5.3. Plant pathogen effects on species evolution In agricultural ecosystems, the susceptibility of crop species to a specific pathogen increases with the evolution of the pathogen, which leads to the advent of a new variety resistant to the disease. This cycle suggests that plant pathogens could drive the evolution of plant species. Nevertheless, how pathogens drive species evolution in natural ecosystems is largely unknown. Lau and Lennon [103] found that plants developed worse (smaller plants, reduced chlorophyll content, fewer flowers, less fecund) in simplified microbial communities than in more complex communities, suggesting that the structure of soil microbial communities may influence natural selection patterns on plant traits. However, direct evidence verifying the role of soil pathogens in these selections is scarce. Since the function of plant pathogens in affecting species diversity has been widely tested [104–105], we presume that plant pathogens can alter plant traits by modifying fitness differences and force plant species to evolve in a beneficial direction [90].

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