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1 2 Effects of phytopathogens on plant community dynamics: a review 3 The State Key Laboratory of Grassland Agro-ecosystems, College of Pastoral Agricultural Science and Technology, 4 Lanzhou University Lanzhou 730020, China 5 Corresponding author email: [email protected] 6 Abstract: 7 CHEN Tao, NAN Zhibiao* The impacts of phytopathogens on agricultural systems, disease controls and economic losses 8 caused by the pathogens are internationally important research subjects. Recently, increasing 9 evidence has shown that phytopathogens play a critical role in mediating competitions among 10 their host plant species. According to Chesson’s coexistence framework, niche differences (i.e., 11 species differences in resource use, host-specific pathogen loads, and other ecosystem processes) 12 are more associated with intra-specific limitation than with inter-specific limitation. However, 13 fitness differences (i.e., variations in competition abilities among plant species) can determine the 14 dominance of plant species. An increase in niche differences tends to promote the coexistence of 15 plant species, whereas an increase in fitness differences tends to exclude competing species. In 16 this review, two types of pathogen mechanisms that could affect plant communities are discussed 17 based on the coexistence framework. Type I is the density-dependent pathogen mechanism, in 18 which disease occurrence in a community is related to the density of host species. In this 19 mechanism, disease transmission increases niche differences as a host species becomes common, 20 and/or reduces niche differences as a host species becomes rare. Type II is the density-independent 21 pathogen mechanism, in which disease transmission does not depend on host plant density. This 22 mechanism mainly focuses on fitness differences. When competitively dominant host plants are 23 more susceptible to pathogens, pathogens can reduce fitness differences among species and 24 thereby improve plant diversity. Alternatively, if the competing species are more resistant than 25 other species to pathogens, fitness differences are prone to be increased. 26 The Janzen-Connell effect (JC effect) and plant-soil feedback theory are characterized by Type 27 I phytopathogen mechanism and are discussed here in details. The JC hypothesis has been mostly 28 applied to forest ecosystems, whereas the plant-soil feedback theory has been applied more widely 29 in several ecosystems. The JC hypothesis assumes that seeds/seedlings around the mother plant 30 are most susceptible to host-specific pathogens. Since seed/seedling mortality caused by 31 pathogens is related to plant density, the JC effect is an example of negative density dependence. 1 32 The plant-soil feedback theory illustrates the interactions between plants and soil. Plants can alter 33 soil properties through the input of organic matter and chemicals, and provide habitats and 34 nutrients for soil organisms, which in turn can affect plant performance. This feedback can be 35 either negative or positive, depending on whether it leads to a net reduction or an enhancement of 36 plant growth when comparing the plant species cultured in soil conditioned by the plant to that in 37 mixed soil. 38 This review summarizes phytopathogen effects on plant diversity, plant invasion, community 39 succession, and addresses some future research challenges. Several research goals are highlighted; 40 for instance, studies of pathogens with multiple hosts and host plants with multiple pathogens are 41 necessary for a better understanding of the role of phytopathogens in plant community dynamics. 42 Research on the interactions of plant pathogen with soil legacy (priority) could provide new 43 insights into the influences of phytopathogen on plant communities during climate change. In 44 addition, a combination of theoretical modeling and field studies would be an effective way to 45 examine the function of phytopathogens in plant community dynamics. 46 47 48 Key words: Plant pathogens;Plant communities; Plant diversity; Coexistence; Jazen-connell hypothesis; Plant-soil feedbacks 49 50 In agricultural ecosystems, plant pathogens not only negatively affect seedling survival and 51 growth, but also reduce crop production and quality, which results in a great economic loss[1-2]. 52 Until now most of the work on plant pathogens has been focused on how to control and lower 53 disease occurrences, while the function of pathogens in natural ecosystems has not been 54 thoroughly investigated. 55 Plant pathogens can transmit horizontally via vectors such as soil, water and insects, as well as 56 vertically via mother plants[3]. Some pathogens are specific for certain plant species, while others 57 that are non-specific have a broad range of hosts. Hence, plant pathogens may play different roles 58 among species within a community[4-5]. In this paper, we summarized the available mechanisms by 59 which plant pathogens affect species composition and community dynamics, reviewed recent 60 research developments in this area, and discussed the possible directions for future research. 2 61 62 1 General roles of plant pathogens in plant communities The interactions between plants and pathogens can promote or exclude species coexistence. 63 Plant pathogens can influence community stabilities when their impact on plant growth relies on 64 host relative abundance[6]. For example, host-specific pathogens increase as their preferred host 65 becomes abundant in a community, thus limit further growth of the host, which is beneficial to the 66 stabilization of the community[7-8]. When the impact of pathogens on communities does not 67 depend on host abundance, it often alters fitness differences among plant species and indirectly 68 affect species coexistence[6]. For instance, some pathogens that have a broad range of hosts can 69 transmit among a variety of plant species. When the infection of these pathogens on rare species 70 exceeds that on dominant species, it will lead to the further growth of highly competitive species, 71 and cause the increase of fitness differences that might destabilize the whole community[9]. 72 2 Mechanisms of plant pathogen effects on plant communities 73 In a community, plant species have niche differences that promote coexistence and fitness 74 differences, which exclude coexistence. Niche differences should overrule fitness differences, if 75 plant species coexist persistently in an ecosystem. This is referred to as Chesson’s coexistence 76 framework [10] (Figure 1). Here we synthesized the major theories on how pathogens influence 77 plant communities based on this framework. The theories include density-dependent mechanism 78 that affects niche differences of plant species, and density-independent mechanism that affects 79 fitness differences (Table 1). 80 81 82 83 (Chesson 2000). The figure is adapted and substantially modified by Mordecai (2011). The x-axis measures the strength of stabilization or 84 2.1 The Janzen-Connell Hypothesis 85 Figure1 The theoretical framework describing how interactions of plants with pathogens influence plant community dynamics destabilization, and the y-axis measures the fitness differences between species. Janzen (1970) and Connell (1971) hypothesized that specific enemies can maintain rainforest 3 86 diversity by controlling the density of dominant species. That is, specific enemies such as 87 predators or pathogens can effectively infect hosts and limit their further growth as host 88 abundance increases in the community. In tropical ecosystems, seed dispersal from seed rains 89 leads to a high seed density near the mother plant, which makes the seeds more susceptible to 90 specific enemies and causes high seed and/or seedling mortality. This phenomenon is called the 91 Janzen-Connell effect (JC effect ). The JC effect is also known as negative density dependence 92 (NDD), as the effect is associated with density of a population and the population was negatively 93 mediated by the enemies[11-12]. 94 To prove the JC effect, ecologists have paid much attention studying the role of pathogens in 95 influencing species diversity. They hypothesized that pathogen accumulation near mother plants 96 can reduce the survival and growth of conspecific seedlings owing to a high seed density, and 97 consequently provide space for plant species with the same resource requirements[13-14]. For 98 example, Augspurger[15] (1983) monitored the seed germination and seedling survival of a 99 wind-dispersed tree Platypodium elegans on Barro Colorado Island, Panama for one year, and 100 found that both the incidence and the rate of seedling damping-off caused by fungal pathgoens 101 were negatively correlated with the distance from the parental tree. Bell et al. [8] (2006) in the 102 Chiquibul Forest Reserve near the Las Cuevas Research Station also examined the relationship 103 between the seedling survival rate of trpoical forest plant Sebastiana longicuspis and the plant 104 population density. Their finding was that seedling survival was three times higher at low density 105 in the non-fungicide-treated plots, whereas it was unaffected by density in the fungicide-treated 106 plots, suggesting that the application of fungicides may kill soil pathogens and increase seedling 107 survival. 108 Though the JC effect was proposed for tropical forest systems, it has also been applied to other 109 ecosystems such as grassland[16] and ocean systems[17]. For instance, Petermann et al. [16] (2008) 110 conducted a controlled greenhouse experiment with 24 species planted in soil from field 111 monocultures, which revealed the JC effect on plant dynamics in the European temperate 112 grasslands. The results showed that the reduction of biomass in monoculture was due to the 113 build-up of soil pathogens, which indicated that the JC effect might play a critical role in driving 114 plant diversity in temperate ecosystems. 115 2.2 Plant-soil feedbacks 4 116 Plants can alter soil properties through the input of organic matter and chemicals, which in 117 turn affect plant performance. This process is referred to as plant-soil feedbacks (PSFs)[18-20]. 118 There is increasing evidence that soil pathogens have an important function in the process of PSFs 119 either by directly infecting plants or indirectly by altering soil properties[21-23]. For example, Mills 120 and Bever (1998)[24] found that Pythium fungi isolated from the roots of Danthonia spicata and 121 Panicum sphaerocarpon was more pathogenic to the two hosts than to the other two species, 122 Anthoxanthum odoratum and Plantago lanceolata, suggesting that the accumulation of 123 species-specific soil pathogens could account for the previous observation of negative feedbacks 124 on plant growth. 125 Plant-soil feedbacks can be positive by improving plant growth, or negative by restraining 126 growth [18] (Figure 2). Most studies on positive PSFs focused on soil mutualists such as AM fungi 127 and N-fixing bacteria that can promote the plant uptake of soil nutrients [25]. The function of soil 128 pathogens during the process of positive PSFs was rarely studied. However, Batten et al. 129 (2006)[26]found that soil conditioned by Aegilops triuncialis exhibited negative effects on the 130 native plant Lasthenia californica by delaying the flowering date and decreasing the aboveground 131 biomass. The results indicate that invasion-induced changes in soil microbial communities may 132 contribute to a positive feedback that increased the chance of successful invasion by Aegilops 133 triuncialis. 134 By contrast, the role of pathogens in negative feedbacks to plants has been extensively studied. 135 A negative feedback is that the increase of plant abundance leads to the build-up of specific 136 pathogens, which in turn limits the further expansion of this plant in the community, and therefore 137 provides space for other inferior species and maintains species diversity [27]. For example, 138 Reinhart (2012)[28]investigated the direction of PSFs in different types of grasslands in Northern 139 Great Plains Steppe ecoregion of North America. He found that negative PSFs were present from 140 rare to dominant species and predominated across the three types of grasslands, suggesting that 141 negative PSFs have a great potential to drive species coexistence in grasslands. 5 142 143 144 Figure 2 Illustration of the interaction mechanisms between soil pathogens and plants. The arrows and circles indicate the direction of 145 Bever, 2003). 146 2.3 Other mechanisms on plant pathogens promoting system stability 147 beneficial and detrimental effects, respectively. The thickness of the lines indicates the relative strength of these effects (Modified from In addition to JC effects and negative PSFs, other pathogen-mediated mechanisms can also 148 explain species coexistence. These mechanisms include density-dependent cost of infection 149 (DDCF)[29] and disease response to host diversity[30]. One good example of DDCF is the 150 promotion of vegetative growth by increasing the cost of sexual reproduction[31]. For instance, a 151 castrating endophyte infection benefits the growth of Agrostis at low density, but problems arise at 152 high density due to the reduced seed production[32]. The theory of disease response to host 153 diversity is widely used in agriculture[6]. An example of this theory is that increasing crop species 154 can reduce the occurrence of diseases. 155 2.4 Mechanisms on plant pathogens destabilizing systems 156 Apart from promoting species coexistence, pathogens can also exclude species in communities, 157 resulting in the destabilization of ecosystems[33-34]. This principle contains two important 158 mechanisms: positive PSFs that has been discussed above, and pathogen spillover that we will 159 address as follows. 160 In the pathogen spillover mechanism, some plant species that are highly resistant to specific 161 pathogens can be regarded as pathogen reservoirs. When the abundance of hosts in a community 162 increases, pathogen reservoirs accumulate and the performance of less competitive species is 163 impaired, resulting in the dominance of host plants in the community[9]. For example, Cobb et al. 164 (2010)[35] studied the function of Phytophthora ramorum, a shared exotic pathogen, in the 165 competition of canopy trees in California coastal redwood forests. The results showed that the 166 inoculation of P. ramorum on California bay laurel (Umbellularia californica) had a great impact 167 on the mortality of a competing species, tanoak (Lithocarpus densiflorus). Beckstead et al. 6 168 (2010)[36] also found that an invasive annual weed cheatgrass (Bromus tectorum) acted as a 169 reservoir for Pyrenophora semeniperda, a multiple-host fungal seed pathogen, and had appreciable 170 influences on the co-occurring native grasses. 171 2.5 Effects of plant pathogens on fitness differences 172 Pathogens can also influence the composition and dynamics of communities by altering fitness 173 differences regardless of host abundance. Pathogens may decrease fitness differences via infecting 174 highly competitive species, or increase fitness differences through infecting inferior species[6]. 175 Mechanisms relating to lower fitness differences consist of equalizing trade-offs[37-38], enemy 176 release of invading plants[39], and agriculture and biocontrol[40], while mechanisms associated with 177 increased fitness differences include pathogen-driven succession[41] and highly virulent 178 epidemics[42] (Table 1). To date, most of the work on fitness differences emphasizes how to 179 promote species coexistence by reducing the competitive abilities of dominant species, and how to 180 benefit invaders by lowering the performance of native species. For example, Borer et al. (2007) 181 [43] 182 California’s native species and contributed to the invasion of European annual grasses. However, 183 the evidence of above mechanisms affecting community dynamics is still lacking. found that the prevalence of Barely yellow dwarf viruses reduced the dominance of 184 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 Negative plant-soil feedbacks Density-dependent attack Density-dependent cost of infection Disease response to host diversity b) Destabilization: disease transmission increases as a species becomes rare Pathogen spillover Positive plant-soil feedbacks B) Density-independent pathogens a) Reduced fitness differences:competitively dominant species experience the greatest cost during pathogen infections Equalizing trade-offs Enemy release of invading plants Agriculture and biocontrol b) Fitness hierarchy reversal/increased fitness differences:susceptible hosts face extreme fitness costs Pathogen-driven succession Highly virulent epidemics 7 grasslands[16];forests[7,13, 44-45]; grasslands [47-50];fields[24,51];forests [52,53]; grasslands[54]; forests[55] fields[32, 56,57] grasslands[58,59]; fields[60-62] grasslands[9]; forests [33,63] grasslands [26,34] grasslands [37,38, 64]; forests[65,66]; fields [67] forests [39] fields [40, 68] deserts [69-71]; forests; fields [72] forests [42] 185 Note:Modified from Mordecai (2011). 186 3 Impacts of plant pathogens on species diversity, biological invasion, and community 187 succession 188 Both JC effects and PSFs aim to explain the role of pathogens in plant communities, and thus 189 the two mechanisms share some similar features. The JC effect is related to host density, while a 190 negative PSF is associated with host abundance. In a typical example, Pack and Clay (2003)[46] 191 in the temperate forests of North America found that seedlings close to their parents were more 192 susceptible to Pythium fungi. The possible explanations are that the intensity of Pythium fungi was 193 higher near the parent trees due to a high seed density (a JC effect), or that the build-up of Pythium 194 close to the parents reduced the survival of seedlings to maintain species diversity in the 195 community (a negative PSF). Besides the similarities, JC effects and PSFs differ in specific 196 research areas. The JC effect puts emphasis on how pathogens affect species diversity and 197 productivity in forests, while PSFs involve pathogen effects on community dynamics[46], 198 succession[73], and invasion[74] and could be applied to a wider range of ecosystems (forests, 199 grasslands and agricultural ecosystems, etc.). 200 3.1 Janzen-Connell hypothesis studies 201 The JC effect was firstly proposed for tropical forest ecosystems, and therefore most of the 202 work has been done with tropical trees[75]. This is possibly because sufficient rainfall and suitable 203 temperature proliferate soil pathogens, which in turn bring about a greater impact on tropical 204 forests[76]. However, the study of Hille Ris Lambers et al. (2002)[7] in temperate deciduous forests 205 of North Carolina argues that JC effects are more prevalent at tropical latitudes. They reported that 206 the proportion of species affected by soil pathogens in temperate forests is equivalent to that in 207 tropical forests. 208 Although the effects of pathogens on plants seem not to be limited in forests, the application of 209 JC effects to other ecosystems are rare, except few research conducted in grasslands[16]. A possible 210 reason is that other ecosystems such as grasslands may not be as significant as forest ecosystems 211 in maintaining the global climate, which led researchers to conduct more investigations on forests 212 than on grasslands. Another more important reason might be that the belowground roots of various 213 species intersect with each other in grasslands, making it difficult to determine the effects of soil 214 pathogens on a particular species at the population level. Therefore, future work on JC effects in 8 215 grasslands should be conducted at the community level. 216 3.2 Interactions between pathogens and plant diversity 217 Ecologists have done a lot of work to determine the role of fungal pathogens and insect 218 herbivores in structuring plant diversity[13-14]. For example, Bagchi et al. (2014)[45] performed a 219 field experiment in Chiquibul Forest Reserve, Belize to test whether the JC effect has a 220 community-wide role in maintaining tropical forest diversity. Experimental plots were treated with 221 fungicides and insecticides, respectively, and seedling emergence and survival in these plots were 222 observed. The results showed that seedling establishment was negatively density dependent (NDD) 223 and species diversity was maintained at a high level in the untreated plots, whereas the effects of 224 NDD was barely observed in the fungicide-treated plots and seedling species diversity dropped 225 greatly. By contrast, the insecticide application did not alter species diversity, though it greatly 226 increased seedling recruitment and caused a marked shift in species composition. This is the first 227 field study explicitly demonstrating that fungal pathogens are more important than insects in 228 determining niche differences and species diversity[77]. 229 Pathogens affect species diversity, which in turn affects the intensity of pathogens. The loss of 230 plant diversity can either increase or decrease the occurrence of disease on a theoretical basis, but 231 most studies showed that it increased disease transmission[78]. For example, Schnitzer et al. (2011) 232 [58] 233 and a series of field experiments, and found that plant disease decreased with increased diversity 234 and the productivity was increased by 500%. A similar study was done by Maron et al. (2011)[59] 235 in western Montana grasslands, where the effects of soil pathogens on plant productivity was 236 assessed by fungicide application. The results showed that the aboveground biomass was 237 positively correlated to plant diversity in the untreated plots, whereas this relationship did not exist 238 in the fungicide-treated plots. Fungicide application increased the plant production by 141% in the 239 low-diversity plot and only by 33% in the high-diversity plot, indicating that soil pathogen 240 intensity was inversely proportional to plant diversity. 241 3.3 Explanations for biological invasions 242 studied the effects of soil pathogens on plant productivity by combining an analytical model There are several explanations for the success of plant invasions. One explanation is that the 243 new community is lacking in specific pathogens for invaders, which suffer from a negative 244 feedback by soil pathogens in their original community[79]. For example, Klironomos (2002)[74] 9 245 performed an experiment investigating the role of soil microbes in PSFs with five native and five 246 invasive plant species. He found that when grown in monoculture, the native species suffered 247 more seriously from specific fungal pathogens than the invasive species. Further studies revealed 248 that it was caused by the lack of specific fungal pathogens when invasive plants entered the new 249 habitat, rather than by a positive PSF resulted from AMF[80]. 250 The second explanation for invasion success is that even though exotic plant species 251 introduced to a new habitat may experience a negative PSF originated from soil pathogens, the 252 degree of feedback is far less than that to the native species[81]. For instance, Mangla et al. (2008) 253 [82] 254 weed, Chromolaena odorata, resulted in a dramatic rise of generalist soil borne fungi, Fusarium 255 semitectum, and created a negative feedback for native plant species. However, a study by Nijjer et 256 al. (2007)[83] in Big Thicket National Preserve (BTNP) in east Texas, USA, found that a stronger 257 negative PSF exhibited on the invasive plant species Sapium sebiferum than on native species, 258 indicating that soil pathogens may act as an inhibitor to limit the further expansion of invasive 259 species when they occur in high abundance. reported that in the Western Ghats of India, the arrival of an extensively destructive tropical 260 The failure of exotic plants introduced to a new habitat is probably due to the change of PSFs 261 during the invasion process[84]. For example, Diez et al. (2010)[85] found that the direction of PSF 262 for 12 exotic plants was negatively correlated with the invasion time. 263 3.4 Community succession driven by PSFs 264 By far, the role of PSFs in community succession has been extensively studied 265 worldwide[41,86].The direction of PSFs varies at different successional stages[87]. In the early 266 successional stage, positive PSFs dominate across the community[88]. Since the original soil is 267 short of nutrients, soil mutualists such as AM fungi and N-fixing bacteria may promote the uptake 268 of soil nutrients by plants, thereby a positive PSF is displayed[89]. With the increase of plant 269 abundance, specific soil pathogens start to cause negative PSFs by reducing the competitive ability 270 of the early species and promoting the growth of the late species[90]. A typical example of this 271 negative PSF is the succession of a foredune grass Ammophila arenaria, which performed very 272 well in mobile dunes as it could escape from soil pathogens. However, the grass degenerated in 273 stable dunes, probably because the exposure of the roots to soil pathogens created negative PSFs. 274 In addition, primary successional species in abandoned fields are more susceptible to soil 10 275 276 pathogens than secondary successional species[73]. The early succession contributes to the establishment of soil biota that can boost the 277 development of a community and lead to a secondary succession[91]. Kardol et al. (2013)[87] held 278 the opinion that the early stage of secondary succession is associated with negative PSFs, which 279 accelerates the turnover of plant species, whereas the late stage of secondary succession is 280 associated with positive PSFs, which is beneficial to community stability. With the development 281 of succession, both plant species and soil biota change constantly, making the effects of PSFs on 282 community dynamics in later stages unclear. Hou (2008 )[92] investigated the survival of seed 283 and/or seedlings by applying fungicides in plots with different grazing intensities in western China. 284 The results indicate that livestock grazing had an impact on soil pathogens. However, further 285 research is needed to address the combined effects of grazing and soil pathogens in community. 286 4 Future challenges 287 The research in plant pathogens affecting community composition and dynamics is an 288 important branch of species coexistence study. Nevertheless, most of the work was based on a 289 specific plant species with a specialized pathogen. How pathogens with multiple hosts and host 290 plants with multiple pathogens interact with each other still remain unclear. For example, the JC 291 effects were extensively studied on the survival of conspecific plant seedlings exposed to a high 292 density of soil specific pathogens, but the influences of pathogens on neighboring species were not 293 well studied[26]. 294 The study of PSFs is usually performed by comparing the growth of a plant species in soil 295 conditioned by its own (home) and that in soil conditioned by a mixture of other plants (foreign). 296 Plants can change soil properties as well as the composition of soil microorganisms. The 297 differences in soil chemical compositions may also result in a difference in plant growth; therefore, 298 the effects of soil pathogens could be overestimated in some cases[20]. In addition, the variance of 299 experimental designs and data analysis can either amplify or diminish the effect of pathogens on 300 plant growth[93]. Furthermore, soil legacies generated by field plants could be long-standing, even 301 though the soil has been sterilized[94]. As for the first problem, we can separate the effects caused 302 by soil chemicals through measuring the chemical contents of the soil. The second and the third 303 problems cannot be solved at present; hence new approaches or novel technologies are required 304 for future research. 11 305 306 4.1 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 307 has disappeared completely from the community. This is referred to as soil legacies[95]. 308 Correspondingly, the first arrival species in a community can suppress the growth of the late 309 arrival species, which is coined as priority effects[96]. Both soil legacies and priority effects have 310 great impacts on species diversity and productivity[97]. Grman and Suding (2010) [98] believed that 311 priority effects are associated with plant competition, as the first-coming species occupy space and 312 utilize resources and suppress the growth of the second-coming plants. Van de Voorde et al. 313 (2011)[99] found that the growth of the early successional Jacobaea vulgaris was inhibited by its 314 own-conditioned soil, and also by half of the co-occurring plants, suggesting that the performance 315 of early successional plants can be decreased directly by the legacy effects of conspecifics, as well 316 as indirectly by that of co-occuring plants. These studies imply that soil legacies and priority 317 effects could exert great influences on the composition and succession of communities; however, 318 the mechanisms of the two effects remain unclear. They may be caused by the combined effects of 319 soil abiotic and biotic properties, soil microorganism activities, and plant competitions. We believe 320 that soil pathogens play a key role in soil legacies and priority effects, but the hypothesis needs to 321 be tested in future studies. 322 4.2 Plant pathogens responding to climate change 323 Climate change can directly or indirectly influence the activities of soil microorganisms[100]. 324 For example, the rise of temperature can directly activate most soil pathogens, and promote the 325 decomposition of organic matter, which in turn can indirectly stimulate the activities of soil 326 pathogens[101]. Recent studies showed that soil microorganisms have significant function in an 327 ecosystem in response to climate change. For instance, De Vries et al. (2012) [102] found that the 328 extensively-managed grassland soil with fungal-based food web was more adaptable to drought 329 than the intensively-managed wheat soil with bacterial-based food web. At present, studies 330 probing the behaviors of soil pathogens in response to climate change are still lacking. 331 4.3 Plant pathogen effects on species evolution 332 In agricultural ecosystems, the susceptibility of crop species to a specific pathogen increases 333 with the evolution of the pathogen, which leads to the advent of a new variety resistant to the 334 disease. This cycle suggests that plant pathogens could drive the evolution of plant species. 12 335 Nevertheless, how pathogens drive species evolution in natural ecosystems is largely unknown. 336 Lau and Lennon (2011)[103] found that plants developed worse (smaller plants, reduced chlorophyll 337 content, fewer flowers, less fecund) in simplified microbial communities than in more complex 338 communities, suggesting that the structure of soil microbial communities may influence natural 339 selection patterns on plant traits. However, direct evidence verifying the role of soil pathogens in 340 these selections is scarce. Since the function of plant pathogens in affecting species diversity has 341 been widely tested[104-105], we presume that plant pathogens can alter plant traits by modifying 342 fitness differences and force plant species to evolve in a beneficial direction[90]. 343 4.4 Application of theoretical models 344 Although conducting field experiments is the ideal way to test ecological hypotheses, these 345 experiments are usually difficult to manipulate in the field. For example, it seems impossible to 346 design field experiments for long term or for endangered species. In these cases, the problems 347 could be solved effectively by theoretical modeling [106]. For example, Petermann et al. (2008)[16] 348 investigated the effects of plant pathogens on European grassland communities using a 349 combination of field experiments and parameterized models, and found that negative PSFs played 350 a key role in maintaining plant traits. In addition, Borer et al. (2007)[43] , who used a model with 351 field-estimated parameters, found that the dominance of California’s perennial grasslands was 352 decreased by the infection of barley and cereal yellow dwarf viruses, which was result of the 353 invasion of exotic annual grasses. So far, the application of modeling is confined to the population 354 level. Therefore, it would be more useful to the pathogen function study in ecology, if modeling is 355 extended to a community or an ecosystem level[6]. 356 4.5 Further studies on multiple-hosts and multiple-pathogens 357 Theoretical models inferred that community stabilization occurs when disease transmission 358 within species exceeds that across species, and the converse causes community destabilization, 359 where highly competitive species exclude the inferior species[107-109]. A similar inference is that 360 two plant species sharing the same pathogen exclude each other, although they can coexist with 361 the pathogen when stand alone[107]. Since these inferences are waiting to be verified, additional 362 studies on pathogens with multiple hosts, and host plants with multiple pathogens are necessary 363 for a better understanding of the role of phytopathogens in plant community dynamics. 364 13 365 366 367 368 369 370 371 372 373 374 375 376 377 378 379 380 381 382 383 384 385 386 387 388 389 390 391 392 393 394 395 396 397 398 399 400 401 402 403 404 405 406 407 408 Acknowledgements We greatly appreciate associate professor Wang Jing, Wan Changgui and Mike Christensen for editing English language of this paper. This research was financially supported by the National Basic Research Program of China (2014CB138702). References [1] Matson P A, Parton W J, Power A G, Swift M J. Agricultural intensification and ecosystem properties. Science, 1997, 277(5325): 504-509. [2] Brown J K, Hovmøller M S. Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. 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