Molecular mechanisms underlying microbial disease control in intercropping

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Shusheng Zhu, Jean-Benoit Morel

To cite this version:

Shusheng Zhu, Jean-Benoit Morel. Molecular mechanisms underlying microbial disease control in intercropping. Molecular Plant-Microbe Interactions, American Phytopathological Society, 2019, 32 (1), pp.20-24. �10.1094/MPMI-03-18-0058-CR�. �hal-02628350�

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Molecular

mechanisms

underlying

microbial

disease

control

in

1

intercropping

2 3

ZHU S1,2 and MOREL JB3*

4 5

1

State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan 6

Agricultural University, Kunming, Yunnan, China 7

2

Key Laboratory of Agro-Biodiversity and Pest Management of Education Ministry of China, 8

Yunnan Agricultural University, Kunming, Yunnan, China 9

3

BGPI, INRA, CIRAD, SupAgro, Univ. Montpellier, Montpellier, France 10

*: corresponding author: jeanbenoit.morel@inra.fr, Phone +33499624838, Fax

11 +33499624822 12 13 Summary 14

Many reports indicate that intercropping, which usually consists in growing two species next 15

to each other, reduces the incidence of microbial diseases. Besides mechanisms operating at 16

the field level like inoculum dilution, there is recent evidence that plant-centered mechanisms 17

with identified plant molecules and pathways are also involved. First, plants may trigger the 18

induction of resistance in neighboring plants by the well-known mechanism of induced 19

resistance. Second, molecules produced by one plant, either above or below ground, can 20

directly inhibit pathogens or indirectly trigger resistance through the induction of the plant 21

immune system in neighboring plants. Third, competition for resources like light or nutrients 22

may indirectly modify the expression of the plant immune system. The conceptual 23

frameworks of non-kin/stranger recognition and competition may be useful to further 24

Molecular Plant-Microbe Interactions "First Look" paper • http://dx.doi.org/10.1094/MPMI-03-18-0058-CR • posted 07/11/2018

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investigate the molecular mechanisms underlying crop protection in interspecific plant 25

mixtures. 26

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Introduction 27

Economic, societal and environmental concerns are imposing changes in our agriculture 28

models. In particular, there is a global trend towards re-introducing diversity in our agro-29

systems since it has long been shown to increase plant health (Kessing and Ostfeld, 2016; 30

Mundt, 2002). Intercropping is a subset of diverse cropping systems that provide multiple 31

eco-systemic effects including disease control (Gaba et al., 2015). Several definitions of 32

intercropping can be found and here we will consider the cases where two crops from 33

different species are grown in close proximity, at the same time. Intercropping includes strips 34

of different crops as well as complete, intermingled mixtures of several species. The 35

beneficial effects of intercropping systems on insect resistance have been reviewed 36

(Ratnadass et al., 2012) and are not discussed here. Yield in intercropping systems is often 37

more elevated than in the corresponding monoculture (Li et al., 2014) and this is strongly 38

connected to a reduction of microbial disease (Li et al., 2009). 39

Among 206 studies representing more than 240 unique intercrop-disease combinations, 73% 40

showed reduced impact of disease and only 7% showed an increase (Boudreau, 2013). For 41

instance, wheat-faba bean intercropping reduced powdery mildew on wheat by 49% (Chen et 42

al., 2007) and Ascochyta blight was reduced by 82% on faba beans intercropped with triticale

43

(Fernández-Aparicio et al., 2010). These values obtained in field studies highlight the strong 44

potential of intercropping for disease control. 45

As proposed by Boudreau (2013), a “theoretical framework based on a mechanistic 46

understanding [could] allow a more methodical and efficient designer intercrop strategy”. 47

Many factors beyond plant level interactions have been proposed to explain enhanced 48

resistance seen in intercropping systems (Boudreau, 2013; Gaba et al., 2015; Ratnadass et al., 49

2012) and are out of scope of this review. They include inoculum dilution, spore dispersal 50

interference (Figure 1A) and micro-environmental modifications. The scope of this review is 51

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to examine reports on plant-centered mechanisms that could be responsible for reduced 52

susceptibility to microbial diseases in intercropping systems of annual crops. We propose a 53

simple framework involving plant-derived signals (including light and exudates) and the plant 54

immune system (understood here as the molecular responses normally triggered upon 55

infection) as the key players to explain pathogen suppression in intercropping (Figure 1B). 56

57

Disease reduction through pathogen inhibition by allelochemicals 58

Plant allelochemicals, some of those having antimicrobial properties, result from exudation, 59

decomposition, leaching or volatilization (Weir et al., 2004; Massalah et al., 2017). In 60

intercropping systems, while pathogens adapted to one plant species can overcome host 61

chemical barriers, adapted pathogens cannot. Antimicrobial compounds released by non-62

host plants can help neighboring host plants to suppress disease. Indeed, there is increasing 63

evidence from intercropping systems that root exudates released by non-host plants play an 64

important role in suppression of plant pathogens. Here we illustrate this phenomenon with 65

examples for soil-borne fungi, oomycete, bacteria, and nematodes. 66

For fungal soil-borne pathogens, root exudates of intercropped species can protect 67

neighboring crop plants by directly inhibiting spore germination and mycelial growth, thus 68

reducing pathogen populations in the soil. This mechanism has been documented in many 69

systems with soil-borne fungal pathogens, such as Fusarium spp (Hao et al., 2010), 70

Verticillium dalhiae (Fu et al., 2015), and Cylindrocladium parasiticum (Gao et al., 2014).

71

Allelochemicals, especially phenolic acids (such as p-coumaric acid and cinnamic acid), have 72

been described as major antifungal chemicals in root exudates (Hao et al., 2010; Gao et al., 73

2014; Ren et al., 2008). 74

Plant-parasitic nematodes can also be inhibited by root exudates from non-host plants. For 75

instance, some Asteraceae species have been shown to suppress plant-parasitic nematodes 76

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when intercropped with susceptible crops (for reviews Tsay et al., 2004). Various nematicidal 77

compounds produced by Asteraceae plants, such as thiophenes and thiarubrines, have been 78

shown to negatively affect plant-parasitic nematodes and thus help neighbor plants in 79

intercropping system by reducing nematode population sizes (Tsay et al., 2004). In addition to 80

direct allelochemical effects on the nematode life cycle, some root exudate compounds 81

produced by non-host plants can reduce nematode damage by modifying the behavior of the 82

nematode. For example, lauric acid in crown daisy (Chrysanthemum coronarium) root 83

exudates can attract Meloidogyne incognita and induce nematode death at low concentration, 84

while it repels the nematode from roots at higher concentration. This pattern results from the 85

interference of lauric acid with the expression of a nematode gene encoding a neuromodulator 86

peptide involved in chemotaxis (Dong et al., 2014). Solanum sisymbriifolium, produces high 87

levels of hatching agents, and is a resistant trap crop for potato cyst nematodes (Globodera 88

spp.) (Timmermans et al., 2010; Dias et al., 2012). This plant is an excellent candidate to 89

intercrop with a nematode susceptible host for potato cyst nematode population suppression. 90

For soil-borne Oomycete pathogens, some non-host plant roots can attract zoospores that later 91

are killed by antimicrobial secreted substances against which these zoospores are not adapted. 92

This mechanism has been well studied for Phytophthora disease control in the maize-pepper 93

intercropping system. Non-host maize plants could form a “root wall” below the ground that 94

restricts the spread of zoospores in the field and thus indirectly protect host pepper plants. The 95

maize roots attract zoospores of P. capsici into the “root wall” and simultaneously secrete 96

antimicrobial compounds, such as 2,4-Dihydroxy-7-methoxy-2H-1,4-benzoxazin-3(4H) 97

(DIMBOA), that kill zoospores (Yang et al., 2014); this strategy has been termed “attract and 98

kill”. It differs slightly from the push-pull mechanism for insect control in intercropping 99

where one plant repels the insect towards another attractive one (where it remains) (Ratnadass 100

et al., 2012). This “attract and kill” phenomenon has been found for several plant species

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including rapeseed (Fang et al., 2016), garlic, Chinese chive and fennel (Zhu S, unpublished 102

data). Many plants could be selected as potential intercropping species for the management of 103

soil-borne Oomycete pathogens. The existence of this strategy has not been reported in 104

intercropping systems for bacterial disease suppression. 105

There are a limited number of volatile organic compounds (VOCs) that can directly inhibit 106

pathogen growth (references in Heil and Karban, 2010). For instance, several volatile 107

molecules produced by Chinese chives could inhibit Fusarium oxysporum f. sp cubense, a 108

soil-borne pathogen of banana (Zhang et al., 2013). Whether VOCs can directly inhibit the 109

growth of foliar pathogens in intercropping remains unexplored. 110

111

Modification of the plant immune system by neighbors 112

In contrast to the direct inhibition of pathogens by allelochemicals described above, some 113

mechanisms involved in intercropping require the participation of plant immune responses. 114

Two major mechanisms, further illustrated below, could lead to the induction of resistance 115

towards microbes in intercropping systems. First, a pathogen adapted to one plant may land 116

on a non-host, neighboring plant, and activate the plant immune system. Second, a molecule 117

(e.g. root exudate) and/or a perturbation of the environment (e.g. shade or competition for 118

nutrients) by one plant could trigger the activation of an immune response in a neighboring 119

plant. We provide below several examples illustrating these mechanisms. 120

Induction of the plant immune system by non-adapted pathogens produced by neighbors 121

Induced resistance has been documented in varietal mixtures where different genotypes of the 122

same species are grown in the same field (Mundt, 2002). The proposed mechanism is that the 123

virulent, adapted pathogen will multiply on the susceptible hosts, and disseminate spores to 124

genetically resistant neighbors where they will induce the plant immune system that will be 125

effective against another pathogen yet adapted to this plant. In the case of intercropping two 126

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plant species (rather than distinct varieties of the same crop), resistance could be induced by 127

pathogen propagules produced by the susceptible species landing on the neighbor non-host 128

species. Non-host induced resistance has been shown for different pathogens in the context of 129

intercropping (Ding et al., 2015). When this mechanism is at play, the resistance of one crop 130

relies on the susceptibility of the neighboring one. This contrasts with the simultaneous 131

reduction of disease on two intercropped species; as exemplified by the reduction of both leaf 132

blight on potato and northern leaf blight on maize when these two plants were intercropped 133

(Li et al., 2009). However, this mechanism could operate belowground; for instance one may 134

speculate that a plant recruiting a specific microbial community could trigger in the 135

neighboring plant an enhancement of the plant immune system. 136

Modification of the expression of the plant immune system in intercropping situations 137

Recent studies provide evidence that (i) growing two plants from different species next to 138

each other affects the expression of markers related to the plant immune system, and that (ii) 139

crop protection is observed when adapted pathogens challenge such plants. When watermelon 140

was intercropped with wheat, Phenylalanine Ammonia Lyase (PAL; involved in the 141

biosynthesis of secondary metabolites) activity was higher and the induction of several 142

defense-related genes was enhanced upon infection compared to watermelon grown alone (Xu 143

et al., 2015). This correlated with a strong reduction of disease incidence associated with the

144

soil-borne pathogen Fusarium oxysporum on watermelon. When intercropped with onion, 145

tomato showed an enhanced induction of genes involved in secondary metabolites synthesis 146

and responses to biotic stress (as measured by RNA-Seq). This molecular response correlated 147

with a decrease of wilt on tomato caused by the soil-borne pathogen Verticillium dalhiae (Fu 148

et al., 2015).

149

Partial control of the pathogenic fungus Cylindrocladium parasiticum can be achieved on 150

soybean by intercropping with maize (Gao et al., 2014). In this situation, soybean 151

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pathogenesis-related (PR) genes were induced to higher levels after infection when maize and 152

soybean root interacted with each other. No significant change in expression of these defense-153

related genes was observed when root contact was prevented. This suggests that a diffusible 154

signal from maize roots induced the expression of most PR genes tested as well as the PAL 155

gene in soybean roots. Quite interestingly, exudates from maize (but not from soybean) were 156

shown to contain salicylic acid, a potent inducer of defense-genes and systemic acquired 157

resistance (SAR; Fu and Dong, 2013), making this compound a good candidate for being part 158

of the signal. 159

There are, however, few studies identifying molecules responsible for the modification of 160

expression of the plant immune system in intercropping. Intercropping maize and pepper can 161

reduce blight on pepper roots caused by Phytophthora capsici (Yang et al., 2014) as well as 162

foliar disease on maize caused by the necrotrophic fungal pathogen Bipolaris maydis (Ding et 163

al., 2015). More specifically, root exudates from healthy pepper could reduce lesions caused

164

by B. maydis on maize plants (Ding et al., 2015). The expression of marker genes from 165

several defense pathways related to the plant immune system was measured in roots and 166

shoots of healthy maize plants treated with exudates from healthy pepper. An induction of the 167

AOS (Allene Oxide Synthetase) and AOC (Allene Oxide Cyclase) genes involved in the

168

biosynthesis of jasmonic acid was detected in maize roots. Although jasmonic acid was not 169

directly measured, these results are consistent with the role of this molecule in defense against 170

necrotrophic pathogens (Campos et al., 2014). A slight induction of the genes involved in 171

DIMBOA biosynthesis was also observed in maize plants pre-treated with pepper exudates. 172

This correlated with the accumulation of this secondary metabolite in the roots and shoots of 173

maize plants. DIMBOA and its major derivative were later shown to have an antimicrobial 174

activity on B. maydis in vitro. Thus, an unknown element of root exudates from pepper could 175

trigger some sort of systemic acquired resistance in maize. Interestingly, besides its 176

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antimicrobial function, DIMBOA and some of its derivatives were shown to affect histone 177

deacetylases and subsequently the transcription of several hundreds of plant genes in 178

Arabidopsis, among which a large set are known to be involved in response to biotic stress

179

(Venturelli et al., 2015). Therefore, one can speculate that some molecule(s) from pepper 180

exudates activate defense-related genes in maize roots and the production of molecules, 181

including DIMBOA, which would exert their effects through direct antimicrobial activity (as 182

in Yang et al., 2014) and indirectly through the further activation of defense-related genes. 183

This example suggests that molecules known for their allelopathic effects on microbes (see 184

above) could also affect the plant immune system. More recently, it was shown that p-185

coumaric acid secreted by rice roots could inhibit the germination of fungal spores and 186

constitutively induce PR gene expression in watermelon, conferring protection against F. 187

oxysporum when directly applied to watermelon (Ren et al., 2008; 2016). Likewise, a large

188

set of potent inducers of the plant immune system like salicylic acid (Khorassni et al., 2011) 189

and jasmonic acid (Strehmel et al., 2014) have been found in root exudates. 190

Finally, VOCs emitted by neighboring plants could also play a role in intercropping by 191

modifying plant resistance (reviewed in Heil and Karban, 2010). However, the majority of the 192

reports on VOCs in intercropping deal with the induction of defense against insects and there 193

are only few reports on the role of VOCs in intercropping against microbial diseases (e.g. 194

Gomez-Rodrıguez et al., 2003). 195

Stranger recognition may change the expression of the plant immune system 196

Several studies investigating plant adaptation to non-kin/stranger recognition also provide 197

evidence that expression of plant immune system can be influenced by neighboring plants. 198

Stranger recognition, which is well-known in animals, is defined as the ability to differentiate 199

related individuals from non-related ones either within species (conspecific) or between 200

species (heterospecific) (Biedrzycki and Bais, 2010). The latter situation best represents what 201

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is found in intercropping situations. In Arabidopsis, transcriptome analysis of roots in 202

conspecific competition experiments involving different ecotypes (a situation in between 203

conspecific and heterospecific competition) identified four categories of genes: transporters, 204

auxin-related, secondary metabolite and pathogen response genes that differed among 205

treatments (Biedrzycki et al., 2011). In particular, it was shown that PR genes were more 206

highly expressed in the case of plants grown next to non-kin. However, this over-induction of 207

defense was not correlated with reduced susceptibility to the bacterium Pseudomonas tomato. 208

When examining analysis of heterospecific competition, a global trend emerges with respect 209

to its effects on the expression of the plant immune system. A pioneer study by Schmidt and 210

Baldwin (2006) showed that several defense genes were expressed to higher levels in 211

Solanum nigrum plants cultivated with various interspecific competitors compared to those

212

grown alone. Broz et al (2010) showed that growing strangers (Festuca idahoensis) in the 213

neighborhood of Centaurea maculosa constitutively modified the production of secondary 214

metabolites associated with defense against pests compared to the situation where only C. 215

maculosa plants were grown. However, it was hard to conclude from this study whether

216

intercropping had a direct impact on herbivore resistance in both species. Arabidopsis plants 217

grown together with the weak plant competitor Hieracium pilosella were shown to express 218

higher defense-related genes like PRs in leaves than when grown with congeners, and the 219

overall expression pattern remarkably resembled that observed upon oomycete infection 220

(although no oomycete was detected in these experiments; Schmid et al., 2013). Jasmonic 221

acid-dependent defense seems to be affected by heterospecific competition: in soybean/canola 222

competition experiments, a negative regulator of JA was down-regulated by competition 223

(Horvath et al., 2015) while JA biosynthesis genes were induced in maize/canola competition 224

experiments (Moriles et al., 2012). This somehow mirrors the observation made in the case of 225

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maize/pepper intercropping presented above where root exudates from pepper could mimic 226

the effects of intercropping (Ding et al., 2015). 227

The mechanisms behind non-kin/stranger recognition in plants have been little studied but 228

unidentified root exudates seem to play a role in Arabidopsis (Biedrzycki and Bais, 2010). It 229

is likely that some of the allelopathic compounds produced by roots and known to participate 230

in competition may also be responsible for the modification of defense in intercropping. For 231

instance, the volatile alpha-pinene, produced by the roots of many plant species when 232

competing with other species, was shown to increase H2O2 production and the activity of

233

several enzymes related to the oxidative burst (Singh et al., 2006), which is also involved in 234

the response to pathogens. Since alpha-pinene was initially described as a potent inhibitor of 235

root growth required for plant-plant competition, this example suggests that the detrimental 236

effects of plant-plant competition may also indirectly contribute to an enhancement of the 237

plant immune system and therefore to an ecologically positive effect (by protecting their 238

neighbors). 239

Relationships between nutrition, light and disease in intercropping 240

Intercropping is well-known to improve yield and this effect is in part due to improved 241

nutrition. For instance, the uptake of P and micro-nutrients like Fe, Zn and Mn is improved in 242

several intercropping systems (Li et al., 2014). On the other hand, mineral nutrition is 243

paramount for plant health and competition for nutrients may strongly impact plant 244

physiology (Dordas, 2009). One may thus expect indirect effects on plant health in 245

intercropping through plant nutrition. For instance, increasing P, Fe, Zn or Mn reduces in 246

most cases disease susceptibility (Dordas, 2009), consistent with disease suppression in 247

intercropping systems. Yet, in the case of nitrogen, there is a paradox between its improved 248

uptake in intercropping and the reduction of disease (Chen et al., 2007). Indeed, for most 249

obligate pathogens, nitrogen increases plant susceptibility (Dordas, 2009). For instance, the 250

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increase of N in wheat leaves intercropped with faba bean was associated with a reduction 251

(and not an increase) of disease caused by powdery mildew on wheat (Chen et al., 2007). The 252

mechanisms that allow increased N content without increasing disease thus merit further 253

investigation. 254

Other mechanisms linking plant defense to competition-related pathways may also occur in 255

intercropping. For instance, shade avoidance, one of plant’s responses to competition for light, 256

is in part regulated by the ratio of red and far-red light perceived by plants, a ratio that can be 257

affected in intercropping situations (Zhu et al., 2014). Shade-avoidance has been shown to 258

affect the expression of many classical defense-related genes and this was associated with 259

modifications of the susceptibility of plants to various pathogens (reviewed in Ballaré et al., 260 2012). 261 262 Future challenges 263

Intercropping thus seems to directly and indirectly affect the plant immune system. Although 264

only few molecules in root exudates have been shown to induce the plant immune system, 265

there is yet no proof that they are responsible for the increased protection observed in 266

intercropping. Mutants for the production of these molecules will be required to test this 267

hypothesis. It remains difficult to assess whether intercropping is priming the plant immune 268

system, enabling plants to over-react only upon pathogen attack or constitutively activating 269

strong defenses. This question is critical to answer, as both strategies are likely to have 270

different effects of plant fitness and thus yield. 271

Identifying the molecular mechanisms underlying disease reduction in intercropping 272

represents a major technical challenge. Indeed, as shown above, competition effects are at 273

play in most experimental systems and are thus difficult to exclude from the equation. 274

Researchers should always keep in mind that the plant immune system and competition are 275

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intermingled by several means; measuring traits associated with these two biological 276

processes is needed in experimental systems designed to study intercropping. Some technical 277

solutions have also been developed in the field of allelopathy (He et al., 2012) and may be 278

useful to establish the respective roles of molecular communication and competition. 279

Many studies cited in this review were conducted under controlled laboratory conditions. 280

There is thus a need to demonstrate the relevance of these mechanisms in the field. There are 281

indeed only a limited number of examples indicating that patterns observed in controlled 282

conditions translate into the field. For instance, Fu et al (2015) used the manual inoculation 283

with Verticillium dahlia of tomato intercropped with onion to alleviate possible effects from 284

“root wall” or inhibition of the pathogen. An enhanced induction of defense could be shown 285

in the field and it explained as much as 36% of the disease reduction. More field experiments 286

with controlled inoculation should be performed to test whether plant-centered mechanisms 287

(Figure 1B) significantly contribute to disease reduction in intercropping and differentiate 288

these from the other effects operating at the field level in such agronomical systems (Figure 289

1A). 290

Communication in plants has received increased attention in recent decades (Heil and Karban, 291

2010). However, several communication channels and molecules are still unexplored, and 292

their roles in disease reduction in intercropping have been poorly investigated. Volatile 293

organic compounds released by plants can induce and prime plant defense against pathogens 294

(Pierick et al., 2014). Beyond pest control, the participation of such molecules in disease 295

control in intercropping against microbes remains to be evaluated. 296

Different crops may select and attract specific microbes by secreting specific root exudates 297

and, therefore, alter the composition and diversity of microbial communities in the 298

rhizosphere. For instance, the exudates of maize, one of the most popular crops used in 299

intercropping, have been shown to attract some plant-beneficial bacteria (Neal et al., 2012). In 300

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the watermelon/rice intercropping system, strong changes of microbial communities were 301

observed, with bacterial populations increasing by more than two-fold in watermelon 302

rhizosphere intercropped with rice (Ren et al., 2008). However, the link between these 303

changes in microbial community and disease protection in intercropping remains to be 304

established. 305

As it is clear that some species mixtures work better for protecting their neighbors than others 306

(see for instance Fernandez-Aparicio et al., 2010; Boudreau, 2013), it will be important to 307

investigate the potential of a large combination of plant species to provide additional solutions 308

for crop protection. Understanding why disease severity can sometimes increase in 309

intercropping will also be important to improve this agronomic practice. 310

311

Acknowledgements 312

We are thankful to Dr HUANG H, Dr LIU Y and Dr FREVILLE H for critical reading, Pr K. 313

PERRY for proofreading this manuscript and the anonymous reviewers. This work was 314

partially funded by a CASDAR project (BURRITOS), the CONTACT project supported by 315

the French ANR program “Investissement d’Avenir” ANR-10-LABX-0001-01, a CAFEA 316

exchange grant (GDT20165300009) to J-B M and the Natural Science Foundation of China 317

(31760535). We apologize for the many studies that could not be cited in this review because 318

of size limitation. 319

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490 491 492 493 494 495 496 497

Figure 1. Field and plant-centered mechanisms underlying microbial disease 498

suppression in intercropping systems. 499

A maize and pepper plant system was chosen to illustrate field (A) and plant-centered (B) 500

mechanisms responsible for the reduction of microbial diseases in intercropping. (A) At the 501

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field level, a pathogen on a first host species (maize) disseminates to a healthy, neighboring 502

host plant (1) with lesser efficiency because of inoculum dilution (2) caused by the 503

intercropped non-host plant (pepper) and also microclimatic changes. On the other hand, a 504

non-host plant species (maize) may create a physical barrier reducing the dispersal of 505

pathogen from host to host (3). (B) Three types of plant-centered mechanisms can contribute 506

to the modification of the plant immune system in intercropping systems: induced resistance, 507

indirect changes in the expression of the plant immune system through competition for 508

resources (e.g. shade avoidance), and direct and indirect effects of the production of 509

molecules (including allelopathic compounds). Above ground mechanisms include induced 510

resistance by non-adapated pathogen (yellow arrow), production of volatile organic 511

compounds (VOCs) that could activate the plant immune system (purple arrows) and/or 512

inhibit the growth of airborne pathogens (black line) and effects like shade-avoidance (red 513

arrow). Below ground mechanisms can be direct with inhibition of pathogens (black line) by 514

root exudates from non-host plant; root exudates can also directly affect the plant immune 515

system of host plants (blue arrow) or affect soil microbial community that may have 516

detrimental effects on pathogens (grey arrows). Nutrition/competition effects (e.g. 517

growth/defense trade-off) can also indirectly affect plant the plant immune system (black 518

dashed arrows). Only mechanisms triggered by a non-host plant (maize) and increasing 519

resistance on host plant (pepper) are shown but reciprocal effects exist. Question marks point 520

to poorly documented mechanisms. Examples are provided in main text. 521

522

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Figure 1. Field and plant-centered mechanisms underlying microbial disease suppression in intercropping systems.

A maize and pepper plant system was chosen to illustrate field (A) and plant-centered (B) mechanisms responsible for the reduction of microbial diseases in intercropping. (A) At the field level, a pathogen on a

first host species (maize) disseminates to a healthy, neighboring host plant (1) with lesser efficiency because of inoculum dilution (2) caused by the intercropped non-host plant (pepper) and also microclimatic

changes. On the other hand, a non-host plant species (maize) may create a physical barrier reducing the dispersal of pathogen from host to host (3). (B) Three types of plant-centered mechanisms can contribute to the modification of the plant immune system in intercropping systems: induced resistance, indirect changes in the expression of the plant immune system through competition for resources (e.g. shade avoidance),

and direct and indirect effects of the production of molecules (including allelopathic compounds). Above ground mechanisms include induced resistance by non-adapated pathogen (yellow arrow), production of volatile organic compounds (VOCs) that could activate the plant immune system (purple arrows) and/or

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Version postprint

inhibit the growth of airborne pathogens (black line) and effects like shade-avoidance (red arrow). Below ground mechanisms can be direct with inhibition of pathogens (black line) by root exudates from non-host

plant; root exudates can also directly affect the plant immune system of host plants (blue arrow) or affect soil microbial community that may have detrimental effects on pathogens (grey arrows).

Nutrition/competition effects (e.g. growth/defense trade-off) can also indirectly affect plant the plant immune system (black dashed arrows). Only mechanisms triggered by a non-host plant (maize) and increasing resistance on host plant (pepper) are shown but reciprocal effects exist. Question marks point to

poorly documented mechanisms. Examples are provided in main text. 93x133mm (150 x 150 DPI)