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- W2891547737 abstract "Mycorrhiza research has traditionally developed into distinct disciplines at different organizational levels from the cellular to ecosystem level. This separation leads to a limited understanding of mycorrhiza functioning and its role within ecosystems. Here, we show how the different disciplines in mycorrhiza research commonly address the same general questions and how these questions are nested in the next organizational level. By integrating different disciplines, these disciplines are able to complement each other and foster the development of a comprehensive understanding of mycorrhizal associations. We introduce two ongoing projects as examples where the integration of disciplines in mycorrhiza research is already common practice. Research on mycorrhizal interactions has traditionally developed into separate disciplines addressing different organizational levels. This separation has led to an incomplete understanding of mycorrhizal functioning. Integration of mycorrhiza research at different scales is needed to understand the mechanisms underlying the context dependency of mycorrhizal associations, and to use mycorrhizae for solving environmental issues. Here, we provide a road map for the integration of mycorrhiza research into a unique framework that spans genes to ecosystems. Using two key topics, we identify parallels in mycorrhiza research at different organizational levels. Based on two current projects, we show how scientific integration creates synergies, and discuss future directions. Only by overcoming disciplinary boundaries, we will achieve a more comprehensive understanding of the functioning of mycorrhizal associations. Research on mycorrhizal interactions has traditionally developed into separate disciplines addressing different organizational levels. This separation has led to an incomplete understanding of mycorrhizal functioning. Integration of mycorrhiza research at different scales is needed to understand the mechanisms underlying the context dependency of mycorrhizal associations, and to use mycorrhizae for solving environmental issues. Here, we provide a road map for the integration of mycorrhiza research into a unique framework that spans genes to ecosystems. Using two key topics, we identify parallels in mycorrhiza research at different organizational levels. Based on two current projects, we show how scientific integration creates synergies, and discuss future directions. Only by overcoming disciplinary boundaries, we will achieve a more comprehensive understanding of the functioning of mycorrhizal associations. In 2000, Miller and Kling stated that ‘to succeed, the mycorrhiza (see Glossary) research community must go beyond their usual disciplinary boundaries and integrate their work with that of other researchers’ [1Miller R.M. Kling M. The importance of integration and scale in the arbuscular mycorrhizal symbiosis.Plant Soil. 2000; 226: 295-309Crossref Scopus (37) Google Scholar]. Although some advances have been made in the 18 years since, mycorrhiza research still largely develops by specializing within different disciplines of biology. During the 19th century, research into arbuscular mycorrhiza commenced with the discovery of fungal structures colonizing roots [2Nägeli C. Pilze im Innern von Zellen.Linnaea. 1842; 16: 278-285Google Scholar, 3Frank A.B. Über die auf Wurzelsymbiose beruhende Ernährung gewisser Bäume durch unterirdische Pilze.Ber. Dtsch. Bot. Ges. 1885; 3: 128-145Google Scholar]. This early research was initially dominated by the descriptions of fungal morphological traits and potential fungal effects on plant performance. Such early research stayed at the organismal level, revealing more about the fungi, and studying effects at the individual host plant level. During the second half of the 20th century, research on mycorrhizae and their interactions developed into two main distinct directions: cellular and, later, subcellular biology on the one hand, and ecology on the other hand. This specialization has led to many crucial discoveries in mycorrhizal biology. Focusing on cellular processes, ultrastructural studies during the 1970s led to the first detailed description of plant–fungal interactions. This included arbuscule formation, the identification of the periarbuscular membrane, as well as identification of the interface (i.e., the contact area between the interaction partners) [4Bonfante P. Anatomy and morphology of VA mycorrhizae.in: Powell C.L. Bagyaraj D.J. VA Mycorrhizae. CRC Press, 1984: 5-33Google Scholar]. On the ecological side, the realization that unequal benefits may be provided to different plant species [5Baylis G.T.S. Root hairs and phycomycetous mycorrhizas in phosphorus-deficient soil.Plant Soil. 1970; 33: 713-716Crossref Scopus (92) Google Scholar] led to investigations of the importance of mycorrhizae in mediating plant adaptation and evolution as well as in structuring plant communities and biogeochemical cycles [6Van der Heijden M.G.A. et al.Mycorrhizal ecology and evolution: the past, the present, and the future.New Phytol. 2015; 205: 1406-1423Crossref PubMed Scopus (975) Google Scholar]. A milestone here was the experimental demonstration of arbuscular mycorrhizal (AM) fungal diversity effects on plant community diversity and productivity [7Van der Heijden M.G.A. et al.Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity.Nature. 1998; 396: 69-72Crossref Scopus (2596) Google Scholar]. With methodological and conceptual advances, the field of mycorrhiza research has extended further following studies on the physiology of plants [8Koide R.T. Mosse B. A history of research on arbuscular mycorrhiza.Mycorrhiza. 2004; 14: 145-163Crossref PubMed Scopus (189) Google Scholar] and on ecosystem effects [7Van der Heijden M.G.A. et al.Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity.Nature. 1998; 396: 69-72Crossref Scopus (2596) Google Scholar, 9Powell J.R. Rillig M.C. Biodiversity of arbuscular mycorrhizal fungi and ecosystem function.New Phytol. 2018; (Published online March 30, 2018)https://doi.org/10.1111/nph.15119Crossref Scopus (186) Google Scholar]. Each of the fields addresses different scales and levels of organization. Consequently, they have developed in distinct directions in terms of the questions addressed, scope, methods, and, perhaps most importantly, training and specialization of researchers. This division of the research field is illustrated by the fact that there are two main international scientific conferences on mycorrhizal research: the International Conference of Mycorrhiza (ICOM), focusing mostly on ecological research on mycorrhiza, and the International Molecular Mycorrhiza Meeting (iMMM), focusing mostly on molecular mycorrhiza research. Albeit effective in many respects, this historic partitioning into separate fields sometimes hinders a comprehensive understanding of how mycorrhizae function and influence their biotic and abiotic environment. For instance, our knowledge of the impact of mycorrhizae on ecosystem functions and services is relatively incomplete. This is due to the context-dependent nature of the symbiosis, which is driven by environmental conditions as well as the species identity of the plant and/or fungal partner. The interaction can exist along a continuum of possible outcomes for the plant, from mutualistic to detrimental [10Chaudhary V.B. et al.MycoDB, a global database of plant response to mycorrhizal fungi.Sci. Data. 2016; 3160028Crossref PubMed Scopus (61) Google Scholar]. Only by developing new investigation models that integrate multiple levels of organization will we be able to understand how environmental context impacts the relationships of plants with their mycorrhizal symbionts. This will allow us to make realistic predictions of the contribution of mycorrhizae to the functioning of ecosystems and to agricultural practices [11Gianinazzi S. et al.Agroecology: the key role of arbuscular mycorrhizas in ecosystem services.Mycorrhiza. 2010; 20: 519-530Crossref PubMed Scopus (569) Google Scholar]. Thus, we argue that mycorrhiza research can reach a new level of insight by integrating the strengths of the increasingly separated research disciplines, both from the cellular to the ecosystem level and vice versa. Here, we highlight how major topics in mycorrhiza research have been independently addressed by different disciplines across different organizational levels, and how they could complement each other. Within each topic, we focus on four organizational levels of life: the cellular and subcellular level (hereafter called the cellular level), the plant physiological level, the plant community level, and the ecosystem level. To stress the gains of integrating research across levels of organization, we present an overview of the benefits they may provide to each other. Moreover, we stress that, among the organizational levels, a consensus on research practices must be reached. Finally, we give recommendations for future directions towards integrative research networks, which aim at a more complete understanding of mycorrhizal associations and their functioning. As proof of concept, we introduce two recently developed projects in which such efforts are already underway. We focus on the two most commonly studied mycorrhizal types, namely AM and ectomycorrhizae (ECM), which are also the most common mycorrhizal symbioses in natural ecosystems. Studies of mycorrhizae at the physiological and cellular level are strongly biased towards AM compared with ECM. However, this imbalance, which is reflected in the predominance of AM compared with ECM examples in our paper, does not impede the validity of the presented framework, because this can in principle be applied to any type of mycorrhizae. Mycorrhiza research spans lower-organizational level processes [e.g., inorganic phosphorus (Pi) uptake and transport mechanisms, and modulation of plant immunity] to higher-organizational levels that affect plant community and ecosystem functioning (e.g., biogeochemical cycles or multitrophic interactions). While most studies focus on one or two levels of organization, mycorrhiza-related processes at one level are likely nested in and, thus, may provide mechanisms underlying the findings of, the next higher level (Figure 1, Key Figure). Here, we illustrate the potential nesting and links across the different organizational levels in mycorrhiza research by using two examples of key topics in mycorrhiza research: Pi uptake and multitrophic interactions. The AM symbiosis provides an effective way (the AM pathway) to scavenge Pi from large volumes of soil and rapidly deliver it to root cortical cells, thereby bypassing direct root Pi uptake. Cellular research revealed Pi transporters involved in the mycorrhizal phosphate uptake pathway. Some of these transporters show constitutive transcript levels in non-mycorrhizal roots [12Rausch C. Bucher M. Molecular mechanisms of phosphate transport in plants.Planta. 2002; 216: 23-37Crossref PubMed Scopus (400) Google Scholar], while others are mostly expressed in arbuscule-containing cells [13Javot H. et al.Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles.Plant Cell Environ. 2007; 30: 310-322Crossref PubMed Scopus (303) Google Scholar] (Figure 1A). These plant Pi transporters are located in the periarbuscular membrane and take up phosphate ions from the periarbuscular space, the apoplastic compartment between the plant periarbuscular membrane and fungal plasma membrane in arbuscule-containing cells. Recent molecular studies demonstrated that specific H+-ATPase proteins in the periarbuscular membrane are required to generate the proton gradient necessary for the action of Pi transporters [14Krajinski F. et al.The H+-ATPase HA1 of Medicago truncatula is essential for phosphate transport and plant growth during arbuscular mycorrhizal symbiosis.Plant Cell. 2014; 26: 1808-1817Crossref PubMed Scopus (94) Google Scholar]. These results are relevant for understanding the regulation of Pi acquisition in the AM symbiosis. However, without addressing the physiological level, this information is not sufficient for determining the relevance of the AM pathway with respect to the direct Pi uptake pathway. The same applies to assessing its net contribution to plant Pi uptake and, thus, plant nutrition and fitness. Plant physiological research revealed that the AM pathway has a major role in Pi uptake and, consequently, in plant growth (Figure 1A). Experiments with single plants and plant communities showed that AM fungi contribute up to 90% of plant P levels [15Jakobsen I. et al.External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L.New Phytol. 1992; 120: 371-380Crossref Scopus (719) Google Scholar, 16Leake J. et al.Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning.Can. J. Bot. 2004; 82: 1016-1045Crossref Google Scholar, 17Smith S.E. Smith F.A. Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales.Annu. Rev. Plant Biol. 2011; 62: 227-250Crossref PubMed Scopus (970) Google Scholar]. However, colonization by different AM fungal species can result in different fitness responses of the plant [18Klironomos J.N. Variation in plant response to native and exotic arbuscular mycorrhizal fungi.Ecology. 2003; 84: 2292-2301Crossref Scopus (860) Google Scholar]. Similarly, colonization by the same AM fungal species does not necessarily result in the same fitness response in different plant species. This indicates that there is considerable functional diversity among plant–AM fungal symbioses. Indeed, AM associations have also been shown to vary in their physiological characteristics [19Cavagnaro T.R. et al.Functional diversity in arbuscular mycorrhizas: exploitation of soil patches with different phosphate enrichment differs among fungal species.Plant Cell Environ. 2005; 28: 642-650Crossref Scopus (116) Google Scholar]. Still, the major forces driving this functional diversity are widely unknown. Combining a cellular approach with physiological experiments is a powerful approach to illuminate mycorrhizal functions, while providing a genetic explanation for the functional variation observed. Such information can even be implemented in the development of biomarkers for the assessment of mycorrhizal functional diversity and for the selection of efficient crop–fungus combinations for increasing agricultural productivity. Moreover, the symbiotic efficiency in terms of plant Pi uptake is further influenced by fungal community composition [7Van der Heijden M.G.A. et al.Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity.Nature. 1998; 396: 69-72Crossref Scopus (2596) Google Scholar]. To predict the net impact of mycorrhizae on Pi uptake, it is essential to combine physiological studies with studies at the community level, where plants are part of complex species interaction networks. To achieve this, it is crucial that techniques, such as high-throughput sequencing, transcriptomics, and metabolomics, are used in the field. Studies at the plant community level showed that both the productivity and composition of plant communities are altered by mycorrhizal associations. Mycorrhizae indirectly cause a redistribution of soil resources among plants (Pi) by enhancing the resource acquisition and competitive abilities of some plants over others [20Collins C.D. Foster B.L. Community-level consequences of mycorrhizae depend on phosphorus availability.Ecology. 2009; 90: 2567-2576Crossref PubMed Scopus (66) Google Scholar]. Furthermore, a greater richness of AM fungal species has been shown not only to increase net primary productivity through Pi supply, but also to maintain a more diverse plant community on which other organisms may depend [9Powell J.R. Rillig M.C. Biodiversity of arbuscular mycorrhizal fungi and ecosystem function.New Phytol. 2018; (Published online March 30, 2018)https://doi.org/10.1111/nph.15119Crossref Scopus (186) Google Scholar]. Directly, Pi allocation among plants is also changed through common mycelial networks (CMNs) [16Leake J. et al.Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning.Can. J. Bot. 2004; 82: 1016-1045Crossref Google Scholar] (Figure 1A). However, our knowledge of Pi transport (and nutrients in general) among plants and carbon transfer between plants and mycorrhizal fungi in CMNs is limited [21Selosse M.A. et al.Mycorrhizal networks: des liaisons dangereuses?.Trends Ecol. Evol. 2006; 21: 621-628Abstract Full Text Full Text PDF PubMed Scopus (331) Google Scholar]. Assessing the potential causes and effects of these resource fluxes on community functioning requires an understanding of the cellular and physiological processes driving this transfer, and the factors regulating these processes. Moreover, abiotic factors, such as soil nutrient availability, as well as micro- and macroclimate, can affect the net impact of mycorrhizae on plant Pi uptake and distribution in the community. The global impact of such factors can only be assessed in ecological settings. Research at the ecosystem level revealed that mycorrhizal associations have a key role in shaping ecosystem structure and function by altering the distribution of P among species, how it is recycled between above–belowground ecosystem compartments, and ultimately retained within an ecosystem [7Van der Heijden M.G.A. et al.Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity.Nature. 1998; 396: 69-72Crossref Scopus (2596) Google Scholar, 22Bender S.F. et al.Mycorrhizal effects on nutrient cycling, nutrient leaching and N2O production in experimental grassland.Soil Biol. Biochem. 2015; 80: 283-292Crossref Scopus (101) Google Scholar] (Figure 1A). All these processes may differ between ecosystem types and are affected by different abiotic factors, such as those mentioned above. This is typically referred to as ‘context dependency’. However, without knowledge of the physiological and plant community perspective on processes of resource distribution among plants via CMNs, it is hard to predict how changes in the processes are affected by different contexts and to identify the drivers of the changes. Cellular biological research on multitrophic interactions with mycorrhizae has yielded two important insights. First, following the exchange of signals during the presymbiotic phase, plants initially recognize mycorrhizal fungi to a certain extent as potential invaders, triggering a mild immune response [23Bonfante P. Genre A. Arbuscular mycorrhizal dialogues: do you speak ‘plantish’ or ‘fungish’?.Trends Plant Sci. 2015; 20: 150-154Abstract Full Text Full Text PDF PubMed Scopus (89) Google Scholar]. This immune response resembles the microbial-associated molecular pattern (MAMP)-triggered immunity (MTI) mounted after pathogen recognition. Such plant responses can subsequently be counteracted by the secretion of fungal effector molecules [24Kloppholz S. et al.A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy.Curr. Biol. 2011; 21: 1204-1209Abstract Full Text Full Text PDF PubMed Scopus (364) Google Scholar, 25Plett J.M. et al.A secreted effector protein of Laccaria bicolor is required for symbiosis development.Curr. Biol. 2011; 21: 1197-1203Abstract Full Text Full Text PDF PubMed Scopus (283) Google Scholar] and/or by the plant perception of MYC factors [26Siciliano V. et al.Transcriptome analysis of arbuscular mycorrhizal roots during development of the prepenetration apparatus.Plant Physiol. 2007; 144: 1455-1466Crossref PubMed Scopus (99) Google Scholar]. As a result of this molecular dialog between both partners, the levels of several defense-related phytohormones and other metabolites can be altered in mycorrhizal roots, and even shoots [27Fernandez I. et al.Defense related phytohormones regulation in arbuscular mycorrhizal symbioses depends on the partner genotypes.J. Chem. Ecol. 2014; 40: 791-803Crossref PubMed Scopus (64) Google Scholar, 28Kaling M. et al.Mycorrhiza-triggered transcriptomic and metabolomic networks impinge on herbivore fitness.Plant Physiol. 2018; 176: 2639-2656Crossref PubMed Scopus (46) Google Scholar]. Second, recent studies suggest that, as a consequence of this modulation of plant immunity by mycorrhizal fungi, mycorrhizal plants can enter into a state of sensitization of the immune system. This defense-primed state allows plants to respond faster and/or stronger when they are challenged by subsequent herbivore and pathogen attack [28Kaling M. et al.Mycorrhiza-triggered transcriptomic and metabolomic networks impinge on herbivore fitness.Plant Physiol. 2018; 176: 2639-2656Crossref PubMed Scopus (46) Google Scholar, 29Jung S.C. et al.Mycorrhiza-induced resistance and priming of plant defenses.J. Chem. Ecol. 2012; 38: 651-664Crossref PubMed Scopus (548) Google Scholar, 30Martinez-Medina A. et al.Recognizing plant defense priming.Trends Plant Sci. 2016; 21: 818-822Abstract Full Text Full Text PDF PubMed Scopus (373) Google Scholar] (Figure 1B). The pathway regulated by the plant hormone jasmonic acid (JA) has a crucial role in plant defense priming [28Kaling M. et al.Mycorrhiza-triggered transcriptomic and metabolomic networks impinge on herbivore fitness.Plant Physiol. 2018; 176: 2639-2656Crossref PubMed Scopus (46) Google Scholar, 31Song Y.Y. et al.Priming of anti-herbivore defense in tomato by arbuscular mycorrhizal fungus and involvement of the jasmonate pathway.J. Chem. Ecol. 2013; 39: 1036-1044Crossref PubMed Scopus (99) Google Scholar]. Although more robust plant defense is usually associated with better performance in times of stress, boosting induced defense responses does not always provide an advantage to the plant [32Douma J.C. et al.When does it pay off to prime for defense? A modeling analysis.New Phytol. 2017; 216: 782-797Crossref PubMed Scopus (30) Google Scholar]. The incorporation of a physiological approach is essential to understand the effects on whole-plant performance. For instance, fundamental questions on the contribution of mycorrhizal-boosted defenses to plant resistance against antagonists, or on their role in herbivore-induced changes in carbon assimilation and partitioning of assimilates, can only be addressed by integrating the mycorrhizal impact on plant defense signaling networks into whole-plant models. Plant physiological research revealed that both AM and ECM fungi induce changes in the immune system of a plant that impact the interaction of the plant with other community members at different trophic levels [33Pozo M.J. Azcon-Aguilar C. Unraveling mycorrhiza-induced resistance.Curr. Opin. Plant Biol. 2007; 10: 393-398Crossref PubMed Scopus (713) Google Scholar] (Figure 1B). Given that mycorrhizal fungi prime plants for JA-signaled defenses, it was speculated that mycorrhizal colonization would predominantly negatively affect leaf-chewing herbivores and necrotrophic pathogens. Both attackers are mostly responsive to JA-mediated defenses [34Wasternack C. Action of jasmonates in plant stress responses and development-applied aspects.Biotechnol. Adv. 2014; 32: 31-39Crossref PubMed Scopus (201) Google Scholar]. At the same time, mycorrhizal colonization would benefit piercing and sap-sucking herbivores, and biotrophic pathogens, which are more responsive to salicylic (SA)-mediated defenses. However, studies showed high variation in the effect of mycorrhizal colonization on plant–herbivore interactions [35Hartley S.E. Gange A.C. Impacts of plant symbiotic fungi on insect herbivores: mutualism in a multitrophic context.Annu. Rev. Entomol. 2009; 54: 323-342Crossref PubMed Scopus (307) Google Scholar]. This suggests that additional factors are involved in determining the final outcome of mycorrhiza–plant–insect interactions [36Biere A. et al.Three-way interactions between plants, microbes and insects.Funct. Ecol. 2013; 27: 567-573Crossref Scopus (112) Google Scholar]. More accurate predictions at the whole-plant level would require a better integration of cellular and physiological studies, providing insight into the mechanisms involved with studies of the ecological function of traits that are influenced by mycorrhizae. Furthermore, this combination of physiological and cell biological information has the potential to provide the foundation for the application of mycorrhizae in pest management strategies. Besides directly affecting plant antagonists, mycorrhizae might influence plant–herbivore interactions by affecting the attraction of natural enemies of insect herbivores [37Schausberger P. et al.Mycorrhiza changes plant volatiles to attract spider mite enemies.Funct. Ecol. 2012; 26: 441-449Crossref Scopus (100) Google Scholar]. Additionally, they can alter the competitive ability of plants within the community [38Wagg C. et al.Mycorrhizal fungal identity and diversity relaxes plant-plant competition.Ecology. 2011; 92: 1303-1313Crossref PubMed Scopus (197) Google Scholar]. Finally, plants can exchange defense-related information with other plants in the community via CMNs, as shown in laboratory studies [39Babikova Z. et al.Arbuscular mycorrhizal fungi and aphids interact by changing host plant quality and volatile emission.Funct. Ecol. 2014; 28: 375-385Crossref Scopus (69) Google Scholar]. Therefore, including the community perspective in real-world scenarios is essential to predict the net impact of mycorrhizae on plant–herbivore interactions at the whole-plant level. The effects of mycorrhization on plant physiology trickle up to influence microbial, animal, and plant community structure and ecosystem functioning [40Lee E.H. et al.Diversity of arbuscular mycorrhizal fungi and their roles in ecosystems.Mycobiology. 2013; 41: 121-125Crossref PubMed Scopus (90) Google Scholar]. Besides modifying aboveground plant productivity, mycorrhizal associations have been shown to influence the diversity of plant species as well as that of higher trophic levels, such as herbivores and parasitoids [41Hempel S. et al.Specific bottom-up effects of arbuscular mycorrhizal fungi across a plant–herbivore–parasitoid system.Oecologia. 2009; 160: 267-277Crossref PubMed Scopus (76) Google Scholar]. Moreover, CMNs connecting mycorrhizal plants within a community act not only as conduits for carbon and mineral nutrients, but also as an underground messaging system (‘signaling highway’) [42Barto E.K. et al.Fungal superhighways: do common mycorrhizal networks enhance below ground communication?.Trends Plant Sci. 2012; 17: 633-637Abstract Full Text Full Text PDF PubMed Scopus (110) Google Scholar]. This allows neighboring plants to activate defenses before they are attacked themselves [43Song Y.Y. et al.Interplant communication of tomato plants through underground common mycorrhizal networks.PLoS One. 2010; 5e13324Crossref PubMed Scopus (173) Google Scholar, 44Babikova Z. et al.Underground signals carried through common mycelial networks warn neighbouring plants of aphid attack.Ecol. Lett. 2013; 16: 835-843Crossref PubMed Scopus (234) Google Scholar] (Figure 1B). Although this phenomenon has been exclusively studied in laboratory settings, CMNs have the potential to determine the outcome of multitrophic interactions beyond the individual plant level, by conferring information about herbivore presence within a community. Consequently, they may also change predator and parasitoid recruitment at the community level. Still, the cost and benefits of interplant signaling, and their evolutionary consequences, remain mostly unknown. Analyzing the impact of CMNs in plant- and insect-related traits at the physiological level and the main mechanisms of interplant signaling at the cellular level will help to address these questions. Typically, in nature, the outcome of such interactions is not exclusively determined by the interaction partners per se. A multitude of environmental factors that can only be measured at the ecosystem level (under field conditions) may strengthen or weaken species interactions. Mycorrhizal fungi alter plant community performance and higher-trophic level community structure, thereby impacting element and energy cycling of the whole ecosystem (Figure 1B). For example, by changing the chemical composition of leaves and roots, mycorrhizae will likely affect the decomposition of plant litter [45Phillips R.P. et al.The mycorrhizal-associated nutrient economy: a new framework for predicting carbon-nutrient couplings in temperate forests.New Phytol. 2013; 199: 41-51Crossref PubMed Scopus (549) Google Scholar], which serves as the main basal resource in the belowground food web. Changes in basal resources affect the trophic structure and multitrophic interactions of the food web, and add to plant community effects on nutrient cycling of the whole ecosystem. Patterns in multitrophic interactions observed at the ecosystem level will remain correlative if not integrated with more mechanistic studies at the plant physiological and community levels. This is also important to apply mycorrhiza research to agriculture and/or crop production. For instance, the application of fertilizers and pesticides is subject to strong political and industrial pressures. Understanding the mechanisms and processes involved in AM function could underpin the development of novel crop plant–mycorrhizal associations for optimal nutrient uptake efficiency and, simultaneously, for higher resistance against antagonists. To create a conceptual framework that transcends individual disciplines in mycorrhiza research, researchers" @default.
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- W2891547737 title "Growing Research Networks on Mycorrhizae for Mutual Benefits" @default.
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- W2891547737 doi "https://doi.org/10.1016/j.tplants.2018.08.008" @default.
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