Three‐way interactions between plants, microbes and insects

Abstract

Plants are important mediators of interactions between their associated microbe and insect communities (Van der Putten et al. 2001; Ohgushi 2005). Changes in plants induced by one species have cascading effects on interactions with other species, shaping their abundances and community structure (Ohgushi 2008). While the consequences of such indirect interactions for community structure have predominantly been examined within the plant-associated insect community (e.g. Van Zandt & Agrawal 2004; Poelman et al. 2008; Utsumi 2011), there is growing evidence that there are similar community-wide impacts of plant-mediated interactions between microbes and insects (e.g. Kluth, Kruess & Tscharntke 2001; Omacini et al. 2001; Katayama, Zhang & Ohgushi 2011; Tack, Gripenberg & Roslin 2012). This highlights the ecological importance of three-way interactions between plants, microbes and insects. The study of such ‘plant–microbe–insect’ (PMI) interactions (Fig. 1) is a research area that has been rapidly expanding in the past two decades. Molecular studies of the mechanisms underlying these three-way interactions, as well as ecological and evolutionary studies of the consequences of PMI interactions in natural communities, have recently given a large impetus to this young field. In this special feature, we have brought together eight papers reviewing different aspects of these recent advances in the field of PMI interactions. Research on PMI interactions has gradually bridged the traditionally separated subdisciplines of plant pathology, insect pathology and entomology. Plant pathologists early on realized that insects were not only important vectors of plant disease, but also one of the factors determining what was then called ‘host predisposition’ (Yarwood 1959; Schoeneweiss 1975). This term was used to describe any environmental alteration of the susceptibility of host plants to their pathogens, prior to their interaction. Similarly, in the 1980s, a series of reviews from entomologists appeared on the effects of plant- and insect-associated microbes on plant resource exploitation by insects (e.g. Jones 1984; Hammond & Hardy 1988), culminating in the seminal book on microbial mediation of plant–insect interactions by Barbosa, Krischick & Jones 1991, which provided the first detailed and fascinating overview of the widespread, diverse and strong roles played by plant- and insect-associated microbes in shaping plant–insect interactions. PMI interactions represent a broad research field, both in terms of the disciplines involved (from molecular biology to community ecology) and in terms of the diversity of types of interactions that it embodies. Microbial mediation of plant–insect interactions (Fig. 1a) is in fact just one of three ramifications of PMI interactions, illustrated in Fig. 1, that further encompass insect mediation of plant–microbe interactions (Fig. 1b) and plant mediation of insect–microbe interactions (Fig. 1c). Microbial mediation of plant–insect interactions involves two basic pathways (Fig. 1a, arrows 1; Fig. 1a, arrows 2). First, plant microbial pathogens and symbionts affect the suitability of their host plants as a resource for herbivorous insects through alteration of their abundance, phenology, morphology, physiology, biochemistry or other aspects that subsequently affect herbivore performance, population dynamics and community structure (Fig. 1a-1; e.g. Hatcher 1995; Stout, Thaler & Thomma 2006; Hartley & Gange 2009; Pineda et al. 2010). One example of such interactions is the induction of defences against herbivores by some phytopathogens (Stout, Thaler & Thomma 2006). Second (Fig. 1a-2), insect microbial pathogens and symbionts affect the ability of their insect hosts to exploit their food plants, exerting a strong influence on their performance, dynamics and specialization on different food plants (e.g. Jones 1984; Janson et al. 2008; Feldhaar 2011; Ferrari & Vavre 2011; Frago, Dicke & Godfray 2012). For example, acquisition of microbial nutritional endosymbionts not only enabled insects to evolve a plant-sap-feeding lifestyle (Takiya et al. 2006), but also facilitates current host shifts of pest insects onto agricultural crops (e.g. Hosokawa et al. 2007). This type of interaction also includes microbial symbionts that are actively transmitted and cultivated by insects to break down plant tissue, such as the fungal gardens of leaf-cutting ants (e.g. Currie et al. 2003). Microbial mediation of plant–insect interactions is mirrored by insect mediation of plant–microbe interactions (Fig. 1b). First (Fig. 1b-1), insects can affect the abundance, accessibility or suitability of host plant tissue for the plant's microbial symbionts and pathogens (Fig. 1b-1; e.g. Hatcher 1995; Rostás, Simon & Hilker 2003; Stout, Thaler & Thomma 2006). Some examples of successful biological control are based on this type of interaction. For instance, the success of the Argentine cactus moth in controlling the invasive prickly pear in Australia in the 1920s was partly based on the fact that its feeding wounds provided access to secondary pathogens that killed the cactus (Caesar 2000). Second (Fig. 1b-2), insects affect plant–microbe interactions as vectors of plant pathogens. The far-reaching consequences of this type of interaction are evident from the knock-on effects of the introduction of disease-vectoring insects that cause severe problems in natural systems and agriculture due both to their introduction of new plant diseases and their enhanced spread of plant diseases that were already present in the area (e.g. Pan et al. 2012). Finally (Fig. 1c), plants can significantly impact insect–microbe interactions. For example, food plant quality can affect the susceptibility of herbivorous insects to their entomopathogens (Fig. 1c-1; Cory & Hoover 2006; Cory & Ericsson 2010) or affect their availability as food for, for example, mycophagous insects, as well as the performance of insect nutritional symbionts (Fig. 1c-2; e.g. Davis & Hofstetter 2012). Since the seminal work by Barbosa, Krischick & Jones (1991), there has been an upsurge of research on PMI interactions, and vast progress has been made, particularly in three areas of research. First, the rise of new molecular methods has revolutionized studies on the molecular mechanisms underlying induced responses of plants to microbes and insects. This has led to detailed insight into the molecular networks underlying signalling and defence activation by plants in response to different guilds of microbes and insects. This insight has been helpful in understanding how plants integrate and prioritize their responses to multiple attackers and to understand observed patterns in the induction of resistance (or susceptibility) to particular guilds of insects by particular guilds of microbes and vice versa. Second, PMI studies are increasingly placed in a community context. Whereas initial studies mainly focused on the effects of PMI interactions at the level of the physiology or individual performance of organisms, there has been an increasing effort to place PMI interaction studies in a community-wide perspective, incorporating interactions with higher trophic levels, effects on community structure and composition and assessing their importance in the context of climate change and biological invasions. In addition, the scope has widened from a focus on phytopathogens and insect herbivores and their endosymbionts to incorporate other classes of organism, such as plant symbionts (e.g. mycorrhizae, rhizobia and endophytes) and rhizobacteria, revealing their important roles in PMI interactions. Third, there has been an increasing effort to understand the role of PMI interactions in the evolution of traits of species involved in the interaction and in eco-evolutionary feedbacks. Below, we introduce the eight papers in this special feature in the context of these new developments. One of the important mechanisms underlying PMI interactions is the induction of plant defences by insects and beneficial or pathogenic microbes that result in cross-resistance or susceptibility. In the past two decades, molecular biologists have made vast progress in unravelling the complex regulation of the plant's induced responses to biotic agents (e.g. Pieterse et al. 2012). This has provided valuable insight into how plants tailor their responses to specific biotic agents and in the potential patterns of cross-induced resistance and susceptibility. The contributions by Pineda et al., Giron et al., Hauser et al. and Ponzio et al. all address aspects of the mechanisms underlying induced plant responses and their consequences for PMI interactions. Induced responses of plants to biotic agents have a complex regulation. Its basis is formed by a network of defence signalling pathways that is regulated by a small set of phytohormones in which salicylic acid (SA), jasmonic acid (JA) and ethylene (ET) play key roles. Biotic attack triggers a specific set of signals, and their timing and composition (the ‘signal signature’) determine the set of downstream defence genes that is subsequently activated (Pieterse & Dicke 2007). The general picture emerging from these studies is that there is broad overlap in the signalling pathways that are triggered by particular types of insects and microbes, but that the pattern of downstream activation of defences is highly specific for the particular plant–attacker combination (De Vos et al. 2005). An important reason for this specificity in the activation of defences is that there are additional levels of regulation of the signal signature, both by the plants and by their attackers. Importantly, signalling pathways are interconnected and ‘crosstalk’, providing an additional level of regulation that gives plants the opportunity to fine-tune and prioritize their defence in response to specific attackers. Pineda et al. (2013) in this issue show that this crosstalk is not restricted to signals coming from the biotic component of the environment. Signalling pathways triggered by abiotic stress interact with those triggered by microbes and insects. This results in strong effects of abiotic stress on plant–microbe, plant–insect and PMI interactions. For instance, the phytohormone abscisic acid (ABA), an important regulator of plant responses to osmotic stress imposed by drought and salt, interacts in a complex, but well understood way with SA, JA and ET. Such information is clearly relevant if we want to predict the impact of environmental change on PMI interactions. The authors provide a review of studies of the effects of abiotic stress on PMI interactions that shows an interesting pattern. In general, plant-mediated effects of microbes on herbivores are enhanced under abiotic stress. In accordance with the observed pattern, the protective effect of beneficial microbes against herbivory and their effect on tolerance to biotic and abiotic stresses appear to be enhanced under the most stressful abiotic conditions, or, as the authors put it, beneficial microbes help plants when they need it most. This raises the interesting question whether this type of crosstalk between signals from the abiotic and biotic environment has evolved as an adaptive plant mechanism, enabling them to regulate the extent to which they accommodate beneficial microbes in response to the extent of abiotic stress that they experience (cf. Thaler, Humphrey & Whiteman 2012). Insight into these mechanisms can provide a better understanding of how the abiotic environment induces shifts between mutualism and antagonism in interactions between plants and their microbial symbionts. Unravelling mechanisms of plant responses in biotic interactions with beneficial and harmful biotic organisms has mainly focused on the role of the plant hormones JA, SA, ET as key players in the signalling network regulating plant growth and defence. The role of other phytohormones as additional regulators in these networks has only recently become fully appreciated (Robert-Seilaniantz, Grant & Jones 2011). Whereas the contribution by Pineda et al. (2013) that was described above highlights the importance of ABA, Giron et al. (2013) in this issue review the role of another phytohormone that is strongly under-represented in studies of plant biotic interactions, namely cytokinins (CKs). Through their effects on source–sink relationships, senescence and plant defence, these phytohormones play an important role in plant biotic interactions. Over evolutionary time, cytokinins have become targets of modulation by microbes and arthropods as a means of controlling plant metabolism to the benefit of these pathogens and herbivores. A striking example are leaf miners that can selectively delay senescence and preserve the nutritional value of the leaf tissue that they inhabit through cytokinin-mediated modulation of the physiology of their host plants leaves. Interestingly, these cytokinin-mediated alterations are not mediated by the insect itself, but by one of its microbial endosymbionts. This illustrates the complexity of such PMI interaction and the role that insect endosymbionts play in expanding the ecological niche of their insect hosts. The review gives a fascinating insight into the diverse roles of cytokinins in biotic interactions and suggests that they play an important role in the regulation of complex source–sink relationships structuring plant-based food webs. Many studies of PMI interactions have documented the consequences of plant-mediated interactions between insects and microbes for the performance of these insects and microbes, but very few have examined the consequences for the fitness of the mediating plant itself to assess how the way in which plants cope with multiple attacks affects their own performance. Hauser et al. (2013) in this issue perform a meta-analysis of the combined effects of plant pathogens and insect herbivores on plant performance. They analyse patterns of additive, synergistic and antagonistic effects of different guilds of insect herbivores and pathogens on plant performance by comparing their combined impact with their impacts as single attackers. Interestingly, molecular studies of the mechanisms underlying induced defence generate predictions as to which guilds of pathogens and herbivores are expected to synergize or antagonize each other's effects on plant fitness. For example, biotrophic pathogens and piercing or sucking insects are signalled through and affected by the same (SA-dependent) defence pathway. We could therefore expect that they will antagonize each other and hence reduce each other's negative impact on plant fitness, resulting in a less-than-additive negative impact based on the sum of their individual effects. Surprisingly, very few of these predictions were supported by the meta-analysis, suggesting that additional factors are involved in determining the joint impact of herbivores and pathogens on plant fitness. An important observation from their work is that overall, pathogens and herbivores are synergistic in their negative effects at the level of individual plant tissues (e.g., shoot biomass), but additive to antagonistic in their effects on whole-plant biomass, corroborating similar findings from earlier studies (Fournier et al. 2006). This strongly suggests that plants can compensate for the ‘extra’ loss of resources from interactions between pathogens and herbivores, so that the synergistic effects at the tissue level disappears at the level of whole-plant performance. In addition to triggering induced direct defences in plants, insects and microbes can also affect indirect The term indirect defence to plant traits that the of the natural of their herbivores. Plant interactions with of their associated other plants, microbes, insects and natural of insects & and are an important of indirect defence. Since plant are strongly by microbes and insects, they are one of the important plant traits mediating community-wide PMI interactions. While effects of individual herbivores or microbes on are well we have understanding of how patterns of are when plants are under multiple Ponzio et al. (2013) in this issue review how by different insect herbivores or by an insect herbivore and a affects work has the importance of phytopathogens as of the patterns of their host modulation is one of the in which the of their insect vectors and their to the of their host plants & & 2011). Ponzio et al. (2013) show that in of insects and pathogens, also pathogens can significantly the pattern of While there are few studies to general it is interesting that the few studies are in with predictions from of signalling interactions. In attack by a microbe and a insect a enhanced to insect herbivory a biotrophic This is in with JA involved in the of important classes of resulting in of biotrophic pathogens are signalled through a that the JA resulting in Such interactions have important consequences for the plant as they can or their indirect defence. The review by Ponzio et al. (2013) therefore highlights the importance of both plant–microbe and plant–insect interactions in studies of the effects of plant on the community dynamics of plant-associated interactions between herbivores can be important in structuring herbivore communities (Ohgushi & 2007). Similarly, we can whether plant-mediated interactions between microbes and herbivores can structure consequences of plant-mediated effects of microbes on herbivores mainly focused on consequences at the level of and studies examined the effects of in plant traits or on the and performance of individual herbivores or on their population it has become that such effects can to the community For instance, microbes effects on insect herbivores through alteration of plant abundance, nutritional quality and defence (Van der Putten et al. 2001; Hartley & Gange exerting effects on insects, both at the species & and community level Zhang & Ohgushi 2011). an example, rhizobia cause to in resulting in higher species and community composition of and herbivores, as well as a higher and diversity of at higher trophic levels Zhang & Ohgushi 2011). Similarly, Omacini et al. that affect the of two species, their of by secondary and the of the food In addition to plant also plant pathogens can affect insect abundances and community composition (e.g. Kluth, Kruess & Tscharntke 2001; & 2008; Tack, Gripenberg & Roslin 2012). the community structure of insects is not only affected by plant induced by herbivores, but also by plant induced by In this & Dicke (2013) review how plant pathogens impact communities of insects at multiple and They show that such effects by a of For instance, in plant quality that affect herbivore can to with the natural in plant quality that affect and feeding can to in the of herbivores at different with effects on the insect & Dicke (2013) a for a community-wide on interactions and the importance of the and of these interactions. They further that studies of plant pathogens structuring herbivore communities are insight into the how herbivores structure communities, is very we have the ecological consequences of plant indirect effects for structuring there has also been increasing in evolutionary consequences of such indirect effects 2011), the biotic context for instance, a can and in a plant–insect interaction. In this & (2013) review evolutionary in PMI interactions. The community context can the pattern of that two species on each other's important For instance, the fitness of of on the they but the and of this interaction are further by the or of a plant et al. 2007). The the or natural the interactions between and & (2013) show that in this way microbes in interactions, herbivores in plant–microbe interactions and plants in interactions and that this has important for understanding of in species interactions. has been in the context of (e.g. interactions. means that that from a particular host population higher fitness on the host from that population that from other host the of these hosts can be strongly by could in fact be to the specific induced by species with which they not is evidence for such complex patterns of For instance, arthropods to the microbial symbionts of their host plants et al. and insect pathogens perform better on hosts when these are feeding on the food plant species from the population from which they when they on food plants & of is to in studies that have a interaction from the biotic context in which the interaction that when these studies that are relevant to the interaction in the The authors be by such complex interactions and studies that a combination of microbe and insect as a for the One of the PMI interactions that have been well from both an ecological and evolutionary are interactions between plants, plant and arthropods that these & 2011). have evolved of host plants by their metabolism to and their host their and the interaction to their Some studies evolutionary of host in with their et al. 2012). studies have focused on how affect and few how vectors affect the and evolution of plant In this et al. (2013) provide a They first review how plant affect physiology and to their of or through of the host they review how affects the of within the as well as their population and They show that of population structure and feeding a strong impact on They further one of the in which and the plant's to and their at the vectors are This is an example of how stresses in the of plant that affect their of by insect a type of PMI interaction in which a plant–insect molecular the of a The papers in this issue the ecological and evolutionary importance of three-way interactions between plants, microbes and insects. Through plant-mediated microbes can structure insect communities insects can structure microbial In the community of microbes can affect between plants and insects. This can rise to strong eco-evolutionary & is a in which the community context evolutionary change in and these evolutionary in in ecological interactions and community While there is growing evidence for such eco-evolutionary within plant-based insect communities 2011), the papers in this issue show that there is opportunity for such in interactions between plants, microbes and insects as The papers also some of the vast progress in unravelling the molecular mechanisms underlying plant responses to beneficial and pathogenic microbes and insects and their modulation by the abiotic environment. Such insight is important for understanding how plants prioritize their defence responses and cope with multiple but also for understanding patterns of cross-induced resistance and susceptibility between microbes and insects, and for how PMI interactions will to environmental their ecological and evolutionary PMI interactions also have for of importance such as biological and are types of interactions between microbes and insects that have synergistic negative effects on plant performance. Such interactions can have effects on but effects in of biological there are also types of interactions that can plant for example, by beneficial plant microbes that plant resistance and tolerance to pest species and other This that there are for PMI interactions to and food which have in with the of interactions. One of the important of PMI interactions in an ecological as well as context is their role in biological invasions. This role is in the contribution of this issue by to species and communities and of plants, microbes and insects. Many that to the success or of plant and are based on biotic interactions & interactions interactions, is how the of complex species interactions plants, microbes and affect In this (2013) reviews whether PMI interactions play a role in or the spread of invasive In PMI interactions appear to invasive species interactions. The of in which PMI interactions invasive species are predominantly of that appear to complex interactions. a the influence of PMI interactions in the of invasive plants, insects and microbes could have consequences for ability to and the contributions in this issue a detailed insight into the mechanisms and ecological and evolutionary roles of PMI interactions, which we will the to this field. We are very to for and for this special feature and to and for their We the for an on interactions by Hauser and and all the for their contributions that formed the basis for this special was supported by and