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Future challenges in plant-microbe-insect interactions

What do herbivore endosymbionts, microbial priming of plant herbivore defence, and plant pathogen-herbivore interactions have in common?  These are all examples of cases where microbes and insects modify plant responses to insects and microbes.  The interactions and organisms in this field are relatively diverse:  microbes in these interactions, for example, can be associated with soil, roots, leaves, or insects themselves and directly or indirectly interact with both plants and insects.  The outcome of these interactions can also be diverse:  insects can enhance the antagonistic impacts of microbes by acting as vectors or even modifying plant tissues; microbes can reduce herbivory by priming plant defensive responses; and viruses and microbes can even alter plant communication with herbivore enemies.  Even more importantly, the outcome of these interactions has important consequences for how we manage pests in agriculture (Barber, Kiers, Hazzard et al., 2013, Orrell & Bennett, 2013) and suppress invasive plants, insects, and microbes (Bennett, 2013).

The goal of this virtual issue, the special session at the International Symposium on Insect-Plant Interactions (16th SIP, 2-6 July 2017 in Tours, France), and the Functional Ecology Special Feature published on this topic in 2013 is to highlight the importance of these interactions, and promote their study from molecular mechanisms through ecological and evolutionary consequences.  

Recent years have seen a tremendous rise in our awareness that insects, plants and their associated microorganisms form complex interactions with possible consequences of each of them on all levels of the trophic chain.  In this Virtual Issue we also want to highlight the need to look across studies and systems to decipher these complex interactions and how they can impair, modulate or promote ecological networks.  Thus we include studies on microbial induction or suppression of plant quality or direct plant herbivore defences (Babikova, Gilbert, Bruce et al., 2014, Panaccione, Beaulieu & Cook, 2014, Whitehead & Bowers, 2014, Mauck, Smyers, De Moraes et al., 2015, Su, Oliver, Xie et al., 2015, Wurst & Ohgushi, 2015, Ueno, Gundel, Omacini et al., 2016, Fuchs, Krischke, Mueller et al., 2017)), endosymbionts of herbivores (Kaltenpoth & Engl, 2014, Oliver, Smith & Russell, 2014, Su et al., 2015, Wagner, Martinez, Ruan et al., 2015, White, McCord, Jackson et al., 2017), pathogen-insect vector interactions (Penaflor, Mauck, Alves et al., 2016), microbial alteration of volatiles and indirect plant defense (Babikova et al., 2014, Ponzio, Weldegergis, Dicke et al., 2016), and even microbial alteration of plant-pollinator interactions (Schaeffer, Mei, Andicoechea et al., 2017).  Studies in this Virtual Issue also highlight the tentative steps being taken in this field that are beginning to address how plant-microbe-insect interactions scale to up to the landscape level (Mauck et al., 2015, Wagner et al., 2015) and how climate changes are likely to alter these interactions (Ueno et al., 2016).

Can we look across the different systems and organisms in this Virtual Issue (and published elsewhere) and ask broader questions?  Within the field of plant-microbe-insect interactions we have collected enough data to answer simple questions such as whether all microbes and all insects have the same influence:  we have found, for example, within these systems, that microbes sometimes suppress or promote insects, and insects sometimes promote or suppress microbes.  Plants can benefit from associating with both insects and microbes, but they can also suffer.  However, these simple answers do not provide clear mechanistic explanations for when we should see these effects.  Thus, we need to turn our attention to looking for more mechanistic commonalities between systems. 

For example, if we were to take a community ecology approach to integrate multiple organisms within a category (plants, insects, or microbes) or multiple types of interactions (multiple mutualists such as pollinators, predators, parasitoids; or multiple antagonists), would we see the same patterns emerging as in simpler systems?  No study within our Virtual Issue has taken this approach, however several studies have broadened their scope to look at effects on multiple interactors within a class (Ponzio et al., 2016), multiple mutualists (White et al., 2017) and multiple antagonists (Penaflor et al., 2016) within plant-microbe-insect systems.  This allows us to also ask whether the same mechanisms that allow microbes to manipulate herbivores (e.g. priming of plant defences and endosymbiont associations) allow microbes to influence plant-pollinator interactions or other interactions with beneficial insects?  There is only a small number of studies on the influence of microbes on pollinators, and the vast majority of these focus on the influence of beneficial microbes on plant pollination (reviewed in Barber & Gorden, 2015).  To expand these studies into true community ecology approaches, researchers should take advantage of the expanding fields like network ecology to draw broader conclusions about the impact of plant-microbe-insect interactions.

Do all insect associated microbes (e.g. vectored pathogens, endosymbionts), even if they are phylogenetically distinct, manipulate insect and plant hosts in a similar manner?  Do all microbes (regardless of their association with soil, plant organs, or insects or their effect (antagonist, commensualist, or mutualist)) use the same molecular mechanisms and prime plant defences against herbivores?  Microbial “priming” prepares plant defences for future attacks by antagonists (such as insect herbivores) by increasing the plant defence response rate and frequently increasing defence compound concentrations (Selosse, Bessis & Pozo, 2014).  This question has been predominantly tested with organisms found in soil or plant organs (reviewed in Pineda, Dicke, Pieterse et al., 2013, Martinez-Medina, Flors, Heil et al., 2016), but has yet to be tested in enough systems to draw strong conclusions. 

Do all microbes (regardless of domain) prime plants or manipulating plant metabolism or morphology using the same compounds and pathways, and thus the variation we observe between systems is due to plant or insect species or genotypic variation?  We have begun to answer this question by identifying the pathways manipulated by individual microbial groups (Van Wees, Van der Ent & Pieterse, 2008, Jung, Martinez-Medina, Lopez-Raez et al., 2012, Pieterse, Zamioudis, Berendsen et al., 2014), and most microbes, but perhaps not all (Pineda et al., 2013), manipulate the jasmonic acid pathway (Pieterse et al., 2014).  However, comparison of priming between microbes from different domains (i.e. bacteria, archaea, eukarya) is currently hindered by the use of a small number of microbes (primarily arbuscular mycorrhizal fungi and plant growth-promoting rhizobacteria (Van Wees et al., 2008, Jung et al., 2012, Pieterse et al., 2014)), different host plants and the measurement of different compounds between studies.  Could convergence in the mechanisms used to manipulate plants within these interactions have derived from gene transfer among microbes?  Focusing on microbial partners and shifting our attention away from the plant and the herbivore should undoubtedly open our eyes to new ways of understanding and exploring these interactions. 

How do insects alter plant-microbe interactions?  How do plant symbionts alter insect-microbe interactions?  The former question has been addressed in only a few systems, particularly herbivore-pathogen interactions (Hauser, Christensen, Heimes et al., 2013) and herbivore-mycorrhizal fungal interactions (Gehring & Bennett, 2009), while the latter has only been addressed superficially within an aphid endosymbiont-arbuscular mycorrhizal fungal system (Bennett, Millar, Gedrovics et al., 2016, Karley, Emslie-Smith & Bennett, 2017).  This leaves open a number of supporting questions such as whether herbivores influence all beneficial microbes equally or whether plants can modify the influence of insects on microbes. 

The above questions are just a handful of those we could ask across systems that would allow us to draw conclusions about all plant-microbe-insect interactions instead of specific interactions.  Once broad conclusions across systems can be drawn we will be able to predict which interactions are likely to increase plant or insect protection, promote positive interactions, or suppress or promote invasive species.  This predictability is crucial to transfer knowledge gains on interactions used in innovative agricultural practices and efficient conservation strategies.

Given the potential importance of plant-microbe-insect interactions in conserving habitats and promoting sustainable agriculture, research also needs to address the influence of anthropogenic changes (climate, land-use, or management) on these interactions.  The vast majority of research in this area has focused on the influence of climate changes on beneficial fungal partners of plants (e.g. Kivlin, Emery & Rudgers, 2013) and insect endosymbionts (reviewed in Wernegreen, 2012), and these research areas are further bolstered by the papers in our Virtual Issue (Oliver et al., 2014, Ueno et al., 2016).  However, even with these contributions, this leaves open wide areas of inquiry that need to be addressed before we can begin to answer questions about whether changes in climate, land use or land management will alter the effective utilization of plant-microbe-insect interactions.

Thus, this Virtual Issue highlights exciting some of the new developments in plant-microbe-insect interactions while shedding light on the new directions of research needed to promote our understanding and utilization of these interactions.

Babikova, Z., Gilbert, L., Bruce, T., Dewhirst, S.Y., Pickett, J.A. & Johnson, D. (2014) Arbuscular mycorrhizal fungi and aphids interact by changing host plant quality and volatile emission. Functional Ecology 28, 375-385.

Barber, N.A. & Gorden, N.L.S. (2015) How do belowground organisms influence plant-pollinator interactions? Journal of Plant Ecology 8, 1-11.

Barber, N.A., Kiers, E.T., Hazzard, R.V. & Adler, L.S. (2013) Context-dependency of arbuscular mycorrhizal fungi on plant-insect interactions in an agroecosystem. Frontiers in Plant Science 4.

Bennett, A.E. (2013) Can plant–microbe–insect interactions enhance or inhibit the spread of invasive species? Functional Ecology 27, 661–671.

Bennett, A.E., Millar, N.S., Gedrovics, E. & Karley, A.J. (2016) Plant and insect microbial symbionts alter the outcome of plant-herbivore-parasitoid interactions: Implications for invaded, agricultural and natural systems. Journal of Ecology 104, 1734-1744.

Fuchs, B., Krischke, M., Mueller, M.J. & Krauss, J. (2017) Herbivore-specific induction of defence metabolites in a grass-endophyte association. Functional Ecology 31, 318-324.

Gehring, C. & Bennett, A. (2009) Mycorrhizal fungal–plant–insect interactions: The importance of a community approach. Environmental Entomology 38, 93-102.

Hauser, T.P., Christensen, S., Heimes, C. & Kiaer, L.P. (2013) Combined effects of arthropod herbivores and phytopathogens on plant performance. Functional Ecology 27, 623-632.

Jung, S.C., Martinez-Medina, A., Lopez-Raez, J.A. & Pozo, M.J. (2012) Mycorrhiza-induced resistance and priming of plant defenses. Journal of Chemical Ecology 38, 651-664.

Kaltenpoth, M. & Engl, T. (2014) Defensive microbial symbionts in Hymenoptera. Functional Ecology 28, 315-327.

Karley, A.J., Emslie-Smith, M. & Bennett, A.E. (2017) Fitness trade-off with parasitism susceptibility in the potato aphid (Macrosiphum euphorbiae Thomas): the role of plant and herbivore identity, soil microbes and water availability. Insect Science In Press.

Kivlin, S.N., Emery, S.M. & Rudgers, J.A. (2013) Fungal symbionts alter plant responses to global change. American Journal of Botany 100, 1445-1457.

Martinez-Medina, A., Flors, V., Heil, M., Mauch-Mani, B., Pieterse, C.M.J., Pozo, M.J., Ton, J., Van Dam, N.M. & Conrath, U. (2016) Recognizing plant defense priming. TRENDS in Plant Science 21, 818-822.

Mauck, K.E., Smyers, E., De Moraes, C.M. & Mescher, M.C. (2015) Virus infection influences host plant interactions with non-vector herbivores and predators. Functional Ecology 29, 662-673.

Oliver, K.M., Smith, A.H. & Russell, J.A. (2014) Defensive symbiosis in the real world -advancing ecological studies of heritable, protective bacteria in aphids and beyond. Functional Ecology 28, 341-355.

Orrell, P. & Bennett, A.E. (2013) How can we exploit above–belowground interactions to assist in addressing the challenges of food security? Frontiers in Plant Science 4, 1-11.

Panaccione, D.G., Beaulieu, W.T. & Cook, D. (2014) Bioactive alkaloids in vertically transmitted fungal endophytes. Functional Ecology 28, 299-314.

Penaflor, M., Mauck, K.E., Alves, K.J., De Moraes, C.M. & Mescher, M.C. (2016) Effects of single and mixed infections of Bean pod mottle virus and Soybean mosaic virus on host-plant chemistry and host-vector interactions. Functional Ecology 30, 1648-1659.

Pieterse, C.M.J., Zamioudis, C., Berendsen, R.L., Weller, D.M., Van Wees, S.C.M. & Bakker, P. (2014) Induced systemic resistance by beneficial microbes. Annual Review of Phytopathology, Vol 52 (ed N.K. Vanalfen), pp. 347-375. Annual Reviews, Palo Alto.

Pineda, A., Dicke, M., Pieterse, C.M.J. & Pozo, M.J. (2013) Beneficial microbes in a changing environment: are they always helping plants to deal with insects? Functional Ecology 27, 574-586.

Ponzio, C., Weldegergis, B.T., Dicke, M. & Gols, R. (2016) Compatible and incompatible pathogen-plant interactions differentially affect plant volatile emissions and the attraction of parasitoid wasps. Functional Ecology 30, 1779-1789.

Schaeffer, R.N., Mei, Y.Z., Andicoechea, J., Manson, J.S. & Irwin, R.E. (2017) Consequences of a nectar yeast for pollinator preference and performance. Functional Ecology 31, 613-621.

Selosse, M.A., Bessis, A. & Pozo, M.J. (2014) Microbial priming of plant and animal immunity: symbionts as developmental signals. Trends in Microbiology 22, 607-613.

Su, Q., Oliver, K.M., Xie, W., Wu, Q.J., Wang, S.L. & Zhang, Y.J. (2015) The whitefly-associated facultative symbiont Hamiltonella defensa suppresses induced plant defences in tomato. Functional Ecology 29, 1007-1018.

Ueno, A.C., Gundel, P.E., Omacini, M., Ghersa, C.M., Bush, L.P. & Martinez-Ghersa, M.A. (2016) Mutualism effectiveness of a fungal endophyte in an annual grass is impaired by ozone. Functional Ecology 30, 226-234.

Van Wees, S.C.M., Van Der Ent, S. & Pieterse, C.M.J. (2008) Plant immune responses triggered by beneficial microbes. Current Opinion in Plant Biology 11, 443-448.

Wagner, S.M., Martinez, A.J., Ruan, Y.M., Kim, K.L., Lenhart, P.A., Dehnel, A.C., Oliver, K.M. & White, J.A. (2015) Facultative endosymbionts mediate dietary breadth in a polyphagous herbivore. Functional Ecology 29, 1402-1410.

Wernegreen, J.J. (2012) Mutualism meltdown in insects: bacteria constrain thermal adaptation. Current Opinion in Microbiology 15, 255-262.

White, J.A., Mccord, J.S., Jackson, K.A., Dehnel, A.C. & Lenhart, P.A. (2017) Differential aphid toxicity to ladybeetles is not a function of host plant or facultative bacterial symbionts. Functional Ecology 31, 334-339.

Whitehead, S.R. & Bowers, M.D. (2014) Chemical ecology of fruit defence: synergistic and antagonistic interactions among amides from Piper. Functional Ecology 28, 1094-1106.

Wurst, S. & Ohgushi, T. (2015) Do plant- and soil-mediated legacy effects impact future biotic interactions? Functional Ecology 29, 1373-1382.