Kessler, Andre

Lucas-Barbosa, Dani

Muola, Anne

PubMed

Kessler, André

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Editorial: Mechanisms underlying plant-pollinator-herbivore interactions

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Frontiers in Plant ScienceOPEN ACCESSEDITED AND REVIEWED BYMani Shrestha,University of Bayreuth, Germany*CORRESPONDENCEAnne Muolaanne.muola@nibio.noSPECIALTY SECTIONThis article was submitted toFunctional Plant Ecology,a section of the journalFrontiers in Plant ScienceRECEIVED 31 August 2022ACCEPTED 12 September 2022PUBLISHED 21 September 2022CITATIONMuola A, Lucas-Barbosa D andKessler A (2022) Editorial:Mechanisms underlying plant-pollinator-herbivore interactions.Front. Plant Sci. 13:1033287.doi: 10.3389/fpls.2022.1033287COPYRIGHT© 2022 Muola, Lucas-Barbosa andKessler. This is an open-access articledistributed under the terms of theCreative Commons Attribution License(CC BY). The use, distribution orreproduction in other forums ispermitted, provided the originalauthor(s) and the copyright owner(s)are credited and that the originalpublication in this journal is cited, inaccordance with accepted academicpractice. No use, distribution orreproduction is permitted which doesnot comply with these terms.TYPE EditorialPUBLISHED 21 September 2022DOI 10.3389/fpls.2022.1033287Editorial: Mechanismsunderlying plant-pollinator-herbivore interactionsAnne Muola1*, Dani Lucas-Barbosa2 and André Kessler31Biotechnology and Plant Health Division, Norwegian Institute of Bioeconomy Research (NIBIO),Tromsø, Norway, 2Department of Crop Sciences , Research Institute of Organic Agriculture FiBL,Frick, Switzerland, 3Department of Ecology and Evolutionary Biology, Cornell University, Ithaca,NY, United StatesKEYWORDSplant defence, pollinator attraction, floral rewards, secondary metabolites,mutualism, antagonism, plant fitnessEditorial on the Research TopicMechanisms underlying plant-pollinator-herbivore interactionsThe success of a particular plant phenotype in any given environment depends onhow well the expression of traits allows plants to negotiate interactions with otherorganisms. Because plants cannot move away from unfavorable conditions, they expresstraits that attract mutualists and repel antagonists. These interaction-mediating traitshave been well studied for plant interactions with herbivores as antagonists andpollinators as mutualists, to an extent that they both became models forunderstanding biotic interactions in general. Recently, these two schools of thought,plant defense theory and pollinator attraction have started to merge as scientists becameaware that many of the plant traits that mediate the respective interaction, areoverlapping. So, both fields of research face the same fundamental question: How doplants attract mutualists and repel antagonists with the same suit of basic traits, muchrelying on secondary metabolites, and within the same information space?This conflict that plants face is most apparent when considering chemical traitsmediating biotic interactions. Plants can produce toxic, anti-digestive and anti-nutritivecompounds that directly protect them against herbivores and pathogens and/or that areinduced following the attack. Moreover, the herbivory-induced production of volatileorganic compounds can attract predators and parasitoids facilitating the top-downcontrol of pest organisms (indirect defenses). Thus, plant secondary metabolism allowsplants to limit the number of potential antagonistic interactors (constitutive defenses)and to involve the entire interaction community in a plant defense strategy (informationtransfer through induced responses; Kessler, 2015). This, however, includes theinteraction with mutualist pollinators as well.Although plant chemistry had been suggested to be important in pollinator attractionfor a long time, actual experimental proof was provided relatively recently (Raguso, 2008).Pollinator rewards (e.g. nectar, pollen, oils) includemany of the same defensive compoundsfrontiersin.org01Muola et al. 10.3389/fpls.2022.1033287as leaves do, consequentially exposing pollinators to those sametraits and suggesting pollinators as potential agents of naturalselection on plant defense traits (Adler, 2000). Themultifunctionality of secondary metabolites suggests diffusereciprocal natural selection on plant secondary metabolism bythe pollinator and herbivore communities associated with a plantas well as the interactor’s ability to cope with plant chemicaldefenses (Ramos and Schiestl, 2019). In addition, this means thatplant defense strategy and mating systems can be expected toimpact ecological interactions and evolutionary paths because ofmetabolic changes in response to interactions with herbivores orpollinators. Indeed, phylogenetic correlations between defensestrategies and mating systems have recently been revealed incomparative studies with Solanaceae (Adler et al., 2012;Campbell and Kessler, 2013). Moreover, plant phenotypicchanges induced by herbivory have been found to affectpollinator behavior, often with significant effects on plant fitness(Kessler et al., 2011; Muola et al., 2017). Despite these findings, themechanisms as well as the evolutionary consequences underlyingthe observed ecological consequences of a shared informationspace between plants, pollinators, and herbivores, remain poorlyunderstood (Lucas-Barbosa, 2016; Rusman et al., 2019).With this special issue we aim to feature impactfuldevelopments in the field to identify the paths forward.Challenges of attracting mutualists while repelling antagonistsare likely to be particularly strong with pollinating herbivores,such as many Lepidopteran species with herbivorous larvae andpollinating adults. Jacobsen and Raguso (2021) show thatdefensive leaf volatiles play a role in host plant selection of thepollinating herbivoreManduca sexta and demonstrate that adultsassess information from leaves differently when choosing betweenforaging and oviposition locations. This raises the interestingquestion if such ontogenetically differential use of chemicalinformation is common or a specific feature of herbivores thatalso function as major pollinators on their host plants and whatdrives the evolution of such differential behavior.Davidowitz et al. (2022) offer a special perspective andpartial answer to the latter question. They also focused onpollinating herbivores to explore the hypothesis that increasedallocation of resources to flight could lead to higher pollinationefficiency of Lepidopteran pollinators, and thus, higher plantfitness. Reciprocally, this also means that if the same insectincreases resource allocation to reproduction instead of flight,herbivore population size is likely to increase with potentiallynegative consequences for plant fitness. Davidowitz et al.propose such resource allocation trade-offs between flight andfecundity in insects as potential drivers of differential selectionon plant defenses and pollinator, herbivore counter defenses, aswell as plant reproductive traits. For example, Villamill et al.(2022) show how herbivory can affect plant sexual expression byteasing apart the effects of herbivory-caused resource limitationand plant responses to herbivory-induced jasmonate signalingon wind-pollinated Mercurialis annua. They found that theFrontiers in Plant Science 02jasmonate-mediated induction reverses the effect of tissue losson male reproductive investment indicating that plant defenceexpression can have consequences for sex allocation andeventually for the evolution of plant sexual systems.Plant-visiting ants are often functional herbivores orpredators, only rarely pollinators. However, Aranda-Rickertet al. (2021) provide the first evidence of distance-dependentcontribution of ants to pollination, but with no effect on plantdefence. They show how ants can offset pollen limitation inisolated females of wind-pollinated Ephedra triandra bycontributing to targeted delivery of airborne pollen while theyconsume the sugary pollination drops. Whether other dioeciousplants lacking male reward for pollinators share similarmechanisms of ambophily remains to be studied. Pollinatorsand herbivores can exert selection on plant reproductive anddefensive traits suggesting conflicting selection pressures. Here,Wu et al. (2021) demonstrate that herbivore-mediated selectioncan generate selective pressures for greater flower production oninsect-pollinated plants. Their study indicates that the variationin the intensity of plant-antagonistic interactions can drivespatial variation in natural selection on floral traits.Despite recent advances, the evolutionary consequences ofthe complex ecological interactions remain poorly understood.The Review by De-la-Cruz et al. (2022) explains how thetraditional experimental and modern methods including next-generation sequencing, metabolomics, and gene-editingtechnologies can enhance our understanding of the genes andtraits involved in mediating complex plant-pollinator-herbivore interactions.We hope that you enjoy this Research Topic and that it givesinspiration for more research uniting the traditionally separatelystudied fields of plant-pollinator and plant-herbivore interactions.Author contributionsAll authors listed have made substantial intellectualcontributions to the work and approved it for publication.Conflict of interestThe authors declare that the research was conducted in theabsence of any commercial or financial relationships that couldbe construed as a potential conflict of interest.Publisher’s noteAll claims expressed in this article are solely those of theauthors and do not necessarily represent those of their affiliatedorganizations, or those of the publisher, the editors and thereviewers. Any product that may be evaluated in this article, orclaim that may be made by its manufacturer, is not guaranteedor endorsed by the publisher.frontiersin.orgMuola et al. 10.3389/fpls.2022.1033287ReferencesAdler, L. S. (2000). The ecological significance of toxic nectar.Oikos 90, 409–420.doi: 10.1034/j.1600-0706.2000.910301.xAdler, L. S., Seifert, M. G., Wink, M., and Morse, G. E. (2012). Reliance onpollinators predicts defensive chemistry across tobacco species. Ecol. Lett. 15, 1140–1148. doi: 10.1111/j.1461-0248.2012.01838.xCampbell, S. A., and Kessler, A. (2013). Plant mating system transitions drive themacroevolution of defense strategies. Proc. Natl. Acad. Sci. U. S. A 110, 3973–3978.doi: 10.1073/pnas.1213867110Kessler, A. (2015). The information landscape of plant constitutive and inducedsecondary metabolite production. Curr. Opin. Insect Sci. 8, 47–53. doi: 10.1016/j.cois.2015.02.002Frontiers in Plant Science 03Kessler, A., Halitschke, R., and Poveda, K. (2011). Herbivory-mediatedpollinator limitation: Negative impacts of induced volatiles on plant–pollinatorinteractions. Ecology 92, 1769–1780. doi: 10.1890/10-1945.1Lucas-Barbosa, D. (2016). Integrating studies on plant–pollinator and plant–herbivore interactions. Trends Plant Sci. 21, 125–133. doi: 10.1016/j.tplants.2015.10.013Raguso, R. A. (2008). Wake up and smell the roses: The ecology and evolution offloral scent. Annu. Rev. Ecology Evolution Systematics 39, 549–569. doi: 10.1146/annurev.ecolsys.38.091206.095601Ramos, S. E., and Schiestl, F. P. (2019). Rapid plant evolution driven by the interactionof pollination and herbivory. Science 364, 193–196. doi: 10.1126/science.aav6962Rusman, Q., Lucas-Barbosa, D., Poelman, E. H., and Dicke, M. (2019). Ecology ofplastic flowers. Trends Plant Sci. 24, 725–740. doi: 10.1016/j.tplants.2019.04.007frontiersin.org

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Editorial: Mechanisms underlying plant-pollinator-herbivore interactions

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