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Plant phenotypic plasticity in the phytobiome: a volatile issue
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ScienceDirect Plant phenotypic plasticity in the phytobiome: a volatile issue Marcel Dicke Plants live in a diverse and dynamic phytobiome, consisting of a microbiome as well as a macrobiome. They respond to arthropod herbivory with the emission of herbivore-induced plant volatiles (HIPV) that are public information and can be used by any member of the phytobiome. Other members of the phytobiome, which do not directly participate in the interaction, may both modulate the induction of HIPV in the plant, as well as respond to the volatiles. The use of HIPV by individual phytobiome members may have beneficial as well as detrimental consequences for the plant. The collective result of phytobiome-modulated HIPV emission on the responses of phytobiome members and the resulting phytobiome dynamics will determine whether and under which circumstances HIPV emission has a net benefit to the plant or not. Only when we understand HIPV emission in the total phytobiome context can we understand the evolutionary consequences of HIPV emission by plants. Address Laboratory of Entomology, Wageningen University, Droevendaalsesteeg 1, 6708PB Wageningen, The Netherlands Corresponding author: Dicke, Marcel ([email protected])
Current Opinion in Plant Biology 2016, 32:17–23 This review comes from a themed issue on Biotic interactions Edited by Consuelo De Moraes and Mark Mescher
http://dx.doi.org/10.1016/j.pbi.2016.05.004 1369-5266/# 2016 Published by Elsevier Ltd.
Introduction Plants are members of complex communities that consist of beneficial and detrimental organisms, ranging from unicellular microbes to multicellular vertebrates, that is, the microbiome and the macrobiome [1,2]. Thus, plants are surrounded by a phytobiome [3] that consists of organisms spanning several orders of magnitude in size [2]. In the midst of this dynamic environment, plants stay put. Those that develop, survive and reproduce best, pass on their genes most abundantly to a new generation of plant individuals and are, therefore, most successful in terms of Darwinian fitness. To achieve this, plants need to minimize interactions with detrimental organisms such as pathogens, herbivores and competitors and maximize www.sciencedirect.com
interactions with beneficial organisms such as mycorrhiza, plant growth promoting rhizobacteria, carnivorous enemies of herbivores, and pollinators. Given that environmental conditions are spatially and temporally dynamic, plants benefit from being able to adjust their phenotype to meet with the variable local conditions. Here, I review how plants deal with interactions with different members of the phytobiome and how — at the same time — the phytobiome context modulates these interactions. I focus on the emission of herbivore-induced plant volatiles (HIPV) in response to arthropod herbivory and the consequences of emitting this public information within a phytobiome context. Especially, I will address how phytobiome members on the one hand modulate the emission of HIPV and on the other hand respond to the HIPV emitted. Finally, I will address the consequences of this induced phenotypic response within the phytobiome context, in terms of the emitter’s fitness.
Perception and recognition of attackers To maximize interactions with beneficial organisms and minimize interactions with detrimental organisms, plants need to be able to recognize and differentiate between community members and adjust their phenotype accordingly. The perception and recognition of herbivores and pathogens is based to a large extent — but not exclusively [4,5] — on chemical recognition. This involves herbivore-associated molecular patterns (HAMPs), damageassociated molecular patterns (DAMPs) and pathogenassociated molecular patterns (PAMPs). HAMPs and PAMPs involve a diversity of compounds. For instance, herbivorous insects produce oral secretions that contain, for example, fatty acid–amino acid conjugates (FACs), sulfur-containing fatty acids (caeliferins), and/or enzymes (b-glucosidases) [6,7]. Moreover, benzyl cyanide, bruchins, phospholipids or small proteins are associated with egg deposition by herbivores [8]. PAMPs include, for example, flagellin, chitin, glycoproteins, and lipopolysaccharides [9]. DAMPs include cell-wall fragments (e.g. oligogalacturonides) and endogenous plant-derived signals that arise from damage caused by pathogen infection or herbivore attack [6,9]. These molecular patterns can be exploited by plants to identify the nature of the organisms that initiate an interaction with them [10]. For instance, plant roots that are exposed to soil-born microbes may use variation in the bacterial elicitor flagellin to discriminate between pathogenic bacteria and mutualistic rhizosphere bacteria. In contrast to the effect of the elicitor flg22, a conserved peptide motif in the flagellar protein of many bacteria, flagellin from the Current Opinion in Plant Biology 2016, 32:17–23
18 Biotic interactions
mutualistic bacterium Mesorhizobium loti did not induce defence responses in Lotus japonicus plants [11]. This indicates that L. japonicus plants can discriminate between pathogenic and symbiotic bacteria. Plants can initiate differential responses to different attackers. For instance, egg deposition by the specialist butterfly Pieris brassicae, whose larvae are voracious herbivores of glucosinolate-containing plants, results in enhanced resistance to conspecific and heterospecific caterpillars in black mustard plants (Brassica nigra). In contrast, egg deposition by the generalist moth Mamestra brassicae, whose larvae upon emergence are likely to move soon to non-brassicaceous neighbouring plants, do not result in such changes in resistance in black mustard plants [12]. Different attackers often elicit different transcriptomic responses [13] and different changes in the phenotype [2,9,14]. Some attackers, although inflicting feeding damage to the plant, may still have an overall benefit to the plant. For instance, attack of coyote tobacco plants (Nicotiana attenuata) by the mirid herbivore Tupiocoris notatus results in the production of secondary metabolites and proteinase inhibitors that reduce feeding by voracious Manduca hornworm caterpillars and results in the attraction of a generalist predatory bug that prefers to feed on the hornworm caterpillars [15]. The direct effects of the mirids on plant fitness are only minor, but their indirect effects can be major [15]. Thus, plants can recognize different members of the phytobiome and respond differentially with changes in their phenotype. This phenotypic plasticity may allow them to maximize interactions with beneficial organisms while minimizing interactions with antagonists. Transcriptomic studies show that major transcriptomic rearrangements may underlie this phenotypic plasticity. For instance, herbivory by Pieris rapae caterpillars leads to differential expression of ca 4000 genes in Arabidopsis plants, infection with the necrotrophic pathogen Botrytis cinerea ca 2100 genes and drought stress ca 4000 genes [16,17]. This indicates that a plant’s physiology is dramatically reprogrammed, related to various physiological processes. This has extensive consequences for the plant’s phenotype in terms of, for example, plant chemistry, morphology, and growth [14,18].
Herbivory-induced plant volatiles Although plants may initiate direct defences against herbivores [14], these attackers may evolve counter-adaptations [19] and, thus, break through plant defences [20– 22]. This may be accomplished by, for example, detoxification of secondary metabolites [20] or by suppressing the induction of direct defences [21,22]. In addition to direct defences, plants can also initiate indirect defences, mediated by, among others, the induced emission of volatiles that attract carnivorous enemies of the herbivores [23]. This phenotypic change disseminates in the community Current Opinion in Plant Biology 2016, 32:17–23
and can influence various organisms. Arthropod herbivory or oviposition result in the emission of a diverse blend of volatiles [8,24], originating from various biosynthetic pathways [25]. These include especially green-leaf volatiles derived from the lipoxygenase biosynthetic pathway, terpenoids, aromatic compounds, nitrogen-containing and sulphur-containing compounds [25,26]. The effects of the emitted blend of volatiles have been extensively investigated for the attraction of carnivorous enemies of the inducing arthropods [24].
Modulation of herbivory-induced plant volatiles by associated organisms The induction of plant volatiles by interactions with herbivores has especially been investigated for individual plant–herbivore interactions. However, neither the plant [1] nor the herbivore [27] are individual entities. Each harbours a diverse community consisting of microbes and sometimes also multicellular organisms such as endophytic insects in plants or juvenile stages of parasitic wasps in herbivores [28]. These associated organisms may modulate the response of the plant to herbivory (Figure 1). Modulation by plant-associated microorganisms
For instance, colonisation of the roots of Phaseolus vulgaris plants with the mycorrhizal fungus Glomus mosseae modifies the volatile blend induced by herbivory by the twospotted spider mite Tetranychus urticae which resulted in an enhanced attraction of a carnivorous enemy of the spider mites, the predatory mite Phytoseiulus persimilis [29]. Colonisation of the roots of Arabidopsis by the plant-growth promoting rhizobacterium (PGPR) Pseudomonas simiae (formerly P. fluorescens) modifies the volatile blends induced by aphid herbivory [30], resulting in a decreased attraction of aphid parasitoids. In contrast, the rhizobacteria modify the caterpillar-induced blend of plant volatiles such that the attraction of parasitoids that attack the caterpillars is enhanced [31]. Colonisation of roots of Lima bean plants (Phaseolus lunatus) by Rhizobia modulates the blend of jasmonic-acid inducible plant volatiles resulting in a decreased attraction of the herbivorous Mexican bean beetle [32]. It remains to be investigated whether the modulation of HIPV emission is a result of an altered nutritional state of the plant when colonised by mycorrhiza, rhizobia or PGPR or due to physiological changes associated with the interaction with the microbes, or a combination of the two. Plants also harbour various endophytic fungi that can provide protection to their host plant in various ways [33], including the emission of constitutive volatiles by roots of endophyte-infected grass plants [34]. To my knowledge no information is available on the modulation of HIPV by endophytes. Yet, fungal endophytes can modulate jasmonic-acid induced plant volatiles [35] and can influence the interaction web of aphids and their parasitoids on the plant [36]. www.sciencedirect.com
Herbivore-induced plant volatiles in the phytobiome Dicke 19
Figure 1
herbivore-induced plant volatile emission
modulated herbivore-induced plant volatile emission
herbivore-associated organisms
second herbivore
plant-associated microorganisms
neighbouring plants
phytobiome
phytobiome
microbiome & macrobiome
microbiome & macrobiome
plant fitness
plant fitness Current Opinion in Plant Biology
Herbivore feeding induces the emission of herbivore-induced plant volatiles (HIPV) by plants and these volatiles affect the behaviour of members of the phytobiome with consequences for plant fitness. Moreover, the interaction of members of the phytobiome with the plant can also modulate the emission of HIPV and consequently affect phytobiome composition and dynamics.
Modulation by a second herbivore species attacking the same plant
When plants induce HIPV they may be under attack of other organisms as well. When two or more organisms attack a plant, the total effect is rarely the sum of the individual effects of each attacker. Herbivores may attenuate or enhance the effects of other herbivores and thus modulate the effects of the HIPV on members of the phytobiome [23,37]. For instance, the infestation of bean plants with a second herbivore attenuates the attraction of an egg parasitoid to volatiles emitted by plants infested with stinkbug eggs [38]. In contrast, pathogen attack of plants infested with caterpillars may enhance the attraction of parasitoids that attack the caterpillars [39]. Thus, a second herbivore modulates the plant’s response with www.sciencedirect.com
consequences for interactions with members of the phytobiome. Modulation by neighbouring plants
Undamaged neighbouring plants may affect the emission of HIPV. Trifolium pratense plants emitted lower numbers and amounts of HIPV when exposed to an undamaged neighbouring conspecific plant. This effect was independent of whether there was contact aboveground, belowground or above-ground and belowground [40]. Shading by neighbouring plants reduces the red (R) to far-red (FR) ratio (R:FR) of sunlight that a plant is exposed to. This leads to enhanced plant growth [41] and interference with JA-mediated and SA-mediated direct defences [42,43]. The exposure to lower R:FR ratios as a result of shading Current Opinion in Plant Biology 2016, 32:17–23
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by neighbours also interferes with the induction of JAinducible volatiles in Arabidopsis thaliana and affects the behaviour of herbivorous caterpillars that forage for a host plant [44]. It will be interesting to extend this to effects on other members of the phytobiome. Plants are also known to respond to volatiles from neighbouring herbivoreinfested plants, for example, with the priming of direct and indirect defences [45]. Subsequent infestation of the primed plant then results in an enhanced emission of HIPV and attraction of carnivorous arthropods [46]. Finally, neighbouring plants may interfere with the behavioural responses of arthropods to HIPV [47,48], although also examples exist where such interference does not occur [49].
responses that may benefit the plant, for example, repellence of herbivores as well as attraction of predators of herbivores, as well as responses that may harm the plant such as the attraction of herbivores or the attraction of hyperparasitoids. Moreover, the plant-associated community may also have plant-mediated feedback mechanisms, where the composition of the community influences plant phenotype and phenology with consequences for trait evolution of individual herbivore species in terms of, for example, feeding preference [68]. Finally, HIPV can be toxic to members of the phytobiome such as microbes and herbivorous insects [69,70]. Thus, the emission of HIPV has a complex effect on the phytobiome with a suite of positive and negative consequences for the plant.
Modulation by herbivore-associated organisms
Fitness consequences
HIPV emission may also be influenced by organisms living within the inducing herbivore, such as larvae of parasitic wasps that feed within the herbivore that induces the volatiles [50,51,52]. The parasitoid larvae feed on the haemolymph and tissues of the herbivore and may modulate the composition of the herbivore’s oral secretion. This alters the induction of HIPV with consequences for the behaviour of herbivores, parasitoids and hyperparasitoids that attack the parasitoids in the herbivore [28,50,51,52]. It is intriguing to see that these effects are specific for the parasitoid species that develops in the herbivore [53]. Also other herbivore-associated organisms such as microbes in the oral secretion of the Colorado potato beetle may modulate herbivore-induced plant defences, which involves attenuation of jasmonicacid mediated induced responses [54]. This suggests that also jasmonic-acid-mediated indirect defences through HIPV may be modulated by such microbes, but this remains to be investigated.
The fitness consequences of HIPV emission have long been debated [18,71–73] because they are not so easily assessed. After all, the emission of HIPV influences various community members and affects community dynamics. Thus, fitness consequences can only be assessed under realistic field conditions where plants are exposed to the full, variable, phytobiome. Several studies have shown that parasitization of herbivores can benefit the plant in term of seed production [74–76] under more or less protected conditions. Moreover, phenotypic changes in response to eggs that result in enhanced parasitoid attraction and reduced herbivore performance resulted in an overcompensation by the plant, resulting in enhanced seed set under field conditions [77]. A dedicated study on the exclusive role of HIPV shows that induced emission of HIPV indeed is associated with fitness benefits. Green-leaf-volatile-silenced N. attenuata plants placed in their natural environment produced twice as many buds in the presence of predatory bugs as control plants, whereas plants silenced for the induced production of anti-digestive proteins had similar bud production as nonsilenced plants [78]. How modulation of HIPV emission by various members of the phytobiome influence the phytobiome-mediated effects of HIPV on plant fitness will be an exciting topic for future studies. This can only be investigated within the complex and dynamic phytobiome context.
Effects of HIPV on the associated animal community Originally, the effects of HIPV were investigated for their effects on carnivorous enemies of the inducing herbivore. These were attracted to the herbivore-infested plants and attacked the herbivore. Thus, the emission of HIPV was coined ‘crying for help’ [55]. So, initially the effects of HIPV were investigated for simple tritrophic food chains consisting of a plant, an herbivore and a carnivore. However, HIPV are public information that can be used by any member of the community. Indeed, there now is evidence for responses by, for example, herbivores [53,56– 58], carnivorous arthropods such as predators and parasitoids [24,59], carnivorous birds [60], entomopathogenic nematodes, [61], hyperparasitoids [51,52], pollinators [62,63], and neighbouring plants [45,64]. Each of these community members responds in its own way, for example, being attracted or repelled, with different temporal and spatial aspects. As a consequence, the change in plant phenotype results in a drastic and dynamic rearrangement of the associated phytobiome [65–67]. This includes Current Opinion in Plant Biology 2016, 32:17–23
Future directions The fact that plants can discriminate between attackers and mutualists, respond to neighbouring competitors or to neighbours that are under actual attack raises the question where the limits are of the perception of their environment by plants. Can they perceive the presence of carnivorous enemies of herbivorous attackers, for example by responding to ant trail pheromones [79], just as they can respond to herbivore pheromones [80] or to the presence of cues from parasitic plants or from flowering plants that can serve as both a source of pollen and receiver of pollen [81]? This is an intriguing question for future research. Subsequently, knowledge of the www.sciencedirect.com
Herbivore-induced plant volatiles in the phytobiome Dicke 21
degree to which plants are informed about the phytobiome composition will elicit questions on how plants deal with information on conflicting situations such as the presence of attackers as well as their natural enemies or competitors. Does this modulate their phenotypically plastic change in HIPV emission? The better plants are informed about their environment, the more relevant are questions on how plant deal with dilemma’s such as to grow or to defend, to invest in immediate reproduction or to delay reproduction, and whether to emit HIPV and stand out or to limit HIPV emission and be less apparent to the members of the phytobiome. So far, research on HIPV has considered the emission of these chemicals a deterministic change in plant phenotype. In the light of the modulations of HIPV emission by phytobiome members, questions on how plants strategically use HIPV within the dynamically changing environmental conditions only gets more exciting dimensions for future research in this field. Future issues to be addressed include the modulation by multiple phytobiome members. For instance, the belowground microbiome is a speciose community [1] with various interactions. How the dynamics of this community influence the plant will be a major but important challenge. Moreover, also the macrobiome is a diverse community [2] and identifying those species that are most important in structuring the community as well as its interactions with plants is an important undertaking for the years to come [82]. Given that carnivores in natural as well as agricultural systems exploit HIPV [18], these issues are not only interesting from a fundamental point of view, but they will also allow to enhance the effectiveness of carnivorous arthropods in environmentally benign pest control strategies.
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42. de Wit M, Spoel SH, Sanchez-Perez GF, Gommers CMM, Pieterse CMJ, Voesenek L, Pierik R: Perception of low red:farred ratio compromises both salicylic acid- and jasmonic aciddependent pathogen defences in Arabidopsis. Plant J 2013, 75:90-103. Experimental study of the effect of reduced R:FR ratio, an early signal of competition, which inhibits SA-dependent and JA-dependent disease resistance responses in Arabidopsis plants. 43. Cerrudo I, Keller MM, Cargnel MD, Demkura PV, de Wit M, Patitucci MS, Pierik R, Pieterse CMJ, Ballare CL: Low red/far-red ratios reduce Arabidopsis resistance to Botrytis cinerea and jasmonate responses via a COI1-JAZ10-dependent, salicylic acid-independent mechanism. Plant Physiol 2012, 158:20422052. 44. Kegge W, Weldegergis BT, Soler R, Vergeer-Van Eijk M, Dicke M, Voesenek L, Pierik R: Canopy light cues affect emission of constitutive and methyl jasmonate-induced volatile organic compounds in Arabidopsis thaliana. New Phytol 2013, 200:861874. 45. Kessler A, Halitschke R, Diezel C, Baldwin IT: Priming of plant defense responses in nature by airborne signaling between Artemisia tridentata and Nicotiana attenuata. Oecologia 2006, 148:280-292. 46. Erb M, Veyrat N, Robert CAM, Xu H, Frey M, Ton J, Turlings TCJ: Indole is an essential herbivore-induced volatile priming signal in maize. Nat Commun 2015, 6:6273. This chemical ecological study employs chemical and genetic tools to show that indole primes plants for HIPV induction, mediated by the phytohormones jasmonate iso-leucine and abscisic acid. 47. Gols R, Bukovinszky T, Hemerik L, Harvey JA, Van Lenteren JC, Vet LEM: Reduced foraging efficiency of a parasitoid under habitat complexity: implications for population stability and species coexistence. J Anim Ecol 2005, 74:1059-1068. 48. Randlkofer B, Obermaier E, Hilker M, Meiners T: Vegetation complexity — the influence of plant species diversity and plant structures on plant chemical complexity and arthropods. Basic Appl Ecol 2010, 11:383-395. 49. Waschke N, Hardge K, Hancock C, Hilker M, Obermaier E, Meiners T: Habitats as complex odour environments: how does plant diversity affect herbivore and parasitoid orientation? PLoS One 2014, 9:e85152. 50. Fatouros NE, Van Loon JJA, Hordijk KA, Smid HM, Dicke M: Herbivore-induced plant volatiles mediate in-flight host discrimination by parasitoids. J Chem Ecol 2005, 31:2033-2047. 51. Poelman EH, Bruinsma M, Zhu F, Weldegergis BT, Boursault AE, Jongema Y, van Loon JJA, Vet LEM, Harvey JA, Dicke M: Hyperparasitoids use herbivore-induced plant volatiles to locate their parasitoid host. PLoS Biol 2012, 10:e1001435. Laboratory and field study demonstrating that parasitoid larvae feeding within herbivores modulate HIPV, resulting in the attraction of hyperparasitoid enemies of the parasitoids. 52. Zhu F, Broekgaarden C, Weldegergis BT, Harvey JA, Vosman B, Dicke M, Poelman EH: Parasitism overrides herbivore identity allowing hyperparasitoids to locate their parasitoid host using herbivore-induced plant volatiles. Mol Ecol 2015, 24:2886-2899. 53. Poelman EH, Zheng SJ, Zhang Z, Heemskerk NM, Cortesero AM, Dicke M: Parasitoid-specific induction of plant responses to parasitized herbivores affects colonization by subsequent herbivores. Proc Natl Acad Sci U S A 2011, 108:19647-19652. 54. Chung SH, Rosa C, Scully ED, Peiffer M, Tooker JF, Hoover K, Luthe DS, Felton GW: Herbivore exploits orally secreted bacteria to suppress plant defenses. Proc Natl Acad Sci U S A 2013, 110:15728-15733. 55. Dicke M, Sabelis MW, Takabayashi J: Do plants cry for help? Evidence related to a tritrophic system of predatory mites, spider mites and their host plants. Symp Biol Hung 1990, 39:127-134. 56. Zakir A, Bengtsson M, Sadek MM, Hansson BS, Witzgall P, Anderson P: Specific response to herbivore-induced de novo synthesized plant volatiles provides reliable information for host plant selection in a moth. J Exp Biol 2013, 216:3257-3263. www.sciencedirect.com
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57. Bruce TJA, Pickett JA: Perception of plant volatile blends by herbivorous insects: — finding the right mix. Phytochemistry 2011, 72:1605-1611. 58. De Moraes CM, Mescher MC, Tumlinson JH: Caterpillar-induced nocturnal plant volatiles repel nonspecific females. Nature 2001, 410:577-580. 59. D’Alessandro M, Turlings TCJ: Advances and challenges in the identification of volatiles that mediate interactions among plants and arthropods. Analyst 2006, 131:24-32. 60. Amo L, Jansen JJ, van Dam NM, Dicke M, Visser ME: Birds exploit herbivore-induced plant volatiles to locate herbivorous prey. Ecol Lett 2013, 16:1348-1355. 61. Turlings TCJ, Hiltpold I, Rasmann S: The importance of rootproduced volatiles as foraging cues for entomopathogenic nematodes. Plant Soil 2012, 358:47-56. 62. Schiestl FP, Kirk H, Bigler L, Cozzolino S, Desurmont GA: Herbivory and floral signaling: phenotypic plasticity and tradeoffs between reproduction and indirect defense. New Phytol 2014, 203:257-266. This study on Brassica rapa plants elucidates a tradeoff between pollinator attraction and parasitoid attraction, which can be alleviated by reduced floral VOC emission and production of more early flowers. 63. Lucas-Barbosa D: Integrating studies on plant–pollinator and plant–herbivore interactions. Trends Plant Sci 2016, 21:125-133. 64. Paschold A, Halitschke R, Baldwin IT: Using ‘mute’ plants to translate volatile signals. Plant J 2006, 45:275-291. 65. Thaler JS: Effect of jasmonate-induced plant responses on the natural enemies of herbivores. J Anim Ecol 2002, 71:141-150. 66. Poelman EH, van Loon JJA, Dicke M: Consequences of variation in plant defense for biodiversity at higher trophic levels. Trends Plant Sci 2008, 13:534-541. 67. Van Zandt PA, Agrawal AA: Community-wide impacts of herbivore-induced plant responses in milkweed (Asclepias syriaca). Ecology 2004, 85:2616-2629. 68. Utsumi S, Ando Y, Roininen H, Takahashi J, Ohgushi T: Herbivore community promotes trait evolution in a leaf beetle via induced plant response. Ecol Lett 2013, 16:362-370. 69. Veyrat N, Robert CAM, Turlings TCJ, Erb M: Herbivore intoxication as a potential primary function of an inducible volatile plant signal. J Ecol 2016, 104:591-600. 70. Gershenzon J, Dudareva N: The function of terpene natural products in the natural world. Nat Chem Biol 2007, 3:408-414. 71. Van der Meijden E, Klinkhamer PGL: Conflicting interests of plants and the natural enemies of herbivores. Oikos 2000, 89:202-208. 72. Hare JD: Ecological role of volatiles produced by plants in response to damage by herbivorous insects. Ann Rev Entomol 2011, 56:161-180.
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73. Poelman EH: From induced resistance to defence in plant– insect interactions. Entomol Exp Appl 2015, 157:11-17. 74. Van Loon JJA, De Boer JG, Dicke M: Parasitoid–plant mutualism: parasitoid attack of herbivore increases plant reproduction. Entomol Exp Appl 2000, 97:219-227. 75. Fritzsche-Hoballah ME, Turlings TCJ: Experimental evidence that plants under caterpillar attack may benefit from attracting parasitoids. Evolut Ecol Res 2001, 3:553-565. 76. Gols R, Wagenaar R, Poelman EH, Kruidhof HM, van Loon JJA, Harvey JA: Fitness consequences of indirect plant defence in the annual weed, Sinapis arvensis. Funct Ecol 2015, 29:10191025. 77. Pashalidou FG, Frago E, Griese E, Poelman EH, van Loon JJA, Dicke M, Fatouros NE: Early herbivore alert matters: plantmediated effects of egg deposition on higher trophic levels benefit plant fitness. Ecol Lett 2015, 18:927-936. Field study demonstrating that egg deposition by butterflies modulates plant phenotype with negative effects on the performance of the emerging caterpillars as well as their parasitoids and hyperparasitoids, and positive effects on the rates of parasitism by primary parasitoids and hyperparasitoids. The overall effect on plant fitness is positive. 78. Schuman MC, Barthel, Baldwin IT: Herbivory-induced volatiles function as defenses increasing fitness of the native plant Nicotiana attenuata in nature. eLife 2012, 1:e00007. Dedicated field study demonstrating that induced emission of HIPV indeed is associated with fitness benefits. Green-leaf-volatilesilenced N. attenuata plants placed in their natural environment produced twice as many buds in the presence of predatory bugs as control plants, whereas plants silenced for the induced production of anti-digestive proteins had similar bud production as non-silenced plants. 79. Czaczkes TJ, Gruter C, Ratnieks FLW: Trail pheromones: an integrative view of their role in social insect colony organization. Ann Rev Entomol 2015, 60:581-599. 80. Helms AM, De Moraes CM, Tooker JF, Mescher MC: Exposure of Solidago altissima plants to volatile emissions of an insect antagonist (Eurosta solidaginis) deters subsequent herbivory. Proc Natl Acad Sci U S A 2013, 110:199-204. Experimental study showing that goldenrod plants exposed to volatiles from males of a specialist herbivorous fly express enhanced defence responses and reduced susceptibility to several herbivores. 81. Caruso CM, Parachnowitsch AL: Do plants eavesdrop on floral scent signals? Trends Plant Sci 2016, 21:9-15. This opinion paper makes the interesting case that plants may eavesdrop on floral scent signals from other plants in the environment that will provide pollen to fertilize their own flowers or serve as recipients of their own pollen. Exploiting floral scent cues is hypothesized to facilitate plant reproductive decisions and thus mating strategies. 82. Poelman EH, Kessler A: Keystone herbivores and the evolution of plant defenses. Trends Plant Sci 2016, 21:477-485.
Current Opinion in Plant Biology 2016, 32:17–23
ScienceDirect Plant phenotypic plasticity in the phytobiome: a volatile issue Marcel Dicke Plants live in a diverse and dynamic phytobiome, consisting of a microbiome as well as a macrobiome. They respond to arthropod herbivory with the emission of herbivore-induced plant volatiles (HIPV) that are public information and can be used by any member of the phytobiome. Other members of the phytobiome, which do not directly participate in the interaction, may both modulate the induction of HIPV in the plant, as well as respond to the volatiles. The use of HIPV by individual phytobiome members may have beneficial as well as detrimental consequences for the plant. The collective result of phytobiome-modulated HIPV emission on the responses of phytobiome members and the resulting phytobiome dynamics will determine whether and under which circumstances HIPV emission has a net benefit to the plant or not. Only when we understand HIPV emission in the total phytobiome context can we understand the evolutionary consequences of HIPV emission by plants. Address Laboratory of Entomology, Wageningen University, Droevendaalsesteeg 1, 6708PB Wageningen, The Netherlands Corresponding author: Dicke, Marcel ([email protected])
Current Opinion in Plant Biology 2016, 32:17–23 This review comes from a themed issue on Biotic interactions Edited by Consuelo De Moraes and Mark Mescher
http://dx.doi.org/10.1016/j.pbi.2016.05.004 1369-5266/# 2016 Published by Elsevier Ltd.
Introduction Plants are members of complex communities that consist of beneficial and detrimental organisms, ranging from unicellular microbes to multicellular vertebrates, that is, the microbiome and the macrobiome [1,2]. Thus, plants are surrounded by a phytobiome [3] that consists of organisms spanning several orders of magnitude in size [2]. In the midst of this dynamic environment, plants stay put. Those that develop, survive and reproduce best, pass on their genes most abundantly to a new generation of plant individuals and are, therefore, most successful in terms of Darwinian fitness. To achieve this, plants need to minimize interactions with detrimental organisms such as pathogens, herbivores and competitors and maximize www.sciencedirect.com
interactions with beneficial organisms such as mycorrhiza, plant growth promoting rhizobacteria, carnivorous enemies of herbivores, and pollinators. Given that environmental conditions are spatially and temporally dynamic, plants benefit from being able to adjust their phenotype to meet with the variable local conditions. Here, I review how plants deal with interactions with different members of the phytobiome and how — at the same time — the phytobiome context modulates these interactions. I focus on the emission of herbivore-induced plant volatiles (HIPV) in response to arthropod herbivory and the consequences of emitting this public information within a phytobiome context. Especially, I will address how phytobiome members on the one hand modulate the emission of HIPV and on the other hand respond to the HIPV emitted. Finally, I will address the consequences of this induced phenotypic response within the phytobiome context, in terms of the emitter’s fitness.
Perception and recognition of attackers To maximize interactions with beneficial organisms and minimize interactions with detrimental organisms, plants need to be able to recognize and differentiate between community members and adjust their phenotype accordingly. The perception and recognition of herbivores and pathogens is based to a large extent — but not exclusively [4,5] — on chemical recognition. This involves herbivore-associated molecular patterns (HAMPs), damageassociated molecular patterns (DAMPs) and pathogenassociated molecular patterns (PAMPs). HAMPs and PAMPs involve a diversity of compounds. For instance, herbivorous insects produce oral secretions that contain, for example, fatty acid–amino acid conjugates (FACs), sulfur-containing fatty acids (caeliferins), and/or enzymes (b-glucosidases) [6,7]. Moreover, benzyl cyanide, bruchins, phospholipids or small proteins are associated with egg deposition by herbivores [8]. PAMPs include, for example, flagellin, chitin, glycoproteins, and lipopolysaccharides [9]. DAMPs include cell-wall fragments (e.g. oligogalacturonides) and endogenous plant-derived signals that arise from damage caused by pathogen infection or herbivore attack [6,9]. These molecular patterns can be exploited by plants to identify the nature of the organisms that initiate an interaction with them [10]. For instance, plant roots that are exposed to soil-born microbes may use variation in the bacterial elicitor flagellin to discriminate between pathogenic bacteria and mutualistic rhizosphere bacteria. In contrast to the effect of the elicitor flg22, a conserved peptide motif in the flagellar protein of many bacteria, flagellin from the Current Opinion in Plant Biology 2016, 32:17–23
18 Biotic interactions
mutualistic bacterium Mesorhizobium loti did not induce defence responses in Lotus japonicus plants [11]. This indicates that L. japonicus plants can discriminate between pathogenic and symbiotic bacteria. Plants can initiate differential responses to different attackers. For instance, egg deposition by the specialist butterfly Pieris brassicae, whose larvae are voracious herbivores of glucosinolate-containing plants, results in enhanced resistance to conspecific and heterospecific caterpillars in black mustard plants (Brassica nigra). In contrast, egg deposition by the generalist moth Mamestra brassicae, whose larvae upon emergence are likely to move soon to non-brassicaceous neighbouring plants, do not result in such changes in resistance in black mustard plants [12]. Different attackers often elicit different transcriptomic responses [13] and different changes in the phenotype [2,9,14]. Some attackers, although inflicting feeding damage to the plant, may still have an overall benefit to the plant. For instance, attack of coyote tobacco plants (Nicotiana attenuata) by the mirid herbivore Tupiocoris notatus results in the production of secondary metabolites and proteinase inhibitors that reduce feeding by voracious Manduca hornworm caterpillars and results in the attraction of a generalist predatory bug that prefers to feed on the hornworm caterpillars [15]. The direct effects of the mirids on plant fitness are only minor, but their indirect effects can be major [15]. Thus, plants can recognize different members of the phytobiome and respond differentially with changes in their phenotype. This phenotypic plasticity may allow them to maximize interactions with beneficial organisms while minimizing interactions with antagonists. Transcriptomic studies show that major transcriptomic rearrangements may underlie this phenotypic plasticity. For instance, herbivory by Pieris rapae caterpillars leads to differential expression of ca 4000 genes in Arabidopsis plants, infection with the necrotrophic pathogen Botrytis cinerea ca 2100 genes and drought stress ca 4000 genes [16,17]. This indicates that a plant’s physiology is dramatically reprogrammed, related to various physiological processes. This has extensive consequences for the plant’s phenotype in terms of, for example, plant chemistry, morphology, and growth [14,18].
Herbivory-induced plant volatiles Although plants may initiate direct defences against herbivores [14], these attackers may evolve counter-adaptations [19] and, thus, break through plant defences [20– 22]. This may be accomplished by, for example, detoxification of secondary metabolites [20] or by suppressing the induction of direct defences [21,22]. In addition to direct defences, plants can also initiate indirect defences, mediated by, among others, the induced emission of volatiles that attract carnivorous enemies of the herbivores [23]. This phenotypic change disseminates in the community Current Opinion in Plant Biology 2016, 32:17–23
and can influence various organisms. Arthropod herbivory or oviposition result in the emission of a diverse blend of volatiles [8,24], originating from various biosynthetic pathways [25]. These include especially green-leaf volatiles derived from the lipoxygenase biosynthetic pathway, terpenoids, aromatic compounds, nitrogen-containing and sulphur-containing compounds [25,26]. The effects of the emitted blend of volatiles have been extensively investigated for the attraction of carnivorous enemies of the inducing arthropods [24].
Modulation of herbivory-induced plant volatiles by associated organisms The induction of plant volatiles by interactions with herbivores has especially been investigated for individual plant–herbivore interactions. However, neither the plant [1] nor the herbivore [27] are individual entities. Each harbours a diverse community consisting of microbes and sometimes also multicellular organisms such as endophytic insects in plants or juvenile stages of parasitic wasps in herbivores [28]. These associated organisms may modulate the response of the plant to herbivory (Figure 1). Modulation by plant-associated microorganisms
For instance, colonisation of the roots of Phaseolus vulgaris plants with the mycorrhizal fungus Glomus mosseae modifies the volatile blend induced by herbivory by the twospotted spider mite Tetranychus urticae which resulted in an enhanced attraction of a carnivorous enemy of the spider mites, the predatory mite Phytoseiulus persimilis [29]. Colonisation of the roots of Arabidopsis by the plant-growth promoting rhizobacterium (PGPR) Pseudomonas simiae (formerly P. fluorescens) modifies the volatile blends induced by aphid herbivory [30], resulting in a decreased attraction of aphid parasitoids. In contrast, the rhizobacteria modify the caterpillar-induced blend of plant volatiles such that the attraction of parasitoids that attack the caterpillars is enhanced [31]. Colonisation of roots of Lima bean plants (Phaseolus lunatus) by Rhizobia modulates the blend of jasmonic-acid inducible plant volatiles resulting in a decreased attraction of the herbivorous Mexican bean beetle [32]. It remains to be investigated whether the modulation of HIPV emission is a result of an altered nutritional state of the plant when colonised by mycorrhiza, rhizobia or PGPR or due to physiological changes associated with the interaction with the microbes, or a combination of the two. Plants also harbour various endophytic fungi that can provide protection to their host plant in various ways [33], including the emission of constitutive volatiles by roots of endophyte-infected grass plants [34]. To my knowledge no information is available on the modulation of HIPV by endophytes. Yet, fungal endophytes can modulate jasmonic-acid induced plant volatiles [35] and can influence the interaction web of aphids and their parasitoids on the plant [36]. www.sciencedirect.com
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Figure 1
herbivore-induced plant volatile emission
modulated herbivore-induced plant volatile emission
herbivore-associated organisms
second herbivore
plant-associated microorganisms
neighbouring plants
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plant fitness Current Opinion in Plant Biology
Herbivore feeding induces the emission of herbivore-induced plant volatiles (HIPV) by plants and these volatiles affect the behaviour of members of the phytobiome with consequences for plant fitness. Moreover, the interaction of members of the phytobiome with the plant can also modulate the emission of HIPV and consequently affect phytobiome composition and dynamics.
Modulation by a second herbivore species attacking the same plant
When plants induce HIPV they may be under attack of other organisms as well. When two or more organisms attack a plant, the total effect is rarely the sum of the individual effects of each attacker. Herbivores may attenuate or enhance the effects of other herbivores and thus modulate the effects of the HIPV on members of the phytobiome [23,37]. For instance, the infestation of bean plants with a second herbivore attenuates the attraction of an egg parasitoid to volatiles emitted by plants infested with stinkbug eggs [38]. In contrast, pathogen attack of plants infested with caterpillars may enhance the attraction of parasitoids that attack the caterpillars [39]. Thus, a second herbivore modulates the plant’s response with www.sciencedirect.com
consequences for interactions with members of the phytobiome. Modulation by neighbouring plants
Undamaged neighbouring plants may affect the emission of HIPV. Trifolium pratense plants emitted lower numbers and amounts of HIPV when exposed to an undamaged neighbouring conspecific plant. This effect was independent of whether there was contact aboveground, belowground or above-ground and belowground [40]. Shading by neighbouring plants reduces the red (R) to far-red (FR) ratio (R:FR) of sunlight that a plant is exposed to. This leads to enhanced plant growth [41] and interference with JA-mediated and SA-mediated direct defences [42,43]. The exposure to lower R:FR ratios as a result of shading Current Opinion in Plant Biology 2016, 32:17–23
20 Biotic interactions
by neighbours also interferes with the induction of JAinducible volatiles in Arabidopsis thaliana and affects the behaviour of herbivorous caterpillars that forage for a host plant [44]. It will be interesting to extend this to effects on other members of the phytobiome. Plants are also known to respond to volatiles from neighbouring herbivoreinfested plants, for example, with the priming of direct and indirect defences [45]. Subsequent infestation of the primed plant then results in an enhanced emission of HIPV and attraction of carnivorous arthropods [46]. Finally, neighbouring plants may interfere with the behavioural responses of arthropods to HIPV [47,48], although also examples exist where such interference does not occur [49].
responses that may benefit the plant, for example, repellence of herbivores as well as attraction of predators of herbivores, as well as responses that may harm the plant such as the attraction of herbivores or the attraction of hyperparasitoids. Moreover, the plant-associated community may also have plant-mediated feedback mechanisms, where the composition of the community influences plant phenotype and phenology with consequences for trait evolution of individual herbivore species in terms of, for example, feeding preference [68]. Finally, HIPV can be toxic to members of the phytobiome such as microbes and herbivorous insects [69,70]. Thus, the emission of HIPV has a complex effect on the phytobiome with a suite of positive and negative consequences for the plant.
Modulation by herbivore-associated organisms
Fitness consequences
HIPV emission may also be influenced by organisms living within the inducing herbivore, such as larvae of parasitic wasps that feed within the herbivore that induces the volatiles [50,51,52]. The parasitoid larvae feed on the haemolymph and tissues of the herbivore and may modulate the composition of the herbivore’s oral secretion. This alters the induction of HIPV with consequences for the behaviour of herbivores, parasitoids and hyperparasitoids that attack the parasitoids in the herbivore [28,50,51,52]. It is intriguing to see that these effects are specific for the parasitoid species that develops in the herbivore [53]. Also other herbivore-associated organisms such as microbes in the oral secretion of the Colorado potato beetle may modulate herbivore-induced plant defences, which involves attenuation of jasmonicacid mediated induced responses [54]. This suggests that also jasmonic-acid-mediated indirect defences through HIPV may be modulated by such microbes, but this remains to be investigated.
The fitness consequences of HIPV emission have long been debated [18,71–73] because they are not so easily assessed. After all, the emission of HIPV influences various community members and affects community dynamics. Thus, fitness consequences can only be assessed under realistic field conditions where plants are exposed to the full, variable, phytobiome. Several studies have shown that parasitization of herbivores can benefit the plant in term of seed production [74–76] under more or less protected conditions. Moreover, phenotypic changes in response to eggs that result in enhanced parasitoid attraction and reduced herbivore performance resulted in an overcompensation by the plant, resulting in enhanced seed set under field conditions [77]. A dedicated study on the exclusive role of HIPV shows that induced emission of HIPV indeed is associated with fitness benefits. Green-leaf-volatile-silenced N. attenuata plants placed in their natural environment produced twice as many buds in the presence of predatory bugs as control plants, whereas plants silenced for the induced production of anti-digestive proteins had similar bud production as nonsilenced plants [78]. How modulation of HIPV emission by various members of the phytobiome influence the phytobiome-mediated effects of HIPV on plant fitness will be an exciting topic for future studies. This can only be investigated within the complex and dynamic phytobiome context.
Effects of HIPV on the associated animal community Originally, the effects of HIPV were investigated for their effects on carnivorous enemies of the inducing herbivore. These were attracted to the herbivore-infested plants and attacked the herbivore. Thus, the emission of HIPV was coined ‘crying for help’ [55]. So, initially the effects of HIPV were investigated for simple tritrophic food chains consisting of a plant, an herbivore and a carnivore. However, HIPV are public information that can be used by any member of the community. Indeed, there now is evidence for responses by, for example, herbivores [53,56– 58], carnivorous arthropods such as predators and parasitoids [24,59], carnivorous birds [60], entomopathogenic nematodes, [61], hyperparasitoids [51,52], pollinators [62,63], and neighbouring plants [45,64]. Each of these community members responds in its own way, for example, being attracted or repelled, with different temporal and spatial aspects. As a consequence, the change in plant phenotype results in a drastic and dynamic rearrangement of the associated phytobiome [65–67]. This includes Current Opinion in Plant Biology 2016, 32:17–23
Future directions The fact that plants can discriminate between attackers and mutualists, respond to neighbouring competitors or to neighbours that are under actual attack raises the question where the limits are of the perception of their environment by plants. Can they perceive the presence of carnivorous enemies of herbivorous attackers, for example by responding to ant trail pheromones [79], just as they can respond to herbivore pheromones [80] or to the presence of cues from parasitic plants or from flowering plants that can serve as both a source of pollen and receiver of pollen [81]? This is an intriguing question for future research. Subsequently, knowledge of the www.sciencedirect.com
Herbivore-induced plant volatiles in the phytobiome Dicke 21
degree to which plants are informed about the phytobiome composition will elicit questions on how plants deal with information on conflicting situations such as the presence of attackers as well as their natural enemies or competitors. Does this modulate their phenotypically plastic change in HIPV emission? The better plants are informed about their environment, the more relevant are questions on how plant deal with dilemma’s such as to grow or to defend, to invest in immediate reproduction or to delay reproduction, and whether to emit HIPV and stand out or to limit HIPV emission and be less apparent to the members of the phytobiome. So far, research on HIPV has considered the emission of these chemicals a deterministic change in plant phenotype. In the light of the modulations of HIPV emission by phytobiome members, questions on how plants strategically use HIPV within the dynamically changing environmental conditions only gets more exciting dimensions for future research in this field. Future issues to be addressed include the modulation by multiple phytobiome members. For instance, the belowground microbiome is a speciose community [1] with various interactions. How the dynamics of this community influence the plant will be a major but important challenge. Moreover, also the macrobiome is a diverse community [2] and identifying those species that are most important in structuring the community as well as its interactions with plants is an important undertaking for the years to come [82]. Given that carnivores in natural as well as agricultural systems exploit HIPV [18], these issues are not only interesting from a fundamental point of view, but they will also allow to enhance the effectiveness of carnivorous arthropods in environmentally benign pest control strategies.
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22 Biotic interactions
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