Microbial Root Mutualists Affect the Predators and Pathogens of Herbivores above Ground: Mechanisms, Magnitudes, and Missing Links

Tao, Leiling; Hunter, Mark D.; Roode, Jacobus C. de

doi:10.3389/fevo.2017.00160

Cited by 22 publications

(24 citation statements)

References 133 publications

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“…Subsequent studies of other virus-plant-vector species combinations have reported similar findings of virus modification of plant VOCs with enhanced vector attraction to infected plants. This phenomenon has been observed for viruses with different transmission mechanisms including persistently, non-persistently, and semi-persistently transmitted viruses [34,99,102,108,109]. In addition to plant viruses, recent evidence suggests that insect-vectored bacterial pathogens also alter plant olfactory cues to enhance their transmission.…”

Section: Influence Of Pathogenic Microbes On Plant-produced Olfactorymentioning

confidence: 87%

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The Role of Plant-Associated Microbes in Mediating Host-Plant Selection by Insect Herbivores

Grunseich

Thompson

Aguirre

et al. 2019

Plants

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There is increasing evidence that plant-associated microorganisms play important roles in shaping interactions between plants and insect herbivores. Studies of both pathogenic and beneficial plant microbes have documented wide-ranging effects on herbivore behavior and performance. Some studies, for example, have reported enhanced insect-repellent traits or reduced performance of herbivores on microbe-associated plants, while others have documented increased herbivore attraction or performance. Insect herbivores frequently rely on plant cues during foraging and oviposition, suggesting that plant-associated microbes affecting these cues can indirectly influence herbivore preference. We review and synthesize recent literature to provide new insights into the ways pathogenic and beneficial plant-associated microbes alter visual, olfactory, and gustatory cues of plants that affect host-plant selection by insect herbivores. We discuss the underlying mechanisms, ecological implications, and future directions for studies of plant-microbial symbionts that indirectly influence herbivore behavior by altering plant traits.

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Section: Influence Of Pathogenic Microbes On Plant-produced Olfactorymentioning

confidence: 87%

“…In this review, we limit our discussion of beneficial plant-associated microbes to their influence on herbivore foraging and oviposition. For a recent review of how beneficial plant-associated microbes alter insect predator and parasitoid behavior, see [34].…”

Section: Beneficial Plant-associated Microbesmentioning

confidence: 99%

The Role of Plant-Associated Microbes in Mediating Host-Plant Selection by Insect Herbivores

Grunseich

Thompson

Aguirre

et al. 2019

Plants

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“…Beneficial soil microbes such as AM fungi are able to alter plant-insect herbivore interactions through several mechanisms, eliciting changes in the availability and quality of plant nutrients, defensive strategies, and stress tolerance [15]. In addition, AM fungi can affect insect herbivores aboveground, both by changing host-plant quality from the bottom-up [13,16,17] and the resistance of insect herbivores to their natural enemies from the top-down [12,18,19]. During the early developmental stages of the symbiosis, plant defense responses are modulated to facilitate AM fungal colonization of roots, which then leads to activation of plant immune responses both at the local level and throughout the plant [17].…”

Section: Introductionmentioning

confidence: 99%

Assessment of Local and Systemic Changes in Plant Gene Expression and Aphid Responses during Potato Interactions with Arbuscular Mycorrhizal Fungi and Potato Aphids

Rizzo

Sherman

Manosalva

et al. 2020

Plants

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This research examined aphid and plant responses to distinct levels (none, low, and high) of arbuscular mycorrhizal (AM) fungal root colonization by studying the association between potato aphids (Macrosiphum euphorbiae), potatoes (Solanum tuberosum), and AM fungi (Rhizophagus intraradices). It extends knowledge on gene expression changes, assessed by RT–qPCR, of ten defense-related genes at two time-points post-herbivory (24 h and 10 days), focusing on aphid-infested local leaves, non-infested systemic leaves, and roots. The results showed that aphid fitness was not altered by AM symbiosis. At 24 h, ETHYLENE RECEPTOR 1 gene expression was repressed in roots of aphid-infested non-mycorrhizal plants and aphid-infested plants with a high level of AM fungal root colonization, but not on aphid-infested plants with a low level of AM fungal root colonization. At 10 days, ALLENE OXIDE CYCLASE and POTATO TYPE I PROTEASE INHIBITOR were upregulated exclusively in local leaves of aphid-infested plants with a low level of AM fungal root colonization. In addition, local and systemic changes in plant gene expression appeared to be regulated exclusively by AM status and aphid herbivory. In summary, the gene expression data provide insights on mycorrhizal potato responses to aphid herbivory and serve as a starting point for future studies using this system.

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“…In terrestrial ecosystems, both top-down and bottom-up forces travel with ease across the traditional soil "boundary, " with plants connecting the interactions that occur between above and belowground organisms (van der Putten et al, 2001;van Dam and Heil, 2011;Hunter, 2016). As a result, soil organisms that are associated with plant roots have the potential to affect herbivore populations above ground both by affecting plant quality for herbivores from the bottom-up (Hartley and Gange, 2009;Koricheva et al, 2009;Jung et al, 2012) and the resistance of herbivores to their natural enemies from the top down (Gange et al, 2003;Rasmann et al, 2017;Tao et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

“…Rootassociated microbes, such as AMF, affect herbivore-natural enemy interactions indirectly by altering plant phenotype (Rasmann et al, 2017;Tao et al, 2017). For instance, AMF increase the attractiveness of plants to natural enemies by changing the volatile emissions of their host plants (Guerrieri et al, 2004;Fontana et al, 2009;Hoffmann et al, 2011;Schausberger et al, 2012;Babikova et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Mycorrhizae Alter Toxin Sequestration and Performance of Two Specialist Herbivores

Meier

Hunter

2018

Front. Ecol. Evol.

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Multitrophic species interactions are shaped by both top-down and bottom-up factors. Belowground symbionts of plants, such as arbuscular mycorrhizal fungi (AMF), can alter the strength of these forces by altering plant phenotype. For example, AMF-mediated changes in foliar toxin and nutrient concentrations may influence herbivore growth and fecundity. In addition, many specialist herbivores sequester toxins from their host plants to resist natural enemies, and the extent of sequestration varies with host plant secondary chemistry. Therefore, by altering plant phenotype, AMF may affect both herbivore performance and their resistance to natural enemies. We examined how inoculation of plants with AMF influences toxin sequestration and performance of two specialist herbivores feeding upon four milkweed species (Asclepias incarnata, A. curassavica, A. latifolia, A. syriaca). We raised aphids (Aphis nerii) and caterpillars (Danaus plexippus) on plants for 6 days in a fully factorial manipulation of milkweed species and level of AMF inoculation (zero, medium, and high). We then assessed aphid and caterpillar sequestration of toxins (cardenolides) and performance, and measured defensive and nutritive traits of control plants. Aphids and caterpillars sequestered higher concentrations of cardenolides from plants inoculated with AMF across all milkweed species. Aphid per capita growth rates and aphid body mass varied non-linearly with increasing AMF inoculum availability; across all milkweed species, aphids had the lowest performance under medium levels of AMF availability and highest performance under high AMF availability. In contrast, caterpillar survival varied strongly with AMF availability in a plant species-specific manner, and caterpillar growth was unaffected by AMF. Inoculation with AMF increased foliar cardenolide concentrations consistently among milkweed species, but altered aboveground biomasses and foliar phosphorous concentrations in a plant species-specific fashion. Increased herbivore sequestration of cardenolides followed AMF-mediated increases in foliar cardenolide concentrations. Aphid performance declined with increasing foliar cardenolide concentrations, while caterpillar survival increased with aboveground biomass. Our findings suggest that by altering plant phenotype, the availability of AMF in soil has the potential to influence both top-down (via sequestration) and bottom up (via plant defense and nutrition) forces that operate on herbivores.

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Microbial Root Mutualists Affect the Predators and Pathogens of Herbivores above Ground: Mechanisms, Magnitudes, and Missing Links

Cited by 22 publications

References 133 publications

The Role of Plant-Associated Microbes in Mediating Host-Plant Selection by Insect Herbivores

The Role of Plant-Associated Microbes in Mediating Host-Plant Selection by Insect Herbivores

Assessment of Local and Systemic Changes in Plant Gene Expression and Aphid Responses during Potato Interactions with Arbuscular Mycorrhizal Fungi and Potato Aphids

Mycorrhizae Alter Toxin Sequestration and Performance of Two Specialist Herbivores

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