Long-distance transport of signals during symbiosis

Staehelin, Christian; Xie, Zhiping; Illana, Antonio; Vierheilig, Horst

doi:10.4161/psb.6.3.13881

Cited by 46 publications

(11 citation statements)

References 70 publications

(112 reference statements)

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“…We observed that differing levels of AMF inoculum availability resulted in differences in the magnitude and direction of herbivore-induced defenses, despite resulting in similar levels of root colonization. Plants maintain a maximum level of AMF colonization and suppress further colonization (Vierheilig et al 2000a, b, Vierheilig 2004, Meixner et al 2005) by regulating phytohormones, including JA and SA (Staehelin et al 2011, Gutjahr 2014, Bucher et al 2014). These hormones play key roles in the regulation of resistance responses of plants to insect herbivores (Pieterse et al 2012(Pieterse et al , 2014.…”

Section: Discussionmentioning

confidence: 99%

Arbuscular mycorrhizal fungi mediate herbivore‐induction of plant defenses differently above and belowground

Meier

Hunter

2018

Oikos

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Plants are exposed to herbivores and symbionts above and below ground. Herbivores above ground alter plant defenses in both leaves and roots, affecting plant–herbivore interactions above and below ground. Root symbionts, such as arbuscular mycorrhizal fungi (AMF), also influence the defenses of leaves and roots, and alter plant responses to herbivory. However, we lack an understanding of how AMF mediate plant responses to herbivores simultaneously in above and belowground plant tissues, despite the ubiquity of such interactions and their consequences for ecological communities. In a full factorial experiment, we subjected plants of four milkweed (Asclepias) species under three levels of AMF inoculum availability to damage by aphids Aphis nerii, caterpillars Danaus plexippus, or no herbivores. We then measured foliar and root cardenolides (chemical defenses), leaf toughness, latex exudation (physical defenses), foliar carbon, nitrogen, and phosphorous concentrations, plant biomass, and levels of AMF colonization of roots. Plants inoculated with AMF generally produced tougher leaves with higher cardenolide concentrations than did plants without AMF. In contrast, root cardenolides were altered by AMF inoculum availability in a plant species‐specific manner. The relative induction or suppression of foliar cardenolides and leaf toughness by herbivores was altered strongly by the level of AMF inoculum available to plants. However, AMF did not influence caterpillar‐induction or aphid‐suppression of root cardenolides. In addition, herbivore feeding induced substantial changes in levels of AMF colonization of roots in a plant species‐specific manner. We demonstrate that the availability of AMF in soil alters herbivore induction and suppression of plant defenses strongly, and does so differently in above and belowground plant tissues. Furthermore, we show that herbivore feeding alters levels of AMF colonization substantially, completing a feedback loop between above‐ and belowground organisms. Our study suggests that indirect interactions between AMF and herbivores may have community‐wide consequences by altering plant phenotype above and below ground.

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Section: Discussionmentioning

confidence: 99%

Arbuscular mycorrhizal fungi mediate herbivore‐induction of plant defenses differently above and belowground

Meier

Hunter

2018

Oikos

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“…This includes the host Autoregulation of Nodulation (AON) and Autoregulation of Mycorrhization (AOM) pathways that control the extent of nodulation and mycorrhization, respectively. 3,4 Classical plant hormones play crucial roles in the nodulation and mycorrhization processes. [5][6][7] Some fundamental effects of these hormones on the gross level of colonisation are compared for the 2 symbioses in Table 1.…”

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Common and divergent roles of plant hormones in nodulation and arbuscular mycorrhizal symbioses

Foo¹,

Ferguson

Reid³

2014

Plant Signaling & Behavior

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All of the classical plant hormones have been suggested to influence nodulation, including some that interact with the Autoregulation of Nodulation (AON) pathway. Leguminous plants strictly regulate the number of nodules formed through this AON pathway via a root-shoot-root loop that acts to suppress excessive nodulation. A related pathway, the Autoregulation of Mycorrhization (AOM) pathway controls the more ancient, arbuscular mycorrhizal (AM) symbiosis. A comparison of the published responses to the classical hormones in these 2 symbioses shows that most influence the symbioses in the same direction. This may be expected if they affect the symbioses via common components of these symbiotic regulatory pathways. However, some hormones influence these symbioses in opposite directions, suggesting a more complex relationship, and probably one that is not via the common components of these pathways. In a recent paper we showed, using a genetic approach, that strigolactones and brassinosteroids do not act downstream of the AON genes examined and argued that they probably act independently to promote nodule formation. Recently it has been shown that the control of nodulation via the AON pathway involves mobile CLE peptide signals. It is therefore suggested that a more direct avenue to determine if the classical hormones play a direct role in the autoregulatory pathways is to further examine whether CLE peptides and other components of these processes can influence, or be influenced by, the classical hormones. Such studies and other comparisons between the nodulation and mycorrhizal symbioses should allow the role of the classical hormones in these critical symbioses to be rapidly advanced.

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“…Although AMF colonization levels increase with increasing inoculum availability (Garrido et al, 2010;Vannette and Hunter, 2011), plants maintain a maximum level of AMF colonization of roots (Vierheilig et al, 2000a,b;Meixner et al, 2005) and suppress further colonization after reaching a critical level (Vierheilig, 2004). Plant regulation of AMF development in roots is controlled by the same plant hormones (Staehelin et al, 2011;Bucher et al, 2014;Gutjahr, 2014;and references therein) that are integral to the development of plant vascular tissues (Lucas et al, 2013) and the resistance responses of plants to insect herbivores (Pieterse et al, 2012(Pieterse et al, , 2014. In our medium AMF treatment, there may have been sufficient inoculum to attain maximum levels of AMF colonization of plant roots.…”

Section: Discussionmentioning

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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Long-distance transport of signals during symbiosis

Cited by 46 publications

References 70 publications

Arbuscular mycorrhizal fungi mediate herbivore‐induction of plant defenses differently above and belowground

Arbuscular mycorrhizal fungi mediate herbivore‐induction of plant defenses differently above and belowground

Common and divergent roles of plant hormones in nodulation and arbuscular mycorrhizal symbioses

Mycorrhizae Alter Toxin Sequestration and Performance of Two Specialist Herbivores

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