Reduced Responsiveness to Volatile Signals Creates a Modular Reward Provisioning in an Obligate Food-for-Protection Mutualism
Plants in more than 100 families secrete extrafloral nectar (EFN) to establish food-for-protection mutualisms with ants. Facultative ant-plants secrete EFN as a jasmonic acid (JA)-dependent response to attract generalist ants. In contrast, obligate ant-plants like the Central American “Swollen-Thorn...
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doaj-e6f963a8f91043299bba20452238b3cf2020-11-24T23:10:00ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2018-07-01910.3389/fpls.2018.01076380307Reduced Responsiveness to Volatile Signals Creates a Modular Reward Provisioning in an Obligate Food-for-Protection MutualismOmar F. Hernández-ZepedaRosario Razo-BelmanMartin HeilPlants in more than 100 families secrete extrafloral nectar (EFN) to establish food-for-protection mutualisms with ants. Facultative ant-plants secrete EFN as a jasmonic acid (JA)-dependent response to attract generalist ants. In contrast, obligate ant-plants like the Central American “Swollen-Thorn Acacias” are colonized by specialized ants, although an individual host can carry ant colonies from different species that differ in the degree of protection they provide. We hypothesized that hosts that associate simultaneously with various partners should produce rewards in a modular manner to preferentially reward high quality partners. To test this hypothesis, we applied JA to distinct leaves and quantified cell wall invertase activity (CWIN; a regulator of nectar secretion) and EFN secretion by these “local” (i.e., treated) and the “systemic” (i.e., non-treated) leaves of the same branch. Both CWIN activity and EFN secretion increased in local and systemic leaves of the facultative ant-plant Acacia cochliacantha, but only in the local leaves of the obligate ant-plant, A. cornigera. The systemic EFN secretion in A. cochliacantha was associated with an enhanced emission of volatile organic compounds (VOCs). Such VOCs function as “external signals” that control systemic defense responses in diverse plant species. Indeed, the headspace of JA-treated branches of A. cochliacantha induced EFN secretion in both plant species, whereas the headspace of A. cornigera caused no detectable induction effect. Analyses of the headspace using GC-MS identified six VOCs in the headspace of A. cochliacantha that were not emitted by A. cornigera. Among these VOCs, β-caryophyllene and (cis)-hexenyl isovalerate have already been reported in other plant species to induce defense traits, including EFN secretion. Our observations underline the importance of VOCs as systemic within-plant signals and show that the modular rewarding in A. cornigera is likely to result from a reduced emission of the systemic signal, rather than from a reduced responsiveness to the signal. We suggest that modular rewarding allows hosts to restrict the metabolic investment to specific partners and to efficiently sanction potential exploiters.https://www.frontiersin.org/article/10.3389/fpls.2018.01076/fullexclusive rewardsextrafloral nectarobligate mutualismsanctionssystemic signalingvolatile signals |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Omar F. Hernández-Zepeda Rosario Razo-Belman Martin Heil |
spellingShingle |
Omar F. Hernández-Zepeda Rosario Razo-Belman Martin Heil Reduced Responsiveness to Volatile Signals Creates a Modular Reward Provisioning in an Obligate Food-for-Protection Mutualism Frontiers in Plant Science exclusive rewards extrafloral nectar obligate mutualism sanctions systemic signaling volatile signals |
author_facet |
Omar F. Hernández-Zepeda Rosario Razo-Belman Martin Heil |
author_sort |
Omar F. Hernández-Zepeda |
title |
Reduced Responsiveness to Volatile Signals Creates a Modular Reward Provisioning in an Obligate Food-for-Protection Mutualism |
title_short |
Reduced Responsiveness to Volatile Signals Creates a Modular Reward Provisioning in an Obligate Food-for-Protection Mutualism |
title_full |
Reduced Responsiveness to Volatile Signals Creates a Modular Reward Provisioning in an Obligate Food-for-Protection Mutualism |
title_fullStr |
Reduced Responsiveness to Volatile Signals Creates a Modular Reward Provisioning in an Obligate Food-for-Protection Mutualism |
title_full_unstemmed |
Reduced Responsiveness to Volatile Signals Creates a Modular Reward Provisioning in an Obligate Food-for-Protection Mutualism |
title_sort |
reduced responsiveness to volatile signals creates a modular reward provisioning in an obligate food-for-protection mutualism |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Plant Science |
issn |
1664-462X |
publishDate |
2018-07-01 |
description |
Plants in more than 100 families secrete extrafloral nectar (EFN) to establish food-for-protection mutualisms with ants. Facultative ant-plants secrete EFN as a jasmonic acid (JA)-dependent response to attract generalist ants. In contrast, obligate ant-plants like the Central American “Swollen-Thorn Acacias” are colonized by specialized ants, although an individual host can carry ant colonies from different species that differ in the degree of protection they provide. We hypothesized that hosts that associate simultaneously with various partners should produce rewards in a modular manner to preferentially reward high quality partners. To test this hypothesis, we applied JA to distinct leaves and quantified cell wall invertase activity (CWIN; a regulator of nectar secretion) and EFN secretion by these “local” (i.e., treated) and the “systemic” (i.e., non-treated) leaves of the same branch. Both CWIN activity and EFN secretion increased in local and systemic leaves of the facultative ant-plant Acacia cochliacantha, but only in the local leaves of the obligate ant-plant, A. cornigera. The systemic EFN secretion in A. cochliacantha was associated with an enhanced emission of volatile organic compounds (VOCs). Such VOCs function as “external signals” that control systemic defense responses in diverse plant species. Indeed, the headspace of JA-treated branches of A. cochliacantha induced EFN secretion in both plant species, whereas the headspace of A. cornigera caused no detectable induction effect. Analyses of the headspace using GC-MS identified six VOCs in the headspace of A. cochliacantha that were not emitted by A. cornigera. Among these VOCs, β-caryophyllene and (cis)-hexenyl isovalerate have already been reported in other plant species to induce defense traits, including EFN secretion. Our observations underline the importance of VOCs as systemic within-plant signals and show that the modular rewarding in A. cornigera is likely to result from a reduced emission of the systemic signal, rather than from a reduced responsiveness to the signal. We suggest that modular rewarding allows hosts to restrict the metabolic investment to specific partners and to efficiently sanction potential exploiters. |
topic |
exclusive rewards extrafloral nectar obligate mutualism sanctions systemic signaling volatile signals |
url |
https://www.frontiersin.org/article/10.3389/fpls.2018.01076/full |
work_keys_str_mv |
AT omarfhernandezzepeda reducedresponsivenesstovolatilesignalscreatesamodularrewardprovisioninginanobligatefoodforprotectionmutualism AT rosariorazobelman reducedresponsivenesstovolatilesignalscreatesamodularrewardprovisioninginanobligatefoodforprotectionmutualism AT martinheil reducedresponsivenesstovolatilesignalscreatesamodularrewardprovisioninginanobligatefoodforprotectionmutualism |
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