Dataset Information

Bacterial detoxification of plant defence secondary metabolites mediates the interaction between a shrub and frugivorous birds.

ABSTRACT: Many plants produce fleshy fruits, attracting fruit-eating animals that disperse the seeds in their droppings. Such seed dispersal results in a conflict between the plant and the animal, as digestion of seeds can be highly beneficial to the animal but reduces plant fitness. The plant Ochradenus baccatus uses the myrosinase-glucosinolates system to protect its seeds. We show that hydrolysis of the O. baccatus fruit glucosinolates by the myrosinase enzyme inhibited digestive enzymes and hampered digestion in naïve individuals of the bird Pycnonotus xanthopygos. However, digestion in birds regularly feeding on O. baccatus fruits was unaffected. We find that Pantoea bacteria, dominating the gut of these experienced birds as well as the fruits, thrive on glucosinolates hydrolysis products in culture. Augmentation of Pantoea protects both naïve birds and plant seedlings from the effects of glucosinolates hydrolysis products. Our findings demonstrate a tripartite interaction, where the plant-bird mutually beneficial interactions are mediated by a communal bacterial tenant.

SUBMITTER: Trabelcy B

PROVIDER: S-EPMC10066296 | biostudies-literature | 2023 Mar

REPOSITORIES: biostudies-literature

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Bacterial detoxification of plant defence secondary metabolites mediates the interaction between a shrub and frugivorous birds.

Trabelcy Beny B Shteindel Nimrod N Lalzar Maya M Izhaki Ido I Gerchman Yoram Y

Nature communications 20230331 1

Many plants produce fleshy fruits, attracting fruit-eating animals that disperse the seeds in their droppings. Such seed dispersal results in a conflict between the plant and the animal, as digestion of seeds can be highly beneficial to the animal but reduces plant fitness. The plant Ochradenus baccatus uses the myrosinase-glucosinolates system to protect its seeds. We show that hydrolysis of the O. baccatus fruit glucosinolates by the myrosinase enzyme inhibited digestive enzymes and hampered d ...[more]

PMID: 37002264

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Project description:Frugivorous birds play an important role in seed dispersal. Alien plant species' seeds are dispersed by local birds in order to establish populations in new habitats. Alien plant species that produce fruits similar to that of native species have the potential to attract local birds, creating new mutualistic systems that are similar to the local ones. In autumn 2018 and 2019, we studied the seed dispersal systems of an alien plant species, Phytolacca americana, and a native species, Cayratia japonica, in a coastal seawall forest. Both plant species' fruit, frugivorous bird foraging behaviors, seed germination rates, and seedling microhabitats were examined to determine whether the alien species had a similar seed dispersal system to that of the native species. Our results showed that P. americana and C. japonica had similar fruit type, color, and ripening period. There was a positive correlation between the percentage rate of fruit ripening and the percentage rate of fruit missing for both plant species, indicating that local frugivorous birds have the potential to sufficiently disperse the alien seeds to enable its spread in the coastal seawall forest (simple linear regression, P. americana: β = 0.863 ± 0.017, R2 adj = 0.978, P < 0.01; C. japonica: β = 0.787 ± 0.034, R2 adj = 0.898, P < 0.01). Eleven bird species consumed the fruits of the alien species or native species during the study period. Similar results were shown across alien and native species in bird foraging behavior (feeding frequency, feeding duration and first stop distance) indicating that a similar seed dispersal relationship had been established between local frugivorous and both plant species. The alien plant had a higher number of fruits carried by birds, suggesting that P. americana had a slightly higher fruit consumption than that of C. japonica (t-test, P < 0.01). Alien plant seedlings grow more abundant in forest gap microhabitat (t-test, P < 0.01). Our results confirmed that bird digestion promotes seed germination success in both plant species. Our study suggests that in a narrow coastal seawall forest, alien plant species can successfully establish their populations by relying on similar seed dispersal systems as the local species.

Project description:Ecosystem invasion by non-native, nitrogen-fixing species is a global phenomenon with serious ecological consequences. However, in the Mediterranean basin few studies addressed the impact of invasion by nitrogen-fixing shrubs on soil quality and hydrological properties at local scale, and the possible effects on succession dynamics and ecosystem invasibility by further species. In this multidisciplinary study we investigated the impact of Genista aetnensis (Biv.) DC., an exotic nitrogen-fixing shrub, on the Vesuvius Grand Cone (Southern Italy). Specifically, we tested the hypotheses that the invasion of G. aetnensis has a significant impact on soil quality, soil hydrological regime, local microclimate and plant community structure, and that its impact increases during the plant ontogenetic cycle. We showed that G. aetnensis, in a relatively short time-span (i.e. ~ 40 years), has been able to build-up an island of fertility under its canopy, by accumulating considerable stocks of C, N, and P in the soil, and by also improving the soil hydrological properties. Moreover, G. aetnensis mitigates the daily range of soil temperature, reducing the exposure of coexisting plants to extremely high temperatures and water loss by soil evaporation, particularly during the growing season. Such amelioration of soil quality, coupled with the mitigation of below-canopy microclimatic conditions, has enhanced plant colonization of the barren Grand Cone slopes, by both herbaceous and woody species. These results suggest that the invasion of G. aetnensis could eventually drive to the spread of other, more resource-demanding exotic species, promoting alternative successional trajectories that may dramatically affect the local landscape. Our study is the first record of the invasion of G. aetnensis, an additional example of the regime shifts driven by N-fixing shrubs in Mediterranean region. Further studies are needed to identity specific management practices that can limit the spread and impacts of this species.

Dataset Information

Bacterial detoxification of plant defence secondary metabolites mediates the interaction between a shrub and frugivorous birds.

Publications

Bacterial detoxification of plant defence secondary metabolites mediates the interaction between a shrub and frugivorous birds.

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