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Specialized naphthoquinones present in Impatiens glandulifera nectaries inhibit the growth of fungal nectar microbes.

ABSTRACT: The invasion success of Impatiens glandulifera (Himalayan balsam) in certain parts of Europe and North America has been partially attributed to its ability to compete for bee pollinators with its rich nectar and due to its capacity to produce and release allelopathic 1,4-naphthoquinones (1,4-NQs) from its roots and leaves. Given that other 1,4-NQs present in the digestive fluids of certain carnivorous plants are proposed to control microbial colonization, we investigated the potential for the 1,4-NQs, 2-methoxy-1,4-naphthoquinone (2-MNQ) and lawsone, to fulfill an analogous role in the nectaries of I. glandulifera. Both 2-MNQ and lawsone were detected in the floral nectaries of I. glandulifera at levels comparable to leaves and roots, but were discovered to be at significantly higher levels in its extra-floral nectaries (EFNs) and to be present in EFN nectar itself. Nectar microbe inhibition assays revealed that the common nectar bacteria Gluconobacter oxydans and Asaia prunellae are not inhibited by 2-MNQ or lawsone, although both compounds were found to inhibit the growth of the common fungal nectar microbes Metschnikowia reukaufii and Aureobasidium pullulans. Taken together, these findings suggest that 2-MNQ and lawsone could serve to protect the rich nectar of I. glandulifera against fungal growth. The high abundance of 2-MNQ and lawsone in I. glandulifera EFNs may also point to an unsuspected mechanism for how allelopathic 1,4-NQs are leached into the soil where they exhibit their known allelopathic effects.

SUBMITTER: Block AK

PROVIDER: S-EPMC6589542 | biostudies-literature | 2019 May

REPOSITORIES: biostudies-literature

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Specialized naphthoquinones present in <i>Impatiens glandulifera</i> nectaries inhibit the growth of fungal nectar microbes.

Block Anna K AK Yakubova Elena E Widhalm Joshua R JR

Plant direct 20190513 5

The invasion success of <i>Impatiens glandulifera</i> (Himalayan balsam) in certain parts of Europe and North America has been partially attributed to its ability to compete for bee pollinators with its rich nectar and due to its capacity to produce and release allelopathic 1,4-naphthoquinones (1,4-NQs) from its roots and leaves. Given that other 1,4-NQs present in the digestive fluids of certain carnivorous plants are proposed to control microbial colonization, we investigated the potential for ...[more]

PMID: 31245775

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Project description:BackgroundInvasive species can be a major threat to native biodiversity and the number of invasive plant species is increasing across the globe. Population genetic studies of invasive species can provide key insights into their invasion history and ensuing evolution, but also for their control. Here we genetically characterise populations of Impatiens glandulifera, an invasive plant in Europe that can have a major impact on native plant communities. We compared populations from the species' native range in Kashmir, India, to those in its invaded range, along a latitudinal gradient in Europe. For comparison, the results from 39 other studies of genetic diversity in invasive species were collated.ResultsOur results suggest that I. glandulifera was established in the wild in Europe at least twice, from an area outside of our Kashmir study area. Our results further revealed that the genetic diversity in invasive populations of I. glandulifera is unusually low compared to native populations, in particular when compared to other invasive species. Genetic drift rather than mutation seems to have played a role in differentiating populations in Europe. We find evidence of limitations to local gene flow after introduction to Europe, but somewhat less restrictions in the native range. I. glandulifera populations with significant inbreeding were only found in the species' native range and invasive species in general showed no increase in inbreeding upon leaving their native ranges. In Europe we detect cases of migration between distantly located populations. Human activities therefore seem to, at least partially, have facilitated not only introductions, but also further spread of I. glandulifera across Europe.ConclusionsAlthough multiple introductions will facilitate the retention of genetic diversity in invasive ranges, widespread invasive species can remain genetically relatively invariant also after multiple introductions. Phenotypic plasticity may therefore be an important component of the successful spread of Impatiens glandulifera across Europe.

Project description:Background:Matrix-assisted laser-desorption and ionisation time-of-flight mass spectroscopy (MALDI-TOF MS) is a powerful tool for the characterisation and/or identification of protein-containing samples. Several MALDI-TOF MS sample-preparation methods are currently available but few of these are well suited to the analysis of plant material. We have recently developed a simple, rapid, and relatively-cheap method for MALDI-TOF MS that is applicable to plant material (in addition to microbial and insect material), and our aim in this study was to distinguish between closely-related plant species and/or between regional biotypes within an invasive weed species using this method with a view to optimising the selection of biological control agents that can be used for weed management. Results:We have employed a combination of principal-component analysis and closest-relatedness diagrams derived from MALDI-TOF MS spectral-comparison data to discriminate between the closely-related Impatiens spp. Impatiens noli-tangere, Impatiens parviflora, Impatiens scabrida, Impatiens balsamina, and two regional biotypes of the invasive weed Impatiens glandulifera. We have also developed a method for sample discrimination based upon comparison between blind-test MALDI-TOF MS spectra and reference-sample spectra. Using this latter method, we have been able to discriminate on the basis of the acid-soluble-protein mass spectra generated between four regional biotypes of I. glandulifera that differ in their susceptibility to the biological control agent Himalayan balsam rust (Puccinia komarovii var. glanduliferae) using mature leaf material. Using younger leaves, discrimination was not possible between these four regional biotypes. Conclusions:MALDI-TOF MS analysis is able to discriminate between closely-related plant species within the genus Impatiens and between regional biotypes of I. glandulifera. Because of this, MALDI-TOF MS holds great promise for improving weed biological control, a management technique which uses highly-specific co-evolved natural enemies for the control of an invasive non-native plant species, through the optimal matching of biological control agents with susceptible target species/regional biotypes.

Dataset Information

Specialized naphthoquinones present in Impatiens glandulifera nectaries inhibit the growth of fungal nectar microbes.

Publications

Specialized naphthoquinones present in <i>Impatiens glandulifera</i> nectaries inhibit the growth of fungal nectar microbes.

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