An unusual tricosatriene is crucial for male fungus gnat attraction and exploitation by sexually deceptive Pterostylis orchids

Hayashi, Tobias; Bohman, Björn; Scaffidi, Adrian; Peakall, Rod; Flematti, Gavin R.

doi:10.1016/j.cub.2021.01.095

Cited by 22 publications

(21 citation statements)

References 56 publications

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“…Within the orchids, pollination by sexual deception has evolved independently on four continents and is employed by hundreds of species spanning multiple lineages of the Orchidaceae ( Peakall et al, 2020 ). The types of pollinators involved are also diverse, and include ants, bees and wasps (Hymenoptera), fungus gnats and other flies (Diptera), and beetles (Coleoptera) ( Gaskett, 2011 ; Bohman et al, 2016 ; Peakall et al, 2020 ; Cohen et al, 2021 ; Hayashi et al, 2021 ). In these cases, pollination is achieved during attempted copulation with the labellum, an often highly modified petal of the orchids.…”

Section: Introductionmentioning

confidence: 99%

Anthocyanin and Flavonol Glycoside Metabolic Pathways Underpin Floral Color Mimicry and Contrast in a Sexually Deceptive Orchid

2022

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Sexually deceptive plants secure pollination by luring specific male insects as pollinators using a combination of olfactory, visual, and morphological mimicry. Flower color is a key component to this attraction, but its chemical and genetic basis remains poorly understood. Chiloglottis trapeziformis is a sexually deceptive orchid which has predominantly dull green-red flowers except for the central black callus projecting from the labellum lamina. The callus mimics the female of the pollinator and the stark color contrast between the black callus and dull green or red lamina is thought to enhance the visibility of the mimic. The goal of this study was to investigate the chemical composition and genetic regulation of temporal and spatial color patterns leading to visual mimicry, by integrating targeted metabolite profiling and transcriptomic analysis. Even at the very young bud stage, high levels of anthocyanins were detected in the dark callus, with peak accumulation by the mature bud stage. In contrast, anthocyanin levels in the lamina peaked as the buds opened and became reddish-green. Coordinated upregulation of multiple genes, including dihydroflavonol reductase and leucoanthocyanidin dioxygenase, and the downregulation of flavonol synthase genes (FLS) in the callus at the very young bud stage underpins the initial high anthocyanin levels. Conversely, within the lamina, upregulated FLS genes promote flavonol glycoside over anthocyanin production, with the downstream upregulation of flavonoid O-methyltransferase genes further contributing to the accumulation of methylated flavonol glycosides, whose levels peaked in the mature bud stage. Finally, the peak anthocyanin content of the reddish-green lamina of the open flower is underpinned by small increases in gene expression levels and/or differential upregulation in the lamina in select anthocyanin genes while FLS patterns showed little change. Differential expression of candidate genes involved in specific transport, vacuolar acidification, and photosynthetic pathways may also assist in maintaining the distinct callus and contrasting lamina color from the earliest bud stage through to the mature flower. Our findings highlight that flower color in this sexually deceptive orchid is achieved by complex tissue-specific coordinated regulation of genes and biochemical pathways across multiple developmental stages.

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Section: Introductionmentioning

confidence: 99%

Anthocyanin and Flavonol Glycoside Metabolic Pathways Underpin Floral Color Mimicry and Contrast in a Sexually Deceptive Orchid

2022

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“…The Pterostylidinae have special symbiotic relationships with mycorrhizal fungi such as Ceratobasidium spp., which are vital for successful seed germination [11,12]. The flowers of these orchids emit sex pheromones that attract male fungus gnats, which attempt to copulate with the flower and in so doing, inadvertently transfer pollen between plants [13].…”

Section: Introductionmentioning

confidence: 99%

Viruses Infecting Greenhood Orchids (Pterostylidinae) in Eastern Australia

Chao

Clements

Mackenzie

et al. 2022

Viruses

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The Australasian biogeographic realm is a major centre of diversity for orchids, with every subfamily of the Orchidaceae represented and high levels of endemism at the species rank. It is hypothesised that there is a commensurate diversity of viruses infecting this group of plants. In this study, we have utilised high-throughput sequencing to survey for viruses infecting greenhood orchids (Pterostylidinae) in New South Wales and the Australian Capital Territory. The main aim of this study was to characterise Pterostylis blotch virus (PtBV), a previously reported but uncharacterised virus that had been tentatively classified in the genus Orthotospovirus. This classification was confirmed by genome sequencing, and phylogenetic analyses suggested that PtBV is representative of a new species that is possibly indigenous to Australia as it does not belong to either the American or Eurasian clades of orthotospoviruses. Apart from PtBV, putative new viruses in the genera Alphaendornavirus, Amalgavirus, Polerovirus and Totivirus were discovered, and complete genome sequences were obtained for each virus. It is concluded that the polerovirus is likely an example of an introduced virus infecting a native plant species in its natural habitat, as this virus is probably vectored by an aphid, and Australia has a depauperate native aphid fauna that does not include any species that are host-adapted to orchids.

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“…It is not known whether Ditassa flowers are deceptive. Representatives of deceptive and pollinator-trapping plant species in other families, such as Aristolochiaceae ( Aristolochia ; [ 25 , 26 , 27 ]), Araceae ( Arisaema ; [ 28 , 29 , 30 , 31 , 32 ]), and orchids (e.g., Pleurothallis [ 33 ], Trichosalpinx [ 34 ], Lepanthes [ 35 ], Pterostylis [ 36 , 37 ]) are likewise known to be visited/pollinated by Phoridae ( Megaselia ), Sciaridae ( B radysia , Corynoptera , Pseudolycoriella ), Chloropidae ( Oscinimorpha ), and Ceratopogonidae ( Forcipomyia ). Furthermore, various economically important crops (e.g., Cacao; [ 38 ]) depend on the same dipteran families and genera for pollination.…”

Section: Discussionmentioning

confidence: 99%

Fly Pollination of Kettle Trap Flowers of Riocreuxia torulosa (Ceropegieae-Anisotominae): A Generalized System of Floral Deception

Heiduk

Meve

Menzel

et al. 2021

Plants

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Elaborated kettle trap flowers to temporarily detain pollinators evolved independently in several angiosperm lineages. Intensive research on species of Aristolochia and Ceropegia recently illuminated how these specialized trap flowers attract particular pollinators through chemical deception. Morphologically similar trap flowers evolved in Riocreuxia; however, no data about floral rewards, pollinators, and chemical ecology were available for this plant group. Here we provide data on pollination ecology and floral chemistry of R. torulosa. Specifically, we determined flower visitors and pollinators, assessed pollen transfer efficiency, and analysed floral scent chemistry. R. torulosa flowers are myiophilous and predominantly pollinated by Nematocera. Pollinating Diptera included, in order of decreasing abundance, male and female Sciaridae, Ceratopogonidae, Scatopsidae, Chloropidae, and Phoridae. Approximately 16% of pollen removed from flowers was successfully exported to conspecific stigmas. The flowers emitted mainly ubiquitous terpenoids, most abundantly linalool, furanoid (Z)-linalool oxide, and (E)-β-ocimene—compounds typical of rewarding flowers and fruits. R. torulosa can be considered to use generalized food (and possibly also brood-site) deception to lure small nematocerous Diptera into their flowers. These results suggest that R. torulosa has a less specific pollination system than previously reported for other kettle trap flowers but is nevertheless specialized at the level of Diptera suborder Nematocera.

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An unusual tricosatriene is crucial for male fungus gnat attraction and exploitation by sexually deceptive Pterostylis orchids

Cited by 22 publications

References 56 publications

Anthocyanin and Flavonol Glycoside Metabolic Pathways Underpin Floral Color Mimicry and Contrast in a Sexually Deceptive Orchid

Anthocyanin and Flavonol Glycoside Metabolic Pathways Underpin Floral Color Mimicry and Contrast in a Sexually Deceptive Orchid

Viruses Infecting Greenhood Orchids (Pterostylidinae) in Eastern Australia

Fly Pollination of Kettle Trap Flowers of Riocreuxia torulosa (Ceropegieae-Anisotominae): A Generalized System of Floral Deception

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