Spatial separation of the cyanogenic β-glucosidase ZfBGD2 and cyanogenic glucosides in the haemolymph of Zygaena larvae facilitates cyanide release
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Spatial separation of the cyanogenic β-glucosidase ZfBGD2 and cyanogenic glucosides in the haemolymph of Zygaena larvae facilitates cyanide release. / Pentzold, Stefan; Jensen, Mikael Kryger; Matthes, Annemarie; Olsen, Carl Erik; Petersen, Bent L; Clausen, Henrik; Møller, Birger Lindberg; Bak, Søren; Zagrobelny, Mika.
In: Royal Society Open Science, Vol. 4, 170262, 2017.Research output: Contribution to journal › Journal article › Research › peer-review
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T1 - Spatial separation of the cyanogenic β-glucosidase ZfBGD2 and cyanogenic glucosides in the haemolymph of Zygaena larvae facilitates cyanide release
AU - Pentzold, Stefan
AU - Jensen, Mikael Kryger
AU - Matthes, Annemarie
AU - Olsen, Carl Erik
AU - Petersen, Bent L
AU - Clausen, Henrik
AU - Møller, Birger Lindberg
AU - Bak, Søren
AU - Zagrobelny, Mika
PY - 2017
Y1 - 2017
N2 - Low molecular weight compounds are typically used by insects and plants for defence against predators. They are often stored as inactive β-glucosides and kept separate from activating β-glucosidases. When the two components are mixed, the β-glucosides are hydrolysed releasing toxic aglucones. Cyanogenic plants contain cyanogenic glucosides and release hydrogen cyanide due to such a well-characterized two-component system. Some arthropods are also cyanogenic, but comparatively little is known about their system. Here, we identify a specific β-glucosidase (ZfBGD2) involved in cyanogenesis from larvae of Zygaena filipendulae (Lepidoptera, Zygaenidae), and analyse the spatial organization of cyanide release in this specialized insect. High levels of ZfBGD2 mRNA and protein were found in haemocytes by transcriptomic and proteomic profiling. Heterologous expression in insect cells showed that ZfBGD2 hydrolyses linamarin and lotaustralin, the two cyanogenic glucosides present in Z. filipendulae. Linamarin and lotaustralin as well as cyanide release were found exclusively in the haemoplasma. Phylogenetic analyses revealed that ZfBGD2 clusters with other insect β-glucosidases, and correspondingly, the ability to hydrolyse cyanogenic glucosides catalysed by a specific β-glucosidase evolved convergently in insects and plants. The spatial separation of the β-glucosidase ZfBGD2 and its cyanogenic substrates within the haemolymph provides the basis for cyanide release in Z. filipendulae. This spatial separation is similar to the compartmentalization of the two components found in cyanogenic plant species, and illustrates one similarity in cyanide-based defence in these two kingdoms of life.
AB - Low molecular weight compounds are typically used by insects and plants for defence against predators. They are often stored as inactive β-glucosides and kept separate from activating β-glucosidases. When the two components are mixed, the β-glucosides are hydrolysed releasing toxic aglucones. Cyanogenic plants contain cyanogenic glucosides and release hydrogen cyanide due to such a well-characterized two-component system. Some arthropods are also cyanogenic, but comparatively little is known about their system. Here, we identify a specific β-glucosidase (ZfBGD2) involved in cyanogenesis from larvae of Zygaena filipendulae (Lepidoptera, Zygaenidae), and analyse the spatial organization of cyanide release in this specialized insect. High levels of ZfBGD2 mRNA and protein were found in haemocytes by transcriptomic and proteomic profiling. Heterologous expression in insect cells showed that ZfBGD2 hydrolyses linamarin and lotaustralin, the two cyanogenic glucosides present in Z. filipendulae. Linamarin and lotaustralin as well as cyanide release were found exclusively in the haemoplasma. Phylogenetic analyses revealed that ZfBGD2 clusters with other insect β-glucosidases, and correspondingly, the ability to hydrolyse cyanogenic glucosides catalysed by a specific β-glucosidase evolved convergently in insects and plants. The spatial separation of the β-glucosidase ZfBGD2 and its cyanogenic substrates within the haemolymph provides the basis for cyanide release in Z. filipendulae. This spatial separation is similar to the compartmentalization of the two components found in cyanogenic plant species, and illustrates one similarity in cyanide-based defence in these two kingdoms of life.
KW - Journal Article
U2 - 10.1098/rsos.170262
DO - 10.1098/rsos.170262
M3 - Journal article
C2 - 28680679
VL - 4
JO - Royal Society Open Science
JF - Royal Society Open Science
SN - 2054-5703
M1 - 170262
ER -
ID: 180936482