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Sequestration and Biosynthesis of Cyanogenic Glucosides in Passion Vine Butterflies and Consequences for the Diversification of Their Host Plants

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Sequestration and Biosynthesis of Cyanogenic Glucosides in Passion Vine Butterflies and Consequences for the Diversification of Their Host Plants Sequestration and biosynthesis of cyanogenic glucosides in passion vine butterflies and consequences for the diversification of their host plants Pinheiro de Castro, Érika C.; Zagrobelny, Mika; Zurano, Juan Pablo; Zikan Cardoso, Márcio; Feyereisen, René; Bak, Søren Published in: Ecology and Evolution DOI: 10.1002/ece3.5062 Publication date: 2019 Document version Publisher's PDF, also known as Version of record Document license: CC BY Citation for published version (APA): Pinheiro de Castro, É. C., Zagrobelny, M., Zurano, J. P., Zikan Cardoso, M., Feyereisen, R., & Bak, S. (2019). Sequestration and biosynthesis of cyanogenic glucosides in passion vine butterflies and consequences for the diversification of their host plants. Ecology and Evolution, 9(9), 5079-5093. https://doi.org/10.1002/ece3.5062 Download date: 02. okt.. 2021 Received: 18 August 2018 | Revised: 13 January 2019 | Accepted: 26 February 2019 DOI: 10.1002/ece3.5062 ORIGINAL RESEARCH Sequestration and biosynthesis of cyanogenic glucosides in passion vine butterflies and consequences for the diversification of their host plants Érika C. Pinheiro de Castro1 | Mika Zagrobelny1 | Juan Pablo Zurano2 | Márcio Zikan Cardoso3 | René Feyereisen1 | Søren Bak1 1Department of Plant and Environmental Sciences, University of Copenhagen, Abstract Frederiksberg C, Copenhagen, Denmark The colorful heliconiine butterflies are distasteful to predators due to their content 2 Department of Systematic and of defense compounds called cyanogenic glucosides (CNglcs), which they biosynthe‐ Ecology, Federal University of Paraiba, João Pessoa, Paraíba, Brazil size from aliphatic amino acids. Heliconiine larvae feed exclusively on Passiflora plants 3Department of Ecology, Federal University where ~30 kinds of CNglcs have been reported. Among them, some CNglcs derived of Rio Grande do Norte, Natal, Rio Grande do Norte, Brazil from cyclopentenyl glycine can be sequestered by some Heliconius species. In order to understand the evolution of biosynthesis and sequestration of CNglcs in these Correspondence Søren Bak, Department of Plant and butterflies and its consequences for their arms race with Passiflora plants, we ana‐ Environmental Sciences, University of lyzed the CNglc distribution in selected heliconiine and Passiflora species. Copenhagen, Frederiksberg C, Copenhagen, Denmark. Sequestration of cyclopentenyl CNglcs is not an exclusive trait of Heliconius, since Email: [email protected] these compounds were present in other heliconiines such as Philaethria, Dryas and Funding information Agraulis, and in more distantly related genera Cethosia and Euptoieta. Thus, it is likely Independent Research Fund Denmark | that the ability to sequester cyclopentenyl CNglcs arose in an ancestor of the Natural Sciences, Grant/Award Number: 1323‐00088; Brazilian National Council Heliconiinae subfamily. Biosynthesis of aliphatic CNglcs is widespread in these but‐ for Scientific Development (CNPq), Grant/ terflies, although some species from the sara‐sapho group seem to have lost this abil‐ Award Number: 306985/2013-6 ity. The CNglc distribution within Passiflora suggests that they might have diversified their cyanogenic profile to escape heliconiine herbivory. This systematic analysis im‐ proves our understanding on the evolution of cyanogenesis in the heliconiine–Passi‐ flora system. KEYWORDS coevolution, cyanide, Heliconius, Lepidoptera, Passiflora, specialized metabolites 1 | INTRODUCTION evolved under the selection pressure from the chemical defenses of their hosts and adapted to handle their toxicity and even to utilize Land plants have been exposed to herbivores for over 430 million these metabolites for their own benefit (Nishida, 2014). years. To cope with this, plants produce a remarkable diversity of spe‐ The distasteful and colorful butterflies of the Heliconiini tribe cialized metabolites that act as chemical protections (Fürstenberg‐ selectively feed as larvae on plants from the Passiflora genus re‐ Hägg, Zagrobelny, & Bak, 2013). In turn, specialist herbivores have gardless of the plants’ chemical defenses which, effective against This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2019 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. Ecology and Evolution. 2019;9:5079–5093. www.ecolevol.org | 5079 5080 | PINHEIRO DE CASTRO et AL. most other herbivores. Due to their larval‐feeding specialization, that the ability to detoxify CNglcs preceded their ability to sequester heliconiines are also called passion vine butterflies. The species these compounds and perhaps even older than the ability to biosyn‐ diversity (more than 70 heliconiine and 600 passion vines) and thesize them (de Castro et al., 2018). multiplicity of feeding guilds found in the heliconiine–Passiflora CNglcs are some of the most ancient and widespread defense system offer a unique comparative potential to address many in‐ compounds produced by plants: Whereas other defense compounds triguing questions on evolutionary and chemical ecology (Gilbert, are typically restricted to a specific plant group, such as glucosino‐ 1991; Jiggins, 2017). The basal heliconiine genera Podotricha, lates in Brassicaceae, CNglcs are broadly distributed in 2,500 species Philaethria, Dryas, Dryadula, Dione, Agraulis, and Eueides (Kozak from ferns to flowering families (Gleadow & Møller, 2014). In insects, et al., 2015) are overall generalists, feeding on many Passiflora CNglc distribution is restricted to a few lineages within Coleoptera species. In contrast, different degrees of host specialization are and Hemiptera, which seem to obtain these compounds from their observed within Heliconius, the most diverse heliconiine genus, diet, and to some lepidopterans (moths and butterflies) where both with some close phylogenetic associations between infragenic biosynthesis and/or sequestration is rather widespread (Zagrobelny, groups of Heliconius and their Passiflora hosts (Arias et al., 2016; Castro, Møller, & Bak, 2018). Engler‐Chaouat & Gilbert, 2007). Heliconius species that perform CNglcs are glycosylated cyanide‐containing compounds that are pupal mating (erato and sara‐sapho groups), an unusual behavior not intrinsically poisonous as glucosides. However, tissue damage where adult males search for female pupae for mating and either caused by, for example, herbivore or predator attack leads to CNglcs penetrate the pupa or mate the female as soon as it emerges, are coming in contact with hydrolytic enzymes (β‐glucosidases and α‐hy‐ characterized by being specialists on Passiflora plants of the sub‐ droxynitrile lyases), which convert these compounds into toxic hy‐ genera Decaloba or Astrophea. Species of melpomene, silvaniforms, drogen cyanide (HCN) and aglycones (Pentzold et al., 2017). Protein and primitive groups (aoede, doris, wallacei), which comprise the and nonprotein amino acids are precursors for the biosynthesis of nonpupal mating clade, are overall specialists on Passiflora species CNglcs and can accordingly be classified as aliphatic, aromatic, or of the subgenus Passiflora (Benson, Brown, & Gilbert, 1975). cyclopentenoid (Figure 1). The aromatic and aliphatic CNglcs are The chemical defense of the genus Passiflora is comprised of dif‐ derived from protein amino acids like phenylalanine and valine and ferent types of cyanogenic glucosides (CNglcs), and the great suc‐ are broadly distributed in the Plant Kingdom (Zagrobelny et al., cess of heliconiines feeding on Passiflora could be due to the prior 2004). Contrarily, cyclopentenyl CNglcs are synthesized from the ability of these butterflies to biosynthesize CNglcs (Nahrstedt & nonprotein amino acid cyclopentenyl glycine and have been so far Davis, 1981). Subsequently, it has been hypothesized that the ability found in five closely related plant families of the Order Malpighiales: to handle the toxicity of CNglcs was one of the crucial traits that al‐ Passifloraceae, Turneraceae, Achariaceae, Salicaceae, and Violaceae lowed the ancestor of heliconiines to feed on these plants, implying (Bjarnholt et al., 2008; Tober & Conn, 1985). OH OH GlcO GlcO OH GlcO OH GlcO OH NC NC NC NC Tetraphyllin A (S) Gynocardin (1S, 4R)Dihydrogynocardin (1S,4R) Epivolkenin (1S, 4R) Deidaclin (R) Teraktophyllin (1R, 4S) Tetraphyllin B (1S, 4S) Volkenin (1R, 4R) CH3 HC3 CH3 HC3 GlcO OR RO OSOO2 NC NC RO CN RO CN (1S, 4R) (1S, 4R) R: Ant = Passibiflorin R: Glc = Tetraphylin B sulphate S R: Glc = Linamarin R: Glc = Lotaustralin R: Bov = Passicapsin R: Rha-Glc = Passicoccin S R: Glc-Glc = Linustatin R: Glc-Glc = Neolinustatin R: Alo = Passitrifasciatin Aromatics R: Glc = Prunasin Sugar Residue Abbreviations RO R: Alo = Passiedulin Aliphatics Glc: glucosyl Rha: rhamnosyl Alo: allosyl R: Glc-Glc = Amygdalin NC Cyclopentenoids Ant: antiarosyl Bov: bocinosyl H R: Rha-Glc = unamed FIGURE 1 Cyanogenic glucoside (CNglcs) structures reported in Passiflora species. Compounds with a gray background were also reported in heliconiines butterflies (Nahrstedt & Davis, 1981; Engler, Spencer, & Gilbert, 2000). Structures with name in gray are enantiomers PINHEIRO DE CASTRO et AL. | 5081 The biosynthetic pathway of aromatic and aliphatic CNglcs has sequester cyclopentenyl CNglcs from Passiflora. The analyses of the been characterized in several plant species. For example, in Lotus cyanogenic potential of Heliconius and other heliconiine species have japonicus the
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