Co-evolution of cyanogenic glucosides in Zygaena larvae and Lotus plants
For more than 420 million years, plants, insects and their predators have co-evolved based on a chemical arms race including deployment of refined chemical defence systems by each player. Herbivorous insects evolve strategies to circumvent the plants chemical defence systems, e.g. by detoxification. The ability to evade the chemical defence system of a particular plant species enables an insect to develop an advantageous niche with few competitors.
In some cases, insects are able to de novo biosynthesize the same or similar defence compounds as the feed plant, which is why they are immediately able to handle the defence compounds when they encounter the plant. These insects use the compounds in their own defence against predators. If the insects develop an ability to sequester the particular compounds from the feed plant, the interaction may become highly beneficial for the insects, as they save energy in their own metabolism and can then grow faster.
We work with the model system of the six-spotted burnet moth (Zygaena filipendulae) and its food plant Lotus corniculatus. Both the plant and the insect contain the cyanogenic glucosides linamarin and lotaustralin which liberate toxic hydrogen cyanide upon breakdown. Moths belonging to the Zygaena family are the only insects known, able to carry out both de novo biosynthesis and sequestration of the same cyanogenic glucosides as those from their food plants.
Linamarin and lotaustralin are used for defense by Z. filipendulae but have also evolved several important functions in the insect life cycle. We have shown the transfer of a nuptial gift of cyanogenic glucosides during mating of Z. filipendulae as well as the possible involvement of hydrogen cyanide in mate attraction and nitrogen metabolism (Zagrobelny et al., 2007a; Zagrobelny et al., 2007b; Zagrobelny et al., 2013a).
The ratio and content of cyanogenic glucosides is tightly regulated in Z. filipendulae, and Zygaena larvae prefer to feed on highly cyanogenic Lotus plants over lowly cyanogenic or acyanogenic Lotus plants, probably to optimize the amount of cyanogenic glucosides available for sequestering (Zagrobelny et al., 2007b). We have also demonstrated that cyanogenic glucosides are taken up intact during sequestration by Z. filipendulae and are rapidly distributed to all tissues, mingling freely with cyanogenic glucosides originating from biosynthesis (Zagrobelny et al., 2013b).
We have solved the biosynthetic pathway of cyanogenic glucosides in Z. filipendulae, and by phylogenetic analysis of the underlying genes, we found that even though plants and the burnet moth larvae synthesize cyanogenic glucosides in essentially the same way using the same enzyme systems, the pathways have evolved convergently (independently) in the two kingdoms (Takos et al., 2011; Jensen et al., 2011).
The elucidation at the molecular level of how an insect have evolved to de novo biosynthesize the exact same natural products as is present in its food plant, what roles the compounds play in the insect life-cycle, and how the insect regulates de novo biosynthesis versus sequestration is the first example of its kind.
- Jensen N.B., Zagrobelny M., Hjernø K., Olsen C.E., Houghton-Larsen J., Borch J., Møller B.L., Bak S. (2011) Convergent evolution in biosynthesis of cyanogenic defence compounds in plants and insects. Nat.Commun. 2, DOI: 10.1038/ncomms1271.
- Pentzold S., Zagrobelny M., Roelsgaard P.S., Møller B.L., Bak S. (2014) The multiple strategies of an insect herbivore to overcome plant cyanogenic glucoside defence. PLoS ONE 9(3): e91337. doi:10.1371/journal.pone.0091337
- Pentzold S., Zagrobelny M., Rook F., Bak S. (2014) How insects overcome two-component plant chemical defence: plant β-glucosidases as the main target for herbivore adaptation. Biological Reviews (doi:10.1111/brv.12066)
- Takos A.M., Knudsen C., Lai D., Kannangara R., Mikkelsen L., Motawia M.S., Olsen C.E., Sato S., Tabata S., Jørgensen K., Møller B.L., Rook F. (2011) Genomic clustering of cyanogenic glucoside biosynthetic genes aids their identification in Lotus japonicus and suggests the repeated evolution of this chemical defence pathway. Plant J. 68, 273-286.
- Zagrobelny M., Bak S., Ekstrøm C.T., Olsen C.E., Møller B.L. (2007a) The cyanogenic glucoside composition of Zygaena filipendulae (Lepidoptera: Zygaenidae) as effected by feeding on wild-type and transgenic lotus populations with variable cyanogenic glucoside profiles. Insect Biochem. Mol. Biol. 37, 10-18.
- Zagrobelny M., Motawie M.S., Olsen C.E., Bak S., Møller B.L. (2013a) Male-to-female transfer of 5-hydroxytryptophan glucoside during mating in Zygaena filipendulae (Lepidoptera). Insect Biochem. Mol. Biol. 43, 1037-1044.
- Zagrobelny M., Motawie M.S., Olsen C.E., Pentzold S., Fürstenberg-Hägg J., Bak S., Møller B.L. (2013b) Sequestration, tissue distribution and developmental transmission of cyanogenic glucosides in a specialist insect herbivore. Insect Biochem. Mol. Biol. In Press.
- Zagrobelny M., Olsen C.E., Bak S., Møller B.L. (2007b) Intimate roles for cyanogenic glucosides in the life cycle of Zygaena filipendulae (Lepidoptera, Zygaenidae). Insect Biochem. Mol. Biol. 37, 1189-1197.