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Quinolizidine and Pyrrolizidine Alkaloid Chemical Ecology – a Mini-Review on Their Similarities and Differences

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Abstract

This mini-review summarizes over 40 years of research on quinolizidine (QAs) and pyrrolizidine alkaloids (PAs). Emphasis is on the chemical ecology of both groups of alkaloids, which serve as general defense compounds against herbivores for the plants producing them. For QAs and PAs, a number of insects (aphids, moths, beetles) have acquired tolerance. These specialists store the alkaloids and use them as defense chemicals against predators. In some PA sequestering moths, the adaptation is even more intricate and advanced. PAs can function as a morphogen to induce the formation of male coremata, inflatable organs that dissipate pheromones. In these insects, PAs are additionally used as a precursor for male pheromones. Female moths utilize their own PAs and those obtained from males via the spermatophore as nuptial gift, to transfer them to the eggs that thus become chemically protected. Novel genomic technologies will allow deeper insights in the molecular evolution of these two classes of alkaloids in plant-insect interactions.

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References

  • Aardema ML, Andolfatto P (2016) Phylogenetic incongruence and evolutionary origins of cardenolide-resistant forms of Na+,K+-ATPase in Danaus butterflies. Evolution 70:1913–1921

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ali JG, Agrawal AA (2012) Specialist versus generalist insect herbivores and plant defense. Trends Plant Sci 17:292–302

    Article  CAS  Google Scholar 

  • Bernays EA, Chapman RF, Hartmann T (2002) A taste receptor neurone dedicated to the perception of pyrrolizidine alkaloids in the medial galeal sensillium of two polyphagous arctiid caterpillars. Physiol Entomol 27:312–321

    Article  CAS  Google Scholar 

  • Bernays EA, Chapman RF, Lamunyon CW, Hartmann T (2003) Taste receptors for pyrrolizidine alkaloids in a monophagous caterpillar. J Chem Ecol 29:1709–1722

    Article  CAS  PubMed  Google Scholar 

  • Bezzerides A, Eisner T (2002) Apportionment of nuptial alkaloidal gifts by a multiply-mated female moth (Utetheisa ornatrix): eggs individually receive alkaloids from more than one male source. Chemoecol 12:213–218

    Article  CAS  Google Scholar 

  • Bogner F, Boppré M (1989) Single cell recordings reveal hydroxydanaidal as the volatile compound attracting insects to pyrrolizidine alkaloids. Entomol Exp Appl 50:171–184

    Article  CAS  Google Scholar 

  • Boppré M (1984) Redefining “pharmacophagy”. J Chem Ecol 10:1151–1154

    Article  PubMed  Google Scholar 

  • Boppré M (1986) Insects pharmacophagously utilising defensive plant chemicals (pyrrolizidine alkaloids). Naturwissenschaften 73:17–26

    Article  Google Scholar 

  • Cogni R, Trigo JR, Futuyma DJ (2012) A free lunch? No cost for acquiring defensive plant pyrrolizidine alkaloids in a specialist arctiid moth (Utetheisa ornatrix). Mol Ecol 21:6152–6162

    Article  CAS  PubMed  Google Scholar 

  • Conner WE, Boada R, Schroeder FC, Gonzalez A, Meinwald J, Eisner T (2000) Chemical defense: bestowal of a nuptial alkaloidal garment by a male moth on its mate. Proc Natl Acad Sci U S A 97:14406–14411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dobler S (2001) Evolutionary aspects of defense by recycled plant compounds in herbivorous insects. Basic Appl Ecol 2:15–26

    Article  CAS  Google Scholar 

  • Dobler S, Dalla S, Wagschal V, Agrawal AA (2012) Community-wide convergent evolution in insect adaptation to toxic cardenolides by substitutions in the Na,K-ATPase. Proc Natl Acad Sci U S A 109:13040–13045

    Article  PubMed  PubMed Central  Google Scholar 

  • Egelhaaf A, Cölln K, Schmitz B, Buck M, Wink M, Schneider D (1990) Organ specific storage of dietary pyrrolizidine alkaloids in the arctiid moth Creatonotos transiens. J Biosci 45 c:115–120

    Google Scholar 

  • Eisner T, Eisner M, Siegler M (2007) Secret weapons: defenses of insects, spiders, scorpions, and other many-legged creatures. Harvard University Press, Boston

    Google Scholar 

  • El-Shazly A, Wink M (2014) Structures, distribution, and biological properties of pyrrolizidine alkaloids of the Boraginaceae. Diversity 6:188–282

    Article  CAS  Google Scholar 

  • Frick KM, Kamphuis LG, Siddique KHM, Singh KB, Foley RC (2017) Quinolizidine alkaloid biosynthesis in lupins and prospects for grain quality improvement. Front Plant Sci 8:87. https://doi.org/10.3389/fpls.2017.00087

    Article  PubMed  PubMed Central  Google Scholar 

  • Gonzalez A, Rossini C, Eisner M, Eisner T (1999) Sexually transmitted chemical defense in a moth (Utetheisa ornatrix). Proc Natl Acad Sci U S A 96:5570–5574

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harborne JB (2014) Introduction to ecological biochemistry. 4th ed. Academic Press, London

  • Hartmann T (1999) Chemical ecology of pyrrolizidine alkaloids. Planta 207:483–495

    Article  CAS  Google Scholar 

  • Hartmann T (2004) Plant-derived secondary metabolites as defensive chemicals in herbivorous insects: a case study in chemical ecology. Planta 219:1–4

    Article  CAS  PubMed  Google Scholar 

  • Hartmann T (2007) From waste products to ecochemicals: fifty years research of plant secondary metabolism. Phytochemistry 68:2831–2846

    Article  CAS  PubMed  Google Scholar 

  • Hartmann T, Witte L (1995) Chemistry, biology and chemoecology of the pyrrolizidine alkaloids. In: Pelletier SW (ed) Alkaloids: Chemical and Biological Perspectives, vol 9. pp 155–233

  • Holzinger F, Wink M (1996) Mediation of cardiac glycoside insensitivity in the monarch (Danaus plexippus): role of an amino acid substitution in the ouabain binding site of Na+,K+ -ATPase. J Chem Ecol 22:1921–1937

    Article  CAS  PubMed  Google Scholar 

  • Holzinger F, Frick C, Wink M (1992) Molecular base for the insensitivity of the monarch (Danaus plexippus) to cardiac glycosides. FEBS Lett 314:477–480

    Article  CAS  PubMed  Google Scholar 

  • Käss E, Wink M (1997) Molecular phylogeny and phylogeography of the genus Lupinus (family Leguminosae) inferred from nucleotide sequences of the RbcL gene and ITS 1+2 sequences of rDNA. Plant Syst Evol 208:139–167

    Article  Google Scholar 

  • Kelly CA, Bowers MD (2016) Preference and performance of generalist and specialist herbivores on chemically defended host plants. Ecol Entomol 41:308–316

    Article  Google Scholar 

  • Laurent P, Braekman J-C Daloze D (2005) Insect chemical defense. Top Curr Chem 240:167–229

    Article  CAS  Google Scholar 

  • Lindigkeit R, Biller A, Buch M, Schiebel HM, Boppré M, Hartmann T (1997) The two faces of pyrrolizidine alkaloids: the role of the tertiary amine and its N-oxide in chemical defense of insects with acquired plant alkaloids. Eur J Biochem 245:626–636

    Article  CAS  PubMed  Google Scholar 

  • Macel M (2011) Attract and deter: a dual role for pyrrolizidine alkaloids in plant-insect interactions. Phytochem Rev 10:75–82

    Article  CAS  PubMed  Google Scholar 

  • Martins CHZ, Cunha BP, Solferini VN, Trigo JR (2015) Feeding on host plants with different concentrations and structures of pyrrolizidine alkaloids impacts the chemical defense effectiveness of a specialist herbivore. PLoS One 10(10):e0141480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mason PA, Singer MS (2015) Defensive mixology: combining acquired chemicals towards defence. Funct Ecol 29:441–450

    Article  Google Scholar 

  • Mende P, Wink M (1987) Uptake of the quinolizidine alkaloid lupanine by protoplasts and isolated vacuoles of suspension-cultured Lupinus polyphyllus cells. Diffusion or carrier-mediated transport? J Plant Physiol 129:229–242

    Article  CAS  Google Scholar 

  • Nevado B, Atchison GW, Hughes CE, Filatov DA (2016) Widespread adaptive evolution during repeated evolutionary radiations in New World lupins. Nat Commun. https://doi.org/10.1038/ncomms12384

  • Pennisi E (2017) How do gut microbes help herbivores? Counting the ways. Science 355:236

    Article  CAS  PubMed  Google Scholar 

  • Petschenka G, Agrawal AA (2016) How herbivores coopt plant defences: natural selection, specialization and sequestration. Curr Opin Insect Sci 14:17–24

    Article  PubMed  Google Scholar 

  • Schmeller T, El-Shazly A, Wink M (1997) Allelochemical activities of pyrrolizidine alkaloids: interactions with neuroreceptors and acetylcholine related enzymes. J Chem Ecol 23:399–416

    Article  CAS  Google Scholar 

  • Schneider D, Boppré M, Zweig J, Horsley SB, Bell TW, Meinwald J, Hansen K, Diehl EW (1982) Scent organ development in Creatonotos moths: regulation by pyrrolizidine alkaloids. Science 215:1264–1265

    Article  CAS  PubMed  Google Scholar 

  • Schulz S (1998) Insect-plant interactions – metabolism of plant compounds to pheromones and allomones by Lepidoptera and leaf beetles. Eur J Org Chem 1998:13–20

    Article  Google Scholar 

  • Schulz S, Francke W, Boppré M, Eisner T, Meinwald J (1993) Insect pheromone biosynthesis: Stereochemical pathway of hydroxydanaidal production from alkaloidal precursors in Creatonotos transiens (Lepidoptera, Arctiidae). Proc Natl Acad Sci U S A 90:6834–6838

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trigo JR (2011) Effects of pyrrolizidine alkaloids through different trophic levels. Phytochem Rev 10:83–98

    Article  CAS  Google Scholar 

  • Vleugels R, Verlinden H, van den Broeck J (2015) Serotonin, serotonin receptors and their action in insects. Neurotransmitter 2:e314

    Google Scholar 

  • von Nickisch-Rosenegk E, Wink M (1993) Sequestration of pyrrolizidine alkaloids in several arctiid moths (Lepidoptera: Arctiidae). J Chem Ecol 19:1889–1903

    Article  Google Scholar 

  • von Nickisch-Rosenegk E, Schneider D, Wink M (1990) Time-course of pyrrolizidine alkaloid processing in the alkaloid exploiting arctiid moth, Creatonotos transiens. J Biosci 45(c):881–894

    Google Scholar 

  • Wang L, Beuerle T, Timbilla J, Ober D (2012) Independent recruitment of a flavin-dependent monooxygenase for safe accumulation of sequestered pyrrolizidine alkaloids in grasshoppers and moths. PLoS One 7(2):e31796

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wink M (1984) N-methylation of quinolizidine alkaloids: an S-adenosyl-L-methionine: cytisine N-methyltransferase from Laburnum anagyroides plants and cell cultures of L. alpinum and Cytisus canariensis. Planta 161:339–344

    Article  CAS  PubMed  Google Scholar 

  • Wink M (1988) Plant breeding: importance of plant secondary metabolites for protection against pathogens and herbivores. Theor Appl Genet 75:225–233

    Article  CAS  Google Scholar 

  • Wink M (1992) The role of quinolizidine alkaloids in plant insect interactions. In: Bernays EA (ed) Insect- plant interactions, vol IV. CRC-Press, Boca Raton, pp 133–169

    Google Scholar 

  • Wink M (1993) In: Waterman P (ed) Quinolizidine alkaloids: In methods in plant biochemistry, vol 8. Academic Press, London, pp 197–239

    Google Scholar 

  • Wink M (2000) Interference of alkaloids with neuroreceptors and ion channels. Bioactive Nat Prod 21:3–129

    Article  CAS  Google Scholar 

  • Wink M (2003) Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective. Phytochemistry 64:3–19

    Article  CAS  PubMed  Google Scholar 

  • Wink M (2018) Plant secondary metabolites modulate insect behaviour- steps towards addiction? Front Physiol 9:364. https://doi.org/10.3389/fphys.2018.00364

    Article  PubMed  PubMed Central  Google Scholar 

  • Wink M, Hartmann T (1978) Cadaverine-pyruvate transamination: the pricipal step of enzymatic quinolizidine alkaloid biosynthesis in Lupinus polyphyllus cell suspension cultures. FEBS Lett 101:343–346

    Article  Google Scholar 

  • Wink M, Hartmann T (1982a) Enzymatic synthesis of alkaloid esters: a tigloyl-CoA: 13-hydroxylupanine O-tigloyl transferase from Lupinus albus. Planta 156:560–565

    Article  CAS  PubMed  Google Scholar 

  • Wink M, Hartmann T (1982b) Localization of the enzymes of quinolizidine alkaloid biosynthesis in leaf chloroplasts of Lupinus polyphyllus. Plant Physiol 70:74–77

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wink M, Römer P (1986) Acquired toxicity- the advantages of specializing on alkaloid-rich lupins to Macrosiphum albifrons (Aphidae). Naturwissenschaften 73:210–212

    Article  CAS  Google Scholar 

  • Wink M, Schneider D (1988) Carrier-mediated uptake of pyrrolizidine alkaloids in larvae of the aposematic and alkaloid exploiting moth, Creatonotos. Naturwissenschaften 75:524–525

    Article  CAS  Google Scholar 

  • Wink M, Schneider D (1990) Fate of plant-derived secondary metabolites in three moth species (Syntomis mogadorensis, Syntomeida epilais, and Creatonotos transiens). J Comp Physiol B 160:389–400

    Article  CAS  Google Scholar 

  • Wink M, Hartmann T, Schiebel HM (1979) A model mechanism for the enzymatic synthesis of lupin alkaloids. Z Naturforsch 34c:704–708

    Article  CAS  Google Scholar 

  • Wink M, Schneider D, Witte L (1988) Biosynthesis of pyrrolizidine alkaloid-derived pheromones in the arctiid moth, Creatonotos transiens: Stereochemical conversion of heliotrine. J Biosci 43c:737–741

    Google Scholar 

  • Wink M, Monttlor C, Bernays EA, Witte L (1991) Uresiphita reversalis (Lepidoptera: Pyralidae): carrier-mediated uptake and sequestration of quinolizidine alkaloids obtained from the host plant Teline monspessulana. Z Naturforsch 46c:1080–1088

    Google Scholar 

  • Wink M, Meißner C, Witte L (1995) Patterns of quinolizidine alkaloids in 56 species of the genus Lupinus. Phytochemistry 38:139–153

    Article  CAS  Google Scholar 

  • Wink M, Schmeller T, Latz-Brüning B (1998) Modes of action of allelochemical alkaloids: interaction with neuroreceptors, DNA and other molecular targets. J Chem Ecol 24:1881–1937

    Article  CAS  Google Scholar 

  • Wink M, Botschen F, Gosmann C, Schäfer H, Waterman PG (2010) Chemotaxonomy seen from a phylogenetic perspective and evolution of secondary metabolism. In: Wink M (ed) Biochemistry of plant secondary metabolism. Blackwell, Oxford, Annual Plant Reviews, vol 40. pp 364–433

  • Zagrobelny M, Moller BL (2011) Cyanogenic glucosides in the biological warfare between plants and insects: the Burnet moth- Birdsfoot trefoil model system. Phytochemistry 72:1585–1592

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

Thomas Hartmann was my PhD supervisor at the Technical University of Braunschweig between 1977 and 1980. From 1980 to 1985 he was a mentor for my Post-Doc studies leading to my habilitation in 1985. I am always thankful to Thomas Hartmann that he had lured me away from zoology into botany and pharmaceutical biology for my PhD studies. What both of us did not know at that time, was that we would develop a serious interest in chemical ecology and the functional aspects of plant alkaloids and various trophic levels. After 40 years of endeavour, I am happy to say that this deviation was worth it.

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  1. Heidelberg University, Institute of Pharmacy and Molecular Biotechnology, INF 364, D-69120, Heidelberg, Germany

    Michael Wink

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Wink, M. Quinolizidine and Pyrrolizidine Alkaloid Chemical Ecology – a Mini-Review on Their Similarities and Differences. J Chem Ecol 45, 109–115 (2019). https://doi.org/10.1007/s10886-018-1005-6

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