Abstract
Staining and histochemistry of volatile organic compounds (VOCs) were performed at different inflorescence developmental stages on nine aroid species; one temperate, Arum italicum and eight tropical from the genera Caladium, Dieffenbachia and Philodendron. Moreover, a qualitative and quantitative analysis of VOCs constituting the scent of A. italicum, depending on the stage of development of inflorescences was also conducted. In all nine species, vesicles were observed in the conical cells of either the appendix or the stamens (thecae) and the staminodes. VOCs were localised in intracellular vesicles from the early stages of inflorescence development until their release during receptivity of gynoecium. This localisation was observed by the increase of both number and diameter of the vesicles during 1 week before receptivity. Afterwards, vesicles were fewer and smaller but rarely absent. In A. italicum, staining and gas chromatography analyses confirmed that the vesicles contained terpenes. The quantitatively most important ones were the sesquiterpenes, but monoterpenes were not negligible. Indeed, the quantities of terpenes matched the vesicles’ size evolution during 1 week. Furthermore, VOCs from different biosynthetic pathways (sesquiterpenes and alkanes) were at their maximum quantity 2 days before gynoecium receptivity (sesquiterpenes and alkanes) or during receptivity (isobutylamine, monoterpenes, skatole and p-cresol). VOCs seemed to be emitted during gynoecium receptivity and/or during thermogenesis, and FADs are accumulated after thermogenesis in the spadix. These complex dynamics of the different VOCs could indicate specialisation of some VOCs and cell machinery to attract pollinators on the one hand and to repulse/protect against phytophagous organisms and pathogens after pollination on the other hand.
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Abbreviations
- ANOVA:
-
Univariate analysis of variance
- GC-MS:
-
Gas chromatography linked to mass spectrometry
- HRMAS:
-
High-resolution magic angle spinning
- NaDi:
-
1-Naphtol and N,N-dimethyl-p-phenylenediamine
- NMR:
-
Nuclear magnetic resonance
- NPMANOVA:
-
Non-parametric multivariate analysis of variance
- OPLS-DA:
-
Orthogonal projections to latent structures discriminant analysis
- VOC:
-
Volatile organic compound
References
Albre J, Quilichini A, Gibernau M (2003) Pollination ecology of Arum italicum (Araceae). Bot J Linn Soc 141:205–214
Angioy A-M, Stensmyr C, Urru I, Puliafito M, Collu I, Hansson BS (2004) Function of the heater: the dead horse arum revisited. Proc R Soc London B 271:S13–S15
Barabé D, Gibernau M, Forest F (2002) Zonal thermogenetic dynamics of two Philodendron species from two different subgenera (Araceae). Bot J Linn Soc 139:79–86
Bröderbauer D, Weber A, Diaz A (2013) The design of trapping devices in pollination traps of the genus Arum (Araceae) is related to insect type. Bot J Linn Soc 172:385–397
Caissard J-C, Joly C, Bergougnoux V, Hugueney P, Mauriat M, Baudino S (2004a) Secretion mechanisms of volatile organic compounds in specialized cells of aromatic plants. Rec Res Dev Cell Biol 2:1–15
Caissard J-C, Meekkijjiroenroj A, Baudino S, Anstett MC (2004b) Production and emission of pollinator attractant on leaves of Chamaerops humilis (Arecaceae). Am J Bot 91:1190–1199
Chartier M, Pélozuelo P, Gibernau M (2011) Do floral odor profiles geographically vary with the degree of specificity for pollinators? Investigation in two sapromyophilous Arum species (Araceae). Ann Soc Entomol Fr 47:71–77
Chartier M, Pélozuelo P, Buatois B, Bessière J-M, Gibernau M (2013) Geographic variations of odour and pollinators, and test for local adaptation by reciprocal transplant of two European Arum species (Araceae). Funct Ecol 27:1367–1381
Chartier M, Gibernau M, Renner SS (2014) The evolution of pollinator/plant interaction types in the Araceae. Evolution 68:1533–1543
David R, Carde J-P (1964) Coloration différentielle des inclusions lipidiques et terpéniques des pseudophylles du Pin maritime au moyen du réactif nadi. CR Acad Sci Paris 258:1338–1340
Diaz A, Kite GC (2002) A comparison of the pollination ecology of Arum maculatum and A. italicum in England. Watsonia 24:171–181
Diaz A, Kite GC (2006) Why be a rewarding trap? The evolution of floral rewards in Arum (Araceae), a genus characterized by saprophilous pollination systems. Biol J Linn Soc 88:257–268
Dötterl S, David A, Boland W, Silberbauer-Gottsberger I, Gottsberger G (2012) Evidence for behavioral attractiveness of methoxylated aromatics in a dynastid scarab beetle-pollinated Araceae. J Chem Ecol 38:1539–1543
Effmert U, Buss D, Rohrbeck D, Piechulla B (2006) Localization of the synthesis and emission of scent compounds within the flower. In: Dudareva N, Pichersky P (eds) Biology of floral scent. Taylor and Francis Group, Boca Raton, pp 105–124
Fahn A (1988) Secretory tissues in vascular plants. New Phytol 108:229–257
Flanagan KA, Webb W, Stowers L (2011) Analysis of male pheromones that accelerate female reproductive organ development. PLoS One 6:e16660
Frey M, Chomet E, Glawischnig E, Stettner C, Grün S, Winklmair A, Eisenreich W, Bacher A, Meeley RB, Briggs SP, Simcox K, Gierl A (1997) Analysis of a chemical plant defense mechanism in grasses. Science 277:696–699
Garg RP, Qian XL, Alemany LB, Moran S, Parry RJ (2008) Investigations of valanimycin biosynthesis elucidation of the role of seryl t-RNA. Proc Natl Acad Sci U S A 105:6543–6547
Gibernau M (2003) Pollinators and visitors of Aroid inflorescences. Aroideana 26:66–83
Gibernau M (2011) Pollinators and visitors of aroid inflorescences: an addendum. Aroideana 34:70–83
Gibernau M, Barabé D, Cerdan P, Dejean A (1999) Beetle pollination of Philodendron solimoesense (Araceae) in French Guiana. Int J Plant Sci 160:1135–1143
Gibernau M, Macquart D, Przetak G (2004a) Pollination in the genus Arum, a review. Aroideana 27:148–166
Gibernau M, Favre C, Talou T, Raynaud C (2004b) Floral odour of Arum italicum. Aroideana 27:142–147
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:1–9
Hudak KA, Thompson JE (1997) Subcellular localization of secondary lipid metabolites including fragrance volatiles in carnation petals. Plant Physiol 114:705–713
Hudak KA, Madey E, Hong Y, Su L, Thompson JE (2000) Immunopurification of H+-ATPase-containing lipid-protein particles from the cytosol of carnation petals. Physiol Plant 109:304–312
Ibanez S, Dötterl S, Anstett M-C, Baudino S, Caissard J-C, Gallet C, Després L (2010) The role of volatile organic compounds, morphology and pigments of globeflowers in the attraction of their specific pollinating flies. New Phytol 188:451–463
Kite GC, Hetterscheid WLA, Lewis MJ, Boyce PC, Ollerton J, Cocklin E, Diaz A, Simmonds MSJ (1998) Inflorescence odours and pollinators of Arum and Amorphophallus (Araceae). In: Owens SJ, Rudall PJ (eds) Reproductive biology. Royal Botanical Gardens, Kew, pp 295–315
Knudsen JT, Tollsten L, Bergström LG (1993) Floral scents—a checklist of volatile compounds isolated by head-space techniques. Phytochemistry 33:253–280
Knudsen JT, Eriksson R, Gershenzon J, Ståhl B (2006) Diversity and distribution of floral scent. Bot Rev 72:1–120
Leport L, Larher F (1991) La proline; marqueur de fertilité et précurseur d’amines chez Arum maculatum L. CR Acad Sci Paris 312:567–572
Maia ACD, Schlindwein C (2006) Caladium bicolor (Araceae) and Cyclocephala celata (Coleoptera, Dynastinae): a well-established pollination system in the Northern Atlantic rainforest of Pernambuco, Brazil. Plant Biol 8:529–534
Maia ACD, Schlindwein C, do Amaral Ferraz Navarro DM, Gibernau M (2010) Pollination of Philodendron acutatum (Araceae) in the Atlantic Forest of northeastern Brazil: a single scarab beetle species guarantees high fruit set. Int J Plant Sci 171:740–748
Maia ACD, Dötterl S, Kaiser R, Silberbauer-Gottsberger I, Teichert H, Gibernau M, do Amaral Ferraz Navarro DM, Schlindwein C, Gottsberger G (2012) The key role of 4-methyl-5-vinylthiazole in the attraction of scarab beetle pollinators: a unique olfactory floral signal shared by Annonaceae and Araceae. J Chem Ecol 38:1072–1080
Maia ACD, Gibernau M, Dötterl S, do Amaral Ferraz Navarro DM, Seifert K, Müller T, Schlindwein C (2013) The floral scent of Taccarum ulei (Araceae): attraction of scarab beetle pollinators to an unusual aliphatic acyloin. Phytochemistry 93:71–78
Marinho CR, Souza CD, Barros TC, Teixeira SP (2014) Scent glands in legume flowers. Plant Biol 16:215–226
Ni J-Q, Robarge WP, Xiao C, Heber AJ (2012) Volatile organic compounds at swine facilities: a critical review. Chemosphere 89:769–788
Nicolè F, Guitton Y, Courtois EA, Moja S, Legendre L, Hossaert-McKey M (2012) MSeasy: unsupervised and untargeted GC-MS data processing. Bioinformatics 28:2278–2280
Partridge M, Murphy DJ (2009) Roles of a membrane-bound caleosin and putative peroxygenase in biotic and abiotic stress responses in Arabidopsis. Plant Physiol Biochem 47:796–806
Pereira J, Schlindwein C, Antonini Y, Maia ACD, Dötterl S, Martins C, Navarro DMDAF, Oliveira R (2014) Philodendron adamantinum (Araceae) lures its single cyclocephaline scarab pollinator with specific dominant floral scent volatiles. Biol J Linn Soc 111:679–691
Quilichini A, Macquart D, Barabé D, Albre J, Gibernau M (2010) Reproduction of the West Mediterranean endemic Arum pictum (Araceae) on Corsica. Plant Syst Evol 287:179–187
Robacker DC, Flath RA (1995) Attractants from Staphylococcus aureus cultures for Mexican fruit fly, Anastrepha ludens. J Chem Ecol 21:1861–1874
Rosahl S, Feussner I (2005) Oxylipins. In: Murphy DJ (ed) Plant lipids, biology, utilisation, and manipulation. Blackwell, Oxford, pp 329–354
Schwerdtfeger M, Gerlach G, Kaiser R (2002) Anthecology in the Neotropical genus Anthurium (Araceae): a preliminary report. Selbyana 23:258–267
Seymour RS, Gibernau M (2008) Respiration of thermogenic inflorescences of Philodendron melinonii: natural pattern and responses to experimental temperatures. J Exp Bot 59:1353–1362
Shimada TL, Takano Y, Shimada T, Fujiwara M, Fukao Y, Mori M, Okazaki Y, Saito K, Sasaki R, Aoki K, Hara-Nishimura I (2013) Leaf oil body as a subcellular factory for the production of a phytoalexin in Arabidopsis. Plant Physiol 164:106–118
Simon EW (1962) Valine decarboxylation in Arum spadix. J Exp Bot 13:1–4
Skubatz H, Kunkel DD (1999) Further study of the glandular tissue of the Sauromatum guttatum (Araceae) appendix. Am J Bot 86:841–854
Skubatz H, Meeuse BJD, Bendich AJ (1989) Oxidation of proline and glutamate by mitochondria of Voodoo lily (Sauromatum guttatum). Plant Physiol 91:530–535
Skubatz H, Kunkel DD, Patt JM, Howald WN, Hartman TG, Meeuse BJD (1995) Pathway of terpene excretion by the appendix of Sauromatum guttatum. Proc Natl Acad Sci U S A 92:10084–10088
Skubatz H, Kunkel DD, Howald WN, Trenkle R, Mookherjee B (1996) The Sauromatum guttatum appendix as an osmophore: excretory pathways, composition of volatiles and attractiveness to insect. New Phytol 134:631–640
Smith BN, Meeuse JD (1966) Production of volatile amines and skatole at anthesis in some Arum Lily species. Plant Physiol 41:343–347
Stökl J, Strutz A, Dafni A, Svatos A, Doubsky J, Knaden M, Sachse S, Hansson BS, Stensmyr MC (2010) A deceptive pollination system targeting drosophilids through olfactory mimicry of yeast. Curr Biol 20:1–7
Trygg J, Wold S (2002) Orthogonal projections to latent structures (OPLS). J Chemom 16:119–128
Turner GW, Gershenzon J, Croteau R (2000) Development of peltate glandular trichomes of peppermint. Plant Physiol 124:665–679
Urru I, Stensmyr MC, Hansson BS (2011) Pollination by brood-site deception. Phytochemistry 72:1655–1666
Whitney HM, Bennett KMV, Dorling M, Sandbach L, Prince D, Chittka L, Glover BJ (2011) Why do so many petals have conical epidermal cells? Ann Bot 108:609–616
Young HJ (1986) Beetle pollination of Dieffenbachia longispatha (Araceae). Am J Bot 73:931–944
Zhuang X, Fiesselmann A, Zhao N, Chen H, Frey M, Chen F (2012) Biosynthesis and emission of insect herbivory-induced indole in rice. Phytochemistry 73:15–22
Acknowledgments
This work was supported by a CNRS grant from the Amazonie II program APR—Biodiversité, écologie chimique et chimie des substances naturelles: Aracées and an Investissement d’Avenir grant of the French Agence Nationale de la Recherche (Centre d’Étude de la Biodiversité Amazonienne (CEBA) ANR-10-LABX-0025). Authors thank Frédéric Hache (Department of Foreign Languages, UJM) and the three anonymous referees for text revision.
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Communicated by: Sven Thatje
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Appendix S1
Optical micrographies of hand-made sections (PDF 763 kb)
Appendix S2
GC-MS analysis of VOCs (data matrix) (PDF 48 kb)
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Leguet, A., Gibernau, M., Shintu, L. et al. Evidence for early intracellular accumulation of volatile compounds during spadix development in Arum italicum L. and preliminary data on some tropical Aroids. Naturwissenschaften 101, 623–635 (2014). https://doi.org/10.1007/s00114-014-1197-8
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DOI: https://doi.org/10.1007/s00114-014-1197-8