Abstract
Although the presence of scent was described for several species of Rhamnaceae, localization, morphology and structure of osmophores were unknown. We studied different species of the tribes Rhamneae (Rhamnoids clade), Pomaderreae, Colletieae, Paliureae (Ziziphoids clade) and the species Alphitonia excelsa (unknown tribe, Ziziphoids clade). We expect to have a better comprehension of these structures and provide information on which morphological and anatomical characters may support the phylogeny of the family. We localized the osmophores in the margins and top of the sepals using neutral red. Histochemical tests were made on transverse hand-cut sections of fresh sepals. Observations were made with stereoscopic and bright field microscopes, scanning and transmission electron microscopes. Papillae were observed in the zones with positive reaction to reagents. Different kinds of hairs are present in the sepal epidermis besides papillae. Epidermal cells present a striate cuticle with canals and cavities. Druses are abundant in most species. The ultrastructure of epidermal and subepidermal cells shows high metabolic activity: there are vesicles, mitochondria, endoplasmic reticulum, dictyosomes, plastids with lipids and starch. The vascularization is well developed and reaches the top of the sepal where the principal area of volatile components production is localized. The location and abundance of papillae are the most important traits that allow us recognize and characterize the osmophores in Rhamnaceae. There are no clear anatomical and morphological features exclusive of one clade or tribe. Therefore, in contrast to other sporophytic structures of this family, osmophores do not seem to have any systematic value.
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Alves RJV, Pinto AC, da Costa AVM, Rezende CM (2005) Zizyphus mauritiana Lam. (Rhamnaceae) and the chemical composition of its floral fecal odor. J Braz Chem Soc 16:654–656
Amela García MT, Galati BG, Hoc PS (2007) Ultrastructure of the corona of scented and scentless flowers of Passiflora spp. (Passifloraceae). Flora Morphol Distrib Funct Ecol Plants 202:302–315. https://doi.org/10.1016/j.flora.2006.08.003
Antoń S, Kamińska M, Stpiczyńska M (2012) Comparative structure of the osmophores in the flowers of Stanhopea graveolens Lindley and Cycnoches chlorochilon Klotzsch (Orchidaceae). Acta Agrobot 65:11–22. https://doi.org/10.5586/aa.2012.054
Aronne G, Wilcock CC (1995) Reproductive lability in pre-dispersal biology of Rhamnus alaternus L. (Rhamnaceae). Protoplasma 187:49–59. https://doi.org/10.1007/BF01280232
Ascensão L, Francisco A, Cotrim H, Pais MS (2005) Comparative structure of the labellum in Ophrys fusca and O. lutea (Orchidaceae). Am J Bot 92:1059–1067
Cerino MC, Richard GA, Torretta JP et al (2015) Reproductive biology of Ziziphus mistol Griseb. (Rhamnaceae), a wild fruit tree of saline environments. Flora Morphol Distrib Funct Ecol Plants 211:18–25. https://doi.org/10.1016/j.flora.2014.12.002
Chapman RF, Bernays EA, Simpson SJ (1981) Attraction and repulsion of the aphid, Cavariella aegopodii, by plant odors. J Chem Ecol 7:881–888. https://doi.org/10.1007/BF00992385
Cseke LJ, Kaufman PB, Kirakosyan A (2007) The biology of essential oils in the pollination of flowers. Nat Prod Commun 2:1934578X0700201225
Curry KJ, McDowell LM, Judd WS, Stern WL (1991) Osmophores, floral features, and systematics of Stanhopea (Orchidaceae). Am J Bot 78:610–623
D’Ambrogio A, Medan D (1993) Comportamiento reproductivo de Colletia paradoxa (Rhamnaceae). Darwiniana 32:1–14
David R, Carde JP (1964) Coloration différentielle dês inclusions lipidique et terpeniques dês pseudophylles du Pin maritime au moyen du reactif nadi. CR Acad Sci Paris D 258:1338–1340
Davies KL, Stpiczyńska M, Gregg A (2005) Nectar-secreting floral stomata in Maxillaria anceps Ames & C. Schweinf. (Orchidaceae). Ann Bot 96:217–227. https://doi.org/10.1093/aob/mci182
de Melo MC, Borba EL, Paiva EAS (2010) Morphological and histological characterization of the osmophores and nectaries of four species of Acianthera (Orchidaceae: Pleurothallidinae). Plant Syst Evol 286:141–151
Devi KR, Atluri JB, Reddi CS (1989) Pollination ecology of Zizyphus mauritiana (Rhamnaceae). Proc Plant Sci 99:223–239. https://doi.org/10.1007/BF03053596
Dizeo de Strittmatter C (1973) Nueva técnica de diafanización. Bol Soc Argent Bot 15:126–129
Dressler R (1993) Phylogeny and classification of orchid family. Cambridge University Press, Cambridge
Dudareva N, Pichersky E (2000) Biochemical and molecular genetic aspects of floral scents. Plant Physiol 122:627–633. https://doi.org/10.1104/pp.122.3.627
Effmert U, Buss D, Rohrbeck D, Piechulla B (2006) Localization of the synthesis and emission of scent compounds within the flower. Biol Flor Scent:105–124
Endress PK (1984) The role of inner staminodes in the floral display of some relic Magnoliales. Plant Syst Evol 146:269–282. https://doi.org/10.1007/BF00989551
Endress PK (1994) Floral structure and evolution of primitive angiosperms: recent advances. Plant Syst Evol 192:79–97
Faegri K, van der Pijl L (1979) The principles of pollination ecology, vol 64, 3rd edn. Pergamon Press, Oxford, pp 6–7
Fahn A (2000) Structure and function of secretory cells. Adv Bot Res 31:37–75
Franken EP, Pansarin LM, Pansarin ER (2016) Osmophore diversity in the catasetum cristatum alliance (Orchidaceae: Catasetinae). Lankesteriana 16:317–327
Gang DR (2005) Evolution of flavors and scents. Annu Rev Plant Biol 56:301–325. https://doi.org/10.1146/annurev.arplant.56.032604.144128
Gonçalves-Souza P, Schlindwein C, Dötterl S, Paiva EAS (2017) Unveiling the osmophores of Philodendron adamantinum (Araceae) as a means to understanding interactions with pollinators. Ann Bot 119:533–543. https://doi.org/10.1093/aob/mcw236
Gotelli MM, Galati BG, Zarlavsky G (2016) Pollen development and anther morphology in 14 species of Rhamnaceae. Plant Syst Evol 302:1433–1444. https://doi.org/10.1007/s00606-016-1342-2
Gotelli MM, Galati BG, Medan D (2017) Morphological and ultrastructural studies of floral nectaries in Rhamnaceae. J Torrey Bot Soc 144:63–73. https://doi.org/10.3159/torrey-d-15-00045.1
Gotelli MM, Galati BG, Zarlavsky G, Medan D (2018) Structure of the style and pollen tube pathway in the Ziziphoid and Rhamnoid clades of Rhamnaceae. Protoplasma 255:501–515. https://doi.org/10.1007/s00709-017-1167-z
Hauenschild F, Matuszak-Renger S, Muellner-Riehl A, Favre A (2016) Phylogenetic relationships within the cosmopolitan buckthorn family (Rhamnaceae) support the resurrection of Sarcomphalus and the description of Pseudoziziphus gen. nov. Taxon 65:47–64. https://doi.org/10.12705/651.4
Hernández MP, Katinas L (2019) Technique for the identification of osmophores in flowers of herbarium material (TIOFH). Protoplasma 256(6):1753–1765. https://doi.org/10.1007/s00709-019-01398-8
Johansen DA (1940) Plant microtechnique. McGraw-Hill Book Company, Inc, London, p 530
Knudsen JT, Eriksson R, Gershenzon J, Ståhl B (2006) Diversity and distribution of floral scent. Bot Rev 72:1–120
Kowalkowska AK, Krawczyńska AT (2019) Anatomical features related with pollination of Neottia ovata (L.) Bluff & Fingerh. (Orchidaceae). Flora Morphol Distrib Funct Ecol Plants 255:24–33. https://doi.org/10.1016/j.flora.2019.03.015
Kowalkowska AK, Margońska HB, Kozieradzka-Kiszkurno M, Bohdanowicz J (2012) Studies on the ultrastructure of a three-spurred fumeauxiana form of Anacamptis pyramidalis. Plant Syst Evol 298:1025–1035. https://doi.org/10.1007/s00606-012-0611-y
Kowalkowska AK, Kozieradzka-Kiszkurno M, Turzyński S (2015) Morphological, histological and ultrastructural features of osmophores and nectary of Bulbophyllum wendlandianum (Kraenzl.) Dammer (B. section Cirrhopetalum Lindl., Bulbophyllinae Schltr., Orchidaceae). Plant Syst Evol 301:609–622
Kowalkowska AK, Turzyński S, Kozieradzka-Kiszkurno M, Wiśniewska N (2017) Floral structure of two species of Bulbophyllum section Cirrhopetalum Lindl.: B. weberi Ames and B. cumingii (Lindl.) Rchb. f. (Bulbophyllinae Schltr., Orchidaceae). Protoplasma 254:1431–1449. https://doi.org/10.1007/s00709-016-1034-3
Maiti S, Mitra A (2017) Morphological, physiological and ultrastructural changes in flowers explain the spatio-temporal emission of scent volatiles in Polianthes tuberosa L. Plant Cell Physiol 58:2095–2111. https://doi.org/10.1093/pcp/pcx143
Marinho CR, Souza CD, Barros TC, Teixeira SP (2014) Scent glands in legume flowers. Plant Biol 16:215–226. https://doi.org/10.1111/plb.12000
Medan D (1991) Reproductive phenology, pollination biology, and gynoecium development in Discaria americana (Rhamnaceae). N Z J Bot 29:31–42. https://doi.org/10.1080/0028825X.1991.10415541
Medan D (1993) Breeding system and maternal success of a perennial hermaphrodite, Discaria americana (Rhamnaceae). N Z J Bot 31:175–184. https://doi.org/10.1080/0028825X.1993.10419492
Medan D (1994) Reproductive biology of Frangula alnus (Rhamnaceae) in southern Spain. Plant Syst Evol 193:173–186. https://doi.org/10.1007/BF00983549
Medan D (2003) Reproductive biology of the Andean shrub Discaria nana (Rhamnaceae). Plant Biol 5:94–102. https://doi.org/10.1055/s-2003-37980
Medan D, Arce ME (1999) Reproductive biology of the Andean-disjunct genus Retanilla (Rhamnaceae). Plant Syst Evol 218:281–298. https://doi.org/10.1007/BF01089232
Medan D, Basilio AM (2001) Reproductive biology of Colletia spinosissima (Rhamnaceae) in Argentina. Plant Syst Evol 229:79–89
Medan D, D’Ambrogio AC (1998) Reproductive biology of the andromonoecious shrub Trevoa quinquenervia (Rhamnaceae). Bot J Linn Soc 126:191–206. https://doi.org/10.1006/bojl.1997.0132
Medan D, Devoto M (2005) Reproductive ecology of a perennial outcrosser with a naturally dissected distribution. Plant Syst Evol 254:173–184. https://doi.org/10.1007/s00606-005-0335-3
Medan D, Devoto M (2017) Ambophily, not entomophily: the reproduction of the perennial Discaria chacaye (Rhamnaceae: Colletieae) along a rainfall gradient in Patagonia, Argentina. Plant Syst Evol 303:841–851. https://doi.org/10.1007/s00606-017-1417-8
Medan D, Montaldo N (2005) Ornithophily in the Rhamnaceae: the pollination of the Chilean endemic Colletia ulicina. Flora 200:339–344. https://doi.org/10.1016/j.flora.2004.12.003
Medan D, Schirarend C (2004) Rhamnaceae. In: Kubitzki K (ed) Flowering plants ·Dicotyledons: Celastrales, Oxalidales, Rosales, Cornales. Ericales. Springer, Berlin Heidelberg, Berlin, Heidelberg, pp 320–338
Medan D, Torretta JP (2015) The reproduction of Colletia hystrix and late-flowering in Colletia (Rhamnaceae: Colletieae). Plant Syst Evol 301:1181–1189. https://doi.org/10.1007/s00606-014-1142-5
Medan D, Zarlavsky G, Bartoloni NJ (2013) Plant reproduction in the high-Andean Puna: Kentrothamnus weddellianus (Rhamnaceae: Colletieae). Plant Syst Evol 299:841–851. https://doi.org/10.1007/s00606-013-0766-1
Medan D, Castillo-Campos G, Zarlavsky G (2015) Floral biology of Adolphia infesta and the reproductive profile of Colletieae (Rhamnaceae). J Pollinat Ecol 16:82–90. https://doi.org/10.26786/1920-7603(2015)12
Nepi M (2007) Nectary structure and ultrastructure. In: Nectaries and nectar. Springer, pp 129–166
O’Brien TP, McCully ME (1981) The study of plant structure principles and selected methods. Termarcarphi, Melbourne
Pacini E, Nepi M (2007) Nectar production and presentation. In: Nicolson SW, Nepi PE (eds) Nectaries and nectar. Springer, Dordrecht, pp 167–214
Paiva EAS, Dötterl S, De-Paula OC et al (2019) Osmophores of Caryocar brasiliense (Caryocaraceae): a particular structure of the androecium that releases an unusual scent. Protoplasma 256:971–981. https://doi.org/10.1007/s00709-019-01356-4
Pearse AGE (1961) Histochemistry. Am J Med Sci 241
PŁachno BJ, Światek P, Szymczak G (2010) Can a stench be beautiful? - Osmophores in stem-succulent stapeliads (Apocynaceae-Asclepiadoideae-Ceropegieae-Stapeliinae). Flora Morphol Distrib Funct Ecol Plants 205:101–105. https://doi.org/10.1016/j.flora.2009.01.002
PŁachno BJ, Stpiczyńska M, Świątek P, Davies KL (2016) Floral micromorphology of the Australian carnivorous bladderwort Utricularia dunlopii, a putative pseudocopulatory species. Protoplasma 253:1463–1473
PŁachno BJ, Stpiczyńska M, Davies KL et al (2017) Floral ultrastructure of two Brazilian aquatic-epiphytic bladderworts: Utricularia cornigera Studnička and U. nelumbifolia Gardner (Lentibulariaceae). Protoplasma 254:353–366
Pridgeon AM, Stern WL (1983) Ultrastructure of Osmophores in Restrepia (Orchidaceae). Am J Bot 70:1233. https://doi.org/10.2307/2443293
Pridgeon AM, Stern WL (1985) Osmophores of Scaphosepalum (Orchidaceae). Bot Gaz 146:115–123. https://doi.org/10.1086/337505
Primack RB (1979) Reproductive biology of Discaria toumatou (Rhamnaceae). N Z J Bot 17:9–13. https://doi.org/10.1080/0028825X.1979.10425156
Prychid CJ, Rudall PJ (1999) Calcium oxalate crystals in monocotyledons: a review of their structure and systematics. Ann Bot 84:725–739. https://doi.org/10.1006/anbo.1999.0975
Richardson JE, Fay MF, Cronk QCB, Bowman D, Chase MW (2000a) A phylogenetic analysis of Rhamnaceae using rbcL and trnL-F plastid DNA sequences. Am J Bot 87:1309–1324
Richardson JE, Fay MF, Cronk QCB, Chase MW (2000b) A revision of the tribal classification of Rhamnaceae. Kew Bull 55:311–340
Sazima M, Vogel S, Cocucci A, Hausner G (1993) The perfume flowers of Cyphomandra (Solanaceae): pollination by euglossine bees, bellows mechanism, osmophores, and volatiles. Plant Syst Evol 187:51–88. https://doi.org/10.1007/BF00994091
Stern WL, Curry KJ, Pridgeon AM (1987) Osmophores of Stanhopea (Orchidaceae). Am J Bot 74:1323–1331. https://doi.org/10.1002/j.1537-2197.1987.tb08747.x
Stpiczyńska M (2001) Osmophores of the fragrant orchid Gymnadenia conopsea L. (Orchidaceae). Acta Soc Bot Pol 70:91–96
Stpiczyńska M, Davies KL, Gregg A (2005) Comparative account of nectary structure in Hexisea imbricata (Lindl.) Rchb.f. (Orchidaceae). Ann Bot 95:749–756. https://doi.org/10.1093/aob/mci081
Stpiczyńska M, Płachno BJ, Davies KL (2018) Nectar and oleiferous trichomes as floral attractants in Bulbophyllum saltatorium Lindl. (Orchidaceae). Protoplasma 255:565–574. https://doi.org/10.1007/s00709-017-1170-4
Swanson E, Cunningham W, Holman R (1980) Ultrastructure of glandular ovarian trichomes of Cypripedium calceolus and C. reginae (Orchidaceae). Am J Bot 67:784–789. https://doi.org/10.1002/j.1537-2197.1980.tb07707.x
Tölke ED, Bachelier JB, de Lima EA et al (2018) Osmophores and floral fragrance in Anacardium humile and Mangifera indica (Anacardiaceae): an overlooked secretory structure in Sapindales. AoB Plants 10:1–14. https://doi.org/10.1093/aobpla/ply062
Van der Pijl L, Dodson C (1966) Orchid flowers, their pollination and evolution. University of Miami Press, Florida
Vogel S (1963) Duftdrüsen im Dienste der Bestäubung: Über Bau und Funktion der Osmophoren. Verlag d. Akad. d. Wiss. ud Litaratur
Vogel S (1990) Duftdrüsen im Dienste der Bestäubung. Routledge
Vogel S, Hadacek F (2004) Contributions to the functional anatomy and biology of Nelumbo nucifera (Nelumbonaceae) III. An ecological reappraisal of floral organs. Plant Syst Evol 249:173–189. https://doi.org/10.1007/s00606-004-0203-6
Vogel S, Martens J (2000) A survey of the function of the lethal kettle traps of Arisaema (Araceae), with records of pollinating fungus gnats from Nepal. Bot J Linn Soc 133:61–100. https://doi.org/10.1006/bojl.1999.0317
Webb CJ (1985) Protandry, pollination, and self-incompatibility in Discaria toumatou. N Z J Bot 23:331–335. https://doi.org/10.1080/0028825X.1985.10425335
Weekley C, Race T (2001) The breeding system of Ziziphus celata Judd and D.W. hall (Rhamnaceae), a rare endemic plant of the Lake Wales Ridge, Florida, USA: implications for recovery. Biol Conserv 100:207–213. https://doi.org/10.1016/S0006-3207(01)00024-6
Wiśniewska N, Kowalkowska AK, Kozieradzka-Kiszkurno M, Krawczyńska AT, Bohdanowicz J (2018) Floral features of two species of Bulbophyllum section Lepidorhiza Schltr.: B. levanae Ames and B. nymphopolitanum Kraenzl. (Bulbophyllinae Schltr., Orchidaceae). Protoplasma 255:485–499
Zarlavsky GE (2014) Histología Vegetal: técnicas simples y complejas. Soc Argentina Botánica, Buenos Aires
Zietsman PC (1990) Pollination of Ziziphus mucronata subsp. mucronata (Rhamnaceae). S Afr J Bot 56:350–355. https://doi.org/10.1016/s0254-6299(16)31064-x
Zini LM, Galati BG, Gotelli M et al (2019) Carpellary appendages in Nymphaea and Victoria (Nymphaeaceae): evidence of their role as osmophores based on morphology, anatomy and ultrastructure. Bot J Linn Soc 20:1–19
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This work was supported by the Universidad de Buenos Aires (UBACyT grant number 20020160100012BA) and PICT 2016-2634.
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Gotelli, M.M., Galati, B.G., Zarlavsky, G. et al. Localization, morphology, anatomy and ultrastructure of osmophores in species of Rhamnaceae. Protoplasma 257, 1109–1121 (2020). https://doi.org/10.1007/s00709-020-01498-w
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DOI: https://doi.org/10.1007/s00709-020-01498-w