Pollen grain morphology of selected allergenic species native to southern South America
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1 Journal of the Torrey Botanical Society 134(4), 2007, pp Pollen grain morphology of selected allergenic species native to southern South America Luis Palazzesi 1,2 and Roberto R. Pujana MACN - Museo Argentino de Ciencias Naturales, Ángel Gallardo 470, C1405, Ciudad de Buenos Aires, Argentina Hernán P. Burrieza DBBE - Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, C1428, Ciudad de Buenos Aires, Argentina Alberto Penas Steinhardt IDEHU - Instituto de Estudios de la Inmunidad Humoral Prof. Ricardo A. Margni Junín 956, 4to piso, C1113, Ciudad de Buenos Aires, Argentina PALAZZESI, L., R. R., PUJANA, (MACN - Museo Argentino de Ciencias Naturales, Ángel Gallardo 470, C1405, Ciudad de Buenos Aires, Argentina), H. P., BURRIEZA (DBBE - Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Pabellón II, C1428, Ciudad Universitaria, Ciudad de Buenos Aires, Argentina), AND A. PENAS STEINHARDT (IDEHU - Instituto de Estudios de la Inmunidad Humoral Prof. Ricardo A. Margni, Junín 956, 4to piso, C1113, Ciudad de Buenos Aires, Argentina). Pollen grain morphology of selected allergenic species native to southern South America. J. Torrey Bot. Soc. 134: Pollen grains of Celtis tala (Celtidaceae), Phytolacca dioica (Phytolaccaceae), Schinopsis balansae (Anacardiaceae) and Solidago chilensis (Asteraceae) are examined with light and scanning electron microscopy, described, and illustrated. These four unrelated species are native to southern South America and considered an important source of skin prick allergy tests. Most relevant pollen characters are compared to those of their closest relatives. Celtis tala (3-, 4-, or 5- porate, verrucate) shares characters with the Celtis africana type in lacking a sunken area around the ora and in having the sculptural elements regularly arranged; Phytolacca dioica (3-colpate) with the Phytolacceae type in being microechinate and microperforate; Schinopsis balansae (3-colporate, striato-reticulate) with some members of the Lithraea molleoides subtype (Anacardiaceae) in having high muri and long striae; Solidago chilensis (3-colporate, echinate) with the Solidago type in being caveate. This study contributes to a better understanding of pollen morphology in species that are especially common to southern South America. Key words: allergenic species, Argentina, pollen morphology. Pollen grains from a variety of common plants can be the source of major allergenic diseases (O Rourke, 1996). Celtis tala Gill. ex Planch (Celtidaceae), Phytolacca dioica L (Phytolaccaceae), Schinopsis balansae Engl (Anacardiaceae) and Solidago chilensis Meyen 1834 (Asteraceae) pollen were reported as allergenic and considered the main native source of skin prick testing (SPT) in southern South America (Carron and Malvarez 1941, De Jong et al. 1998, Baltasat 1 Two anonymous reviewers provided helpful criticisms to earlier drafts. Roberto Gomez (Museo Argentino de Ciencias Naturales) for help with obtaining pollen material, Fabián Tricárico for technical assistance in the scanning electron microscopy and Julián Alvarado for collecting part of the material are greatly acknowledged. Helpful comments have been provided by María Cristina Tellería and Viviana Barreda. 2 Author for correspondence. lpalazzesi@ macn.gov.ar, lpalazzesi@gmail.com Received for publication March 2, 2007, and in revised form August 24, Drago et al. 2007). In this study the morphological patterns of the pollen grains produced by these species were analyzed based on their examination using light and scanning electron microscopy. Phytolacca dioica ( ombú ) and Schinopsis balansae ( quebracho colorado ) are deciduous trees common to humid and warm regions while Celtis tala ( tala ) is a semiperennial tree frequent in seasonally dry areas. Solidago chilensis ( penacho amarillo ) is a perennial herb associated primarily with moist soil environments of South America. Documentation of the pollen flora from southern South America has been the focus of several attempts. Among these, important pollen atlases have been published based on morphological characters of the native flora such as those of Markgraf and D Antoni (1978) from Argentina and Heusser (1971) from Chile. Detailed descriptions and highmagnified images of the specimens analyzed in such accounts, however, are often lacking, though. The descriptions and illustrations of 527
2 528 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 134 the species selected in this study are given for the first time, as previously they have only been mentioned in books or journals with very limited distribution. The present study contributes to our understanding of pollen systematic determinations not only in allergenic analyses but also in those related to aerobiological, melissopalynological, and plant reproductive biological surveys. Materials and Methods. Plants of Celtis tala, Phytolacca dioica, Schinopisis balansae, and Solidago chilensis have been collected in the field and their identity determined using herbarium specimens at the Museo Argentino de Ciencias Naturales BA (Holmgren et al. 1990). Anthers have been removed from both fresh (collected in the field) and dried specimens (housed at MACN herbarium), and acetolysed using Erdtman s method (1960). For light microscopy, pollen samples have been mounted in glycerine jelly on glass slides and then examined by light microscope. Measurements of the polar axis (P), equatorial diameter (E) and exine thickness have been based on 30 pollen grains for each species. The P/E relation has been calculated for each specimen (individual pollen grain). Permanent slides are housed at the Palynological Laboratory of the Museo Argentino de Ciencias Naturales (MACN) under the catalogue numbers BAPA 3288 (Celtis tala), BAPA 3289 (Phytolacca dioica), BAPA 3290 (Schinopsis balansae) and BAPA 3291 (Solidago chilensis). For scanning electron microscopy, acetolyzed pollen grains have been washed in ethanol. Grains have been sputter-coated with goldpalladium and observed using a Philips XL30 scanning electron microscope. The terminology of Punt et al. (2007) has been followed to describe pollen structure and sculpture. Results. A list of the taxa examined, dimensions, collecting information and selected morphological data was included in this study (Table 1). Pollen grain structural descriptions of each taxon are provided in alphabetical order by species. CELTIS TALA (CELTIDACEAE). LM (Figs. 1 A C). Pollen grains triporate (rarely tetraporate or pentaporate), isopolar, spheroidal to suboblate, circular in polar view. Ora mm wide, round to oval, clearly defined (Fig. 1 A), annulate (Fig. 1 C). Exine tectate, mm Table 1. List of species analyzed, figure numbers, pollen grain dimensions, collecting information, and selected remarks. Taxon Figure P (mm) a E(mm) b P/E c Exine (mm) Collection information Remarks 3- (4- or 5-) porate, densely scabrate Argentina: San Luis province. Schinini, 1999, BA spheroidal to suboblate Celtis tala 1A C, 3A B 3-colpate, microechinate and microperforate Argentina: Santa Fé province. Krapovickas, 1982, MACN BA suboblate to spheroidal Phytolacca dioica 1 D F, 2A B 3-colporate, striato-reticulate 5 Argentina: Santa Fé province. Ventura 1904, MACN BA spheroidal to subprolate Schinopsis balansae 1 G I, 2C D 3-colporate, caveate, echinate 5 Argentina: Neuquén province. Daciuk, 1964; MACN BA suboblate to spheroidal Solidago chilensis 1J L, 3C D a Polar diameter measurements. b Equatorial diameter measurements. c Shape based on P/E ratio.
3 2007] PALAZZESI ET AL.: POLLEN OF SOUTH AMERICAN SPECIES 529 FIG. 1. LM photomicrographs of the selected species of this study: (A C) Equatorial view of Celtis tala. A. High focus showing circular ora (arrow). B. Optical section showing the compact exine. C. High focus showing annulate os (arrow). (D F) Equatorial view of Phytolacca dioica. D. High focus showing partially broken nexine (arrow). E. Optical section showing the columellate exine. F. Details of sculpture. (G I) Equatorial view of Schinopsis balansae. G. High focus showing endoapertural area (arrow). H. Optical section showing the columellate exine. I. Details of sculpture. (J L) Polar view of Solidago chilensis. J. High focus showing the columellate exine (arrow). K. Optical section showing the cavea (arrow). L. Details of sculpture. Scale bar 5 5 mm.
4 530 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 134 FIG. 2. SEM photomicrographs of the selected species of this study: (A B) Celtis tala. Note the annulate ora and the scabrate exine; (C D) Phytolacca dioica. Note the microspines and microperforations. Scale bar 5 5 mm. thick, compact in aspect (Fig. 1 B), psilate to scabrate. Dimensions: equatorial diameter mm; polar diameter mm. SEM (Figs. 3 A B). Surface sculpture densely and regularly scabrate. Celtidaceae has been treated as a subfamily of Ulmaceae (Celtidoideae), but a significant body of evidence exists (including pollen characters) that supports their placement as a separate family (Zavada 1983, Ueda et al. 1997, Sytsma et al. 2002). Celtis L. pollen, along with that produced by Aphananthe Planch. and Pteroceltis Maxim. species, comprise one of the five major types in Celtidaceae based mainly on the presence of a granular sexine layer, evident under transmission electron microscopy (Takahashi 1989). In turn, the pollen of some Celtis species were split into two main types based on the presence/absence of a sunken area around the ora and the arrangement of sculptural elements (Sattarian et al. 2006). These are: 1) Celtis australis L. type in which the sunken area around the ora is present and the sculptural elements are irregularly arranged (C. adolfi-friderici Engl., C. australis, C. bifida J. F. Leroy, C. mildbraedii Engl., C. philippensis Blanco, C. prantlii Priemer ex Engl., C. tessmannii Rendle, C.
5 2007] PALAZZESI ET AL.: POLLEN OF SOUTH AMERICAN SPECIES 531 FIG. 3. SEM photomicrographs of the selected species of this study: (A B) Schinopsis balansae. Notethe striato-reticulate and the raised colpal margins at equatorial region (arrow); (C D) Solidago chilensis. Note the presence of subapical channels (arrow). Scale bar 5 5 mm. toka (Forssk.) Hepper & J. R. I. Wood, and C. zenkeri Engl.) and 2) Celtis africana Burm. type in which the sunken area around the ora is absent and the sculptural elements are regularly arranged (C. africana and C. gomphophylla Baker). Based on the characters described, C. tala pollen specimens appear to be closely related to the C. africana type. PHYTOLACCA DIOICA (PHYTOLACCACEAE). LM (Figs. 1 D F). Pollen grains tricolpate, isopolar, suboblate to spheroidal, circular to subcircular in polar view. Colpi mm long and relatively broad; colpus membrane granulate. Exine tectate, mm thick in equatorial areas, thickening towards the poles (Fig. 1 E). Nexine frequently broken off or sectioned through the equatorial region outlining an os-like structure (Fig. 1 D). Dimensions: equatorial diameter mm; polar diameter mm. SEM (Figs. 2 A B). Surface sculpture microechinate and microperforate. The Phytolacca L., Anisomeria D. Don, and Ercilla A. Juss. pollen grains are common to the Phytolacceae tribe. The most distinct characters include supratectal microspines and microperforations (Bortenschlager 1973),
6 532 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 134 also observed on specimens herein studied under SEM. P. dioica is superficially similar to P. octandra L. illustrated by Bortenschlager (1973), although this latter species seems to have the microspines more densely distributed. SCHINOPSIS BALANSAE (ANACARDIACEAE). LM (Figs. 1 G I). Pollen grains tricolporate, isopolar, spheroidal to subprolate, circular to subcircular in polar view. Colpi long and narrow with acute ends; colpus membrane psilate. Ora lalongate (Fig. 1 G), 11 mm 3 2 mm. Exine stratified, semi-tectate, 5 mm thick, slightly thinner towards poles. Nexine thickened along ora. Sexine striate, infrareticulate (Fig. 1 I). Dimensions: equatorial diameter mm; polar diameter mm. SEM (Figs. 2 C D). Colpal margins raised at the equatorial area and often connected with each other forming a bridge (Fig. 2 C). Schinopsis Engl. pollen has been poorly studied to date. S. balansae pollen was recently erected as a distinct morphotype (Anzótegui, 2001). The pollen type includes two subgroups, S. balansae species being placed within the Lithraea molleoides Engl. (Anacardiaceae) subtype. The most diagnostic characters include the high muri as well as the long and tight ridges. The equatorial constriction or bridge at the colpi region appears to be present in most of the taxa involved into the L. molleoides subtype (Anzótegui, 2001), except at least in Schinus fasciculatus I. M. Johnst. (Andrada & Tellería 2005, Fig. 4 A). Further accurate descriptions will likely reveal new and more refined schemes. The morphological overlaps among these taxa highlight the importance of such exine patterns as evidence of their close relationship. SOLIDAGO CHILENSIS (ASTERACEAE). LM (Figs. 1 J L). Pollen grains tricolporate, suboblate to spheroidal, circular to oval in polar view. Colpi long, broad at the equator and narrowing towards the ends; margin diffuse near the polar region. Ora lalongate, diffuse. Exine stratified, tectate, 5 mm thick between spines, echinate. Nexine relatively thick. Sexine columellate, columellae short and distinct (Fig. 1 J). Cavea present (Fig. 1 K). Echinae conical with acute tip, without a cavity. Dimensions: equatorial diameter mm; polar diameter mm. SEM (Figs. 3 C D). Echinae small, conical, very acute tip. Subapical channels present (Fig. 3 C). Solidago L. species have been placed during the last several years into a number of morphological types. The Solidago type was proposed by Faegri and Iversen (1989) in which several caveate taxa such as Aster L., Bidens L., Inula L., and Senecio L. were included. This type is comparatively broad and therefore S. chilensis characters fit well into it. Literature Cited ANDRADA, C. AND M. C. TELLERÍA Pollen collected by honey bees (Apis mellifera L.) from south of Caldén district (Argentina): botanical origin and protein content. Grana 44: ANZÓTEGUI, L. M Anacardiaceae, p In S. M. Pire, L. M. Anzótegui, and G. A. Cuadrado [eds.], Flora Polínica del Nordeste Argentino. Corrientes: Editorial Universitaria de la Universidad Nacional del Nordeste. BALTASAT DRAGO, M., A. F. PINEDA DE LA LOSA, AND R. GUSPÍ BORI Allergy due to Phytolacca dioica. Allergy 62: BORTENSCHLAGER, S Morphologie pollinique des Phytolaccaceae. Pollen et Spores 15: CARRON, R. F. AND H. E. MALVAREZ Polinosis por tala (Celtis tala), reacciones sistemáticas y costitucionales. Prensa Méd. Argent p. DE JONG, N. W., A. M. VERMEULEN, R.GERTH van WIJK, AND H. DE GROOT Occupational allergy caused by flowers. Allergy 53: ERDTAMN, G The acetolysis method. A revised description. Svensk Botanisk Tidskrift 54: FAEGRI, K. AND J. IVERSEN Textbook of Pollen Analysis. Chichester, J. Wiley & Sons, New York, NY. 328 p. HEUSSER, C. J Pollen and spores of Chile. Modern types of the Pteridophyta, Gymnospermae, and Angiospermae. The University of Arizona Press, Tucson, AZ. 167 p. HOLMGREN, P. K., N. H. HOLMGREN, AND L. C. BARNETT Index herbariorum Part I: The herbaria of the world. New York Botanical Garden. 693 p. MARKGRAF, V. AND D ANTONI, H Pollen Flora of Argentina. The University of Arizona Press, Tucson, AZ. 208 p. O ROURKE, M. K Medical Palynology, p In J. Jansonius and D. C. McGregor [eds.], Palynology: Principles and Applications. AASP Foundation, Dallas, TX. PUNT, W., HOEN, P. P., BLACKMORE, S., NILSSON, S., AND LE THOMAS, A Glossary of pollen and spore terminology. Rev. Palaeobot. Palyn. 143: SATTARIAN, A., R. G. VAN DEN BERG, AND L. J. G. VAN DER MAESEN Pollen morphology of African Celtis (Celtidaceae). Feddes Repertorium 117:
7 2007] PALAZZESI ET AL.: POLLEN OF SOUTH AMERICAN SPECIES 533 SYTSMA, K. J., J. MORAWETZ, J. C. PIRES, M. NEPOKROEFF, E.CONTI, M.ZJHRA, J.C.HALL, AND M. W. CHASE Urticalean rosids: circumscription, rosid ancestry, and phylogenetics based on rbcl, trnl-f, and ndhf sequences. Am. J. Bot. 89: TAKAHASHI, M Pollen morphology of Celtidaceae and Ulmaceae: a reinvestigation, p In P. R. Crane and S. Blackmore [eds.], Evolution, Systematics and Fossil History of the Hamamelidae. Clarendon Press, Oxford, UK. UEDA, K., KOSUGE, H., AND TOBE, H A molecular phylogeny of Celtidaceae and Ulmaceae (Urticales) based on rbcl nucleotide sequences. J. Plant Res. 110: ZAVADA, M Pollen morphology of Ulmaceae. Grana 22:
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