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Nigella</Italic> Sl (Ranunculaceae): Identification, Diagnostic Traits, And

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Nigella</Italic> Sl (Ranunculaceae): Identification, Diagnostic Traits, And Int. J. Plant Sci. 172(2):267–284. 2011. Ó 2011 by The University of Chicago. All rights reserved. 1058-5893/2011/17202-0010$15.00 DOI: 10.1086/657676 SEED MORPHOLOGY OF NIGELLA S.L. (RANUNCULACEAE): IDENTIFICATION, DIAGNOSTIC TRAITS, AND THEIR POTENTIAL PHYLOGENETIC RELEVANCE Andreas G. Heiss,1,* Matthias Kropf,y Susanne Sontag,z and Anton Weberz *University of Natural Resources and Life Sciences (BOKU), Institute of Botany, Gregor Mendel-Strasse 33, 1180 Wien, Austria, and Vienna Institute for Archaeological Science (VIAS), Archaeobotany, c/o Institute of Palaeontology, Geozentrum, Althanstrasse 14, 1090 Wien, Austria; yUniversity of Natural Resources and Life Sciences (BOKU), Institute of Integrative Nature Conservation Research, Gregor Mendel-Strasse 33, 1180 Wien, Austria; and zUniversity of Vienna, Faculty Centre of Biodiversity, Department of Structural and Functional Botany, Rennweg 13, 1030 Wien, Austria A comprehensive morphological and anatomical analysis was carried out on seeds of all 15 species currently recognized in the genus Nigella s.l. (including Komaroffia and Garidella). In addition, a selection of six infraspecific taxa was examined. Using testa thin sections, morphometry, and SEM imaging, seed coat characters proved to be a highly diagnostic and powerful tool in species identification. A dichotomous identification key is presented along with seed descriptions, measurements and anatomical details, LM photos, and SEM micrographs. Analyses using maximum parsimony and character mapping onto a DNA-based phylogeny suggest that seed characters will be useful for ongoing phylogenetic studies in the genus. The importance of properly identifying Nigella seeds is highlighted for applied use in archaeobotany and pharmacognosy. Keywords: Garidella, Komaroffia, Nigella, phylogeny, Ranunculaceae, seed morphology. Online enhancements: appendixes. Introduction therefore provide that information for Nigella. Another ap- plied use of seed morphological data lies in the interdisciplin- Seed morphology has developed into an important source ary field of archaeobotany/paleoethnobotany: together with of useful phylogenetic information, following the work of their archaeological contexts, correctly identified plant remains Barthlott (1981, 1984) and increasing throughout the 1990s. are the basis for the reconstruction of migrations of human A number of angiosperm taxa have already been studied in- and plant populations as well as for general investigations tensively in terms of their seed micromorphology, in combina- into the cultural history of plants through human history (see tion with phenetic or phylogenetic analyses at the genus level. Renfrew 1973; Hastorf and Popper 1988; Jacomet and Kreuz Data of this kind are now available across a broad evolution- 1999; Zohary and Hopf 2000). ary range of plant families, such as Schisandraceae (Schisandra Nigella L. (fennel flower, nigella) is a small genus within the and Kadsura; Denk and Oh 2006), Cactaceae (Stenocereus; buttercup family (Ranunculaceae), comprising ;15 species Arroyo-Cosultchi et al. 2006), Oxalidaceae (Oxalis; Obone (Zohary 1983; Do¨nmez and Mutlu 2004) distributed from the 2005), Melastomataceae (Leandra, Miconia, Ossaea,and Middle East (the center of diversity for the genus) to Spain. It Clidemia; Martin et al. 2008), Gentianaceae (Gentiana; is remarkable in several academic and applied respects: (1) it Davitashvili and Karrer 2010), Lamiaceae (Hemigenia and is the only genus of Ranunculaceae with a truly syncarpous Microcorys; Guerin 2005), Plantaginaceae (Veronica; Mun˜ oz- gynoecium (Rohweder 1967); (2) the flowers of the advanced Centeno et al. 2006), and Orchidaceae (Liparis; Tsutsumi species within the genus exhibit an interesting and complex et al. 2007). In Ranunculaceae, most such work has focused pollination mechanism, representing highly specialized ‘‘round- on Aconitum (Tamura 1993; Luo et al. 2005). Seed and fruit about flowers’’ (Sprengel 1793; Weber 1993, 1995); (3) some morphological data, if only of selected species, have also been species, especially Nigella damascena L., are popular ornamental included in the most recent works on Ranunculaceae phylog- plants (Burnie et al. 2008); (4) the seeds of several species have eny (Wang et al. 2009; Emadzade et al. 2010). been in use as a condiment since prehistoric times (Hepper 1990; However, there are additional fields in which seed morphol- Heiss and Oeggl 2005; Salih et al. 2009); and (5) seed oils of N. ogy is of increasing interest. In pharmacognosy, proper iden- sativa L. and N. damascena are of high commercial interest to tification is crucial for quality control of seed accessions. the pharmaceutical and cosmetics industries (Agradi et al. 2002; Detailed information on seed identification is often still miss- Ali and Blunden 2003; Anwar 2005). In recent years, additional ing, especially in the case of the taxa recently studied for phar- Nigella species have moved into the focus of pharmaceutical re- macological research, such as some Nigella species; we will search, such as N. arvensis L., N. integrifolia Regel, N. nigellas- trum (L.) Willk. in Willk. et Lange, N. orientalis L., and N. 1 Author for correspondence; e-mail: [email protected]. segetalis M. Bieb. (Aitzetmu¨ller et al. 1997; Aitzetmu¨ller 1998; Manuscript received June 2010; revised manuscript received October 2010. Ko¨kdil and Yılmaz 2005; Ko¨kdil et al. 2006b). 267 268 INTERNATIONAL JOURNAL OF PLANT SCIENCES The taxonomic position of Nigella s.l. within Ranuncula- seed morphology have been published, two of them consider- ceae as well as the number of species included and their re- ing six taxa (Bahadur et al. 1984; Karcz and Tomczok 1987a), spective delimitations have changed repeatedly. For instance, with the third and most recent study covering 12 taxa (Dadandi previous investigations have placed Nigella and its segregates et al. 2009). In comparison to these, not only is this article Garidella and Komaroffia in the subfamily Ranunculoideae, more comprehensive in terms of the number of Nigella taxa tribe Delphinieae (Hoot 1991; Frohne and Jensen 1998; Ste- studied (21 taxa in 15 species) but also it integrates a wider vens 2001–), or in the Aconitoideae (Takhtajan 2009). How- range of methods, namely microscopic sections, SEM imag- ever, a recent synopsis of molecular and morphological data ing, morphometry, a standardized documentation of the ob- suggests that the group’s affinities within the Ranunculaceae served features, and an evolutionary perspective based on are only weakly supported and must be considered uncertain character mapping onto a previously published phylogenetic (Wang et al. 2009). tree. Taxonomy within the genus has also undergone many Our primary goal in the current study is to demonstrate and changes in recent decades. Currently, Nigella s.l. is commonly document the variability of seed morphology within the genus divided into three genera: Komaroffia Kuntze, Garidella L., Nigella s.l. and to provide quantitative data for a future phy- and Nigella L. s.str., as done by Tamura (1993) and Tutin logenetic reassessment of the whole genus. We attempt to et al. (1964–1983). For overviews of alternative classifica- identify seed characters that might prove useful for this pur- tions, see Gregory (1941) and Zohary (1983). In this work, we pose through phylogenetic analyses and also to document pos- used the monograph of Zohary (1983) as a reference, which sible differences in taxonomic groupings on the basis of seed recognizes 14 species, essentially on the basis of morphological morphology and recent classifications, including the most re- (mainly floral and fruit) and karyological criteria. Nigella s.l. cent monograph (Zohary 1983) and the evolutionary lineages sensu Zohary includes Komaroffia and Garidella at the rank of inferred from a recent molecular analyses (Bittkau and Comes sections (see table 1). For taxa within the N. arvensis aggre- 2008). As a second core part of the article, an identification gate, the work by Strid (1970) deserves mention, since it differs key for the seeds of Nigella is provided. This will serve as from the approach of Zohary (1983) and has been used in vari- a useful tool in the fields of pharmacology and archaeobotany. ous recent studies, such as that of Bittkau and Comes (2008). Molecular investigations at the genus level have been car- ried out only very recently—namely, the analysis of DNA Material and Methods sequences of the internal transcribed spacer (ITS) region repre- senting 25 taxa, 11 of which belong to the N. arvensis ag- Seed Material gregate (Bittkau and Comes 2008)—while analyses of In total, 2229 seeds from 40 seed accessions were investi- chloroplast DNA are still in progress (trnL-trnF, trnK-matK gated, corresponding to 21 taxa (15 species) and originating intron, atpB-rbcL intron; C. Bittkau and H. P. Comes, unpub- from a wide variety of sources: commercial products as well lished data). However, comprehensive and multidisciplinary as seeds from herbaria, collections of botanical gardens, and studies of the taxonomy of Nigella are missing, and there is material collected by the authors (app. A). However, only still no consensus as to whether Nigella should be treated as a single accession was available for 10 of the included taxa, a single genus or split into three. namely, Nigella ciliaris, N. oxypetala, N. stellaris, N. turcica, Seed morphology, representing a potential set of taxonomi- N. unguicularis, and several varieties from the N. arvensis cally informative
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