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JUAN, J. The aim of this study, therefore, was to investigate the systematic utility of seed characteristics. Ornamentation of the periclinal walls could be used to discriminate four morphological types. Orobanche is a large genus mainly distributed throughout subtropical and temperate regions of the northern hemisphere, with the Mediterranean region one of the most important centres of diversity. Orobanche is a genus with approx. The most important differential characteristics of the section Trionychon are branched stems, bracteolate flowers, an entire and campanulated calyx, a blue or purple corolla, white anthers, and the stigma usually white. From a molecular point of view, according to Schneeweiss , the separation of both sections is pronounced, and supports the treatment of the section Trionychon as a separate genus Phelipanche , as previously stated by Teryokhin , The Orobanchaceae is a family of holoparasitic plants, which has been traditionally considered to be closely related to the Scrophulariaceae. Some authors, like Stace , have pointed out the absence of a clear separation between the families, and have highlighted the relationship between hemiparasitic and holoparasitic taxa of both families due to the continuity of their morphological features Kuijt, ; Weber, Previously, Boeshore had carried out a study concerning morphological continuity between the Scrophulariaceae and Orobanchaceae based on different characters such as roots, leaves or inflorescences in order to delimit these families. Other authors such as Hutchinson , Takhtajan and Cronquist consider Orobanchaceae as a different and more advanced family, probably originating from the subfamily Rhinantoideae of the Scrophulariaceae. Later work by Teryokhin considered it as a subfamily Orobanchoideae within the Scrophulariaceae. Recent molecular phylogenetic research on the Scrophulariaceae and Orobanchaceae has provided new data about their delimitation. Young et al. Finally, Olmstead et al. The difficulty in identifying species in the genus Orobanche has been shown by the research of various authors. Among these, we can highlight the palinology carried out by Minkin , Minkin and Eshbaugh and Abu Sbaih et al. The intrinsic taxonomic difficulties of the genus Orobanche are further increased by the fact that important differential characters are observed only with difficulty, or not at all, on dried specimens. With regard to seeds, there are several studies that analyse different aspects such as their chemical composition Velasco et al. Seed morphology was studied in 33 taxa of the Orobanche L. For every taxon, specimens from the populations within the study area were sampled, except for O. In these cases, it being impossible to obtain samples from Iberian populations, specimens from France courtesy of the Herbarium at the Pirenaic Institute of Ecology, CSIC, Jaca and from Germany, respectively, were used. For O. Collectors and localities are shown in the Appendix. Data on the width and length of seeds is based on the measurement of 30— seeds per taxon, by means of direct observation under optical microscopy. The abbreviations of the authorities of plant names follow the standard of Brummit and Powell , and acronyms of the herbariums follow Holmgren et al. Seeds of Orobanche are extremely small, being less than 1 mm in size, with a wide variety of shapes ellipsoid, oblongoid, ovoid, globose, trigonous or tetragonous and a terminal funicular attachment. The seed coat is reticulated with polygonal cells, which range from more or less isodiametric to tangentially elongated, being sometimes irregular. Orobanche seeds usually have a smooth membranous outer periclinal wall, although they can sometimes have a fibrillar aspect due to epicuticular waxes. Both kinds collapse on the inner periclinal wall, thus showing the structure of the latter, which is of very changeable aspect perforate, granulate, rugulose, etc. Observations made using scanning electron microscopy indicated that there are four morphological seed types, recognizable as listed in Table 1. Among the taxa examined, only seeds of O. The differences observed in the diameter of the perforations of the inner periclinal wall suggest separation into three subtypes, as shown in Table 3. Epidermal seed coat cells more or less isodiametric to tangentially elongated, anticlinal walls of medium depth and evenly thickened, with a narrow trough that is noticeable all around the edge of the cells or just at the vertices. Inner periclinal wall of epidermal seed coat cells with perforations of smaller diameter than the thickness of the walls that separate them, sometimes with a small central mammilla. This subtype includes O. Epidermal seed coat cells more or less isodiametric to tangentially elongated, anticlinal walls very deep or of medium depth and evenly thickened with a narrow trough that is evident all around the edge of the cells or just at the vertices. Inner periclinal wall of epidermal seed coat cells with perforations of similar diameter to the thickness of the walls that separate them. Epidermal seed coat cells more or less isodiametric, slightly to very deep and anticlinal walls evenly or unevenly thickened, with a narrow trough that is noticeable just at the vertices of the cells. Inner periclinal wall of seed coat cells with perforations of larger diameter than the thickness of the walls that separate them. This type includes O. Subtype IV B : reticulate inner periclinal wall visible through the outer. Seed shape from ellipsoid to ovoid. Epidermal seed coat cells with inner periclinal wall hidden by fibrillar outer periclinal wall; anticlinal walls of slight or medium depth. Seeds oblongoid, ellipsoid, ovoid to globose. Epidermal seed coat with reticulate inner periclinal wall visible through the fibrillar outer periclinal wall; anticlinal walls slightly to very deep. The results obtained confirm the usefulness of seed characters for the identification of most of the species studied, and highlight the division of the genus into two sections Trionychon and Orobanche , as has been traditionally recognized Beck von Mannagetta, ; Chater and Webb, ; Foley, ; Pujadas, Within each taxon, the size of the seeds is very variable. However, at species level, seed size helps to identify some taxa such as O. Seed shape is also a variable character, ranging from oblongoid, ellipsoid to ovoid, although they are sometimes globose or subglobose. This character is related to its relative position in the capsule, as in the case of the Scrophulariaceae Juan et al. The most extreme case is O. As far as ornamentation is concerned, our results agree with other authors Ungurean, ; Joel, a , b ; Abu Sbaih and Jury, a , b , showing that the genus Orobanche has reticulate seeds, although Teryokhin described them as alveolate due to invagination of the thin outer wall of the epidermal seed coat cells. The periclinal walls of the epidermal seed coat cells are of particular taxonomic interest, especially the inner wall, which remains intact since it is lignified. Therefore, they considered the outer wall to be of greater interest as it allowed them to distinguish four groups of species. In the present study, the epidermal seed coat cells permitted the discrimination of four morphological types, based on observations of both inner and outer periclinal walls. However, it has not been possible to find any correlation between the types or subtypes established in the present study and the sections or groups grex based on the vegetative characters of the different taxa established by Beck von Mannagetta , or on the results of the recent molecular analyses by Schneeweiss , Benharrat et al. Type I, which includes O. Previously, Andary had already found morphological differences in the seeds of this taxon when comparing them with those of other species in the section Orobanche. Its genetic and morphological separation in relation to the rest of the species of the section Orobanche is therefore obvious. Type II section Orobanche , which shows the epidermal seed coat cells with perforate inner periclinal wall that are visible through the smooth outer periclinal wall, includes a greater number of species. Abu Sbaih and Jury a observed that in four species of the section Orobanche O. Moreover, it has been observed that within this group the diameter of such perforations on the inner wall vary amongst species, thus allowing for the distinction of three separate subgroups. This character has previously been used in species of the section Trionychon by Ungurean , who distinguished two groups: one with numerous and small perforations, and the other with scarce, large ones. We agree with this author that the thickening of the inner wall gives seeds their reticulate aspect. This pattern has not previously been observed by other authors Ungurean, ; Joel, a , b ; Abu Sbaih and Jury, a , b. Even through they show the same seed type, these species O. Type IV, as has been pointed out above, includes all species belonging to the section Trionychon except for O. The separation of O. Thus, Schultz includes it in Boulardia under the name of B. More recently, Schneeweiss , despite the fact that he includes it once again within the genus Orobanche as O. Previously, some authors such as Teryokhin have included certain species of the Orobanche genus section Trionychon in the genus Phelipanche , the presence of fibrillar outer periclinal walls of epidermal seed coat cells being one of distinctive characters. Results subsequently obtained in the molecular study carried out by Schneeweiss support this separation. However, in the present work it has been shown that O. Besides, a recent phylogenetic study points out that O. In conclusion, it is clear that there are still several issues to solve. Regarding the two subgroups, IV A and IV B , established on the basis of the visibility of the inner wall of the epidermal cells, these differ from subgroups obtained by other means of analysis Velasco et al. In spite of the homogeneity of the seeds in this genus, pointed out by Abu Sbaih and Jury a , b , our results have enabled us to produced a key Table 5 in a similar manner to the one designed by Joel a for six species from Israel. In our key, most taxa have been separated except for six cases where two or three species have been grouped together O. Some of the features of the Orobanche seeds, such as the terminal insertion and the reticulate ornamentation, show the similarity that exists between this genus and the hemiparasite species of Scrophulariaceae Chuang and Heckard, ; Musselman and Mann, ; Canne, ; Juan et al. In addition, the results of the present study highlight, to some extent, the importance of the morphology of seeds in relation to dispersal or to the establishment of new plants. According to Musselman and Mann , the size of the seeds could be the result of an adaptation of these plants in an attempt to be dispersed through vegetation so as to be as close as possible to the host plant. Similarly, according to Stace , the high production of seeds per capsule is an adaptation of this type of plant aimed at increasing the probability of finding an appropriate host. The membranous outer periclinal wall of the epidermic cells would favour water absorption, thus enhancing the adherence and germination capacity, as in some examples of the family Lamiaceae Ryding, Orobanche alba Stephan ex Willd. Orobanche amethystea Thuill. Alicante, Cap de les Hortes, 17 Apr. Orobanche arenaria Borkh. Orobanche ballotae A. Orobanche caryophyllaceae Sm. Orobanche cernua L. Granada, Sierra Parapanda, 28 Jun. Orobanche crenata Forssk. COA Orobanche crinita Viv. Menorca, ES Castell, 13 Apr. Orobanche cumana Wallr. Sevilla, Km 3 from Ecija to Estepa, 1 Jul. Sevilla, El Coronil, 16 Jun. Orobanche densiflora Reut. Orobanche elatior Sutton subsp. Orobanche foetida Poir. Huelva, El Conquero, 10 Jun. Orobanche gracilis Sm. Orobanche haenseleri Reut. Burgos, Munilla, 31 Jul. Atlantiques Le Piquet de Lhurs, 25 Agu. Orobanche latisquama F. Schultz Batt. Orobanche montserratii A. Orobanche mutelii F. Orobanche nana Reut. Orobanche olbiensis Coss. Pinet beach, Santa Pola, 22 Jun. Orobanche purpurea Jacq. Orobanche ramosa L. Granada, El Jau, 21 Sep. Granada, Cullar de Vega, 5 Oct. Granada, La Zubia, 27 Agu. Madrid, El Escorial, 23 Jun. Orobanche reticulata Wallr. Granada, Sierra Parapanda, Illora, 07 Jun. JACA Scanning electron micrographs of Orobanche seeds. A—C Type I, O. D—L Type II. D—I Type IV. Four morphological seed types of Orobanche as indicated by observations made using scanning electron microscopy. Three subtypes of Type II seeds as indicated by differences observed in the diameter of the perforations of the inner periclinal wall. Seed micromorphology and taxonomy in Orobanche Orobanchaceae. Flora Mediterranea 4 : 41 — The seed micromorphology of the genus Orobanche Orobanchaceae. Proceedings of the 3rd International Workshop on Orobanche and related Striga research. Pollen morphology of the genus Orobanche Orobanchaceae. Andary C. Chemotaxonomical study of the genus Orobanche. Proceedings of the 3 rd International Workshop on Orobanche and related Striga research. Beck von Mannagetta G. Monographie der Gattung Orobanche. Bibliotheca Botanica 19 : 1 — In: Engler A, ed. Das Pflanzenreich, vol IV. Leipzig: Verlag von Wilhelm Engelmann, 1 — Broomrape identification using inter simple sequence repeat ISSR. Application to Tryonychon Wallr and Osproleon section species. Proceeding of the 7th International Parasitic Weed Symposium. Nantes, France, Boeshore I. The morphological continuity of Scrophulariaceae and Orobanchaceae. Authors of plant names. Richmond: Royal Botanic Gardens, Kew. Canne JM. A light and scanning electron microscope study of seed morphology in Agalinis Scrophulariaceae and its taxonomic significance. Systematic Botany 4 : — Systematic Botany 5 : — Flora Europaea, 3. Cambridge: Cambridge University Press, — Seed coat morphology in Cordylanthus Scrophulariaceae and its taxonomic significance. American Journal of Botany 59 : — Cosson ESC. Annales des Sciences Naturelles Botanique Paris, series 3 9 : — Cronquist A. An integrated system of classification of flowering plants. New York: Columbia University Press. Cytogeography and taxonomy of the Portulaca oleracea L. Israel Journal of Botany 27 : — A taxonomic study on the populations of three common species of the genus Orobanche L. Orobanchaceae in Egypt. Plant systematics for the 21 st Century. London: Portland Press, — Foley MJY. Flora Iberica, Madrid: CSIC, 32 — Font Quer P. Barcelona: Labor. Index Herbariorum. Part 1. The herbaria of the world , ed. Regnum Vegetabile Hutchinson J. Evolution and phylogeny of flowering plants. New York: Academic Press. Joel DM. Detection and identification of Orobanche seeds using fluorescence microscopy. Seed Science and Technology 15 : — Identification of Orobanche seeds. Parasitic flowering plants. A key for the identification or Orobanche seeds. Phytoparasitica 16 : — Orobanche cumana , a new adventive weed in Israel. Phytoparasitica 16 : Systematic consideration of microcharacters of fruits and seeds in the genus Verbascum Scrophulariaceae. Annals of Botany 80 : — Seed morphology in Veronica L. Botanical Journal of the Linnean Society : — Estudio de frutos y semillas en Parentucellia Viv. Annals of Botany 84 : 11 — SEM and light microscope observations on fruit and seeds in Scrophulariaceae from southwest Spain and their systematics significance. Annals of Botany 86 : — Kuijt J. The biology of parasitic flowering plant. Lange JMCh. Pugillus plantarum imprimis hispanicarum, quas in itinere —52 legit Jon. Minkin PJ. Pollen morphology of the Orobanchaceae and rhinanthoid Scrophulariaceae with reference to their taxonomy. Pollen morphology of the Orobanchaceae and rhinanthoid Scrophulariaceae. Grana 28 : 1 — A survey of surface characteristics of seeds of Scrophulariaceae and Orobanchaceae using scanning electron microscopy. Phytomorphology 26 : — Novopokrovsky NN , Tzelev P. In: Schischkin BK, ed. Flora of the U. Enfield, NH: Science Publishers, 21 — Disintegration of Scrophulariaceae. American Journal of Botany 88 : — Principles of dispersal in higher plants. Polo JM. Salamanca: — Pujadas A. Pujadas Orobanchaceae , especie nueva. Orobanche L. Orobanchaceae , Sect. Trionychon Wallr. Orobanche almeriensis A. Orobanche tunetana G. Beck Orobanchaceae , especie nueva para el continente europeo. Annals of Botany 91 : — An analysis of genetic variation in natural populations of Orobanche foetida from Spain and Tunisia. Nantes, France, 57 — Ryding O. Pericarp structure and phylogeny within Lamiaceae subfamily Nepetoideae tribe Ocimeae. Nordic Journal of Botany 12 : — Schneeweiss GM. Relationships within Orobanche sect. Tryonychon: insights from its sequences markers. Nantes, France, 49 — Schultz FW. Stace CA. In: Heywood VH, ed. Las plantas con flores. Stearn WT. Botanical Latin. Sutton DA. A revision of the tribe Antirrhineae. Takhtajan A. Outline of the classification of flowering plants Magnoliophyta. Botanical Review 46 : — Teryokhin ES. Orobanche research in the USSR. Progress in Orobanche research. Proceedings of the International Workshop on Orobanche Research. Weed broomrapes, systematics, ontogenesis, biology, evolution. Ungurean L. Polen, esporas y sus aplicaciones. Granada: Facultad de Ciencias, — Fatty acids and tocochromanols in seeds of Orobanche. Phytochemistry 54 : — Weber HC. Zur Evolution des parasitismus bei den Scrophulariaceae und Orobanchaceae. Plant Systematics and Evolution : — Annals of the Missouri Botanical Garden 86 : — Oxford University Press is a department of the University of Oxford. It furthers the University's objective of excellence in research, scholarship, and education by publishing worldwide. Sign In or Create an Account. Sign in through your institution. Annals of Botany Company Journals. Advanced Search. Search Menu. Article Navigation. Close mobile search navigation Article Navigation. Volume Article Contents Abstract. Journal Article. Oxford Academic. Google Scholar. Cite Cite L. Select Format Select format. Permissions Icon Permissions. Open in new tab Download slide. Table 1. Open in new tab. Epidermal cells with smooth outer periclinal wall 2 2. Outer periclinal walls allow vision of the inner one 3 3. Inner periclinal wall granulate or rugulose Type III. Table 2. Table 3. Inner periclinal walls of epidermal seed coat cells with perforations similar in diameter or superior to the thickness of the walls that separate them; small central mammilla absent on cells 2 2. Inner periclinal walls of epidermal seed coat cells with perforations larger in diameter than the thickness of the walls that separate them Subtype II C. Table 4. Table 5. Epidermal seed coat cells with fibrillar outer periclinal walls 20 2. Outer periclinal walls impede vision of inner ones; anticlinal walls thickening at the vertices O. Outer periclinal walls allow vision of inner ones; anticlinal walls of even or uneven thickness 3 3. Epidermal seed coat cells with rugulose or granulate inner periclinal wall 18 4. Cells of inner periclinal wall without a central mammilla 6 5. Inner periclinal wall of epidermal seed coat cells with perforations of diameter similar to or greater than the thickness of the walls that separate them 9 7. Epidermal seed coat cells in the mid and insertion areas tangentially elongated and isodiametric at the opposite end O. Epidermal seed coat cells isodiametric on the entire surface 8 8. Anticlinal wall junctures with a narrow trough that is visible all around the edge of the cells O. Anticlinal wall junctures with a narrow trough that is evident at the vertices of the cells O. Perforations with a diameter which is larger than the thickness of the separating wall 16 Epidermal seed coat cells with anticlinal walls of medium depth 13 Anticlinal wall junctures with a narrow trough that is visible all around the edge of the cells 12 Tangentially elongated epidermal seed coat cells, whose size decreases at the area of insertion; seeds ovoid to oblong O. Isodiametric epidermal seed coat cells on the entire surface; seeds ovoid to subglobose O. Anticlinal wall junctures with a narrow trough that is evident at the vertices of the cells 15 Epidermal seed coat cells tangentially elongated which and narrow and decrease at the area of insertion O. Epidermal seed coat cells more or less isodiametric or irregular O. Epidermal seed coat cells tangentially elongated O. Epidermal seed coat cells more or less isodiametric O. Epidermal seed coat cells with anticlinal walls of remarkable depth and unevenly thickened O. Epidermal seed coat cells with anticlinal walls of slight or medium depth and evenly thickened 17 Seeds trigonous to tetragonal O. Seeds ovoid to oblongoid O. Epidermal seed coat cells with anticlinal walls of remarkable depth O. Epidermal seed coat cells with anticlinal walls of medium depth 19 Epidermal seed coat cells tangentially elongated or irregular; seeds oblongoid O. Epidermal seed coat cells more or less isodiametric at the vertices, tangentially elongated over the rest of the surface; seeds ovoid to ellipsoid O. Reticulate inner periclinal wall visible through the outer one 24 Epidermal seed coat cells with anticlinal walls of slight depth, and a narrow trough that is visible all around the edge of the cells O. Epidermal seed coat cells with anticlinal walls of medium depth and a narrow trough that is evident just at the vertices 22 Epidermal seed coat cells with anticlinal walls unevenly thickened O. Epidermal seed coat cells with anticlinal walls evenly thickened 23 Epidermal seed coat cells with anticlinal walls of medium depth O. Epidermal seed coat cells with anticlinal walls of remarkable depth 26 Anticlinal walls evenly thickened O. Anticlinal walls unevenly thickened O. Issue Section:. Download all slides. Views 1, More metrics information. Total Views 1, Email alerts Article activity alert. Advance article alerts. New issue alert. Receive exclusive offers and updates from Oxford Academic. Citing articles via Web of Science Latest Most Read Most Cited Integrating datasets from herbarium specimens and images to treat a Neotropical myrtle species complex. High frequency of ambophily in a Brazilian campos de altitude. Among- and within-population variation in germination response shapes ecological resilience in the Mediterranean cliff species Brassica incana. Responses of oak seedlings to increased herbivory and drought: a possible trade-off? Offspring may succeed well next to their relatives, but it needs particular traits. More from Oxford Academic. Biological Sciences. Ecology and Conservation. Evolutionary Biology. Plant Sciences and Forestry. Science and Mathematics. Authoring Open access Purchasing Institutional account management Rights and permissions. Get help with access Accessibility Contact us Advertising Media enquiries. Inner periclinal walls of epidermal seed coat cells with perforations smaller in diameter than the thickness of the walls that separate them; a small central mammilla sometimes present on cells. Inner periclinal walls of epidermal seed coat cells with perforations similar in diameter or superior to the thickness of the walls that separate them; small central mammilla absent on cells. Inner periclinal walls of epidermal seed coat cells with perforations similar in diameter to the thickness of the walls that separate them. Inner periclinal walls of epidermal seed coat cells with perforations larger in diameter than the thickness of the walls that separate them. Inner periclinal wall of epidermal seed coat cells with perforations of smaller diameter than the thickness of the walls that separate them. Inner periclinal wall of epidermal seed coat cells with perforations of diameter similar to or greater than the thickness of the walls that separate them. Epidermal seed coat cells in the mid and insertion areas tangentially elongated and isodiametric at the opposite end. Tangentially elongated epidermal seed coat cells, whose size decreases at the area of insertion; seeds ovoid to oblong. Epidermal seed coat cells tangentially elongated which and narrow and decrease at the area of insertion. Epidermal seed coat cells more or less isodiametric at the vertices, tangentially elongated over the rest of the surface; seeds ovoid to ellipsoid. Epidermal seed coat cells with anticlinal walls of slight depth, and a narrow trough that is visible all around the edge of the cells. Epidermal seed coat cells with anticlinal walls of medium depth and a narrow trough that is evident just at the vertices.

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