Embryology and its character evolution in Staphyleaceae Author(s): Takuya Ishida and Toru Tokuoka Source: Plant Systematics and Evolution, Vol. 303, No. 10 (December 2017), pp. 1317-1329 Published by: Springer Stable URL: https://www.jstor.org/stable/44853800 Accessed: 06-07-2021 08:50 UTC JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at https://about.jstor.org/terms Springer is collaborating with JSTOR to digitize, preserve and extend access to Plant Systematics and Evolution This content downloaded from 86.59.13.237 on Tue, 06 Jul 2021 08:50:30 UTC All use subject to https://about.jstor.org/terms Plant Syst Evol (2017) 303:1317-1329 (jjj CrossMark https://doi.org/10.1007/s00606-017-1455-2 ORIGINAL ARTICLE Embryology and its character evolution in Staphyleaceae Takuya Ishida1 • Toru Tokuoka1 Received: 13 February 2017 / Accepted: 18 August 2017 / Published online: 5 September 2017 © Springer-Verlag GmbH Austria 2017 Abstract The family Staphyleaceae, which was Keywords recently Dalrympelea • Embryology • Seed coat • reorganized into the two genera Staphylea and Dalrympelea Staphylea • Staphyleaceae based on molecular phylogenetic analyses, is sister to a clade of Crossosomataceae, Guamatelaceae, and Stachyuraceae in the order Crossosomatales. In contrast to Crossosomata- Introduction ceae and Stachyuraceae, the embryology of Staphyleaceae has been scarcely studied. We carried out a literature sur- Staphyleaceae Martynov comprises the two genera vey and examined three additional species of each genus in Staphylea and Dalrympelea and 43-48 species (Simmons order to better understand the evolution of the embryological 2007), and is distributed not only in the Northern Hemi- characters in the family. Characters were nearly identical sphere of both the old and new world, but also extends south across examined species. Staphyleaceae shared most char- beyond the equator in Ecuador, Peru, Bolivia, and Southeast acters of nucellus, megagametophyte, and integuments with Asia to Papua New Guinea. The relationships of the family Stachyuraceae with the exception of several embryological have been controversial, and it had previously been placed in characters. The presence of a nucellar cap was found to be the Celastrales (Bessey 1915; Rendle 1925; Wettstein 1935; informative and supports the close relationship between Scholz 1964) or the Sapindales (Hutchinson 1926, 1973; Staphyleaceae and Stachyuraceae. We also investigated the Cronquist 1981, 1988; Takhtajan 1997). However, recent evolution of variable characters among Crossosomataceae, molecular phylogenetic studies have placed the family in Stachyuraceae, and Staphyleaceae. Staphyleaceae species the Crossosomatales, which comprises the seven families share the presence of a single archesporial cell and absence Aphloiaceae, Geissolomataceae, Strasburgeriaceae, Staphyl- of an aril as symplesiomorphies. The presence of less than eaceae, Guamatelaceae, Stachyuraceae, and Crossosomata- five parietal cells in the nucellus is a possible synapomorphy ceae (Angiosperm Phylogeny Group 2003, 2009, 2016). for the genus Staphylea , while presence of vascular bundles Staphyleaceae are sister to a clade of Crossosomataceae, in the testa is a possible synapomorphy for Staphyleaceae. Guamatelaceae, and Stachyuraceae. The remaining other Our observations support the identification of the seed coat three families form a clade in the order (Nandi et al. 1998; as mesotestal. Several variant embryological characters Savolainen et al. 2000a, b; Soltis et al. 2000). within the family are discussed. Classification within the family has also been con- troversial. The family previously comprised five genera, Euscaphis , Huertia, Staphylea , Tapiscia , and Turpinia Handling editor: Louis P. Ronse De Craene. (Bentham and Hooker 1867; Cronquist 1981). Recent stud- ies led to Tapiscia and Huertia being separated to form Ē3 Toru Tokuoka Tapisciaceae (Huerteales), and the remaining three genera tokuoka. toru @ shizuoka.ac.jp forming Staphyleaceae (Takhtajan 1997). Simmons (2002) conducted a molecular phylogenetic analysis using 4060 1 Department of Biological Science, Faculty of Science, Shizuoka University, Ohya, Suruga-ku, Shizuoka 422-8529, aligned nucleotide positions from the internal transcribed Japan spacer (ITS), 3' trnK intron, 23S-16S spacer, trnL intron, Springer This content downloaded from 86.59.13.237 on Tue, 06 Jul 2021 08:50:30 UTC All use subject to https://about.jstor.org/terms 1318 T. Ishida, T. Tokuoka and the rps'2-rpl20 cells are radially elongated in Staphylea japonicaspacer and S. pin- of 27 species of the three gen- era. Based on nata, but arethese flattened in Dalrympelea results, grandis (= Turpinia Staphylea and Turpinia (but not the monotypie grandis). A multiplicative Euscaphis) and sclerotic mesotesta, degen- were polyphyletic, and the family was reorganized erated endotesta, and tegmenaccordingly have been described (Guérin into the two genera, Staphylea and Dalrympelea. 1901; Netolitzky 1926; Corner In 1976). On thethis basis of these scheme, the genus Staphylea com- prises 23 species observations, Corner (1976, including p. 1 1) suggested that the type the Euscaphis species and some Turpinia species; of seed coat was exotestal, but thatDalrympelea this would have to be consists of the remaining 21 species of confirmed Turpiniaby further samples. Corner (1976) also observed (Simmons 2002). However, another study suggested vascular bundles in the seedthat coat, and noted that thethe vascular monotypie Euscaphis is a sister taxon to the bundles evidently clade spread from the chalaza of and form a plexusStaphylea and Turpinia (Wen et al. unpublished in the innerdata layer of the testal in mesophyll inHuang four species of et al. 2015). Embryology Staphyleaceae. has The presence offrequently vascular bundles in the testa provided useful evidence for relationships is a possible significantbetween synapomorphy for the family andand within various families (Tobe 1989). The embryology warrants further investigation, including detailed morpho- of Staphyleaceae has received some attention (Guérin logical studies, of this species. 1901; Mottier 1914; Narayana 1960; Dick- ison 1986; Matthews This paper presents a description of almost all embry-and Endress 2005). The anatropous, crassinucellate, ological characters ofand Staphyleaceae bybitegmic combining data ovule and characters of the anthers in Staphyleaavailable from earlier studies with new results. Basedtrifoliata, on S. colchica , and Dalrympe- lea montana embryological (= evidence,Turpinia we also discuss the evolution of nepalensis) were described before (Guérin 1901; embryological Narayana characters within the Crossosomatales. 1960; Dickison 1986; Matthews and Endress 2005). However, the development of the nucellus, integuments, endosperm, and embryo are scarcely known. On the other Materials andhand, methods the embryology of Stachyuraceae and Crossosomataceae has been well investigated (see table in Kimoto and Flower budsTokuoka and fruits of Staphylea bumalda DC., 5. japon-1999), although Guamatelaceae has never been icastudied (Thunb.) Simmons, and Dalrympelea embryologically. ternata (Nakai) Thus, the evolution of the embryological Simmons were collected and fixed charactersin FA A (5 parts stock within the clade of the four families including formalin; 5 parts glacial acetic acid;Staphyleaceae 90 parts 50% ethanol). could be clarified by the addition of Collectiona datathorough and developmental stages of materials exam-study of Staphyleaceae. Among the embryological ined are presented characters, in Table 1 . the presence of a nucellar cap is a feature of Alltaxonomie embryological characters were observed usingimportance in several families (Johri et al. 1992). microtomeDalrympelea sections. Materials were dehydrated through a montana and Stachyuraceae share nucellar caps r-butyl alcoholwith series, and then embeddedtwo in Paraplast withto three cell layers (Narayana 1960; Kimoto and a meltingTokuoka point of 57-58°C for microtoming. 1999), If the seeds but no information is available for the other were too hardStaphyleaceae. to be sectioned, they were softened with a The seed coat structure has also been useful in estab- mixture of 10 parts glycerol, 3 parts 10% aerosol OT, and lishing relationships between and within families (Tokuoka 90 parts water for about 1 week, following Tokuoka and and Tobe 2001, 2002, 2003; Tokuoka 2007). The structure Tobe (2001) (also Schmid and Turner 1977). Serial sec- of the seed coat has been studied in five species of the two tions 6 pm in thickness were stained with Heidenhain's genera of Staphyleaceae including Euscaphis japonica. The hematoxylin, safranin, and fast green FCF, and mounted morphology of the exotesta varied within the family; the in Entellan. Table 1 Examined species of Staphyleaceae and collections Species Collection Developmental stages Staphylea bumalda DC Japan. Shizuoka. Ishida 1 30428 1, 1305101, 1305221, 1 30607 1 , Youngest flower buds to mature fruits 1406011, 1407231, 1409161 (KYO) Staphylea japonica (Thunb.) Simmons Japan. Shizuoka. Ishida 1 30508 1 , 1 305 1 3 1 , 1 3052