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Phylogenetic Relationships of Salix L. Subg. Salix Species (Salicaceae) According to Sequencing Data of Intergenic Spacers of the Chloroplast Genome and ITS Rdna V

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Phylogenetic Relationships of Salix L. Subg. Salix Species (Salicaceae) According to Sequencing Data of Intergenic Spacers of the Chloroplast Genome and ITS Rdna V ISSN 10227954, Russian Journal of Genetics, 2014, Vol. 50, No. 8, pp. 828–837. © Pleiades Publishing, Inc., 2014. Original Russian Text © V.Yu. Barkalov, M.M. Kozyrenko, 2014, published in Genetika, 2014, Vol. 50, No. 8, pp. 940–949. PLANT GENETICS Phylogenetic Relationships of Salix L. subg. Salix Species (Salicaceae) according to Sequencing Data of Intergenic Spacers of the Chloroplast Genome and ITS rDNA V. Yu. Barkalov and M. M. Kozyrenko Institute of Biology and Soil Science, Far Eastern Branch of the Russian Academy of Sciences, Vladivostok, 690022 Russia email: [email protected] Received January 29, 2014 Abstract—A phylogenetic analysis based on a comparison of nucleotide sequences of six regions (petN– psbM, trnD–trnT, trnC–petN, psaA–ycf3, petG–trnP, and rpoB–trnC) of cpDNA and ITS rDNA allowed for elucidating the relationship among species and sections belonging to the Salix subgenus and, more generally, to the Salix genus, as well as revealing the relations of the Chosenia genus. The definition of the subgenera Pleuradenia (including the Urbanianae section and the Chosenia genus), Salix (without the Triandrae sec tion), Triandrae, and Longifoliae is essentially consistent with current classification schemes of the Salix genus. The previously defined genera of Chosenia and Toisusu (Urbanianae) are not only merged with the Salix genus but are also closely related between themselves. The Protitea subgenus only corresponds to the American species of the Humboldtianae section (S. humboldtiana, S. amygdaloides, S. gooddingii). The rela tionship of S. chaenomeloides, which is a nomenclatural type of this subgenus, as well as the relationship of the Wilsonia section, remains unresolved. The Humboldtianae section should be interpreted more narrowly, apparently, separating Acmophyllae and Tetraspermae sections from it. The monotypic American Floridanae section is related to the Salix, Salicaster, Tetraspermae, and Wilsonia sections. DOI: 10.1134/S1022795414070035 INTRODUCTION proposed a subdivision of the Salix genus into three subgenera: Chosenia, Salix, and Vetrix. The genus of Salix L. includes 300 to 450 species, which are especially widespread in areas of Eurasia Molecular genetic studies with the use of nuclear and North America [1–4] with cold and temperate and chloroplast markers revealed a number of discrep climates and diversified in the mountains of southwest ancies in the traditional classification of Salix based China [1, 5, 6]. The genus represents one of the most mainly on morphological characteristics (e. g., [1, 3, complex taxonomical groups of flowering plants, with 13, 14]). For the first time, the suggested phylogenetic its intrinsic broad range of variability and interspecific relationships among 18 taxons of Salicaceae family, hybridization. The classification schemes of the Salix including Chosenia and a few representatives of Salix, genus, as well as the entire Salicaceae family in the were reconstructed based on the sequences of two narrow meaning, remain contradictory. Researchers internal transcribed spacers (ITS1, ITS2)[1–2] and in Russia traditionally consider the genus Chosenia the 5.8S rRNA gene (ITS rDNA) from the nuclear Nakai as a separate one [1, 2, 7–9] or accept the genus ribosomal operon [15]. Samples of Chosenia and Salix of Toisusu Kimura too [2, 10, 11]. A.K. Skvortsov [1– constituted a monophyletic group with high signifi 5] subdivided the Eurasian species of the Salix genus cance; however, the results give no clear support to any into three subgenera: Salix, Chamaetia (Dumort.) specific affiliation of Chosenia arbutifolia (Pall.) Nasarov, and Vetrix (Dumort.) Dumort. Ohashi [4] A. K. Skvortsov (reffered to as C. bracteosa (Turcz. ex assumed a broad concept of the Salix classification Trautv.) Nakai). Based on the analysis of the rbcL gene and subdivided the willows of Japan into six subgen of the chloroplast DNA (cpDNA) were shown that era: Pleuradenia Kimura, Chosenia (Nakai) H. species from three recognized genera Chosenia, Salix Ohashi, Protitea Kimura, Chamaetia, Salix, and and Toisusu form a monophilitic group [16]. However, Vetrix. Argus, while studying the New World Salix spe the data did not clarify the relationship of this group of cies [3], assumed the American Longifolae section to constituents. According to the results of the analysis of be a separate subgenus rank—Salix L. subgen. Longi the three markers (rbcL, trnD–trnT, and atpB–rbcL) foliae (Andersson) Argus, and placed the sections of cpDNA [17], Chosenia was included into Salix as Humboldtianae and Floridanae in the Protitea subge the separate subgenus rank. Also, it was suggested to nus. Chen et al. [12], based on a cladistics analysis, subdivide Salix s.1. into four subgenera: Triandrae, 828 PHYLOGENETIC RELATIONSHIPS 829 Salix (excluding the sections Triandrae and Urbani Subalbae anae), Chosenia (including the Urbanianae section), and Vetrix (includes species from the previously defined subgenera Vetrix and Chamaetia). This did not Salix confirm the view of Chao et al., who recognized the Pleiarina Raf. genus [18]. Based on a comparison of the ITS rDNA and matK gene sequences [19] partly Wilsonia Triandrae supported the mostrecent intragenus classification of (Glandulosae) (Amygdalinae) New World willows [20]. Also, the relationships of Ira nian and Chinese Salix species were studied with the use of sequencing of ITS rDNA and trnL–F cpDNA Salicaster [21], and ITS rDNA [22], respectively. (Pentandrae) Humboldtianae Species of the Salix subgenus substantially prevail in wormtemperate and partly in tropical climates [1], and only a few of them are capable of inhabiting cold Urbanianae Longifoliae areas. In the Russian Far East, this group numbers six species, including two introduced species S. alba L. and S. babylonica L. Chosenia is widespread in north east Asia, penetrating deep into the permafrost areas of Chosenia SakhaYakutia and Chukotka. Since the Salix subgenus is characterized by differ ent sets of ancestral characters, it is particularly rich in Fig. 1. Phylogenetic scheme of Salix L. (Skvortsov [1]). taxonomic problems [19]. As was fairly noted by Skvortsov [1, page 76], “a significant discrepancy caster Dumort. (Pentadrae (Borrer) C.K. Schneid.), between the individual types therein can be identified, Humboldtianae Pax, Floridanae Dorn, Urbanianae (See and it is difficult to single out any particular type that men) C.K. Schneid, Subalbae Koidz., Longifoliae would be the most primitive in all respects: certain sec Andersson, Triandrae Dumort. (Amigdalinae W.D.J. tions are more primitive with respect to some features, Koch), and Wilsonia K.S. Hao ex C.F. Fang et A.K. others – with respect to other features”. According to Skvortsov (Glandulosae Kimura). The goal of this his view, this subgenus probably should be considered study is to clarify the phylogenetic relationship of spe as a natural (not polyphyletic) entity. Figure 1 shows cies and sections belonging to the Salix subgenus, as the author’s attempt to reconstruct the phylogenetic well as to identify the phylogenetic connections of connections within the Salix subgenus [1]. Chosenia based on a comparison of the nucleotide Unlike Skvortsov, Argus [3] noted that the Salix sequences of the intergenic spacers of petN–psbM, subgenus, on the modern treatments [1, 13, 23], is trnD–trnT, trnC–petN, psaA–ycf3, petG–trnP, and morphologically heterogeneous based on the combi rpoB–trnC of the chloroplast genome, and also ITS nation of primitive and progressive characters and he rDNA. suggested its polyphyletic. The volume of the Salix sub genus, as well as the Salix genus itself, is controversial because it results from the set of characters of different MATERIALS AND METHODS taxonomic importance. Moreover, some authors attempt Total genomic DNA of six species: Salix cardio to divide this subgenus using a single character, for phylla Trautv. et C. A. Mey. (Toisusu cardiophylla instance, a bud scale type [24, 25] or the number of (Trautv. et C. A. Mey.) Kimura), S. nipponica Franch. stamens [26]. Kimura [25] divided it into two subgen et Sav., S. pierotii Miq., S. pseudopentandra (Flod.) era, Protitea and Euitea, taking into account the bud Flod., S. arbutifolia (Chosenia arbutifolia), and Popu scale type, whereas Chao and Gong [26] referred all lus suaveolens Fisch., were isolated from leaf tissue multistamen willows (3–15 stamens) to the genus of dried in silica gel using a DNeasy Plant Mini Kit Pleiarina Raf. As is known, Skvortsov [1] did not agree (Qiagen, Hilden, Germany) according to the manu with the attempts to split the subgenus Salix into facturer’s instructions. The samples of this species smaller subgenera, but noted the most isolated posi were collected in natural populations (Table 1) and tion of two sections Urbanianae and Longifoliae and deposited in the collection of the Institute of Biology discussed their possible definition as separate subgen and Soil Sciences of the Far Eastern Branch of the era. Because of the similarity between Salix and Cho Russian Academy of Sciences (VLA). The authors of senia, this author also assumed considering Chosenia the taxon names were taken from the database of as a subgenus [7]. International Plant Names Index (IPNI; In this study, we use Skvortsov’s classification of http://www.ipni.org/ipni/authorssearchpage.do). Salix [1, 7]. In the Northern Hemisphere, the Salix Amplification of ITS rDNA and the petN–psbM, subgenus is subdivided into the sections Salix, Sali trnD–trnT, trnC–petN, psaA–ycf3, petG–trnP,
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