The position of two recently described endemic taxa in the system of the genus Saussurea (Asteraceae)

Abstract

Two new species of the genus Saussurea, endemic to the Chuya Steppe, wast intermountain depression in the south-east of the Russian part of the Altai Mountains, have recently been described on a morphological and phylogenetic basis. Saussurea draconis was found to be closely related to S. salsa and S. turgaiensis from S. sect. Laguranthera. Saussurea × magica was found to originate from the hybridisation between S. amara and S. daurica, belonging to S. sect. Theodorea and S. sect. Laguranthera, respectively. The polyphyly of the latter has been repeatedly demonstrated by the results of molecular phylogenetic analyses, and the position of the species of ser. Salsae (to which S. salsa, S. turgaiensis and S. daurica belong) in this section raises, in particular, obvious doubts. This prompted us to undertake an investigation of the aforementioned species, with a view to clarifying their systematic position, based on an analysis of the ITS1-5.8S-ITS2, rsp16-trnQ, ndhF-rpl32, ycf4-cemA regions and a comparative morphological analysis. The results of this investigation led to the conclusion that the position of S. × magica in S. subgen. Theodorea sect. Theodorea is confirmed. Saussurea salsa, S. daurica, S. turgaiensis, S. kaschgarica and S. pseudosalsa, i.e. species of the ser. Salsae, as well as S. draconis, were transferred from S. subgen. Saussurea sect. Laguranthera to S. subgen. Theodorea sect. Theodorea.

Acta Biologica Sibirica 10: 1479–1486 (2024)

doi: 10.5281/zenodo.14286645

Corresponding author: Daniil V. Yusupovsky (unitycoredown@gmail.com)

Academic editor: R. Yakovlev | Received 29 October 2024 | Accepted 18 November 2024 | Published 9 December 2024

http://zoobank.org/E4EC1760-E84B-403A-8E49-96BFC9A315DF

Citation: Yusupovsky DY, Pyak EA (2024) The position of two recently described endemic taxa in the system of the genus Saussurea (Asteraceae). Acta Biologica Sibirica 10: 1479–1486. https://doi.org/10.5281/zenodo.14286645

Keywords

Altai Mountains, taxonomic position, Theodorea, Salsae, Saussurea draconis, Saussurea×magica

Introduction

Recently, S. draconis Yusupovsky & E. Pjak was described as a new species, and S. × magica Yusupovsky & E. Pjak was described as a new nothospecies originated from the hybridisation between S. amara (L.) DC. and S. daurica Adams, based on phylogenetic and morphological data (Yusupovsky and Pyak 2024). As a result of this work, the systematic position of both the new species and the new nothospecies remained unclear. Saussurea draconis, which is closely related to S. salsa Spreng. and S. turgaiensis B. Fedtsch., was provisionally placed in S. subgen. Saussurea DC. sect. Laguranthera (C. A. Meyer ex Endlicher) Lipsch. However, the polyphyly of this section and the close affinity of the species belonging to S. sect. Laguranthera ser. Salsae Lipsch. to the species belonging to S. subgen. Theodorea (Cass.) Lipsch. sect. Theodorea (Cass.) Lipsch., has already been demonstrated previously, as shown by the results of molecular analyses by Raab-Straube (2003), Kita et al. (2004), Wang et al. (2009), Xu et al. (2019). Saussurea × magica was preliminary placed in S. subgen. Theodorea sect. Theodorea on the basis of the presence of membranous purple appendages on the phyllaries, which is the main diagnostic morphological feature of the section, but the parental species of S. × magica, i.e. S. amara and S. daurica, belong to the sections Theodorea and Laguranthera, respectively. This highlights the necessity for a molecular and morphological investigation of this group to accurately determine the systematic position of the recently described species.

Materials and methods

To study the systematic position of these taxa, we included DNA sequences of 51 species from S. subgen. Theodorea sect. Theodorea (16 of 22 species), S. subgen. Saussurea sect. Laguranthera (21 species), S. subgen. Saussurea (2 species from S. sect. Rosulascentes (Kitam.) Lipsch., 2 species from S. sect. Lagurostemon (Cass.) DC., 2 species from S. sect. Strictae C. B. Clarke, 1 species from S. sect. Gymnocline Franch., 3 species from S. sect. Saussurea), S. subgen. Eriocoryne (DC.) Hook. f. sect. Eriocoryne (Wall. ex DC.) Hook. f. (2 species) and S. subgen. Amphilaena (Stschegl.) Lipsch. sect. Amphilaena (Stschegl.) Lipsch. (2 species) to construct phylogenetic networks and midpoint-rooted phylogenetic trees. In total, 120 sequences were downloaded from GenBank and 36 sequences were generated for this study. All voucher specimens (see Suppl. material 1: Table 1) were deposited in the P.N. Krylov Herbarium of Tomsk State University (TK), NCBI GenBank accession numbers are listed in Suppl. material 2: Table 2. The morphological analyses were based on both field observations and herbarium specimens, either collected by the authors or previously deposited in the herbaria (TK, MW, LE). Detailed floral morphology was observed from dried herbarium material using a Zeiss Stemi 508 stereo microscope (Carl Zeiss, Oberkochen, Germany).

Total genomic DNA was extracted from silica gel dried young leaves using a commercially available kit, D-Plants-250 (Biolabmix, Novosibirsk, Russia). All amplification primers and detailed amplification protocol are presented in the previous study (Yusupovsky and Pyak 2024). Neighbor-net phylogenetic networks based on ITS1-5.8S-ITS2 and concatenated ITS1-5.8S-ITS2 and rsp16-trnQ + ndhF-rpl32+ ycf4-cemA data sets were constructed in SplitsTree 4 (Huson and Bryant 2006) using uncorrected Hamming distances. Phylogenetic trees were constructed using the Bayesian and Maximum likelihood methods based on ITS1-5.8S-ITS2 data set. Bayesian analyses were conducted using Mr.Bayes 3.2.6 (Ronquist et al. 2012) with four simultaneous Markov Chain Monte Carlo (MCMC) of 1000000 generations, with one tree sampled every 500 generations until the average deviation of split frequencies reached a value below 0.01. The optimal evolutionary model was identified using MrModelTest 2.3 (Nylander 2004) and PAUP (Swofford 2003), in accordance with AIC, which was determined to be GTR+G. Maximum likelihood tree was reconstructed using IQ-TREE 1.6.12 (Nguyen et al. 2015) with the best-fit model TNe+G4 calculated using ModelFinder (Kalyaanamoorthy et al. 2017). Branch support was obtained through the using of 100000 ultra-fast bootstrap replicates (Hoang et al. 2018). Reconstructed phylogenetic trees were drawn in the FigTree 1.4.4 (Rambaut 2012).

Result

The topologies of the ITS1-5.8S-ITS2 phylogenetic trees yielded by Maximum likelihood and Bayesian analyses were found to be congruent. Consequently, only the Maximum likelihood tree is presented (Fig. 1B). The phylogenetic analysis revealed that S. salsa, S. turgaiensis, S. kaschgarica Rupr., S. pseudosalsa and S. daurica, which belong to ser. Salsae (Lipschitz 1979), as well as S. draconis and S. × magica, form a strongly supported clade (PP = 1, BS = 100) with all species of sect. Theodorea included in the analysis, with the exception of S. nematolepis Ling, S. pseudomalitiosa Lipsch. and S. chingiana Hand.-Mazz., resulted to be sister to the species of sect. Laguranthera (PP = 0.99, BS = 82). Possible network-like evolutionary relationships among the studied species, reconstructed based on the ITS1-5.8S-ITS2 marker, are in agreement with the results of the ML and BA analyses about the main groups (Fig. 1A). The combined ITS1-5.8S-ITS2 and rsp16-trnQ + ndhF-rpl32 + ycf4-cemA data sets yielded a splits graph that did not show incongruence between the nuclear and chloroplast datasets, indicating a lack of conflict in the position of S. draconis, S. × magica, S. salsa, S. turgaiensis, S. kaschgarica, S. pseudosalsa and S. daurica within sect. Theodorea (Fig. 2). The obtained splits graph confirms the close affinity of S. draconis, S. × magica and the species belonging to ser. Salsae with S. amara, S. japonica (Thunb.) DC., S. pinnatidentata Lipsch., S. pulchella (Fisch.) Fisch., S. paradoxa Lipsch., S. ceterachifolia Lipsch., S. laciniata Ledeb., S. runcinata DC., S. robusta Ledeb. belonging to sect. Theodorea. This group is well separated (BS = 99.9) from all other species belonging to sect. Laguranthera included in the study.

Comparative morphological analysis of the included species revealed that the representatives of sect. Theodorea possess a complex morphology of vegetative and generative organs. Saussurea laciniata, S. ramosa Lipsch., S. ceterachifolia, S. runcinata, S. paradoxa, S. alata DC. are characterised by the presence of fleshy leaves, phyllaries with a small and membranous purple appendage at the apex and few to many stems. Saussurea salsa, S. turgaiensis, S. kaschgarica, S. pseudosalsa and S. draconis are also characterised by the presence of fleshy leaves, few to many stems (solitary to few in S. pseudosalsa), but their phyllaries are without a membranous appendage at the apex. Saussurea robusta and S. nematolepis have non fleshy leaves, solitary stem, and the phyllaries without membranous appendage, but apically subulate and reflexed. Saussurea japonica (Thunb.) DC., S. pulchella, S. amara, S. pseudomalitiosa and S. chingiana are characterised by non fleshy leaves, solitary stem and phyllaries with a small and membranous purple appendage. Saussurea prostrata C. Winkl., S. pinnatidentata Lipsch. and S. × magica possess fleshy leaves, solitary stem (solitary to few in S. prostrata) and phyllaries with a small and membranous purple appendage. All the mentioned species have straw-coloured pappus (S. daurica is characterised by white pappus, but populations with straw-colored pappus are found in nature, S. × magica is characterised by straw-colored below middle and white above middle pappus) and anther basal appendages with lacerate tails. Morphological comparisons with the species belonging to sect. Laguranthera are presented in Figure 1C.

Discussion

The position of the species belonging to ser. Salsae in sect. Theodorea is supported by both molecular and comparative morphological analyses. Saussurea salsa, S. turgaiensis, S. kaschgarica, S. pseudosalsa, S. daurica, i.e. 5 of 6 species of ser. Salsae, as well as recently described S. draconis, need to be transferred in sect. Theodorea. The provisional placement of S. × magica in sect. Theodorea by Yusupovsky and Pyak (2024) is confirmed. Saussurea famintziniana Krasn., the only species of ser. Salsae which was not included in the phylogenetic analyses, requires further special study to establish its systematic position, we prefer to leave it in sect. Laguranthera until more data is available.

The monophyly of subgen. Theodorea remains unconfirmed even after the transfer of the aforementioned taxa, as the position of three species endemic to China, S. nematolepis, S. pseudomalitiosa and S. chingiana, remains unclear and requires detailed analysis. Furthermore, five species (S. ladyginii Lipsch., S. chinnampoensis H. Lév. & Vaniot, S. tsoongii Y.S. Chen, S. jurineoides H.C. Fu, S. malitiosa Maxim.) grown predominantly in China remain unstudied. This underscores the necessity for further research and complete revision of the subgenus. According to the results of comparative morphological analysis, the presence of appendages, which have traditionally been used as the main diagnostic character of the section, cannot be employed as an independent, but only in combination with other vegetative and generative organ characteristics, such as leaf texture, colour of the pappus and anther appendages. Moreover, habitat is found to be very important for differentiating the sections Laguranthera and Theodorea, thus, representatives of the first section occur mainly on rocky, stony and clay steppe slopes, representatives of the second section occur mainly in intermountain basins, preferring moist solonetz steppe habitats.

Acknowledgements

The research was supported by the grant of the Russian Science Foundation (project No. 23-24-00400).

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Supplementary material 1

Table1. NCBI GenBank accession numbers, all newly generated sequences are in bold

Authors: Daniil V. Yusupovsky, Elizaveta A. Pyak Data type: table

Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.

Link: http://journal.asu.ru/biol/article/view/16509/14075

Supplementary material 2

Table2. Origins of plant materials used in the study

Authors: Daniil V. Yusupovsky, Elizaveta A. Pyak Data type: table

Link: http://journal.asu.ru/biol/article/view/16509/14076