Reinterpreting the phylogenetic position and taxonomic revision of the genus Pterocyclus (Apiaceae, Apioideae) based on nrITS, complete plastid genome, and morphological evidence

Abstract

The classification of species in the genus Pterocyclus has been a topic of concern, as they were initially considered members of Pleurospermum (Apiaceae) in the Flora of China. However, the intergeneric and infrageneric classifications of Pterocyclus and its allies, such as Hymenidium and Pleurospermum, have been controversial. To address these issues, we performed phylogenetic analyses using one nuclear marker (nrITS) from 167 accessions, including 137 species (including five species of Pterocyclus), and 105 plastid genes from 82 accessions representing 82 species (including five species of Pterocyclus) of Apiaceae. We used both maximum likelihood and Bayesian approaches to deduce phylogenetic relationships of Pterocyclus and its allies. Furthermore, we conducted morphometric analyses that specifically targeted the mericarp morphology, and compared the structural differences in their plastid genomes. Based on these findings, we suggest the following revisions to the classification of Pterocyclus and its allies: (i) Pterocyclus should encompass five species (Pterocyclus angelicoides, Pterocyclus forrestii, Pterocyclus rotundatus, Pterocyclus tibeticus, and Pterocyclus wolffianus), all of which are all monophyletic and placed in the Komarovieae; (ii) Pterocyclus rivulorum shows both phylogenetic and mericarp morphological similarities to Hymenidium apiolens and Hymenidium dentatum, which belongs to the Hymenidium Clade, thus we provisionally transfer it to Hymenidium; (iii) Pleurospermum longicarpum is considered conspecific with Pterocyclus angelicoides based on morphological descriptions in the Flora Xizangica; (iv) we describe and illustrate Pterocyclus tibeticus as a new species; and (v) Pterocyclus wolffianus should be recognized as a valid species and not considered a synonym of Pterocyclus forrestii.

Keywords

Apiaceae / morphology / phylogeny / plastid genome / Pleurospermum / Pterocyclus / taxonomy

References

1	H Akaike. 1974. A new look at the statistical model identification. IEEE Transactions on Automatic Control 19: 716–723.
2	F Altinordu, L Peruzzi, Y Yu, XJ He. 2016. A tool for the analysis of chromosomes: Karyotype. Taxon 65: 586–592.
3	TG Burland. 2000. DNASTAR's Lasergene sequence analysis software. Bioinformatics Methods and Protocols 132: 71–91.
4	BC Carstens, LL Knowles. 2007. Estimating species phylogeny from gene-tree probabilities despite incomplete lineage sorting: An example from Melanoplus grasshoppers. Systematic Biology 56: 400–411.
5	S Chen, Y Zhou, Y Chen, J Gu. 2018. Fastp: An ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34: i884–i890.
6	CA Danderson, SR Downie, M Hermann. 2018. Rampant polyphyly in the Arracacia clade (Apiaceae) and an assessment of the phylogenetic utility of 20 noncoding plastid loci. Molecular Phylogenetics and Evolution 118: 286.
7	K De Queiroz. 2007. Species concepts and species delimitation. Systematic Biology 56: 879–886.
8	L Diels. 1912. Umbelliferae. Notes from the Royal Botanic Garden Edinburgh 5: 287–292.
9	N Dierckxsens, P Mardulyn, G Smits. 2016. NOVOPlasty: De novo assembly of organelle genomes from whole genome data. Nucleic Acids Research 45: e18.
10	SR Downie, K Spalik, DS Katz-Downie, JP Reduron. 2010. Major clades within Apiaceae subfamily Apioideae as inferred by phylogenetic analysis of nrDNA ITS sequences. Plant Diversity and Evolution 128: 111–136.
11	MAE Feist, SR Downie, AR Magee, MR Liu. 2012. Revised generic delimitations for Oxypolis and Ptilimnium (Apiaceae) based on leaf morphology, comparative fruit anatomy, and phylogenetic analysis of nuclear rDNA ITS and cpDNA trnQ-trnK intergenic spacer sequence data. Taxon 61: 402–418.
12	KT Fu, YC Ho. 1979. Pleurospermum. In: Flora Reipublicae Popularis Sinicae. Beijing: Science Press. 55: 133–184.
13	BE Goodson, SK Rehman, RK Jansen. 2011. Molecular systematics and biogeography of Descurainia (Brassicaceae) based on nuclear ITS and non-coding chloroplast DNA. Systematic Biology 36: 957–980.
14	W Gou, XL Guo, SD Zhou, XJ He. 2021. Phylogeny and taxonomy of Meeboldia, Sinodielsia and their relatives (Apiaceae: Apioideae) inferred from nrDNA ITS, plastid DNA intron (rpl16 and rps16) sequences and morphological characters. Phytotaxa 482: 121–142.
15	S Greiner, P Lehwark, R Bock. 2019. OrganellarGenomeDraw (OGDRAW) version 1.3.1: Expanded toolkit for the graphical visualization of organellar genomes. Nucleic Acids Research 47: W59–W64.
16	XL Guo, W Gou, C Peng, SD Zhou, XJ He. 2020. New insights into the phylogenetic position of Hymenidium dentatum (Apioideae, Apiaceae) inferred from nrDNA and morphological evidence. Phytotaxa 452: 46–54.
17	XL Guo, CB Wang, J Wen, SD Zhou, XJ He. 2018. Phylogeny of Chinese Chamaesium (Apiaceae: Apioideae) inferred from ITS, cpDNA and morphological characters. Phytotaxa 376: 001–016.
18	R Hijmans, L Guarino, M Cruz, E Rojas. 2001. Computer tools for spatial analysis of plant genetic resources data: 1. DIVA-GIS. Plant Genetic Resources Newsletter 127: 15–19.
19	DT Hoang, O Chernomor, A Von Haeseler, BQ Minh, LS Vinh. 2018. UFBoot2: Improving the ultrafast bootstrap approximation. Molecular Biology and Evolution 35: 518–522.
20	CM Hurvich, CL Tsai. 1989. Regression and time series model selection in small samples. Biometrika 76: 297–307.
21	SS Jakob. 2006. A chloroplast genealogy of Hordeum (Poaceae): Long-term persisting haplotypes, incomplete lineage sorting, regional extinction, and the consequences for phylogenetic inference. Molecular Biology and Evolution 23: 1602–1612.
22	SB Jia, XL Guo, SD Zhou, XJ He. 2019. Hansenia pinnatiinvolucellata is conspecific with H. weberbaueriana (Apiaceae) based on morphology and molecular data. Phytotaxa 418: 203–210.
23	S Kalyaanamoorthy, BQ Minh, TKF Wong, A Von Haeseler, LS Jermiin. 2017. ModelFinder: Fast model selection for accurate phylogenetic estimates. Nature Methods 14: 587–589.
24	K Katoh, J Rozewicki, KD Yamada. 2017. MAFFT online service: Multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics 20: 1160–1166.
25	M Kearse, R Moir, A Wilson, S Stones-Havas, M Cheung, S Sturrock, S Buxton, A Cooper, S Markowitz, C Duran, T Thierer, B Ashton, P Meintjes, A Drummond. 2012. Geneious basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647–1649.
26	E Kljuykov, M Liu, T Ostroumova, M Pimenov, P Tilney, BE Wyk, J Staden. 2004. Towards a standardised terminology for taxonomically important morphological characters in the Umbelliferae. South African Journal of Botany 70: 488–496.
27	AG Klotzsch, FA Garcke. 1862. Die botanischen Ergebnisse der Reise des Prinzen Waldemar von Preussen in den Jahren 1846 und 1847. Berlin: Desker.
28	MA Koch, R Karl, C Kiefer, IA Al-Shehbaz. 2010. Colonizing the American continent: Systematics of the genus Arabis in North America (Brassicaceae). American Journal of Botany 97: 1040–1057.
29	JB Lack, RS Pfau, GM Wilson. 2010. Demographic history and incomplete lineage sorting obscure population genetic structure of the Texas mouse (Peromyscus attwateri). Journal of Mammalogy 91: 314–325.
30	J Liu, Y Wang, A Wang, O Hideaki, R Abbott. 2006. Radiation and diversification within the Ligularia-Cremanthodium-Parasenecio complex (Asteraceae) triggered by uplift of the Qinghai-Tibetan Plateau. Molecular Phylogenetics and Evolution 38: 31–49.
31	D Lyskov, G Degtjareva, T Samigullin, M Pimenov. 2015. Systematic placement of the Turkish endemic genus Ekimia (Apiaceae) based on morphological and molecular data. Turkish Journal of Botany 39: 673–680.
32	K Mummenhoff, P Linder, N Friesen, JL Bowman, JY Lee, A Franzke. 2004. Molecular evidence for bicontinental hybridogenous genomic constitution in Lepidium sensu stricto (Brassicaceae) species from Australia and New Zealand. American Journal of Botany 91: 254–261.
33	N Myers, RA Mittermeier, CG Mittermeier, GAB da Fonseca, J. Kent 2000. Biodiversity hotspots for conservation priorities. Nature 403: 853–858.
34	LT Nguyen, HA Schmidt, A von Haeseler, BQ Minh. 2014. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32: 268–274.
35	MG Pimenov. 2017. Updated checklist of Chinese Umbelliferae: Nomenclature, synonymy, typification, distribution. Turczaninowia 20: 106–239.
36	MG Pimenov, EV Kljuykov. 1999. New nomenclatural combinations for Chinese Umbelliferae. Feddes Repertorium 110: 481–491.
37	MG Pimenov, EV Kljuykov. 2000a. Taxonomic revision of Pleurospermum Hoffm. and related genera of Umbelliferae II. The genera Pleurospermum, Pterocyclus, Trachydium, Keraymonia, Pseudotrachydium, Aulacospermum, and Hymenolaena. Feddes Repertorium 111: 517–534.
38	MG Pimenov, EV Kljuykov. 2000b. Taxonomic revision of Pleurospermum Hoffm. and related genera of Umbelliferae III. The genera Physospermopsis and Hymenidium. Feddes Repertorium 111: 535–552.
39	MG Pimenov, EV Kijuykov, MV Leonov. 2000. Taxonomic revision of Pleurospermum Hoffm. and related genera of Umbelliferae I. General part. Feddes Repertorium 111: 499–515.
40	M Piwczyński, R Puchałka, K Spalik. 2015. The infrageneric taxonomy of Chaerophyllum (Apiaceae) revisited: New evidence from nuclear ribosomal DNA ITS sequences and fruit anatomy. Botanical Journal of the Linnean Society 178: 298–313.
41	DA Pollard, VN Iyer, AM Moses, MB Eisen. 2006. Widespread discordance of gene trees with species tree in Drosophila: Evidence for incomplete lineage sorting. PloS Genetics 2: e173.
42	FD Pu, MF Watson. 2005. Apiaceae. In: Wu ZY, Raven PH eds. Flora of China. Beijing: Science Press; St. Louis: Missouri Botanical Garden Press. 14: 1–205.
43	XJ Qu, MJ Moore, DZ Li, TS Yi. 2019. PGA: A software package for rapid, accurate, and flexible batch annotation of plastomes. Plant Methods 15: 1–12.
44	A Rambaut, AJ Drummond, D Xie, G Baele, MA Suchard. 2018. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67: 901–904.
45	F Ronquist, M Teslenko, PVD Mark, DL Ayres, A Darling, S Höhna, B Larget, L Liu, SJP Huelsenbeck. 2012. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539–542.
46	M Ruhsam, HS Rai, S Mathews, TG Ross, SW Graham, LA Raubeson, W Mei, PI Thomas, MF Gardner, RA Ennos, PM Hollingsworth. 2015. Does complete plastid genome sequencing improve species discrimination and phylogenetic resolution in Araucaria? Molecular Ecology Resources 15: 1067–1078.
47	R Schmickl, MH Jørgensen, AK Brysting, MA Koch. 2010. The evolutionary history of the Arabidopsis lyrata complex: A hybrid in the amphi-Beringian area closes a large distribution gap and builds up a genetic barrier. BMC Evolutionary Biology 10: 98.
48	RH Shan, ZH Pan. 1983. Pleurospermum. In: Wu CY ed. Flora Xizangica. Bejing: Science Press. 1: 423–438.
49	R Shimizu-Inatsugi, J Lihová, H Iwanaga, H Kudoh, K Marhold, O Savolainen, K Watanabe, VV Yakubov, KK Shimizu. 2009. The allopolyploid Arabidopsis kamchatica originated from multiple individuals of Arabidopsis lyrata and Arabidopsis halleri. Molecular Ecology 18: 4024–4048.
50	K Spalik, JP Reduron, SR Downie. 2004. The phylogenetic position of Peucedanum sensu lato and allied genera and their placement in tribe Selineae (Apiaceae, subfamily Apioideae). Plant Systematics and Evolution 243: 189–210.
51	K Spalik, A Wojewódzka, SR Downie. 2001. The evolution of fruit in Scandiceae subtribe Scandicinae (Apiaceae). Canadian Journal of Botany 79: 1358–1374.
52	DM Spooner, H Ruess, M Iorizzo, D Senalik, P Simon. 2017. Entire plastid phylogeny of the carrot genus (Daucus, Apiaceae): Concordance with nuclear data and mitochondrial and nuclear DNA insertions to the plastid. American Journal of Botany 104: 296–312.
53	CM Valiejo-Roman, EI Terentieva, MG Pimenov, EV Kljuykov, TH Samigullin, PM Tilney. 2012. Broad polyphyly in Pleurospermum s. l. (Umbelliferae-Apioideae) as inferred from nrDNA ITS and chloroplast sequences. Systematic Biology 37: 573–581.
54	H Wolff. 1930. Umbelliferae Asiaticae novae relictae. III. Feddes Repertorium 27: 301–335.
55	QY Xiao, HY Hu, F Tong, MJ Li, XJ He. 2017. Semenovia torilifolia is conspecific with S. malcolmii (Apiaceae) based on morphology and molecular data. Phytotaxa 321: 225–240.
56	QY Xiao, Y Yu, DF Xie, XL Guo, XJ He. 2018. Angelica oncosepala and Heracleum yunnanense are synonyms and refer to a species of Tetrataenium (Apiaceae). Nordic Journal of Botany 36: 01563.
57	Y Yu, SR Downie, XJ He, XL Deng, L Yan. 2011. Phylogeny and biogeography of Chinese Heracleum (Apiaceae tribe Tordylieae) with comments on their fruit morphology. Plant Systematics and Evolution 296: 179–203.
58	D Zhang, F Gao, I Jakovlić, H Zou, GT Wang. 2019. PhyloSuite: An integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. Molecular Ecology Resources 20: 348–352.
59	J Zhou, X Gong, SR Downie, H Peng. 2009. Towards a more robust molecular phylogeny of Chinese Apiaceae subfamily Apioideae: Additional evidence from nrDNA ITS and cpDNA intron (rpl16 and rps16) sequences. Molecular Phylogenetics and Evolution 53: 56–68.
60	J Zhou, H Peng, SR Downie, ZW Liu, X Gong. 2008. A molecular phylogeny of Chinese Apiaceae subfamily Apioideae inferred from nuclear ribosomal DNA internal transcribed spacer sequences. Taxon 57: 402–416.
61	J Zhou, J Wei, J Niu, X Liu, Z Liu. 2021. Molecular phylogenetics of Pterocyclus (Apiaceae) based on nrDNA its sequences: Revised circumscription with a restored species. Phytotaxa 498: 131–138.