Phylogenomics and morphological evolution of the mega-diverse genus Artemisia (Asteraceae: Anthemideae): implications for its circumscription and infrageneric taxonomy

Bohan Jiao; Chen Chen; Meng Wei; Guohao Niu; Jiye Zheng; Guojin Zhang; Jiahao Shen; Daniel Vitales; Joan Vallès; Filip Verloove; Andrey S Erst; Akiko Soejima; Iraj Mehregan; Goro Kokubugata; Gyu-Young Chung; Xuejun Ge; Lianming Gao; Yuan Yuan; Cyprien Joly; Florian Jabbour; Wei Wang; Leila M Shultz; Tiangang Gao

doi:10.1093/aob/mcad051

Phylogenomics and morphological evolution of the mega-diverse genus Artemisia (Asteraceae: Anthemideae): implications for its circumscription and infrageneric taxonomy

Ann Bot. 2023 May 15;131(5):867-883. doi: 10.1093/aob/mcad051.

Authors

Bohan Jiao^{1

2

3}, Chen Chen^{1

2

3}, Meng Wei^{1

2

3}, Guohao Niu^{1

2

3}, Jiye Zheng^{1

2

3}, Guojin Zhang^{1

2

3}, Jiahao Shen^{1

2

3

4}, Daniel Vitales⁵, Joan Vallès⁶, Filip Verloove⁷, Andrey S Erst^{8

9}, Akiko Soejima¹⁰, Iraj Mehregan¹¹, Goro Kokubugata¹², Gyu-Young Chung¹³, Xuejun Ge¹⁴, Lianming Gao^{15

16}, Yuan Yuan¹⁷, Cyprien Joly¹⁸, Florian Jabbour¹⁸, Wei Wang^{1

2

3}, Leila M Shultz¹⁹, Tiangang Gao^{1

2

3}

Affiliations

¹ State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China.
² China National Botanical Garden, Beijing 100093, China.
³ University of Chinese Academy of Sciences, Beijing 100049, China.
⁴ Institute of Botany, Jiangsu Province and Chinese Academy of Sciences (Nanjing Botanical Garden Mem. Sun Yat-Sen), Nanjing 210014, China.
⁵ Institut Botànic de Barcelona (IBB, CSIC-Ajuntament de Barcelona), Pg. del Migdia, s.n., 08038 Barcelona, Spain.
⁶ Laboratori de Botànica - Unitat associada al CSIC, Facultat de Farmàcia i Ciències de l'Alimentació -Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, Av. Joan XXIII 27-31, 08028 Barcelona, Catalonia, Spain.
⁷ Meise Botanic Garden, Nieuwelaan 38, B-1860 Meise, Belgium.
⁸ Laboratory Herbarium (NS), Central Siberian Botanical Garden, Russian Academy of Sciences Russia, Novosibirsk, 630090, Zolotodolinskaya st. 101, Russia.
⁹ Tomsk State University, Laboratoryof Systematics and Phylogeny of Plants (TK), Tomsk 634050, Russia.
¹⁰ Faculty of Advanced Science and Technology, Kumamoto University, 2-39-1 Kurokami, Chuo-ku, Kumamoto, 860-8555, Japan.
¹¹ Laboratory for Plant Molecular Phylogeny and Systematics, Department of Biology, Science and Research Branch, Azad University, Tehran, Iran.
¹² Department of Botany, National Museum of Nature and Science, Amakubo 4-1-1, Tsukuba, Ibaraki 305-0005, Japan.
¹³ Department of Forest Science, Andong National University, 1375 Gyeongdong-ro Andong, Gyeongsangbuk-do, 36729, Republic of Korea.
¹⁴ Center of Conservation Biology, Core Botanical Gardens, Chinese Academy of Sciences, Guangzhou 510650, China.
¹⁵ CAS Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, Yunnan 650201, China.
¹⁶ Lijiang National Forest Biodiversity National Observation and Research Station, Kunming Institute of Botany, Chinese Academy of Sciences, Lijiang, Yunnan 67410, China.
¹⁷ National Resource Center for Chinese Meteria Medica, Chinese Academy of Chinese Medical Sciences, 100700, Beijing, China.
¹⁸ Institut de Systématique Evolution Biodiversité (ISYEB), Muséum national d'Histoire naturelle, CNRS, Sorbonne Université, EPHE, Université des Antilles, 57 rue Cuvier CP39, 75005 Paris, France.
¹⁹ Department of Wildland Resources, Utah State University, Logan, UT 84322-5230, USA.

Abstract

Background and aims: Artemisia is a mega-diverse genus consisting of ~400 species. Despite its medicinal importance and ecological significance, a well-resolved phylogeny for global Artemisia, a natural generic delimitation and infrageneric taxonomy remain missing, owing to the obstructions from limited taxon sampling and insufficient information on DNA markers. Its morphological characters, such as capitulum, life form and leaf, show marked variations and are widely used in its infrageneric taxonomy. However, their evolution within Artemisia is poorly understood. Here, we aimed to reconstruct a well-resolved phylogeny for global Artemisia via a phylogenomic approach, to infer the evolutionary patterns of its key morphological characters and to update its circumscription and infrageneric taxonomy.

Methods: We sampled 228 species (258 samples) of Artemisia and its allies from both fresh and herbarium collections, covering all the subgenera and its main geographical areas, and conducted a phylogenomic analysis based on nuclear single nucleotide polymorphisms (SNPs) obtained from genome skimming data. Based on the phylogenetic framework, we inferred the possible evolutionary patterns of six key morphological characters widely used in its previous taxonomy.

Key results: The genus Kaschgaria was revealed to be nested in Artemisia with strong support. A well-resolved phylogeny of Artemisia consisting of eight highly supported clades was recovered, two of which were identified for the first time. Most of the previously recognized subgenera were not supported as monophyletic. Evolutionary inferences based on the six morphological characters showed that different states of these characters originated independently more than once.

Conclusions: The circumscription of Artemisia is enlarged to include the genus Kaschgaria. The morphological characters traditionally used for the infrageneric taxonomy of Artemisia do not match the new phylogenetic tree. They experienced a more complex evolutionary history than previously thought. We propose a revised infrageneric taxonomy of the newly circumscribed Artemisia, with eight recognized subgenera to accommodate the new results.

Keywords: Artemisia; generic delimitation; genome skimming; infrageneric taxonomy; morphological evolution; phylogenomics; taxonomy.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Artemisia* / genetics
Cell Nucleus
Phylogeny
Plant Leaves