Origin and evolution of the South American endemic Artemisia species (Asteraceae): evidence from molecular phylogeny, ribosomal DNA and genome size data
Jaume Pellicer A B F , Teresa Garnatje C , Julián Molero A , Fatima Pustahija D E , Sonja Siljak-Yakovlev D and Joan Vallès AA Laboratori de Botànica, Facultat de Farmàcia, Universitat de Barcelona, Avinguda Joan XXIII s/n, 08028 Barcelona, Catalonia, Spain.
B Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3AB, United Kingdom.
C Institut Botànic de Barcelona (CSIC-ICUB), Passeig del Migdia s/n, Parc de Montjuïc, 08038 Barcelona, Catalonia, Spain.
D Ecologie, Systématique, Evolution, UMR CNRS 8079, Université Paris-Sud, Bâtiment 360, 91405 Orsay Cedex, France.
E Faculty of Forestry, University of Sarajevo, Zagrebacka 20, 71000 Sarajevo, Bosnia and Herzegovina.
F Corresponding author. Email: jaumepellicer@ub.edu
Australian Journal of Botany 58(7) 605-616 https://doi.org/10.1071/BT10047
Submitted: 18 February 2010 Accepted: 1 August 2010 Published: 27 October 2010
Abstract
Genus Artemisia is thought to have reached the Americas across the Bering Strait from Asia during the late Tertiary, but the systematic position of the South American endemic species and the migration routes towards the south have not yet been studied. We used nuclear DNA sequences to unravel the interspecific relationships among the South American Artemisia and their connections with the remaining species of the genus, as well as using fluorescent in situ hybridisation and genome size assessments to characterise this polyploid complex. Most of the species are clustered in a monophyletic clade, nested within the American endemic clade, with the exception of A. magellanica Sch. Bip., which appears segregated from the other American species and constitutes a clade together with A. biennis Willd. Fluorescent in situ hybridisation and genome size data revealed that monoploid genome size remains quite constant across ploidy levels and a proportional increase of ribosomal loci was detected, a dynamic not usually found in this genus. The results are discussed in the light of evolutionary processes which occur in plants, and plausible origins for the South American endemic species are hypothesised.
Acknowledgements
Authors thank Drs. A. Rovira (Universitat de Barcelona, Catalonia, Spain) and M. Dematteis (Instituto de Botánica del Nordeste, Argentina) for their assistance in field collections. We also thank O. Robin (Université de Paris-Sud, France) for her technical support in molecular cytogenetics, as well as Drs. J. Comas, R. Álvarez and R. González (Universitat de Barcelona, Catalonia, Spain), for their help in flow cytometry assays. Two anonymous reviewers are also acknowledged for their valuable suggestions on the draft, and Dr Laura Kelly (Royal Botanic Gardens, Kew, England, United Kingdom) for her improvements in the English language. This work was subsidised by DGICYT (Spanish Government; projects CGL2007–64839-C02–01/BOS and CGL2007–64839-C02–02/BOS) and by the Generalitat de Catalunya (projects: 2005-SGR-00344 and 2009-SGR-00439). J. P. received a predoctoral grant from the Spanish Government (FPI program).
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Appendix 1. List of specimens included in the phylogenetic analysis. For the species newly sequenced (in bold), localities, voucher references and/or collection numbers are indicated
INGROUP. A. annua L. ITS (Tkach et al. 2008) AM398847; ETS (Tkach et al. 2008) AM397956. A. arborescens L. ITS (Torrell et al. 1999) AF045393, AF079945; (Pellicer et al. 2010) FJ642934. A. arenaria DC. ITS (Sanz et al. 2008) EF063639, EF063640; ETS (Sanz et al. 2008) DQ028897. A. argentea L’Her. ITS (Pellicer et al. 2010) FJ642971, FJ643007; ETS (Pellicer et al. 2010) FJ642935. A. aschurbajewi C. Winkl.ITS (Torrell et al. 1999) AF504170, AF504143; ETS (Sanz etal. 2008) DQ028838. A. atrata Lam.(Pellicer et al. 2010) FJ642973, FJ643009; ETS (Pellicer et al. 2010) FJ642937. A. barrelieri Besser ITS (Torrell et al. 1999) AF045410, AF79961; ETS (Sanz et al. 2008) DQ028875. A. biennis Willd. (1) United States of America, Utah: Uinta National Forest, Santaquin canyon, on ruderal soils. 31.viii.2008. Leg. S. Garcia, ED McArthur, SC Sanderson & J. Vallès (BCN3329). ITS GU902816 GU902828; ETS GU902840. A. biennis Willd. (2) Canada, Mississauga: University campus, on a road margin. 22.x.2008. Leg. J. Pellicer (BCN 3330). ITS GU902817 GU902829; ETS GU902841. A. biennis Willd. (3) ITS (Tkach et al. 2008) AM398851; ETS (Tkach et al. 2008) AM398032. A. caerulescens L. ITS (Torrell et al. 1999) AF045409, AF079960; ETS (Sanz et al. 2008) DQ28872. A. caespitosa Ledeb. ITS (Tkach et al. 2008) AM398855; ETS (Tkach et al. 2008) AM397957. A. campestris L. ITS (Torrell et al. 1999) AF045398, AF079950; ETS (Sanz et al. 2008) DQ028854. A. cana Pursh. ITS (Torrell et al. 1999) AF045413, AF079965; ETS (Sanz et al. 2008) DQ028882. A. changaica Krasch. ITS (Tkach et al. 2008) AM398858; ETS (Tkach et al. 2008) AM397965. A. commutata Besser ITS (Tkach et al. 2008) AM398860; ETS (Tkach et al. 2008) AM397967. A. copa Phyl. (1) Argentina. Salta. Los Andes Dept. Quirón slope, 25 km W from Santa Rosa de los Pastos Grandes. 3600 m. 15-ii-2007. Leg. M. Dematteis 2549 (CTES). ITS GU902806 GU902818; ETS GU902830. A. copa Phyl. (2) Argentina. Salta. Los Andes Dept. San Antonio de los Cobres, on the way to the “tren de las nubes”, Concordia mine. 4117 m. 19-iii-2009. Leg. J. Molero & A. Rovira (BCN 67985). ITS GU902807 GU902819; ETS GU902831. A. cretacea Kotov ITS (Pellicer et al. 2010) FJ642975 FJ643011; ETS (Pellicer et al. 2010) FJ642939. A. crithmifolia L. ITS (Torrell et al. 1999) AF045399, AF079962; ETS (Sanz et al. 2008) DQ028856. A. dolosa Krasch. ITS (Tkach et al. 2008) AM398864; ETS (Tkach et al. 2008) AM397971. A. dracunculus L. ITS (Torrell et al. 1999) AF504172, AF504145; ETS (Sanz et al. 2008) DQ028859. A. echegarayi Hieron. (1) Argentina. Mendoza. Las Heras Dept. 5.3 km NE from Uspallata, on the way to Villavicencio. 1800 m. 12-ii-2007. Leg. M. Dematteis 2481 (CTES). ITS GU902810 GU902822; ETS GU902834. A. echegarayi Hieron. (2) Argentina. Mendoza. Las Heras Dept. Uspallata valley, on the way to Calingasta. 1900 m. 30-ii-2007. M. Dematteis 2663 (CTES). ITS GU902811 GU902823; ETS GU902835. A. giraldii Pamp. ITS (Pellicer et al. 2010) FJ642979, FJ643015; ETS (Pellicer et al. 2010) FJ642943. A. glauca Pall. ITS (Tkach et al. 2008) AM398871, ETS (Tkach et al. 2008) AM397978. A. globosa Krasch. ITS (Pellicer et al. 2010) FJ642980, FJ643016; ETS (Pellicer et al. 2010) FJ642944. A. gobica (Krasch.) Grubov. ITS (Tkach et al. 2008) AM398876, ETS (Tkach et al. 2008) AM397983. A. koidzumii Nakai ITS (Tkach et al. 2008) AM398884, ETS (Tkach et al. 2008) AM308035. A. laciniata Willd. ITS (Tkach et al. 2008) AM398886, ETS (Tkach et al. 2008) AM397991. A. magellanica Sch. Bip. (1) Argentina. N. Patagonia, Chubut Dept. Route 40 from Esquel to El Bolsón, km 1807, Madero stream (sandy bank with round slopes). 925 m. 15-iii-2009. Leg. J. Molero & A. Rovira (BCN 67989). ITS GU902814 GU902826; ETS GU902838. A. magellanica Sch. Bip. (2) Argentina. Santa Cruz. Lago Buenos Aires Dept. 79 km NW from the Perito Moreno. 5-ii-1975. Leg. Boelcke et al. 16125 (LP). ITS GU902815 GU902827; ETS GU902839. A. maritima L. ITS (Pellicer et al. 2010) FJ642987, FJ643023; ETS (Pellicer et al. 2010) FJ642951. A. marschalliana Spreng. ITS (Torrell et al. 1999) AF505177, AF504150; ETS (Sanz et al. 2008) DQ028858. A. medioxima Krasch. ex Poljakov ITS (Pellicer et al. 2010) FJ642988, FJ643024; ETS (Pellicer et al. 2010) FJ642952. A. mendozana DC. var. mendozana. (1) Argentina. Mendoza. Las Heras Dept. Natural Reserve of Villavicencio. Quebrada de Villavicencio. 1600 m. 30-ix-2006. Leg. J. Molero & A. Rovira (BCN 67987). ITS GU902812 GU902824; ETS GU902836. A. mendozana DC. var. mendozana. (2) Argentina. Mendoza. Las Heras Dept. Natural Reserve of Villavicencio. Quebrada del Toro. 2000 m. 30-ix-2006. Leg. J. Molero & A. Rovira (BCN 67986). ITS GU902813 GU902825; ETS GU902837. A. mendozana DC. var.paramilloensis F.A. Roig & J.A. Ambrosetti. (1)Argentina. Mendoza. Las Heras Dept. Moorlands of Uspallata, close to the Darwin’s Araucaria. 2980 m. 30-ix-2006. Leg. J. Molero & A. Rovira (BCN 67988). ITS GU902808 GU902820; ETS GU902832. A. mendozana DC. var.paramilloensis F.A. Roig & J.A. Ambrosetti. (2) Argentina. Mendoza. Las Heras Dept. Moorlands of Uspallata hills. 3100 m. 12-ii-2007. Leg. M. Dematteis 2659 (CTES). ITS GU902809 GU902821; ETS GU902833.A. momiyamae Kitam. ITS (Pellicer et al. 2010) FJ642989, FJ643025; ETS (Pellicer et al. 2010) FJ642953. A. monostachya Ledeb. ITS (Tkach et al. 2008) AM398896; ETS (Tkach et al. 2008) AM398000. A. montana Pamp. ITS (Pellicer et al. 2010) FJ642991, FJ643027; ETS (Pellicer et al. 2010) FJ642955. A. nova Nelson ITS (Torrell et al. 1999) AF045412, AF060462; ETS (Sanz et al. 2008) DQ028883. A. palustris L. ITS (Tkach et al. 2008) AM398902; ETS (Tkach et al. 2008) AM398006. A. princeps Pamp. ITS (Tkach et al. 2008) AM398905; ETS (Tkach et al. 2008) AM398009. A. ramosa C.Sm. ex Link. in Buch ITS (Pellicer et al. 2010) FJ642994, FJ643030; ETS (Pellicer et al. 2010) FJ642958. A. rubripes ITS (Pellicer et al. 2010) FJ642995, FJ643031; ETS (Pellicer et al. 2010) FJ642959. A. schrenkiana Ledeb. ITS (Pellicer et al. 2010) FJ642997, FJ643033; ETS (Pellicer et al. 2010) FJ642961. A. sericea Weber ITS (Tkach et al. 2008) AM398916; ETS (Tkach et al. 2008) AM398019. A. sieversiana Ehrh. ex Willd. ITS (Tkach et al. 2008) AM398917; ETS (Tkach et al. 2008) AM398020. A. sphaerocephala Krasch. ITS (Tkach et al. 2008) AM398918; ETS (Tkach et al. 2008) AM398021. A. stolonifera (Maxim.) V.L. Komarov ITS (Pellicer et al. 2010) FJ643000, FJ643036; ETS (Pellicer et al. 2010) FJ642964. A. subulata Nakai ITS (Pellicer et al. 2010) FJ643001, FJ643037; ETS (Pellicer et al. 2010) FJ642965. A. tanacetifolia L. ITS (Tkach et al. 2008) AM398923; ETS (Tkach et al. 2008) AM398026. A. taurica Less. ITS (Pellicer et al. 2010) FJ643003, FJ643039; ETS (Pellicer et al. 2010) FJ642967. A. thuscula Cav. ITS (Tkach et al. 2008) AM398924; ETS (Tkach et al. 2008) AM39027. A. tournefortiana Rchb. ITS/ETS (Pellicer et al. in prep). A. tridentata Nutt. ITS (Torrell et al. 1999) AF045411, AF079963; ETS (Sanz et al. 2008) DQ028884. A. vulgaris L. ITS (Tkach et al. 2008) AM398927, ETS (Tkach et al. 2008) AM398029. A. xerophytica Krasch. ITS (Tkach et al. 2008) AM398929; ETS (Tkach et al. 2008) AM398031.
OUTGROUP. Ajania fastigata (C. Winkl.) Poljakov ITS (Torrell et al. 1999) AF504169, AF504142; ETS (Sanz et al. 2008) DQ028868. Dendranthema maximowiczii (Komarov) Tzevelev ITS (Sanz et al. 2008) DQ028923, DQ028910; ETS (Sanz et al. 2008) DQ028899. Dendranthema zawadskii (Herbich) Tzevelev ITS (Sanz et al. 2008) DQ028924, DQ028911; ETS (Sanz et al. 2008) DQ028901. Filifolium sibiricum (L.) Kitam. ITS (Pellicer et al. 2010) FJ643006, FJ643042; ETS (Pellicer et al. 2010) FJ642970. Kaschgaria brachanthemoides (C. Winkl.) Poljakov ITS (Torrell et al. 1999) AF504189, AF504162; ETS (Sanz et al. 2008) DQ028865. Kaschgaria komarovii (Krasch. et Rubtzov) Poljakov ITS (Sanz et al. 2008) DQ028925, DQ028912; ETS (Sanz et al. 2008) DQ028902. Neopallasia pectinata (Pall.) Poljakov ITS (Sanz et al. 2008) DQ028927, DQ028927; ETS (Sanz et al. 2008) DQ028914.
References
Pellicer J, Garcia S, Canela MÁ, Garnatje T, Korobkov AA, Twibell JD, Vallès J (2010) Genome size dynamics in Artemisia L. (Asteraceae, Anthemideae): following the track of polyploidy. Plant Biology 12, 820–830.
Sanz M, Vilatersana R, Hidalgo O, Garcia-Jacas N, Susanna A, Schneeweiss GM, Vallès J (2008) Molecular phylogeny and evolution of floral characters of Artemisia and allies (Anthemideae, Asteraceae): evidence from nrDNA ETS and ITS sequences. Taxon 57, 1–13.
Tkach VN, Hoffmann MH, Röser M, Korobkov AA, Von Hagen KB (2008) Parallel evolutionary patterns in multiple lineages of arctic Artemisia L. (Asteraceae). Evolution 62, 184–198.
Torrell M, Garcia-Jacas N, Susanna A, Vallès J (1999) Infrageneric phylogeny of the genus Artemisia L. (Asteraceae, Anthemideae) based on nucleotide sequences of nuclear ribosomal DNA internal transcribed spacers (ITS). Taxon 48, 721–736.
