Phylogenetic relationships of Chinese Adiantum based on five plastid markers

Abstract

Adiantum consists of about 150–200 species mostly with a pantropical distribution, yet the classifications of Adiantum have been based primarily on regional studies. Confounding the clarity of reconstructing the evolutionary history of Adiantum is that previous molecular phylogenetic studies suggest that a separate and distinctive clade, the vittarioids, may be derived from within Adiantum. Five plastid markers (atpA, atpB, rbcL, trnL-F and rps4-trnS) are employed to assess the monophyly of Adiantum, and construct the molecular phylogeny of Chinese Adiantum. Our analyses support the monophyly of Adiantum. All temperate Adiantum species form a clade nested within the pantropical grade, suggesting a tropical origin of Adiantum. Six main clades are supported within Chinese Adiantum, which are only partially consistent with Lin’s classification of the genus. Series Caudata is polyphyletic with series Gravesiana nested within one subgroup of series Caudata. The prolonged whip-like stolon at the apex of the fronds is the defining character for series Caudata, but it may have evolved multiple times. Adiantum reniforme with the simple fronds is sister to series Venusta, which has a decompound lamina with many flabellate to cuneate segments. Series Veneri-capilliformia is not monophyletic, with A. capillus-veneris sister to series Flabellulata except for A. diaphanum, and A. edentulum sister to series Pedata. Series Flabellulata is biphyletic with A. diaphanum nested within the pantropical grade. The phylogeny suggests that convergent evolution in frond architecture has occurred in Adiantum.

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Acknowledgments

We thank Xiao Cheng, Yu-xiao Zhang, Li-Yaung Kuo, Akiko Soejima and Tom Heutte for sample collection, and Elizabeth Zimmer for providing primers. The study was supported by the National Natural Science Foundation of China (Grant no. 31070199, 30800063), the Project of Knowledge Innovation Program of the Chinese Academy of Sciences (Grant no.: 2010KIBA02), the Research Fund for the Large-scale Scientific Facilities of the Chinese Academy of Sciences (Grant no. 2009-LSF-GBOWS-01), and the John D. and Catherine T. MacArthur Foundation (to J. Wen, R. Ree and G. Mueller).

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Correspondence to Jun Wen or De-Zhu Li.

Appendices

Appendix 1

Voucher information and GenBank accession numbers for taxa used in the phylogenetic study on Adiantum. Taxon, voucher specimen (herbarium), collection locality, and GenBank accession number in the order of rbcL, atpB, atpA, trnL-F, and rps4-trnS.

Adiantum aethiopicum L.; J. Wen 10780 (US); New Zealand; JF935350; JF935432; JF937305; JF980695; JF980616.

Adiantum aleuticum (Rupr.) C.A. Paris; Heutte s.n. (US); Alaska, USA; JF935362; JF935447; JF937320; JF980709; JF980631.

Adiantum bonatianum Brause; J.-M. Lu 216 (KUN); Yunnan, China; JF935294; JF935371; JF937247; JF980639; JF980556.

Adiantum capillus-junonis Rupr.; J.-M. Lu 111 (KUN); Guangxi, China; JF935314; JF935395; JF937269; JF980662; JF980578.

Adiantum capillus-veneris L.; J. Wen 10360 (US); Russia; JF935345; JF935427; JF937300; JF980690; JF980611.

Adiantum capillus-veneris; J.-M. Lu 138 (KUN); Guangxi, China; JF935320; JF935401; JF937274; JF980666; JF980584.

Adiantum capillus-veneris; J.-M. Lu 295 (KUN); Chongqing, China; JF935322; JF935403; JF937276; JF980667; JF980586.

Adiantum capillus-veneris; J. Wen 8192 (US); Chongqing, China; JF935332; JF935413; JF937286; JF980676; JF980597.

Adiantum capillus-veneris; J. Wen 8297 (US); Luzon, the Philippines; JF935334; JF935415; JF937288; JF980678; JF980599.

Adiantum capillus-veneris var. dissectum (Mart. Et Galeot.) Ching; J.-M. Lu 118 (KUN); Guangxi, China; JF935318; JF935399; JF937273; JF980665; JF980582.

Adiantum caudatum L.; J.-M. Lu 209 (KUN); Hainan, China; JF935296; JF935373; JF937249; JF980641; JF980558.

Adiantum chienii Ching; J.-M. Lu 568 (KUN); Fujian, China; JF935303; JF935381; JF937256; JF980649; JF980565.

Adiantum chilense Kaulf.; J. Wen 7313 (US); Nuble, Chile; JF935336; JF935418; JF937291; JF980681; JF980602.

Adiantum cuneatum Langsd & Fisch; J. Wen 10119 (US); West Java, Indonesia; JF935339; JF935421; JF937294; JF980684; JF980605.

Adiantum cunninghamii Hook.; J. Wen 10782 (US); New Zealand; JF935351; JF935433; JF937306; JF980696; JF980617.

Adiantum davidii Franch.; J.-M. Lu 344 (KUN); Shanxi, China; JF935310; JF935391; JF937265; JF980659; JF980574.

Adiantum davidii; J. Wen 8015 (US); Gansu, China; JF935319; JF935400; ——; ——; JF980583;

Adiantum davidii; X. Cheng 001(KUN); Yunnan, China; JF935316; JF935397; JF937271; ——; JF980580.

Adiantum davidii var. longispinum Ching; J.-M. Lu 247 (KUN); Yunnan, China; JF935292; JF935369; JF937245; JF980638; JF980554.

Adiantum diaphanum Blume; J.-M. Lu 208 (KUN); Hainan, China; JF935301; JF935379; JF937254; JF980647; JF980563.

Adiantum diaphanum; J.-M. Lu 558 (KUN); Fujian, China; JF935304; JF935382; JF937257; JF980650; JF980566.

Adiantum diaphanum; J. Wen 10727 (US); Indonesia; ——; JF935439; JF937312; JF980702; JF980623.

Adiantum edentulum H. Christ; J.-M. Lu 222 (KUN); Yunnan, China; JF935291; JF935368; JF937244; JF980637; JF980553.

Adiantum edentulum f. muticum (Ching) Y. X. Lin; J.-M. Lu 226 (KUN); Yunnan, China; JF935290; JF935367; JF937243; JF980636; JF980552.

Adiantum edgeworthii Hook.; J.-M. Lu 114 (KUN); Guangxi, China; JF935311; JF935392; JF937266; JF980660; JF980575.

Adiantum excisum Kunze; J. Wen 7326 (US); Concepcion, chile; JF935337; JF935419; JF937292; JF980682; JF980603.

Adiantum fengianum Ching; J.-M. Lu 228 (KUN); Yunnan, China; JF935308; JF935388; JF937262; JF980656; JF980571.

Adiantum fimbriatum Christ; J.-M. Lu 215 (KUN); Yunnan, China; JF935321; JF935402; JF937275; ——; JF980585.

Adiantum fimbriatum var. shensiense (Ching) Ching; J.-M. Lu 227 (KUN); Yunnan, China; JF935293; JF935370; JF937246; ——; JF980555.

Adiantum flabellulatum L.; J.-M. Lu 192 (KUN); Guizhou, China; JF935315; JF935396; JF937270; JF980663; JF980579.

Adiantum flabellulatum; J.-M. Lu 450 (KUN); Guangdong, China; JF935295; JF935372; JF937248; JF980640; JF980557.

Adiantum flabellulatum; J. Wen 6585 (US); Hainan, China; JF935325; JF935406; JF937279; JF980670; JF980589.

Adiantum formosanum Tagawa; L.-Y. Kuo 430 (TAIF); Taiwan, China; ——; JF935384; ——; JF980652; JF980568.

Adiantum formosum R. Br.; J. Wen 10779 (US); New Zealand; JF935352; JF935434; JF937307; JF980697; JF980618.

Adiantum fulvum Raoul; J. Wen 10781 (US); New Zealand; JF935353; JF935435; JF937308; JF980698; JF980619.

Adiantum gravesii Hance; J.-M. Lu 129 (KUN); Guangxi, China; JF935312; JF935393; JF937267; ——; JF980576.

Adiantum gravesii; J.-M. Lu 451 (KUN); Guangdong, China; JF935317; JF935398; JF937272; JF980664; JF980581.

Adiantum hispidulum Sw.; J. Wen 10243 (US); Sulawesi, Indonesia; JF935341; JF935423; JF937296; JF980686; JF980607.

Adiantum hispidulum; J. Wen 10771 (US); Virginia cultivated, USA; JF935349; JF935431; JF937304; JF980694; JF980615.

Adiantum hispidulum; L.-Y. Kuo 1675 (TAIF); Taiwan, China; ——; JF935377; ——; JF980645; ——.

Adiantum induratum H. Christ; J.-M. Lu 210 (KUN); Hainan, China; JF935309; JF935389; JF937263; JF980657; JF980572.

Adiantum jordanii C.H. Mull.; J. Wen 10778 (US); Califoria,USA; JF935348; JF935430; JF937303; JF980693; JF980614.

Adiantum juxtapositum Ching; J.-M. Lu 575 (KUN); Fujian, China; JF935305; JF935383; JF937258; JF980651; JF980567.

Adiantum leveillei H. Christ; J.-M. Lu 163 (KUN); Guangxi, China; JF935313; JF935394; JF937268; JF980661; JF980577.

Adiantum lianxianense Ching and Y.X. Lin; J.-M. Lu 441 (KUN); Guangdong, China; JF935306; JF935385; JF937259; JF980653; JF980569.

Adiantum malesianum Ghatak; J.-M. Lu 050 (KUN); Yunnan, China; JF935297; JF935374; JF937250; JF980642; JF980559.

Adiantum mariesii Baker; J.-M. Lu 120 (KUN); Guangxi, China; JF935302; JF935380; JF937255; JF980648; JF980564.

Adiantum myriosorum Baker; J.-M. Lu 297 (KUN); Chongqing, China; JF935359; JF935444; JF937317; JF980706; JF980628.

Adiantum pedatum L.; J. Wen 10100 (US); Maryland, USA; JF935361; JF935446; JF937319; JF980708; JF980630.

Adiantum pedatum; J.-M. Lu 343 (KUN); Shanxi, China; JF935360; JF935445; JF937318; JF980707; JF980629.

Adiantum pedatum; A. Soejima 1087 (US); Osaka, Japan; JF935363; JF935448; JF937321; JF980710; JF980632.

Adiantum peruvianum Klotzsch; J.-M. Lu 338 (KUN); India; JF935288; JF935365; JF937241; JF980634; JF980550.

Adiantum philippense L.; J.-M. Lu 001 (KUN); Yunnan, China; JF935331; ——; ——; ——; JF980596.

Adiantum philippense; J. Wen 8257 (US); Luzon, the Philippines; JF935330; JF935412; JF937285; JF980675; JF980595.

Adiantum philippense; J. Wen 10206 (US); Indonesia; JF935340; JF935422; JF937295; JF980685; JF980606.

Adiantum princeps T. Moore; J. Wen 10777 (US); Yucatan, Mexico; JF935356; JF935438; JF937311; JF980701; JF980622.

Adiantum raddianum C. Presl; J. Wen 9521 (US); Antsiranana, Madagascar; JF935323; JF935404; JF937277; JF980668; JF980587.

Adiantum raddianum; J.-M. Lu 589 (KUN); Shenzhen cultivated, China; JF935307; JF935387; JF937261; JF980655; JF980570.

Adiantum reniforme var. sinense Y.X. Lin; J.-M. Lu 238 (KUN); Hubei, China; JF935287; JF935364; JF937240; JF980633; JF980549.

Adiantum roborowskii Maxim.; J.-M. Lu 279 (KUN); Chongqing, China; JF935289; JF935366; JF937242; JF980635; JF980551.

Adiantum roborowskii; J.-M. Lu 280 (KUN); Chongqing, China; JF935298; JF935375; JF937251; JF980643; JF980560.

Adiantum roborowskii var. taiwanianum (Tagawa) Shieh; Wade 909 (TAIF); Taiwan, China; ——; JF935386; JF937260; JF980654; ——.

Adiantum sinicum Ching; J.-M. Lu 269 (KUN); Yunnan, China; JF935300; JF935378; JF937253; JF980646; JF980562.

Adiantum soboliferum Wall.; Y.-X. Zhang 009 (KUN); Yunnan, China; JF935299; JF935376; JF937252; JF980644; JF980561.

Adiantum sp. ; J. Wen 6773 (US); Costa Rica; ——; JF935440; JF937313; ——; JF980624.

Adiantum sp. ; J. Wen 6893 (US); Cartago, Costa Rica; ——; JF935417; JF937290; JF980680; JF980601.

Adiantum sp. ; J. Wen 8295 (US); Luzon, the Philippines; JF935329; JF935411; JF937284; JF980674; JF980594.

Adiantum sp. ; J. Wen 8296 (US); Luzon, the Philippines; ——; JF935410; JF937283; ——; JF980593.

Adiantum sp. ; J. Wen 8333 (US); Malaysia; JF935344; JF935426; JF937299; JF980689; JF980610.

Adiantum sp. ; J. Wen 8681 (US); Oaxaca, Mexico; JF935338; JF935420; JF937293; JF980683; JF980604.

Adiantum sp. ; J. Wen 9616 (US); Antsiranana, Madagascar; JF935326; JF935407; JF937280; JF980671; JF980590.

Adiantum sp. ; J. Wen 9648 (US); Antsiranana, Madagascar; JF935327; JF935408; JF937281; JF980672; JF980591.

Adiantum sp. ; Nee and Wen 53798 (US); Bolivia; ——; JF935390; JF937264; JF980658; JF980573.

Adiantum sp. ; Nee and Wen 53851 (US); Bolivia; JF935333; JF935414; JF937287; JF980677; JF980598.

Adiantum sp. ; Nee and Wen 53885 (US); Bolivia; JF935335; JF935416; JF937289; JF980679; JF980600.

Adiantum tenerum Sw.; J. Wen 10775 (US); Yucatan, Mexico; JF935355; JF935437; JF937310; JF980700; JF980621.

Adiantum viridescens Colenso; J. Wen 10783 (US); New Zealand; JF935354; JF935436; JF937309; JF980699; JF980620.

Adiantum viridimontanum C.A. Paris; Paris 856 (US); Vermont, USA; JF935347; JF935429; JF937302; JF980692; JF980613.

Cheilanthes eckloniana Mett.; J. Wen 10088 (US); Kwazulu Natal, South Africa; JF935343; JF935425; JF937298; JF980688; JF980609.

Pellaea sp.; J. Wen 9479 (US); Ihosy, Madagascar; JF935324; JF935405; JF937278; JF980669; JF980588.

Pellaea sp.; J. Wen 9490 (US); Toamasina, Madagascar; JF935328; JF935409; JF937282; JF980673; JF980592.

Pellaea calomelanos (Sw.) Link; J. Wen 10082 (US); Kwazulu Natal, South Africa; JF935346; JF935428; JF937301; JF980691; JF980612.

Peteri sp.; J. Wen 10179 (US); Indonesia; JF935342; JF935424; JF937297; JF980687; JF980608.

Vittaria flexuosa Fée; WP1246 (KUN); Vietnam; JF935357; JF935441; JF937314; JF980703; JF980625.

Vittaria flexuosa; WP1506 (KUN); Vietnam; ——; JF935442; JF937315; JF980704; JF980626.

Vittaria sp.; J. Wen 6478 (US); Yunnan, China; JF935358; JF935443; JF937316; JF980705; JF980627.

Appendix 2

Samples included in the 3-marker analyses of Adiantum.

Taxon: rbcL GenBank accessions, atpB GenBank accessions, atpA GenBank accessions.

Acrostichum danaeifolium: EF452129, EF452008, EF452065;

Adiantopsis radiata: EF452131, EF452010, EF452067;

Adiantum raddianum: U05906, U93840, EF452071;

Adiantum tenerum: EF452134, EF452014, EF452072;

Adiantum tetraphyllum: EF452135, EF452015, EF452073;

Anetium citrifolium: U21284, EF452017, EF452075;

Antrophyum latifolium: EF452138; EF452018, EF452076;

Asplenium unilaterale: EF452140, EF452020, EF452078;

Astrolepis sinuata: EF452141, EF452021, EF452079;

Blechnum occidentale:U05909, U93838, EF452080;

Ceratopteris richardii: AB059585, AY612691, EF452082;

Coniogramme fraxinea: AM177359, AY612693, AM176470;

Cryptogramma crispa: EF452148, EF452027, EF452087;

Dennstaedtia punctilobula: U05918, U93836, EF452090;

Haplopteris elongata: EF452153, EF452035, EF452096;

Hecistopteris pumila: U21286, EF452036, EF452097;

Jamesonia verticalis: EF452155, EF452038, EF452099;

Llavea cordifolia: U27726, EF452039, EF452100;

Monogramma graminea: EF452157, EF452040, EF452102;

Nephrolepis cordifolia: U05933, EF452041, EF452103;

Neurocallis praestantissima: EF452158, EF452042, EF452104;

Notholaena aschenborniana: EF452159, EF452043, EF452105;

Onychium japonicum: U05641, EF452045, EF452107;

Pellaea intermedia: EF452163, EF452047, EF452109;

Polytaenium cajenense: U20934, EF452052, EF452114;

Pteridium esculentum: U05940, U93834, EF452115;

Pteris argyraea: EF452169, EF452054, EF452117;

Pterozonium brevifrons: EF452175, EF452061, EF452124;

Vittaria graminifolia: U21295, EF452064, EF452128.

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Lu, JM., Wen, J., Lutz, S. et al. Phylogenetic relationships of Chinese Adiantum based on five plastid markers. J Plant Res 125, 237–249 (2012). https://doi.org/10.1007/s10265-011-0441-y

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Keywords

  • Adiantum
  • China
  • Diversification
  • Molecular phylogeny
  • Plastid markers
  • Pteridaceae