Research Article |
Corresponding author: Lei Duan ( duanlei@scbg.ac.cn ) Academic editor: Pavel Stoev
© 2016 Lei Duan, Xue Yang, Peiliang Liu, Gabriel Johnson, Jun Wen, Zhaoyang Chang.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Duan L, Yang X, Liu P, Johnson G, Wen J, Chang Z (2016) A molecular phylogeny of Caraganeae (Leguminosae, Papilionoideae) reveals insights into new generic and infrageneric delimitations. PhytoKeys 70: 111-137. https://doi.org/10.3897/phytokeys.70.9641
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Based on sequence data of nuclear ITS and plastid matK, trnL-F and psbA-trnH markers, the phylogeny of the subtribes Caraganinae and Chesneyinae in tribe Caraganeae was inferred. The results support the monophyly of each of the subtribes. Within subtribes Caraganinae, Calophaca and Halimodendron are herein transferred into Caragana to ensure its generic monophyly. The subtribe Chesneyinae is composed of four well-supported genera: Chesneya, Chesniella, Gueldenstaedtia and Tibetia. Based on phylogenetic, morphological, distributional and habitat type evidence, the genus Chesneya was divided into three monophyletic sections: C. sect. Chesneya, C. sect. Pulvinatae and C. sect. Spinosae. Chesneya macrantha is herein transferred into Chesniella. Spongiocarpella is polyphyletic and its generic rank is not maintained. The position of Chesneya was incongruent in the nuclear ITS and the plastid trees. A paternal chloroplast capture event via introgression is hypothesized for the origin of Chesneya, which is postulated to have involved the common ancestor of Chesniella (♂) and that of the Gueldenstaedtia – Tibetia (GUT) clade (♀) as the parents.
Caragana , Chesneya , Chesniella , chloroplast capture, generic delimitation, phylogeny
Caraganeae Ranjbar is a mid-sized tribe in Leguminosae, established by
A few recent studies referred to the concept of Caraganeae. Molecular work of
Within the subtribe Caraganinae, the genus Caragana has attracted much attention (
The genera Chesneya and Gueldenstaedtia formed a well-supported clade (
We herein employ sequence data from nrDNA ITS and plastid matK, trnL-F and psbA-trnH to a) test the monophyly of Caraganeae and its subtribes; b) estimate the phylogeny of genera in Caraganeae; and c) discuss the taxonomic implications of this phylogeny on the generic and the infrageneric classification of the tribe.
Our sampling was designed largely following the generic demarcations in Flora Reipublicae Popularis Sinicae (
To better resolve the relationships of subtribes Caraganinae and Chesneyinae, 11 Galegeae species (8 genera) and 5 Hedysareae species (4 genera) were also sampled. Cicer microphyllum Royle ex Bentham, Dalbergia hupeana Hance, Lathyrus latifolius L., Robinia pseudoacacia L., Trifolium repens L. and Wisteria sinensis (Sims) Sweet were selected as outgroups based on previous studies (
Total genomic DNAs were extracted from silica-gel dried leaves or herbarium material using the Plant DNA Extraction Kit - AGP965/960 (AutoGen, Holliston, MA, USA) or the DNeasy Plant Mini Kit (Qiagen, Valencia, USA). Polymerase chain reactions (PCR) were prepared in 25µL containing 1.5 mM MgCl2, 0.2 mM of each dNTP, 0.4 mM of each primer, 1 U of Taq polymerase (Bioline, Aberdeen, Scotland, UK), and using 10–50 ng (2.5 µL) template DNAs, following
Sequences were assembled with Geneious 7.1 (http://www.geneious.com/), and aligned using MUSCLE 3.8.31 (
Phylogenetic analyses were carried out using Bayesian inference (BI;
In the BI, the Markov chain Monte Carlo (MCMC) search was run by two replicates for 10,000,000 generations, sampling one tree every 1,000 generations. After the first 2,500,000 generations (2,500 trees) were discarded as burn-in, a 50% majority-rule consensus tree and posterior probabilities were obtained among the remaining trees. Results were checked using the program Tracer 1.5 (
Sequence characteristics are shown in Table
Bayesian tree of the nrDNA ITS data, showing relationships of genera in subtribes Caraganinae, Chesneyinae and their close relatives. The labeled sections of Gueldenstaedtia and Tibetia followed
Bayesian tree of the concatenated plastid data of matK, trnL-F and psbA-trnH sequences, showing genera in subtribes Caraganinae, Chesneyinae and their close relatives. The labeled sections of Gueldenstaedtia and Tibetia followed
Sequence characteristics with gaps as missing data: alignment length, the number of the constant, variable and potential parsimony-informative (Pi) sites, and the best-fit nucleotide substitution model determined by AIC.
Dataset | Length | Constant | Variable | Pi | Model |
---|---|---|---|---|---|
ITS1 | 266 | 81 | 185 | 148 | GTR+I+G |
5.8S | 164 | 143 | 21 | 14 | TrNef+I+G |
ITS2 | 279 | 113 | 166 | 131 | GTR+G |
matK | 807 | 485 | 322 | 189 | GTR+G |
trnL-F | 1412 | 921 | 491 | 279 | TVM+I+G |
psbA-trnH | 793 | 472 | 321 | 175 | TIM1+G |
In the ITS tree (Fig.
Subtribe Caraganinae contained three genera, within which Calophaca was monophyletic (PP = 1, LBS = 96%), but Calophaca and Halimodendron were embedded within the paraphyletic Caragana. Within subtribe Chesneyinae, Gueldenstaedtia (PP = 1, LBS = 100%) and Tibetia (PP = 1, LBS = 100%) were each monophyletic and together they formed a clade (the GUT clade, shown in blue; PP = 1, LBS = 100%). Two accessions of former Chesneya macrantha Cheng f. ex H.C.Fu constituted a robustly supported branch nested in a monophyletic Chesniella (displayed in green; PP = 0.98, LBS = 89%), while other accessions of Chesneya formed another clade (Chesneyas.s.; shown in red; PP = 1, LBS = 100%; Fig.
Similar to the ITS results, the plastid tree (Fig.
Caraganeae comprises ca. 100 species distributed in temperate Asia, extending to eastern Europe (
Subtribe Caraganinae is composed of Calophaca, Caragana and Halimodendron (
Within Caraganinae, Halimodendron contains only H. halodendron (Pall.) Druce with its distribution roughly overlapping with that of Calophaca (
Calophaca morphologically resembles Caragana, and it is only distinguished from the latter by its imparipinnate leaves, rachises without thorns, and relatively denser racemes (
The taxonomy of Caragana has been investigated by various authors (
At the sectional level, our ITS tree (Fig.
At the infra-sectional level, Car. ser. Bracteolatae Kom. and Car. ser. Spinosae are well-supported by our results (not labeled in the trees). Our results are therefore not completely congruent with
The subtribe Chesneyinae, as established by
This subtribe contains ca. 50 species and differs from the Astragalean clade by twisted valves (e.g., in Chesneya), but a few species of Astragalus also have twisted legumes. Taxa of Chesneyinae are distinguished from Hedysareae by their dehiscent pods (
Distribution (A) and representative plants (B–H) of genera in Chesneyinae. A red – Chesneya, green – Chesniella, blue – Gueldenstaedtia and yellow – Tibetia B Chesneya acaulis C Chesneya spinosa D Chesneya nubigena E Chesniella macrantha F Chesniella ferganensis G Gueldenstaedtia verna H Tibetia yadongensis.
The ITS and plastid topologies are incongruent within Chesneyinae. Chesneyas.s. formed a clade with the GUT clade in the ITS tree (Fig.
Allopolyploidy can be ruled out for two reasons. First, taxa within Chesneyinae are diploid (
ILS and chloroplast capture seem more likely mechanisms for the present case (
Compared to the biparental inheritance of the nuclear genome, plastid DNA of angiosperms is usually uniparentally transmitted, especially maternally (
We herein hypothesize a chloroplast capture event in the origin of Chesneyas.s. as follows. The common ancestor of Chesniella served as the putative paternal parent of Chesneyas.s. (sister to Chesneyas.s. in the plastid tree; Fig.
Analyses of
Chesneya is the type genus of Chesneyinae, with ca. 35 species (see Fig.
Chesneya macrantha is nested within a monophyletic Chesniella according to our ITS tree (Fig.
After its establishment by
The presently demarcated Chesneya was assigned into three strongly supported sections herein (as in the key of Chesneya proposed by
The infra-sectional relationships within C. sect. Chesneya are basically unresolved in our ITS trees (Fig.
The xeric C. sect. Chesneya grows on dry slopes or desert margins of northwestern China, Mongolia and central Asia (see Fig.
Most previous workers did not accept the generic status of Chesniella, treating it within Chesneya (
Gueldenstaedtia is a small genus comprised of ca. 10 species and is distinguished from Chesneya by its palmately nerved wing petals (vs. pinnately in Chesneya) and non-twisted pod valves (vs. twisted) (see Fig.
Gueldenstaedtia and Tibetia were each supported to be monophyletic, and the two genera together form the GUT clade (Figs
Within Tibetia, two accessions of T. himalaica (Baker) H.P.Tsui grouped together, which were sister to T. yadongensis H.P.Tsui (Figs
Calophaca Fisch. ex DC., Prod. 2: 270. 1825, syn. nov.
Type: Calophaca wolgarica Fisch., Prod. 2: 270. 1825.
Halimodendron Fisch. ex DC., Prod. 2: 269. 1825, syn. nov.
Type: Halimodendron halodendron (Pall.) Druce, Rep. Bot. Soc. Exch. Club Brit. Isles 4: 626. 1917.
Caragana arborescens Lam., Encycl. 1(2): 615. 1785.
Shrubs, subshrubs or rarely small trees. Stipules caducous or persistent. Leaves paripinnate, rarely imparipinnate (C. sect. Calophaca), 4–27-foliolate; leaflet blades with margin entire. Lax raceme or fascicled flowers axillary, or flowers solitary. Calyx tubular or campanulate, base usually oblique, teeth 5. Corolla yellow, purple, pink or white; standard ovate to suborbicular, clawed or reflexed at margin; wings and keel often auriculate. Stamens diadelphous (9+1). Ovary sessile to stipitate, with ovule 1-many; style filiform. Pod inflated, compressed, cylindric or linear, dehiscent or rarely indehiscent (C. sect. Halimodendron), with twisted or thickened valve.
This genus contains ca. 100 species, ranging from eastern Europe, Caucasus, western and central Asia, Sino-Himalayan region to Mongolia and Siberia.
Calophaca Fisch. ex DC., Prod. 2: 270. 1825.
Type: Calophaca wolgarica Fisch., Prod. 2: 270. 1825.
This section includes 5–8 species, distributed in Caucasus, central Asia, northwestern Xinjaing, Innner Mongolia and Shanxi of China.
Halimodendron Fisch. ex DC., Prod. 2: 269. 1825.
Type: Halimodendron halodendron (Pall.) Druce, Rep. Bot. Soc. Exch. Club Brit. Isles 4: 626. 1917.
Caragana halodendron (Pallas) Dumont de Courset, Bot. Cult. 3: 513. 1802.
This section is monotypic and distributes in Caucasus, northeastern Turkey, northern Iran, northern Afghanistan, northern Pakistan, central Asia, western Mongolia, Shanxi and Xinjiang of China.
1 | Leaves imparipinnate; ovary sessile | Car. sect. Calophaca |
– | Leaves paripinnate; ovary subsessile or stipitate | 2 |
2 | Racemose; pedicel non-articulate; pods inflated, indehiscent, valve thickened; seeds few | Car. sect. Halimodendron |
– | 2–5 flowers in fascicles, or solitary flower; pedicel articulate; pods compressed, cylindric or linear, dehiscent, valve twisted; seeds many | 3 |
3 | Petiole and rachis always caducous; leaves pinnate | Car. sect. Caragana |
– | Petiole and rachis persistent, usually spinelike; leaves pinnate or digitate | 4 |
4 | Leave digitate | Car. sect. Frutescentes |
– | Leave pinnate or partly digitate | 5 |
5 | Leave digitate or pinnate with 4 leaflets on short branchlets, leave pinnate on long branchlets | Car. sect. Spinosae |
– | Leaves pinnate | 6 |
6 | Petiole and rachis persistent | Car. sect. Jubatae |
– | Petiole and rachis persistent on long branchlets, caducous on short branchlets | Car. sect. Bracteolatae |
Spongiocarpella Yakovlev & N.Ulziykhutag, Bot. Zhur. 17(2): 249. 1987. syn. nov.
Type: Spongiocarpella nubigena (D.Don) Yakovl., Bot. Zhur. 17(2): 249. 1987, based on Chesneya nubigena (D.Don) Ali. (see blow)
Chesneya rytidosperma Jaub. et Spach, Ill. Pl. Orient. 1(5): 93. 1842.
Chesneya sect. Macrocarpon Boriss., Fl. U.S.S.R. 11: 280. 1945. syn. nov.
Type: Chesneya rytidosperma Jaub. et Spach, Ill. Pl. Orient. 1(5): 93. 1842.
This section includes the majority of Chesneya species. It can be diagnosed by reduced stems and caducous petiole and rachis. It contains ca. 20 xeric species, ranging from desert and dry slope of northwestern China and western Tibet to central and western Asia and Caucasus.
Spongiocarpella Yakovlev & N. Ulziykhutag, Bot. Zhur. 17(2): 249. 1987.
Type: Spongiocarpella nubigena (D.Don) Yakovl., Bot. Zhur. 17(2): 249. 1987.
Chesneya nubigena (D.Don) Ali, Scientist (Karachi) iii: 4. 1959.
This psychric section is composed of C. nubigena, C. polystichoides (Hand.-Mazz.) Ali and C. purpurea. It differs from other sections by blackened, curved and non-spiny petiole and rachis, distributed on high-altitude slope in eastern Himalayas and southern and eastern Tibet.
Chesneya spinosa P.C.Li, Acta Phytotax. Sin. 19(2): 236. 1981.
This monotypic section is recognized by its hardened-spiny petiole and rachis. It is restricted in high-altitude psychrophytic rocky slope in southern Tibet.
1 | Plant non-pulvinate, petiole and rachis caducous, leaflet apices truncate or emarginate | C. sect. Chesneya |
– | Plant pulvinate, petiole and rachis persistent, leaflet apices acute | 2 |
2 | Petiole and rachis hardened and spiny, leaflet apices with short spines | C. sect. Spinosae |
– | Petiole and rachis blackened and curved, leaflet apices without short spines | C. sect. Pulvinatae |
Chesneya macrantha Cheng f. ex H.C.Fu, Fl. Intramongol. 3: 291. 1977.
Information of the type specimen was not included in its protolog, which was recorded in Acta Phytotax. Sin. 19(2): 237. 1981: China. Inner Mongolia: Baganmao, 29 May 1931, T.N.Liou 2146 (holotype:
CHINA. Ningxia: Mt. Helan, 1200m, May 15 1923, R.C.Ching 108 (
Dry slopes in Mongolia and Inner Mongolia, Ningxia and Xinjiang of China.
We are grateful to the curators of the following herbaria for providing leaf samples, seeds or DNA samples:
Voucher information and GenBank accession numbers
Data type: Multi-records
Explanation note: Data are arranged in the order: taxon name, locality, collector(s), collection number and herbarium, GenBank accession numbers for ITS, matK, trnL-trnF, psbA-trnH. Newly generated sequences are indicated by an asterisk (*); missing sequences are indicated by a dash (–).