Chin Bull Bot ›› 2015, Vol. 50 ›› Issue (5): 549-564.doi: 10.11983/CBB15164

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Phylogenetic Reconstruction of Tribal Relationships in Asteroi- deae (Asteraceae) with Low-copy Nuclear Genes

Mian Liu1,2, Caifei Zhang1,2*, Chien-Hsun Huang1,2, Hong Ma1,2*   

  1. 1School of Life Sciences, Fudan University, Shanghai 200438, China
    2Institute of Plant Biology, Fudan University, Shanghai 200438, China
  • Received:2015-08-15 Accepted:2015-09-05 Online:2015-10-09 Published:2015-09-01
  • Contact: Zhang Caifei,Ma Hong
  • About author:? These authors contributed equally to this paper

Abstract:

Asteroideae is the largest subfamily of the daisy family, Asteraceae, with more species than most other angiosperm families. Previous phylogenetic relationships of Asteroideae tribes were mostly based on chloroplast genes, which are uniparentally inherited and could not reflect the entire evolutionary histories. Especially considering the widespread phenomenon of hybridization in Asteraceae, low-copy nuclear genes with biparental inheritance can better serve as phylogenetic markers, for a more complete understanding of their evolution. To resolve the intertribal relationships in Asteroideae, transcriptomic datasets were newly generated by sequencing 20 species and additional datasets for 11 species downloaded from NCBI, representing 13 tribes and all 3 supertribes of this subfamily. Extensive sequence analyses of the 31 datasets resulted in the selection of 47 orthologous nuclear genes for phylogenetic reconstruction. Using the supermatrix analyses and coalescent estimates, we obtained robust and highly supported species trees, which are in agreement with each other. New intertribal phylogenies of Asteroideae revealed that: (1) the supertribe Senecionodae should be merged into the supertribe Asterodae; (2) Anthemideae possibly originated from a hybrid of ancestors of Senecioneae and Astereae; and (3) Coreopsideae is probably also hybrid originated. This study demonstrates that low-copy nuclear genes are good markers for infra-familial phylogenetic reconstruction and provides a foundation for future studies of phylogeny of Asteraceae and other angiosperm families.

Key words: Asteraceae, Asteroideae, low-copy nuclear genes, phylogeny, transcriptome-sequencing

Figure 1

Flow chart of bioinformatics pipeline"

Table 1

Samples used in this study and their information"

Tribe Species Locality Accession No. Voucher
Anthemideae Achillea millefolium Campus of Penn State University, USA - Zhang Ning, B20AM
Anthemideae Artemisia chamaemelifolia NCBI SRX096997 -
Anthemideae Tanacetum parthenium NCBI ERX337163 -
Astereae Symphyotrichum subulatum Chenshan Botanical Garden, Shanghai - Liu Mian, CSLM02
Astereae Eurybia divaricata Campus of Penn State University, USA - Ma Hong, HM213
Astereae Solidago gigantea Penn State College, USA - Ma Hong, HM157
Athroismeae Centipeda minima Beijing Botanical Garden of CAS - Gao Tiangang, GTG03
Calenduleae Osteospermum jucundum Glasgow, UK - Ma Hong, HM366
Calenduleae Calendula officinalis Beijing Botanical Garden, Beijing - Zhang Caifei, 3395
Cichorieae Sonchus asper Campus of Penn State University, USA - Zhang Ning, A10SA
Cichorieae Lactuca serriola NCBI SRX098217 -
Coreopsideae Cosmos bipinnatus Xuancheng, Anhui - Liu Mian, AH06
Coreopsideae Bidens frondosa Campus of Penn State College, USA - Ma Hong, HM208
Eupatorieae Stevia rebaudiana NCBI - -
Eupatorieae Ageratum conyzoides Mt. Tianmu, Zhejiang SRX255224 Liu Mian, TMS08
Eupatorieae Mikania micrantha Indonesia - Gao Tiangang, GTG5498
Gnaphalieae Helichrysum petiolare NCBI SRX202783 -
Gnaphalieae Leontopodium smithianum Mt. Dongling, Beijing - Yang Ji, YJ08
Helenieae Gaillardia pulchella Chenshan Botanical Garden, Shanghai - Liu Mian, CSLM07
Heliantheae Helianthus tuberosus Mt. Tianmu, Zhejiang - Liu Mian, TMS15
Heliantheae Iva annua NCBI SRX255215 -
Heliantheae Echinacea purpurea NCBI SRX085117 -
Inuleae Duhaldea cappa Campus of Nanjing University, Nanjing - Yang Ji, YJLM09
Inuleae Inula linariifolia Mt. Zijin, Nanjing - Liu Mian, YJLM04
Madieae Arnica montana NCBI SRX096987 -
Millerieae Sigesbeckia pubescens Mt. Tianmu, Zhejiang - Liu Mian, TMS01
Millerieae Galinsoga quadriradiata Mt. Tianmu, Zhejiang - Liu Mian, TMS02
Millerieae Guizotia scabra NCBI SRX255223 -
Senecioneae Euryops pectinatus Campus of Fudan University, Shanghai - Liu Mian, FDU01
Senecioneae Senecio aethnensis NCBI SRX328503 -
Senecioneae Petasites hybridus NCBI SRX096999 -

Figure 2

Reference species tree of Asteroideae for selecting orthologous genesIn this tree, the relationships among the tribes, or those between genera of the same tribe, are not specified."

Table 2

The systematic information of 47 unigene matrices, respectively"

Unigene Length (bp) VS VS (%) IS IS (%) MS (%)
433680 1 290 809 62.71 637 49.38 1.67
433783 462 293 63.42 228 49.35 0.89
433651 1 158 656 56.65 530 45.77 4.54
435322 1 281 716 55.89 553 43.17 3.74
435258 1 236 707 57.20 518 41.91 13.26
431587 864 479 55.44 362 41.90 2.49
432845 675 368 54.52 276 40.89 1.81
431540 1 152 637 55.30 470 40.80 3.73
432103 741 394 53.17 296 39.95 8.29
435225 1 395 765 54.84 539 38.64 16.34
432720 1 104 575 52.08 408 36.96 7.53
432475 828 402 48.55 305 36.84 4.98
432118 588 317 53.91 215 36.56 4.30
435156 1 740 913 52.47 634 36.44 22.01
435256 885 436 49.27 322 36.38 3.75
435114 1 140 547 47.98 406 35.61 3.58
434310 993 459 46.22 353 35.55 5.39
432389 1 902 928 48.79 675 35.49 5.17
435299 591 290 49.07 209 35.36 3.59
432317 1 320 624 47.27 463 35.08 3.20
435127 1 569 730 46.53 550 35.05 10.70
435193 1 491 799 53.59 522 35.01 10.09
435154 1 374 663 48.25 478 34.79 4.13
431821 1 323 621 46.94 459 34.69 5.00
433235 1 560 696 44.62 538 34.49 2.20
434795 1 164 525 45.10 394 33.85 2.46
435112 2 835 1332 46.98 949 33.47 19.43
433741 777 326 41.96 259 33.33 3.40
432132 807 362 44.86 267 33.09 3.22
433969 684 303 44.30 225 32.89 0.22
433433 1 362 557 40.90 441 32.38 0.23
435159 558 244 43.73 178 31.90 4.09
433560 951 425 44.69 303 31.86 2.42
432107 1 188 473 39.81 376 31.65 1.30
432280 1 209 506 41.85 381 31.51 2.13
433255 795 318 40.00 249 31.32 1.41
435277 1 359 552 40.62 419 30.83 2.44
435118 876 388 44.29 268 30.59 2.46
433710 969 414 42.72 294 30.34 1.81
432233 1 059 455 42.97 319 30.12 3.78
432926 1 014 442 43.59 299 29.49 5.14
433740 726 285 39.26 212 29.20 0.95
433176 789 329 41.70 226 28.64 1.08
434314 942 436 46.28 269 28.56 3.59
435311 444 165 37.16 125 28.15 0.20
434176 1 296 482 37.19 351 27.08 3.19
433486 741 292 39.41 194 26.18 0.38
Average 1 090 520 47.53 382 34.95 4.63

Figure 3

A maximum likelihood tree using 47 nuclear genes for 29 Asteroideae species The numbers on each node are support values of ML and Bayesian analyses, respectively. Asterisks stand for bootstrap of 100% or posterior probability of 1.0."

Figure 4

Coalescent-based species tree of Asteroideae estimated from 47 gene treesThe numbers on each node are bootstrap support values. Asterisks stand for bootstrap of 100%."

Figure 5

Comparison of Intertribal phylogenies of Asteroideae based on different data sets(A) Cladogram based on chloroplast genes (revised from Panero and Funk (2002, 2008) and Panero et al. (2014)); (B) Cladogram based on concatenated alignment of 47 nuclear genes used by present work. For all clades, bootstrap values of MP or ML analyses are all ≥70%. The shaded areas show obvious incongruences on both trees."

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