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

doi:10.11983/CBB15164

Abstract

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

Mian Liu, Caifei Zhang, Chien-Hsun Huang, Hong Ma. Phylogenetic Reconstruction of Tribal Relationships in Asteroi- deae (Asteraceae) with Low-copy Nuclear Genes[J]. Chinese Bulletin of Botany, 2015, 50(5): 549-564.

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URL: https://www.chinbullbotany.com/EN/10.11983/CBB15164

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Figures/Tables 7

References 71

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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	-

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	-

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

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

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