Phylogeny of Trigonotis in China—with a special reference to its nutlet morphology and plastid genome

doi:10.1016/j.pld.2023.03.004

Plant Diversity ›› 2023, Vol. 45 ›› Issue (04): 409-421.DOI: 10.1016/j.pld.2023.03.004

Phylogeny of Trigonotis in China—with a special reference to its nutlet morphology and plastid genome

Xue-Min Xu^a, Dan-Hui Liu^b, Shi-Xin Zhu^a, Zhen-Long Wang^a, Zhen Wei^a, Quan-Ru Liu^b

a. School of Life Sciences, Zhengzhou University, Zhengzhou, 450001, China;
b. College of Life Sciences, Beijing Normal University, Beijing, 100875, China

收稿日期:2022-07-27 修回日期:2023-03-01 出版日期:2023-07-25 发布日期:2023-08-21
通讯作者: Zhen Wei,E-mail:weizhen@zzu.edu.cn
基金资助:
This project was funded by the Science and Technology Basic Work, Ministry of Science and Technology, China (2013FY112100 to Q.L.); National Natural Science Foundation of China (31700175 to Z.W.); Fostering Project for Young Teachers of Zhengzhou University, China (JC21343014 to Z.W.).

Phylogeny of Trigonotis in China—with a special reference to its nutlet morphology and plastid genome

Xue-Min Xu^a, Dan-Hui Liu^b, Shi-Xin Zhu^a, Zhen-Long Wang^a, Zhen Wei^a, Quan-Ru Liu^b

a. School of Life Sciences, Zhengzhou University, Zhengzhou, 450001, China;
b. College of Life Sciences, Beijing Normal University, Beijing, 100875, China

Received:2022-07-27 Revised:2023-03-01 Online:2023-07-25 Published:2023-08-21
Contact: Zhen Wei,E-mail:weizhen@zzu.edu.cn
Supported by:
This project was funded by the Science and Technology Basic Work, Ministry of Science and Technology, China (2013FY112100 to Q.L.); National Natural Science Foundation of China (31700175 to Z.W.); Fostering Project for Young Teachers of Zhengzhou University, China (JC21343014 to Z.W.).

摘要/Abstract

摘要： The genus Trigonotis comprises nearly 60 species mainly distributed in East and Southeast Asia. China has the largest number of Trigonotis species in the world, with a total of 44 species, of which 38 are endemic. Nutlet morphology is useful for the taxonomic delimitation of Trigonotis. However, there are still controversial circumscriptions of nutlet shape in some species. In previous studies, interspecies phylogenetic relationships were inferred using few DNA markers and very few taxa, which possibly led to erroneous or incomplete conclusions. In this study, the nutlet morphology of 39 Trigonotis taxa and the characteristics of 34 complete chloroplast genomes (29 taxa) were investigated and analyzed. Then, the phylogenetic relationships were discussed within this genus based on complete chloroplast genomes. To the best of our knowledge, this study is the first comprehensive analysis of nutlet morphology and complete chloroplast genome of Trigonotis. Based on nutlet morphology, Trigonotis can be divided into two groups: Group 1, hemispherical or oblique tetrahedron with carpopodiums, and Group 2, inverted tetrahedron without carpopodiums. The chloroplast genome of Trigonotis exhibited a typical quadripartite structure, including 84–86 protein-coding, 37 transfer RNA, and 8 ribosomal RNA genes, with a total length of 147,247–148,986 bp. Genes in the junctions were well conserved in Trigonotis, similar to those in other Boraginaceae s.str. species. Furthermore, Trigonotis chloroplast genomes showed relatively high diversity, with more conserved genic regions than intergenic regions; in addition, we detected 14 hot spots (Pi > 0.005) in non-coding regions. Phylogenetic analyses based on chloroplast genome data identified highly resolved relationships between Trigonotis species. Specifically, Trigonotis was divided into two clades with strong support: one clade included species with hemispherical or oblique tetrahedron nutlets with carpopodiums and bracts, whereas the other clade included species with inverted tetrahedron nutlets without carpopodiums or bracts. Our results may inform future taxonomic, phylogenetic, and evolutionary studies on Boraginaceae.

关键词: Trigonotis, Nutlet morphology, Plastid genome, Genome structure, Phylogenetic analysis

Abstract: The genus Trigonotis comprises nearly 60 species mainly distributed in East and Southeast Asia. China has the largest number of Trigonotis species in the world, with a total of 44 species, of which 38 are endemic. Nutlet morphology is useful for the taxonomic delimitation of Trigonotis. However, there are still controversial circumscriptions of nutlet shape in some species. In previous studies, interspecies phylogenetic relationships were inferred using few DNA markers and very few taxa, which possibly led to erroneous or incomplete conclusions. In this study, the nutlet morphology of 39 Trigonotis taxa and the characteristics of 34 complete chloroplast genomes (29 taxa) were investigated and analyzed. Then, the phylogenetic relationships were discussed within this genus based on complete chloroplast genomes. To the best of our knowledge, this study is the first comprehensive analysis of nutlet morphology and complete chloroplast genome of Trigonotis. Based on nutlet morphology, Trigonotis can be divided into two groups: Group 1, hemispherical or oblique tetrahedron with carpopodiums, and Group 2, inverted tetrahedron without carpopodiums. The chloroplast genome of Trigonotis exhibited a typical quadripartite structure, including 84–86 protein-coding, 37 transfer RNA, and 8 ribosomal RNA genes, with a total length of 147,247–148,986 bp. Genes in the junctions were well conserved in Trigonotis, similar to those in other Boraginaceae s.str. species. Furthermore, Trigonotis chloroplast genomes showed relatively high diversity, with more conserved genic regions than intergenic regions; in addition, we detected 14 hot spots (Pi > 0.005) in non-coding regions. Phylogenetic analyses based on chloroplast genome data identified highly resolved relationships between Trigonotis species. Specifically, Trigonotis was divided into two clades with strong support: one clade included species with hemispherical or oblique tetrahedron nutlets with carpopodiums and bracts, whereas the other clade included species with inverted tetrahedron nutlets without carpopodiums or bracts. Our results may inform future taxonomic, phylogenetic, and evolutionary studies on Boraginaceae.

Key words: Trigonotis, Nutlet morphology, Plastid genome, Genome structure, Phylogenetic analysis

Xue-Min Xu, Dan-Hui Liu, Shi-Xin Zhu, Zhen-Long Wang, Zhen Wei, Quan-Ru Liu. Phylogeny of Trigonotis in China—with a special reference to its nutlet morphology and plastid genome[J]. Plant Diversity, 2023, 45(04): 409-421.

参考文献

[1] Abramoff, M.D., Magalhaes, P.J., Ram, S.J., 2004. Image processing with image J. Biophotonics Intern. 11, 36-42.
[2] Akcin, O.E., 2007. Nutlets micromorphology of some Onosoma L. (Boraginaceae) species from Turkey. Biologia 62, 684-689. https://doi.org/10.2478/s11756-007-0126-0.
[3] Al-Shehbaz, I.A., 1991. The genera of Boraginaceae in the southeastern United States. J. Arnold Arbor. Supplementary Series 1, 1-169. https://doi.org/10.5962/p.315943.
[4] Amiryousefi, A., Hyvonen, J., Poczai, P., 2018. IRscope: an online program to visualize the junction sites of chloroplast genomes. Bioinformatics 34, 3030-3031. https://doi.org/10.1093/bioinformatics/bty220.
[5] Binzet, R., Akcin, O.E., 2009. Nutlet size, shape and surface ornamentation in 14 Onosma species (Boraginaceae). Acta Bot. Croat. 68, 117-126.
[6] Chacon, J., Luebert, F., Hilger, H.H., et al., 2016. The borage family (Boraginaceae s.str.): a revised infrafamilial classification based on new phylogenetic evidence, with emphasis on the placement of some enigmatic genera. Taxon 65, 523-546. https://doi.org/10.12705/653.6.
[7] Chen, Q., Zhang, D., 2019. The complete chloroplast genome sequence of Onosma paniculatum Bur. et Franch. (Boraginaceae), a medicinal plant in Yunnan and its adjacent regions. Mitochondrial DNA Part B-Resour. 4, 3330-3332. https://doi.org/10.1080/23802359.2019.1673230.
[8] Chen, Y., Chen, Y., Shi, C., et al., 2018. SOAPnuke: a MapReduce acceleration-supported software for integrated quality control and preprocessing of high-throughput sequencing data. GigaScience 7, 1-6. https://doi.org/10.1093/gigascience/gix120.
[9] Cohen, J.I., 2014. A phylogenetic analysis of morphological and molecular characters of Boraginaceae: evolutionary relationships, taxonomy, and patterns of character evolution. Cladistics 30, 139-169. https://doi.org/10.1111/cla.12036.
[10] Daniell, H., Lin, C.S., Yu, M., et al., 2016. Chloroplast genomes: diversity, evolution, and applications in genetic engineering. Genome Biol. 17, 134. https://doi.org/10.1186/s13059-016-1004-2.
[11] Dong, W., Xu, C., Cheng, T., et al., 2013. Sequencing angiosperm plastid genomes made easy: a complete set of universal primers and a case study on the phylogeny of Saxifragales. Genome Biol. Evol. 5, 989-997. https://doi.org/10.1093/gbe/evt063.
[12] Dong, W.P., Liu, J., Yu, J., et al., 2012. Highly variable chloroplast markers for evaluating plant phylogeny at low taxonomic levels and for DNA barcoding. PLoS One 7, e35071. https://doi.org/10.1371/journal.pone.0035071.
[13] Doyle, J.J., Doyle, J.L., Doyle, J.A., et al., 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull. 19, 11-15.
[14] Fior, S., Li, M., Oxelman, B., et al., 2013. Spatiotemporal reconstruction of the Aquilegia rapid radiation through next-generation sequencing of rapidly evolving cpDNA regions. New Phytol. 198, 579-592. https://doi.org/10.1111/nph.12163.
[15] Frazer, K.A., Pachter, L., Poliakov, A., et al., 2004. VISTA: computational tools for comparative genomics. Nucleic Acids Res. 32, W273-W279. https://doi.org/10.1093/nar/gkh458.
[16] Greiner, S., Lehwark, P., Bock, R., 2019. OrganellarGenomeDRAW (OGDRAW) version 1.3.1: expanded toolkit for the graphical visualization of organellar genomes. Nucleic Acids Res. 47, W59-W64. https://doi.org/10.1093/nar/gkz238.
[17] Guo, X., Wang, X., Wang, Q., et al., 2020. The complete chloroplast genome sequence of Borago officinalis Linn. (Boraginaceae) and its phylogenetic analysis. Mitochondrial DNA Part B-Resour. 5, 1461-1462. https://doi.org/10.1080/23802359.2020.1741467.
[18] Hao, J.C., Yan, R.Y., Liu, Q.R., 2017. Trigonotis jiaochengensis sp. nov. (Boraginaceae) from shanxi, China. Nord. J. Bot., Le 35, 63-68. https://doi.org/10.1111/njb.01216.
[19] He, Y., Xu, X.M., Liu, Q.R., 2021. The complete chloroplast genome of Onosma fuyunensis Y. He & Q.R. Liu and its phylogenetic analysis. Mitochondrial DNA Part B-Resour. 6, 3142-3143. https://doi.org/10.1080/23802359.2020.1861567.
[20] Huo, Y., Gao, L., Liu, B., et al., 2019. Complete chloroplast genome sequences of four Allium species: comparative and phylogenetic analyses. Sci. Rep. 9, 12250. https://doi.org/10.1038/s41598-019-48708-x.
[21] Ikeda, K., Sato, S., Matoba, H., et al., 2013. Molecular cytogenetic analysis of the critically endangered Trigonotis radicans var. radicans and var. sericea and allied species in Japan. Cytologia 78, 297-303. https://doi.org/10.1508/cytologia.78.297.
[22] Jansen, R.K., Wojciechowski, M.F., Sanniyasi, E., et al., 2008. Complete plastid genome sequence of the chickpea (Cicer arietinum) and the phylogenetic distribution of rps12 and clpP intron losses among legumes (Leguminosae). Mol. Phylogenet. Evol. 48, 1204-1217. https://doi.org/10.1016/j.ympev.2008.06.013.
[23] Jansen, R.K., Ruhlman, T.A., 2012. Plastid genomes of seed plants. In: Bock, R., Knoop, V. (Eds.), Genomics of Chloroplasts and Mitochondria. Springer, Dordrecht, pp. 103-126. https://doi.org/10.1007/978-94-007-2920-9_5.
[24] Jiang, W., Tan, W., Gao, H., et al., 2020. Transcriptome and complete chloroplast genome of Glycyrrhiza inflata and comparative analyses with the other two licorice species. Genomics 112, 4179-4188. https://doi.org/10.1016/j.ygeno.2020.07.007.
[25] Jin, J.J., Yu, W.B., Yang, J.B., et al., 2020. GetOrganelle: a fast and versatile toolkit for accurate de novo assembly of organelle genomes. Genome Biol. 21, 241. https://doi.org/10.1186/s13059-020-02154-5.
[26] Johnston, I.M., 1937. Studies in the Boraginaceae, Ⅻ. J. Arnold Arbor. 18, 1-25. https://doi.org/10.5962/p.185358.
[27] Katoh, K., Rozewicki, J., Yamada, K.D., 2019. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings Bioinf. 20, 1160-1166. https://doi.org/10.1093/bib/bbx108.
[28] Kung, H-W., Wang, W-T., 1989. Boraginaceae. In: Flora Reipublicae Popularis Sinica, vol. 64. Beijing: Science Press, pp. 177-207.
[29] Langstrom, E., Chase, M.W., 2002. Tribes of Boraginoideae (Boraginaceae) and placement of Antiphytum, Echiochilon, Ogastemma and Sericostoma: a phylogenetic analysis based on atpB plastid DNA sequence data. Plant Systemat. Evol. 234, 137-153. https://doi.org/10.1007/s00606-002-0195-z.
[30] Leister, D., 2003. Chloroplast research in the genomic age. Trends Genet. 19, 47-56. https://doi.org/10.1016/s0168-9525(02)00003-3.
[31] Li, L., Hu, Y., He, M., et al., 2021. Comparative chloroplast genomes: insights into the evolution of the chloroplast genome of Camellia sinensis and the phylogeny of Camellia. BMC Genom. 22, 138. https://doi.org/10.1186/s12864-021-07427-2.
[32] Li, X., Yang, Y., Henry, R.J., et al., 2015. Plant DNA barcoding: from gene to genome. Biol. Rev. Camb. Phil. Soc. 90, 157-166. https://doi.org/10.1111/brv.12104.
[33] Liu, E., Yang, C., Liu, J., et al., 2019a. Comparative analysis of complete chloroplast genome sequences of four major Amorphophallus species. Sci. Rep. 9, 809. https://doi.org/10.1038/s41598-018-37456-z.
[34] Liu, H., Su, Z., Yu, S., et al., 2019b. Genome comparison reveals mutation hotspots in the chloroplast genome and phylogenetic relationships of Ormosia species. BioMed Res. Int. e7265030. https://doi.org/10.1155/2019/7265030.
[35] Lowe, T.M., Chan, P.P., 2016. TRNAscan-SE On-line: integrating search and context for analysis of transfer RNA genes. Nucleic Acids Res. 44, 54-57. https://doi.org/10.1093/nar/gkw413.
[36] Menezes, A.P.A., Resende-Moreira, L.C., Buzatti, R.S.O., et al., 2018. Chloroplast genomes of Byrsonima species (Malpighiaceae): comparative analysis and screening of high divergence sequences. Sci. Rep. 8, 2210. https://doi.org/10.1038/s41598-018-20189-4.
[37] Nazaire, M., Hufford, L., 2012. A broad phylogenetic analysis of Boraginaceae: implications for the relationships of Mertensia. Syst. Bot. 37, 758-783. https://doi.org/10.1600/036364412x648715.
[38] Nguyen, L.T., Schmidt, H.A., von Haeseler, A., et al., 2015. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268-274. https://doi.org/10.1093/molbev/msu300.
[39] Palmer, J.D., 1985. Comparative organization of chloroplast genomes. Annu. Rev. Genet. 19, 325-354. https://doi.org/10.1146/annurev.ge.19.120185.001545.
[40] Park, I., Yang, S., Song, J.H., et al., 2020. Dissection for floral micromorphology and plastid genome of valuable medicinal Borages Arnebia and Lithospermum (Boraginaceae). Front. Plant Sci. 11, 606463. https://doi.org/10.3389/fpls.2020.606463.
[41] Petersen, G., Aagesen, L., Seberg, O., et al., 2011. When is enough, enough in phylogenetics? A case in point from Hordeum (Poaceae). Cladistics 27, 428-446. https://doi.org/10.1111/j.1096-0031.2011.00347.x.
[42] Popov, M.G., 1953. Boraginaceae. In: Shishkin, B.K. (Ed.), Flora of the URSS, vol. 19. Izdatel’stvo Akademii Nauk SSSR, Leningrad, pp. 97-718.
[43] Qian, S., Zhang, Y., Lee, S.Y., 2021. Comparative analysis of complete chloroplast genome sequences in Edgeworthia (Thymelaeaceae) and new insights into phylogenetic relationships. Front. Genet. 12, 643552. https://doi.org/10.3389/fgene.2021.643552.
[44] Rambaut, A., 2014. Molecular Evolution, Phylogenetics and Epidemiology. http://tree.bio.ed.ac.uk/software/figtree/(accessed May 31, 2019).
[45] Rambaut, A., Drummond, A.J., Xie, D., et al., 2018. Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Syst. Biol. 67, 901-904. https://doi.org/10.1093/sysbio/syy032.
[46] Raubeson, L.A., Peery, R., Chumley, T.W., et al., 2007. Comparative chloroplast genomics: analyses including new sequences from the angiosperms Nuphar advena and Ranunculus macranthus. BMC Genom. 8, 174. https://doi.org/10.1186/1471-2164-8-174.
[47] Riedl, H., 1967. Boraginaceae. In: Rechinger, K.H. (Ed.), Flora Iranica. Akademische Druckund Verlagsanstalt, Graz, pp. 1-281.
[48] Rieseberg, L.H., Soltis, D.E., 1991. Phylogenetic consequences of cytoplasmic gene flow in plants. Trends Plant Sci. 5, 65-84.
[49] Rogalski, M., do Nascimento, V.L., Fraga, H.P., et al., 2015. Plastid genomics in horticultural species: importance and applications for plant population genetics, evolution, and biotechnology. Front. Plant Sci. 6, 586. https://doi.org/10.3389/fpls.2015.00586.
[50] Ronquist, F., Teslenko, M., van der Mark, P., et al., 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539-542. https://doi.org/10.1093/sysbio/sys029.
[51] Rozas, J., Ferrer-Mata, A., Sanchez-DelBarrio, J.C., et al., 2017. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol. Biol. Evol. 34, 3299-3302. https://doi.org/10.1093/molbev/msx248.
[52] Smidt, E.C., Paez, M.Z., Vieira, L., et al., 2020. Characterization of sequence variability hotspots in Cranichideae plastomes (Orchidaceae, Orchidoideae). PLoS One 15, e0227991. https://doi.org/10.1371/journal.pone.0227991.
[53] Song, Y., Zhang, Y., Xu, J., et al., 2019. Characterization of the complete chloroplast genome sequence of Dalbergia species and its phylogenetic implications. Sci. Rep. 9, 20401. https://doi.org/10.1038/s41598-019-56727-x.
[54] Stover, B.C., Muller, K.F., 2010. TreeGraph 2: combining and visualizing evidence from different phylogenetic analyses. BMC Bioinf. 11, 7. https://doi.org/10.1186/1471-2105-11-7.
[55] Sun, J., Sun, R., Liu, H., et al., 2021. Complete chloroplast genome sequencing of ten wild Fragaria species in China provides evidence for phylogenetic evolution of Fragaria. Genomics 113, 1170-1179. https://doi.org/10.1016/j.ygeno.2021.01.027.
[56] Takahashi, K., Terai, Y., Nishida, M., et al., 2001. Phylogenetic relationships and ancient incomplete lineage sorting among cichlid fishes in Lake Tanganyika as revealed by analysis of the insertion of retroposons. Mol. Biol. Evol. 18, 2057-2066. https://doi.org/10.1093/oxfordjournals.molbev.a003747.
[57] Takhtajan, A., 1997. Diversity and Classification of Flowering Plants. New York: Columbia University Press.
[58] Tian, S., Lu, P., Zhang, Z., et al., 2021. Chloroplast genome sequence of Chongming lima bean (Phaseolus lunatus L.) and comparative analyses with other legume chloroplast genomes. BMC Genom. 22, 194. https://doi.org/10.1186/s12864-021-07467-8.
[59] Trinh, N.A., Nguyen, H.T.T., Park, S.J., 2012. Phylogenetic relationships of the Korean Trigonotis Steven (Boraginaceae) based on chloroplast DNA (cpDNA) and nuclear ribosomal markers (nrDNA) region. Korean J. Polar Res. 25, 753-761. https://doi.org/10.7732/kjpr.2012.25.6.753.
[60] Twyford, A.D., Ness, R.W., 2017. Strategies for complete plastid genome sequencing. Mol. Ecol. Resour. 17, 858-868. https://doi.org/10.1111/1755-0998.12626.
[61] Wang, C.J., 1982. Taxonomic and phytogeographic studies on Chinese species Trigonotis Stev. Acta Bot. Yunnanica 4, 31-45.
[62] Wang, W., Messing, J., 2011. High-throughput sequencing of three Lemnoideae (duckweeds) chloroplast genomes from total DNA. PLoS One 6, e24670. https://doi.org/10.1371/journal.pone.0024670.
[63] Wang, W.T., 1980. A revision of the genus Microula (Boraginaceae). Acta Phytotaxon. Sin. 18, 266-282.
[64] Wang, W.T., 2007. Trigonotis jinfoshanica, a new species of Boraginaceae from SW China. Guihaia 27, 143-145.
[65] Wang, W.T., 2010. New taxa of Boraginaceae from China. Guihaia 30, 429-439.
[66] Wang, W.T., 2016. Two new species of Boraginaceae from xizang. Bull. Bot. Res. 36, 321-323.
[67] Wang, Y., Wang, S., Liu, Y., et al., 2021. Chloroplast genome variation and phylogenetic relationships of Atractylodes species. BMC Genom. 22, 103. https://doi.org/10.1186/s12864-021-07394-8.
[68] Weigend, M., Gottschling, M., Selvi, F., et al., 2010. Fossil and extant western hemisphere boragineae, and the polyphyly of “Trigonotideae” riedl (Boraginaceae: boraginoideae). Syst. Bot. 35, 409-419. https://doi.org/10.1600/036364410791638423.
[69] Weigend, M., Luebert, F., Selvi, F., et al., 2013. Multiple origins for hound's tongues (Cynoglossum L.) and navel seeds (Omphalodes Mill.) - the phylogeny of the borage family (Boraginaceae s.str.). Mol. Phylogenet. Evol. 68, 604-618. https://doi.org/10.1016/j.ympev.2013.04.009.
[70] Weigend, M., Selvi, F., Thomas, D.C., et al., 2016. Boraginaceae. In: Kadereit, J.W., Bittrich, V. (Eds.), Flowering Plants. Eudicots. The Families and Genera of Vascular Plants, vol. 14. Springer, Cham, pp. 41-102.
[71] Wicke, S., Schneeweiss, G.M., de Pamphilis, C.W., et al., 2011. The evolution of the plastid chromosome in land plants: gene content, gene order, gene function. Plant Mol. Biol. 76, 273-297. https://doi.org/10.1007/s11103-011-9762-4.
[72] Wortley, A.H., Rudall, P.J., Harris, D.J., et al., 2005. How much data are needed to resolve a difficult phylogeny? Case study in Lamiales. Syst. Biol. 54, 697-709. https://doi.org/10.1080/10635150500221028.
[73] Xiong, A.S., Peng, R.H., Zhuang, J., et al., 2009. Gene duplication, transfer, and evolution in the chloroplast genome. Biotechnol. Adv. 27, 340-347. https://doi.org/10.1016/j.biotechadv.2009.01.012.
[74] Xu, X.M., Liu, D.H., He, Y., et al., 2020. Trigonotis motuoensis (Boraginaceae), a new species from Xizang, China. Phytotaxa 461, 233-242. https://doi.org/10.11646/phytotaxa.461.4.1.
[75] Yao, M., Li, X., Li, W., et al., 2012. Overview of pharmacological research of Trigonotis stev. J. Anhui Agric. Sci. 40, 5130-5131. https://doi.org/10.13989/j.cnki.0517-6611.2012.09.190.
[76] Yu, W.T., Jacques, F.M.B., Chen, S.T., et al., 2012. Nutlet micro-morphology of the genus Microula (Boraginaceae) from the Qinghai-Tibetan plateau, and its systematic implications. Nord. J. Bot. 30, 596-612. https://doi.org/10.1111/j.1756-1051.2011.01336.x.
[77] Zhang, D., Gao, F., Jakovlic, I., et al., 2020. PhyloSuite: an integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. Mol. Ecol. Resour. 20, 348-355. https://doi.org/10.1111/1755-0998.13096.
[78] Zhang, X., Sun, Y., Landis, J.B., et al., 2020. Plastome phylogenomic study of Gentianeae (Gentianaceae): widespread gene tree discordance and its association with evolutionary rate heterogeneity of plastid genes. BMC Plant Biol. 20, 340. https://doi.org/10.1186/s12870-020-02518-w.
[79] Zhang, X.F., Landis, J.B., Wang, H.X., et al., 2021. Comparative analysis of chloroplast genome structure and molecular dating in Myrtales. BMC Plant Biol. 21, 219. https://doi.org/10.1186/s12870-021-02985-9.
[80] Zhu, G.L., Riedl, H., Kamelin, R., 1995. Boraginaceae. In: Wu, Z-Y., Raven, P.H. (Eds.), Flora of China, vol. 16. Science Press, Beijing; Missouri Botanical Garden Press, St. Louis, pp. 329-427.

Phylogeny of Trigonotis in China—with a special reference to its nutlet morphology and plastid genome

Phylogeny of Trigonotis in China—with a special reference to its nutlet morphology and plastid genome

PDF (PC)

可视化

摘要/Abstract

引用本文

使用本文

参考文献

相关文章 6

编辑推荐

Metrics

本文评价

[1]	Yu-Feng Gu, Jiang-Ping Shu, Yi-Jun Lu, Hui Shen, Wen Shao, Yan Zhou, Qi-Meng Sun, Jian-Bing Chen, Bao-Dong Liu, Yue-Hong Yan. Insights into cryptic speciation of quillworts in China[J]. Plant Diversity, 2023, 45(03): 284-301.
[2]	Chao Liu, Huan-Huan Chen, Li-Zhou Tang, Phyo Kay Khine, Li-Hong Han, Yu Song, Yun-Hong Tan. Plastid genome evolution of a monophyletic group in the subtribe Lauriineae (Laureae, Lauraceae)[J]. Plant Diversity, 2022, 44(04): 377-388.
[3]	Kai-Wen Jiang, Rong Zhang, Zhong-Fu Zhang, Bo Pan, Bin Tian. DNA barcoding and molecular phylogeny of Dumasia (Fabaceae: Phaseoleae) reveals a cryptic lineage[J]. Plant Diversity, 2020, 42(05): 376-385.
[4]	Virginia M. Mwanzia, Ding-Xuan He, Andrew W. Gichira, Yan Li, Boniface K. Ngarega, Mwihaki J. Karichu, Peris W. Kamau, Zhi-Zhong Li. The complete plastome sequences of five Aponogeton species (Aponogetonaceae): Insights into the structural organization and mutational hotspots[J]. Plant Diversity, 2020, 42(05): 334-342.
[5]	Liuqing Ma, Pengfei Ma, Dezhu Li. The first complete plastid genome of Burmannia disticha L. from the mycoheterotrophic monocot family Burmanniaceae[J]. Plant Diversity, 2018, 40(05): 232-237.
[6]	Jiaojun Yu, Chaobo Wang, Xun Gong. Degeneration of photosynthetic capacity in mixotrophic plants, Chimaphila japonica and Pyrola decorata (Ericaceae)[J]. Plant Diversity, 2017, 39(02): 80-88.