The first complete plastid genome of Burmannia disticha L. from the mycoheterotrophic monocot family Burmanniaceae

doi:10.1016/j.pld.2018.07.004

Abstract

Abstract:

Burmanniaceae is one major group within the monocot order Dioscoreales that has not had its plastome sequenced. Members of Burmanniaceae are mostly achlorophyllous, although the genus Burmannia also includes autotrophs. Here, we report sequencing and analysis of the first Burmanniaceae plastid genome from Burmannia disticha L.. This plastome is 157,480 bp and was assembled as a circular sequence with the typical quadripartite structure of plant plastid genomes. This plastome has a regular number of potentially functional genes with a total of 111, including 78 protein coding genes, 4 ribosomal RNA (rRNA) genes, and 29 tRNA genes. The ratio of the total length of genic:intergenic DNA is 1.58:1, and the mean length of intergenic regions is 398 bp, the longest being 1918 bp. The overall GC content of the B. disticha plastome is 34.90%, and the IR regions in B. disticha are more GC rich (39.50%) than the LSC (32.30%) and SSC (28.80%) regions. Phylogenetic analysis of protein-coding sequences from plastomes of related species in the order Dioscoreales support a clade comprising Burmanniaceae and Dioscoreaceae. This phylogenetic placement is congruent with previous findings based on nuclear and mitochondrial evidence.

Key words: Burmannia disticha, Burmanniaceae, Plastome, Phylogenetic analysis

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.

References

Altschul, S.F., Gish, W., Miller, W., et al., 1990. A basic local alignment search tool. J. Mol. Biol. 215 (3), 403-410.
Angiosperm Phylogeny Group, 2003. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants:APG Ⅱ. Bot. J. Linn. Soc. 141, 399-436.
Angiosperm Phylogeny Group, 1998. An ordinal classification for the families of flowering plants. Ann. Mo. Bot. Gard. 4, 531-553.
Barrett, C.F., Davis, J.I., 2012. The plastid genome of the mycoheterotrophic Corallorhiza striata (Orchidaceae) is in the relatively early stages of degradation. Am. J. Bot. 99, 1513-1523.
Barrett, C.F., Freudenstein, J.V., Li, J., et al., 2014. Investigating the path of plastid genome degradation in an early-transitional clade of heterotrophic orchids, and implications for heterotrophic angiosperms. Mol. Biol. Evol. 31 (12), 3095-3112.
Bolin, J.F., Tennakoon, K.U., Majid, M.B.A., et al., 2017. Isotopic evidence of partial mycoheterotrophy in Burmannia coelestis (Burmanniaceae). Plant Spec. Biol. 32, 74-80.
Bodin, S.S., Kim, J.S., Kim, J.H., 2016. Phylogenetic inferences and the evolution of plastid DNA in Campynemataceae and the mycoheterotrophic Corsia dispar D.L Jones & B. Gray (Corsiaceae). Plant Mol. Biol. Rep. 34, 192-210.
Caddick, L.R., Rudall, P.J., Wilkin, P., et al., 2002a. Phylogenetics of Dioscoreales based on combined analyses of morphological and molecular data. Bot. J. Linn. Soc. 138, 123-144.
Caddick, L.R., Wilkin, P., Rudall, P.J., et al., 2002b. Yams reclassified:a recircumscription of Dioscoreaceae and Dioscoreales. Taxon 51, 103-114.
Davis, C.C., Xi, Z.X., Mathews, S., 2014. Plastid phylogenomics and green plant phylogeny:almost full circle but not quite there. BMC Biol. 12 (1), 11.
Davis, J.I., Stevenson, D.W., Petersen, G., et al., 2004. A phylogeny of the monocots, as inferred from rbcL and atpA sequence variation, and a comparison of methods for calculating jackknife and bootstrap values. Syst. Biol. 29, 467-510.
Delannoy, E., Fujii, S., Francs-Small, C.D.C., et al., 2011. Rampant gene loss in the underground orchid Rhizanthella gardneri highlights evolutionary constraints on plastid genomes. Mol. Biol. Evol. 28, 2077-2086.
Doyle, J.J., Doyle, J.L., 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull. 19, 11-15.
Jonker, F., 1938. A Monograph of the Burmanniaceae, vol. 51. Meeded Bot. Mus. Herb. Rijks Univ. Utrecht, Utrecht, pp. 1-279.
Kearse, M., Moir, R., Wilson, A., et al., 2012. Geneious Basic:an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28 (12), 1647-1649.
Lam, V.K.Y., Merckx, V.S.F.T., Graham, S.W., 2016. A few-gene plastid phylogenetic framework for mycoheterotrophic monocots. Am. J. Bot. 103 (4), 692-708.
Lam, V.K.Y., Gomez, M.S., Graham, S.W., 2015. The highly reduced plastome of mycoheterotrophic Sciaphila (Triuridaceae) is colinear with its green relatives and is under strong purifying selection. Genome Biol. Evol. 7, 2220-2236.
Langmead, B., Salzberg, S.L., 2012. Fast gapped-read alignment with Bowtie 2. Nat. Meth. 9, 357-359.
Lim, G.S., Barrett, C.F., Pang, C.C., et al., 2016. Drastic reduction of plastome size in the mycoheterotrophic Thismia tentaculata relative to that of its autotrophic relative Tacca chantrieri. Am. J. Bot. 103, 1-9.
Liu, C., Shi, L.C., Zhu, Y.J., et al., 2012. CpGAVAS, an integrated web server for the annotation, visualization, analysis, and GenBank submission of completely sequenced chloroplast genome sequences. BMC Genom. 13, 715.
Logacheva, M.D., Schelkunov, M.I., Nuraliev, M.S., et al., 2014. The plastid genome of mycoheterotrophic monocot Petrosavia stellaris exhibits both gene losses and multiple rearrangements. Genome Biol. Evol. 6 (1), 238-246.
Logacheva, M.D., Schelkunov, M.I., Penin, A.A., 2011. Sequencing and analysis of plastid genome in mycoheterotrophic orchid Neottia nidus-avis. Genome Biol. Evol. 3, 1296-1303.
Lohse, M., Drechsel, O., Kahlau, S., et al., 2013. Organellar Genome DRAW-a suite of tools for generating physical maps of plastid and mitochondrial genomes and visualizing expression datasets. Nucleic Acids Res. 41, 575-581.
Luo, R., Liu, B., Xie, Y., et al., 2012. SOAPdenovo2:an empirically improved memoryefficient short-read de novo assembler. Giga Sci. 1, 18.
Mennes, C.B., Lam, V.K.Y., Rudall, P.J., et al., 2015. Ancient Gondwana break-up explains the distribution of the mycoheterotrophic family Corsiaceae (Liliales). J. Biogeogr. 42 (6), 1123-1136.
Mennes, C.B., Smets, E.F., Moses, S.N., et al., 2013. New insights in the long-debated evolutionary history of Triuridaceae (Pandanales). Mol. Phylogenet. Evol. 69, 994-1004.
Merckx, V., Chatrou, L.W., Lemaire, B., et al., 2008. Diversification of myco-heterotrophic angiosperms:evidence from Burmanniaceae. BMC Evol. Biol. 8 (1), 178.
Merckx, V., Schols, P., Maas-Van, D.K.H., et al., 2006. Phylogeny and evolution of Burmanniaceae (Dioscoreales) based on nuclear and mitochondrial data. Am. J. Bot. 93 (11), 1684-1698.
Rai, H.S., O'Brien, H.E., Reeves, P.A., et al., 2003. Inference of higher-order relationships in the cycads from a large chloroplast data set. Mol. Phylogenet. Evol. 29, 350-359.
Ruhlman, T., Jansen, R.K., 2014. The plastid genomes of flowering plants. In:Maliga, P. (Ed.), Chloroplast Biotechnology. Humana Press, New York, pp. 33-38.
Schattner, P., Brooks, A.N., Lowe, T.M., 2005. The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res. 33, 686-689.
Schelkunov, M.I., Shtratnikova, V.Y., Nuraliev, M.S., et al., 2015. Exploring the limits for reduction of plastid genomes:a case study of the mycoheterotrophic orchids Epipogium aphyllum and Epipogium roseum. Genome Biol. Evol. 7 (4), 1179-1191.
Soltis, D.E., Soltis, P.S., Chase, M.W., et al., 2000. Angiosperm phylogeny inferred from 18S rDNA, rbcL, and atpB sequences. Bot. J. Linn. Soc. 133, 381-461.
Stamatakis, A., 2006. RAxML-VI-HPC:maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688-2690.
Tamura, K., Dudley, J., Nei, M., et al., 2007. MEGA4:molecular evolutionary genetics analysis (mega) software version 4.0. Mol. Biol. Evol. 24, 1596-1599.
Wang, R.J., Cheng, C.L., Chang, C.C., et al., 2008. Dynamics and evolution of the inverted repeat-large single copy junctions in the chloroplast genomes of monocots. BMC Evol. Biol. 8, 36.
Wolfe, K.H., Morden, C.W., Palmer, J.D., 1992. Function and evolution of a minimal plastid genome from a nonphotosynthetic parasitic plant. Proc. Natl. Acad. Sci. U. S. A. 89 (22), 10648-10652.
Wyman, S.K., Jansen, R.K., Boore, J.L., 2004. Automatic annotation of organellar genomes with DOGMA. Bioinformatics 20, 3252-3255.
Zhang, D.X., 2001. Phylogenetic reconstruction of Burmannia L. (Burmanniaceae):a preliminary study. Acta Phytotaxon. Sin. 39 (3), 203-223.
Zhang, D., Saunders, R.M.K., 2000. Systematics of the Burmannia coelestis complex(Burmanniaceae). Nord. J. Bot. 20, 385-394.

[1]	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.
[2]	Rivontsoa A. Rakotonasolo, Soejatmi Dransfield, Thomas Haevermans, Helene Ralimanana, Maria S. Vorontsova, Meng-Yuan Zhou, De-Zhu Li. New insights into intergeneric relationships of Hickeliinae (Poaceae: Bambusoideae) revealed by complete plastid genomes [J]. Plant Diversity, 2023, 45(02): 125-132.
[3]	Shi-Yu Lv, Xia-Ying Ye, Zhong-Hu Li, Peng-Fei Ma, De-Zhu Li. Testing complete plastomes and nuclear ribosomal DNA sequences for species identification in a taxonomically difficult bamboo genus Fargesia [J]. Plant Diversity, 2023, 45(02): 147-155.
[4]	Yan-Ling Xu, Hao-Hua Shen, Xin-Yu Du, Lu Lu. Plastome characteristics and species identification of Chinese medicinal wintergreens (Gaultheria, Ericaceae) [J]. Plant Diversity, 2022, 44(06): 519-529.
[5]	Yao-Ke Li, Julian Harber, Chuan Peng, Zhi-Qiang Du, Yao-Wu Xing, Chih-Chieh Yu. Taxonomic synopsis of Berberis (Berberidaceae) from the northern Hengduan mountains region in China, with descriptions of seven new species [J]. Plant Diversity, 2022, 44(05): 505-517.
[6]	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.
[7]	Shiou Yih Lee, Ke-Wang Xu, Cui-Ying Huang, Jung-Hyun Lee, Wen-Bo Liao, Yong-Hong Zhang, Qiang Fan. Molecular phylogenetic analyses based on the complete plastid genomes and nuclear sequences reveal Daphne (Thymelaeaceae) to be non-monophyletic as current circumscription [J]. Plant Diversity, 2022, 44(03): 279-289.
[8]	Mengqing Zhe, Le Zhang, Fang Liu, Yiwei Huang, Weishu Fan, Junbo Yang, Andan Zhu. Plastid RNA editing reduction accompanied with genetic variations in Cymbidium, a genus with diverse lifestyle modes [J]. Plant Diversity, 2022, 44(03): 316-321.
[9]	Jia-Xin Yang, Shuai Peng, Jun-Jie Wang, Shi-Xiong Ding, Yan Wang, Jing Tian, Han Yang, Guang-Wan Hu, Qing-Feng Wang. Morphological and genomic evidence for a new species of Corallorhiza (Orchidaceae: Epidendroideae) from SW China [J]. Plant Diversity, 2021, 43(05): 409-419.
[10]	Xiaoping Li, Yamei Zhao, Xiongde Tu, Chengru Li, Yating Zhu, Hui Zhong, Zhong-Jian Liu, Shasha Wu, Junwen Zhai. Comparative analysis of plastomes in Oxalidaceae: Phylogenetic relationships and potential molecular markers [J]. Plant Diversity, 2021, 43(04): 281-291.
[11]	Bibo Yang, Liangda Li, Jianquan Liu, Lushui Zhang. Plastome and phylogenetic relationship of the woody buckwheat Fagopyrum tibeticum in the Qinghai-Tibet Plateau [J]. Plant Diversity, 2021, 43(03): 198-205.
[12]	Luxian Liu, Yonghua Zhang, Pan Li. Development of genomic resources for the genus Celtis (Cannabaceae) based on genome skimming data [J]. Plant Diversity, 2021, 43(01): 43-53.
[13]	Han-Rui Bai, Oyetola Oyebanji, Rong Zhang, Ting-Shuang Yi. Plastid phylogenomic insights into the evolution of subfamily Dialioideae (Leguminosae) [J]. Plant Diversity, 2021, 43(01): 27-34.
[14]	Hong Wu, Peng-Fei Ma, Hong-Tao Li, Guo-Xiong Hu, De-Zhu Li. Comparative plastomic analysis and insights into the phylogeny of Salvia (Lamiaceae) [J]. Plant Diversity, 2021, 43(01): 15-26.
[15]	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.