Abstract
In this study, a novel endophytic fungus, Diaporthe orixae, and a new host record of Diaporthe caryae were obtained from a medicinal plant, Orixa japonica in southern China. Phylogenetic analyses based on a combination of ITS, tef1-α, β-tub, cal, and his3 datasets confirmed that D. orixae is a distinct species, which is sister to D. sackstonii (BRIP 54669b). Diaporthe orixae sp. nov. differs from D. sackstonii in having larger conidiomata and smaller conidiogenous cells and alpha conidia on morphological examination. The new species and new host record are reported with taxonomic descriptions and illustrations.
References
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Chernomor, O., Von Haeseler, A. & Minh, B.Q. (2016) Terrace aware data structure for phylogenomic inference from supermatrices. Systematic biology 65: 997–1008.
Dissanayake, A.J., Phillips, A., Hyde, K.D., Yan, J. & Li, X. (2017) The current status of species in Diaporthe. Mycosphere 8 (5): 1106–1156. https://doi.org/10.5943/mycosphere/8/5/5
Dissanayake, A.J., Chen, Y.Y. & Liu, J.K. (2020a) Unravelling Diaporthe species associated with woody hosts from Karst Formations (Guizhou) in China. Journal of Fungi 6 (4): 251. https://doi.org/10.3390/jof6040251
Dissanayake, A.J., Bhunjun, C.S., Maharachchikumbura, S.S.N. & Liu, J.K. (2020b) Applied aspects of methods to infer phylogenetic relationships amongst fungi. Mycosphere 11: 2653–2677. https://doi.org/10.5943/mycosphere/11/1/18
Funayama, S., Tanaka, R., Kumekawa, Y., Noshita, T., Mori, T., Kashiwagura, T. & Murata, K. (2001) Rat small intestine muscle relaxation alkaloids from Orixa japonica leaves. Biological and Pharmaceutical Bulletin 24: 100–102. https://doi.org/10.1248/bpb.24.100
Guarnaccia, V. & Crous, P.W. (2017) Emerging citrus diseases in Europe caused by species of Diaporthe. IMA fungus 8 (2): 317–334. https://doi.org/10.5598/imafungus.2017.08.02.07
Gao, Y., Liu, F., Duan, W., Crous, P.W. & Cai, L. (2017) Diaporthe is paraphyletic. IMA fungus 8 (1): 153–187. https://doi.org/10.5598/imafungus.2017.08.01.11
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Guo, Y.S., Crous, P.W., Bai, Q., Fu, M., Yang, M.M., Wang, X.H., Du, Y.M., Hong, N., Xu, W.X. & Wang, G.P. (2020) High diversity of Diaporthe species associated with pear shoot canker in China. Persoonia-Molecular Phylogeny and Evolution of Fungi 45: 132–162. https://doi.org/10.3767/persoonia.2020.45.05
Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95–98.
Hoang, D.T., Chernomor, O., Von Haeseler, A., Minh, B.Q. & Vinh, L.S. (2018) UFBoot2: improving the ultrafast bootstrap approximation. Molecular Biology and Evolution 35: 518–522. https://doi.org/10.1093/molbev/msx281
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Hyde, K.D., Jeewon, R., Chen, Y.J., Bhunjun, C.S., Calabon, M.S., Jiang, H.B., Lin, C.G., Norphanphoun, C., Sysouphanthong, P., Pem, D., Tibpromma, S., Zhang, Q., Doilom, M., Jayawardena, R.S., Liu, J.K., Maharachchikumbura, S.S.N., Phukhamsakda, C., Phookamsak, R., Al-Sadi, A.M., Thongklang, N., Wang, Y., Gafforov, Y., Jones, E.B.G. & Lumyong, S. (2020) The numbers of fungi: is the descriptive curve flattening? Fungal Diversity 103: 219–271. https://doi.org/10.1007/s13225-020-00458-2
Jeewon, R. & Hyde, K.D. (2016) Establishing species boundaries and new taxa among fungi: recommendations to resolve taxonomic ambiguities. Mycosphere 7 (11): 1669–1677. https://doi.org/10.5943/mycosphere/7/11/4
Katoh, K., Rozewicki, J. & Yamada, K.D. (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in bioinformatics 20: 1160–1166. https://doi.org/10.1093/bib/bbx108
Liu, X.C., Lai, D., Liu, Q.Z., Zhou, L., Liu, Q. & Liu, Z.L. (2016) Bioactivities of a new pyrrolidine alkaloid from the root barks of Orixa japonica. Molecules 21 (12): 1665. https://doi.org/10.3390/molecules21121665
Miller, M.A., Pfeiffer, W. & Schwartz, T. (2010) Creating the CIPRES Science Gateway for Inference of Large Phylogenetic Trees. In: SC10 Workshop on Gateway Computing Environments (GCE10). New Orleans, LA. pp. 1–8. https://doi.org/10.1109/GCE.2010.5676129
Mostert, L., Crous, P.W., Kang, J.C. & Phillips, A.J.L. (2001) Species of Phomopsis and a Libertella sp. occurring on grapevines with specific reference to South Africa: morphological, cultural, molecular and pathological characterization. Mycologia 93: 146–167. https://doi.org/10.1080/00275514.2001.12061286
Nisa, H., Kamili, A.N., Nawchoo, I.A., Shafi, S., Shameem, N. & Bandh, S.A. (2015) Fungal endophytes as prolific source of phytochemicals and other bioactive natural products: a review. Microbial Pathogenesis 82: 50–59. https://doi.org/10.1016/j.micpath.2015.04.001
Nguyen, L.T., Schmidt, H.A., Von Haeseler, A. & Minh, B.Q (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32: 268–274. https://doi.org/10.1093/molbev/msu300
Nylander, J.A.A. (2004) MrModeltest Version 2. Program Distributed by the Author. Evolutionary Biology Centre, Uppsala University, Uppsala.
O’Donnell, K. & Cigelnik, E. (1997) Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are noorthologous. Molecular Phylogenetics and Evolution 7: 103–116. https://doi.org/10.1006/mpev.1996.0376
Ono, H., Kuwahara, Y. & Nishida, R. (2004) Hydroxybenzoic acid derivatives in a nonhost rutaceous plant, Orixa japonica, deter both oviposition and larval feeding in a Rutaceae-feeding swallowtail butterfly, Papilio xuthus L. Journal of chemical ecology 30 (2): 287–301. https://doi.org/10.1023/B:JOEC.0000017978.73061.a0
Rambaut, A. & Drummond, A. (2008) FigTree: Tree figure drawing tool, version 1.2. 2. Institute of Evolutionary Biology, University of Edinburgh.
Rashmi, M., Kushveer, J.S., Sarma, V.V. (2019) A worldwide list of endophytic fungi with notes on ecology and diversity. Mycosphere 10 (1): 798–1079. https://doi.org/10.5943/mycosphere/10/1/19
Rehner, S.A & Uecker, F.A. (1994) Nuclear ribosomal internal transcribed spacer phylogeny and host diversity in the coelomycete Phomopsis. Canadian Journal of Botany 72: 1666–1674. https://doi.org/10.1139/b94-204
Santos, J.M., Correia, V.G. & Phillips, A.J.L. (2010) Primers for mating-type diagnosis in Diaporthe and Phomopsis: their use in teleomorph induction in vitro and biological species definition. Fungal Biology 114: 255–270. https://doi.org/10.1016/j.funbio.2010.01.007
Santos, J.M., Vrande?i?, K., ?osi?, J., Duvnjak, T. & Phillips, A.J.L. (2011) Resolving the Diaporthe species occurring on soybean in Croatia. Persoonia: Molecular Phylogeny and Evolution of Fungi 27: 9–19. https://doi.org/10.3767/003158511X603719
Saravanakumar, K., Sriram, B., Sathiyaseelan, A., Hu, X., Mariadoss, A.V.A., MubarakAli, D. & Wang, M.H. (2021) Molecular identification, volatile metabolites profiling, and bioactivities of an indigenous endophytic fungus (Diaporthe sp.). Process Biochemistry 102: 72–81. https://doi.org/10.1016/j.procbio.2020.12.002
Stamatakis, A. (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Su, H., Kang, J.C., Cao, J.J., Mo, L. & Hyde, K.D. (2014) Medicinal plant endophytes produce analogous bioactive compounds. Chiang Mai Journal of Science 41 (1): 1–13.
Thompson, S.M., Tan, Y.P., Shivas, R.G., Neate, S.M., Morin, L., Bissett, A. & Aitken, E.A.B. (2015) Green and brown bridges between weeds and crops reveal novel Diaporthe species in Australia. Persoonia: Molecular Phylogeny and Evolution of Fungi 35: 39–49. https://doi.org/10.3767/003158515X687506
Thompson, S.M., Tan, Y.P., Young, A.J., Neate, S.M., Aitken, E.A. & Shivas, R.G. (2011) Stem cankers on sunflower (Helianthus annuus) in Australia reveal a complex of pathogenic Diaporthe (Phomopsis) species. Persoonia 27: 80–89. https://doi.org/10.3767/003158511X617110
Udayanga, D., Castlebury, L.A., Rossman, A.Y. & Hyde, K.D. (2014) Species limits in Diaporthe: molecular re-assessment of D. citri, D. cytosporella, D. foeniculina and D. rudis. Persoonia: Molecular Phylogeny and Evolution of Fungi 32: 83–101. https://doi.org/10.3767/003158514X679984
Udayanga, D., Liu, X., Crous, P.W., McKenzie, E.H., Chukeatirote, E. & Hyde, K.D. (2012) A multi-locus phylogenetic evaluation of Diaporthe (Phomopsis). Fungal diversity 56 (1): 157–171. https://doi.org/10.1007/s13225-012-0190-9
Udayanga, D., Xingzhong, L., McKenzie, E.H.C., Chukeatirote, E., Bahkali, A.H.A. & Hyde, K.D. (2011) The genus Phomopsis: biology, applications, species concepts and names of common pathogens. Fungal Diversity 50: 189–225. https://doi.org/10.1007/s13225-011-0126-9
Uecker, F.A. (1988) A world list of Phomopsis names with notes on nomenclature, morphology and biology. Mycologia Memoir 13: 1–231.
Vaidya, G., Lohman, D.J. & Meier, R. (2011) SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics 27 (2): 171–180. https://doi.org/10.1111/j.1096-0031.2010.00329.x
Wang, X., Guo, Y., Du, Y., Yang, Z., Huang, X., Hong, N., Xu, W. & Wang, G. (2021) Characterization of Diaporthe species associated with peach constriction canker, with two novel species from China. MycoKeys 80: 77–90. https://doi.org/10.3897/mycokeys.80.63816
Wehmeyer, L.E. (1933) The genus Diaporthe Nitschke and its segregates. University of Michigan Studies, Science Series 9: 1–349.
Yang, Q., Fan, X.L., Guarnaccia, V. & Tian, C.M. (2018) High diversity of Diaporthe species associated with dieback diseases in China, with twelve new species described. MycoKeys 39: 97–149. https://doi.org/10.3897/mycokeys.39.26914
Yang, Q., Jiang, N. & Tian, C.M. (2020) Three new Diaporthe species from Shaanxi province, China. MycoKeys 67: 1–18. https://doi.org/10.3897/mycokeys.67.49483
Yang, Q., Jiang, N. & Tian, C.M. (2021) New species and records of Diaporthe from Jiangxi Province, China. MycoKeys 77: 41–64. https://doi.org/10.3897/mycokeys.77.59999
Ying, Z., Yan, M., Zhou, M., He, X. & Cheng, R. (2021) Characterization of the complete chloroplast genome of the medicinal plant Orixa japonica (Rutaceae) in Zhejiang Province and its phylogenetic analysis within family Rutaceae. Mitochondrial DNA Part B 6: 1734–1736. https://doi.org/10.1080/23802359.2021.1931511
Chernomor, O., Von Haeseler, A. & Minh, B.Q. (2016) Terrace aware data structure for phylogenomic inference from supermatrices. Systematic biology 65: 997–1008.
Dissanayake, A.J., Phillips, A., Hyde, K.D., Yan, J. & Li, X. (2017) The current status of species in Diaporthe. Mycosphere 8 (5): 1106–1156. https://doi.org/10.5943/mycosphere/8/5/5
Dissanayake, A.J., Chen, Y.Y. & Liu, J.K. (2020a) Unravelling Diaporthe species associated with woody hosts from Karst Formations (Guizhou) in China. Journal of Fungi 6 (4): 251. https://doi.org/10.3390/jof6040251
Dissanayake, A.J., Bhunjun, C.S., Maharachchikumbura, S.S.N. & Liu, J.K. (2020b) Applied aspects of methods to infer phylogenetic relationships amongst fungi. Mycosphere 11: 2653–2677. https://doi.org/10.5943/mycosphere/11/1/18
Funayama, S., Tanaka, R., Kumekawa, Y., Noshita, T., Mori, T., Kashiwagura, T. & Murata, K. (2001) Rat small intestine muscle relaxation alkaloids from Orixa japonica leaves. Biological and Pharmaceutical Bulletin 24: 100–102. https://doi.org/10.1248/bpb.24.100
Guarnaccia, V. & Crous, P.W. (2017) Emerging citrus diseases in Europe caused by species of Diaporthe. IMA fungus 8 (2): 317–334. https://doi.org/10.5598/imafungus.2017.08.02.07
Gao, Y., Liu, F., Duan, W., Crous, P.W. & Cai, L. (2017) Diaporthe is paraphyletic. IMA fungus 8 (1): 153–187. https://doi.org/10.5598/imafungus.2017.08.01.11
Glass, N.L. & Donaldson, G. (1995) Development of primer sets designed for use with PCR to amplify conserved genes from filamentous ascomycetes. Applied and Environmental Microbiology 61: 1323–1330. https://doi.org/10.1128/aem.61.4.1323-1330.1995
Gomes, R., Glienke, C., Videira, S., Lombard, L., Groenewald, J. & Crous, P. (2013) Diaporthe: a genus of endophytic, saprobic and plant pathogenic fungi. Persoonia 31: 1–41. https://doi.org/10.3767/003158513X666844
Guo, Y.S., Crous, P.W., Bai, Q., Fu, M., Yang, M.M., Wang, X.H., Du, Y.M., Hong, N., Xu, W.X. & Wang, G.P. (2020) High diversity of Diaporthe species associated with pear shoot canker in China. Persoonia-Molecular Phylogeny and Evolution of Fungi 45: 132–162. https://doi.org/10.3767/persoonia.2020.45.05
Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95–98.
Hoang, D.T., Chernomor, O., Von Haeseler, A., Minh, B.Q. & Vinh, L.S. (2018) UFBoot2: improving the ultrafast bootstrap approximation. Molecular Biology and Evolution 35: 518–522. https://doi.org/10.1093/molbev/msx281
Hyde, K.D. & Soytong, K. (2008) The fungal endophyte dilemma. Fungal Diversity 33 (33): 163–173.
Hyde, K.D., Jeewon, R., Chen, Y.J., Bhunjun, C.S., Calabon, M.S., Jiang, H.B., Lin, C.G., Norphanphoun, C., Sysouphanthong, P., Pem, D., Tibpromma, S., Zhang, Q., Doilom, M., Jayawardena, R.S., Liu, J.K., Maharachchikumbura, S.S.N., Phukhamsakda, C., Phookamsak, R., Al-Sadi, A.M., Thongklang, N., Wang, Y., Gafforov, Y., Jones, E.B.G. & Lumyong, S. (2020) The numbers of fungi: is the descriptive curve flattening? Fungal Diversity 103: 219–271. https://doi.org/10.1007/s13225-020-00458-2
Jeewon, R. & Hyde, K.D. (2016) Establishing species boundaries and new taxa among fungi: recommendations to resolve taxonomic ambiguities. Mycosphere 7 (11): 1669–1677. https://doi.org/10.5943/mycosphere/7/11/4
Katoh, K., Rozewicki, J. & Yamada, K.D. (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in bioinformatics 20: 1160–1166. https://doi.org/10.1093/bib/bbx108
Liu, X.C., Lai, D., Liu, Q.Z., Zhou, L., Liu, Q. & Liu, Z.L. (2016) Bioactivities of a new pyrrolidine alkaloid from the root barks of Orixa japonica. Molecules 21 (12): 1665. https://doi.org/10.3390/molecules21121665
Miller, M.A., Pfeiffer, W. & Schwartz, T. (2010) Creating the CIPRES Science Gateway for Inference of Large Phylogenetic Trees. In: SC10 Workshop on Gateway Computing Environments (GCE10). New Orleans, LA. pp. 1–8. https://doi.org/10.1109/GCE.2010.5676129
Mostert, L., Crous, P.W., Kang, J.C. & Phillips, A.J.L. (2001) Species of Phomopsis and a Libertella sp. occurring on grapevines with specific reference to South Africa: morphological, cultural, molecular and pathological characterization. Mycologia 93: 146–167. https://doi.org/10.1080/00275514.2001.12061286
Nisa, H., Kamili, A.N., Nawchoo, I.A., Shafi, S., Shameem, N. & Bandh, S.A. (2015) Fungal endophytes as prolific source of phytochemicals and other bioactive natural products: a review. Microbial Pathogenesis 82: 50–59. https://doi.org/10.1016/j.micpath.2015.04.001
Nguyen, L.T., Schmidt, H.A., Von Haeseler, A. & Minh, B.Q (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32: 268–274. https://doi.org/10.1093/molbev/msu300
Nylander, J.A.A. (2004) MrModeltest Version 2. Program Distributed by the Author. Evolutionary Biology Centre, Uppsala University, Uppsala.
O’Donnell, K. & Cigelnik, E. (1997) Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are noorthologous. Molecular Phylogenetics and Evolution 7: 103–116. https://doi.org/10.1006/mpev.1996.0376
Ono, H., Kuwahara, Y. & Nishida, R. (2004) Hydroxybenzoic acid derivatives in a nonhost rutaceous plant, Orixa japonica, deter both oviposition and larval feeding in a Rutaceae-feeding swallowtail butterfly, Papilio xuthus L. Journal of chemical ecology 30 (2): 287–301. https://doi.org/10.1023/B:JOEC.0000017978.73061.a0
Rambaut, A. & Drummond, A. (2008) FigTree: Tree figure drawing tool, version 1.2. 2. Institute of Evolutionary Biology, University of Edinburgh.
Rashmi, M., Kushveer, J.S., Sarma, V.V. (2019) A worldwide list of endophytic fungi with notes on ecology and diversity. Mycosphere 10 (1): 798–1079. https://doi.org/10.5943/mycosphere/10/1/19
Rehner, S.A & Uecker, F.A. (1994) Nuclear ribosomal internal transcribed spacer phylogeny and host diversity in the coelomycete Phomopsis. Canadian Journal of Botany 72: 1666–1674. https://doi.org/10.1139/b94-204
Santos, J.M., Correia, V.G. & Phillips, A.J.L. (2010) Primers for mating-type diagnosis in Diaporthe and Phomopsis: their use in teleomorph induction in vitro and biological species definition. Fungal Biology 114: 255–270. https://doi.org/10.1016/j.funbio.2010.01.007
Santos, J.M., Vrande?i?, K., ?osi?, J., Duvnjak, T. & Phillips, A.J.L. (2011) Resolving the Diaporthe species occurring on soybean in Croatia. Persoonia: Molecular Phylogeny and Evolution of Fungi 27: 9–19. https://doi.org/10.3767/003158511X603719
Saravanakumar, K., Sriram, B., Sathiyaseelan, A., Hu, X., Mariadoss, A.V.A., MubarakAli, D. & Wang, M.H. (2021) Molecular identification, volatile metabolites profiling, and bioactivities of an indigenous endophytic fungus (Diaporthe sp.). Process Biochemistry 102: 72–81. https://doi.org/10.1016/j.procbio.2020.12.002
Stamatakis, A. (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Su, H., Kang, J.C., Cao, J.J., Mo, L. & Hyde, K.D. (2014) Medicinal plant endophytes produce analogous bioactive compounds. Chiang Mai Journal of Science 41 (1): 1–13.
Thompson, S.M., Tan, Y.P., Shivas, R.G., Neate, S.M., Morin, L., Bissett, A. & Aitken, E.A.B. (2015) Green and brown bridges between weeds and crops reveal novel Diaporthe species in Australia. Persoonia: Molecular Phylogeny and Evolution of Fungi 35: 39–49. https://doi.org/10.3767/003158515X687506
Thompson, S.M., Tan, Y.P., Young, A.J., Neate, S.M., Aitken, E.A. & Shivas, R.G. (2011) Stem cankers on sunflower (Helianthus annuus) in Australia reveal a complex of pathogenic Diaporthe (Phomopsis) species. Persoonia 27: 80–89. https://doi.org/10.3767/003158511X617110
Udayanga, D., Castlebury, L.A., Rossman, A.Y. & Hyde, K.D. (2014) Species limits in Diaporthe: molecular re-assessment of D. citri, D. cytosporella, D. foeniculina and D. rudis. Persoonia: Molecular Phylogeny and Evolution of Fungi 32: 83–101. https://doi.org/10.3767/003158514X679984
Udayanga, D., Liu, X., Crous, P.W., McKenzie, E.H., Chukeatirote, E. & Hyde, K.D. (2012) A multi-locus phylogenetic evaluation of Diaporthe (Phomopsis). Fungal diversity 56 (1): 157–171. https://doi.org/10.1007/s13225-012-0190-9
Udayanga, D., Xingzhong, L., McKenzie, E.H.C., Chukeatirote, E., Bahkali, A.H.A. & Hyde, K.D. (2011) The genus Phomopsis: biology, applications, species concepts and names of common pathogens. Fungal Diversity 50: 189–225. https://doi.org/10.1007/s13225-011-0126-9
Uecker, F.A. (1988) A world list of Phomopsis names with notes on nomenclature, morphology and biology. Mycologia Memoir 13: 1–231.
Vaidya, G., Lohman, D.J. & Meier, R. (2011) SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics 27 (2): 171–180. https://doi.org/10.1111/j.1096-0031.2010.00329.x
Wang, X., Guo, Y., Du, Y., Yang, Z., Huang, X., Hong, N., Xu, W. & Wang, G. (2021) Characterization of Diaporthe species associated with peach constriction canker, with two novel species from China. MycoKeys 80: 77–90. https://doi.org/10.3897/mycokeys.80.63816
Wehmeyer, L.E. (1933) The genus Diaporthe Nitschke and its segregates. University of Michigan Studies, Science Series 9: 1–349.
Yang, Q., Fan, X.L., Guarnaccia, V. & Tian, C.M. (2018) High diversity of Diaporthe species associated with dieback diseases in China, with twelve new species described. MycoKeys 39: 97–149. https://doi.org/10.3897/mycokeys.39.26914
Yang, Q., Jiang, N. & Tian, C.M. (2020) Three new Diaporthe species from Shaanxi province, China. MycoKeys 67: 1–18. https://doi.org/10.3897/mycokeys.67.49483
Yang, Q., Jiang, N. & Tian, C.M. (2021) New species and records of Diaporthe from Jiangxi Province, China. MycoKeys 77: 41–64. https://doi.org/10.3897/mycokeys.77.59999
Ying, Z., Yan, M., Zhou, M., He, X. & Cheng, R. (2021) Characterization of the complete chloroplast genome of the medicinal plant Orixa japonica (Rutaceae) in Zhejiang Province and its phylogenetic analysis within family Rutaceae. Mitochondrial DNA Part B 6: 1734–1736. https://doi.org/10.1080/23802359.2021.1931511