Calycosiphonia or Kupeantha (Coffeeae, Rubiaceae)? A morphological and molecular study of a new species from the Albertine Rift
Abstract
Field work in the Kibira National Park (Burundi), located in the Kivu-Ruwenzori system of the Afromontane Region, revealed the existence of a new species clearly belonging to the Argocoffeopsis-Calycosiphonia clade (Coffeeae, Rubiaceae). The species shows striking heterophylly: the plagiotropous branches have several nodes bearing reduced or even scaly leaves. For the rest, it shares characters with Calycosiphonia and Kupeantha. Therefore, a morphological comparison with the clade is done, as well as molecular phylogenetic analyses. The morphology of the novelty is closer to Kupeantha than to Calycosiphonia, inter alia because the anthers have no transverse septa, in contrast to the multilocellate anthers of Calycosiphonia. However, the molecular data advocate for a position in Calycosiphonia – a result weakening the morphological distinction between Calycosiphonia and Kupeantha. The former genus is no longer restricted to species with transverse septa in the anthers and with placental outgrowths around the seed. The new species is formally described as Calycosiphonia albertina Ntore & Robbr. sp. nov. Nomenclaturally, this placement is also the most conservative option. A taxonomic treatment, illustrations, a geographical distribution map, and a preliminary conservation assessment are provided. The previous inclusion of Calycosiphonia pentamera in Kupeantha based on morphology is here corroborated by molecular analyses.
References
Ali S.J. & Robbrecht E. 1991. Remarks on the tropical Asian and Australian taxa included in Diplospora or Tricalysia (Rubiaceae-Ixoroideae-Gardenieae). Blumea 35: 279–305.
Alvarez-Aguirre M.G., Cheek M. & Sonké B. 2021. Kupeantha yabassi (Coffeeae-Rubiaceae), a new Critically Endangered shrub species of the Ebo Forest area, Littoral Region, Cameroon. Kew Bulletin 76: 735–743. https://doi.org/10.1007/s12225-021-09982-z
Andreasen K. & Bremer B. 1996. Phylogeny of the subfamily Ixoroideae (Rubiaceae). Opera Botanica Belgica 7: 119–138.
Andreasen K. & Bremer B. 2000. Combined phylogenetic analysis in the Rubiaceae-Ixoroideae: morphology, nuclear and chloroplast DNA data. American Journal of Botany 87 (11): 1731–1748. https://doi.org/10.2307/2656750
Andrews S. 2010. FastQC. A quality control tool for high throughput sequence data. Available from https://www.bioinformatics.babraham.ac.uk/projects/fastqc/ [accessed 7 Sep. 2023].
Arriola A.H., Davis A.P., Davies N.M., Meve U., Liede-Schumann S. & Alejandro G.J.D. 2018. Using multiple plastid DNA regions to construct the first phylogenetic tree for Asian genera of Coffeeae (Ixoroideae, Rubiaceae). Botanical Journal of the Linnean Society 188: 132–143. https://doi.org/10.1093/botlinnean/boy059
Aveling C. 2010. World Heritage in the Congo Basin. UNESCO World Heritage Centre, Paris.
Bachman S., Moat J., Hill A.W., de la Torre J. & Scott B. 2011 Supporting Red List threat assessments with GeoCAT: geospatial conservation assessment tool. ZooKeys 150: 117–126. https://doi.org/10.3897/zookeys.150.2109
Bridson D.M. & Verdcourt B. 2003. Rubiaceae. In: Pope G.V. (ed.) Flora Zambesiaca. Volume 5, part 3. Royal Botanic Gardens, Kew, Richmond.
Cheek M., Alvarez-Aguirre M.G., Grall A., Sonké B., Howes M.-J.R. & Larridon I. 2018. Kupeantha (Coffeeae, Rubiaceae), a new genus from Cameroon and Equatorial Guinea. PLoS ONE 13: e0199324. https://doi.org/10.1371/journal.pone.0199324
Cheek M. & Dawson S. 2000. A synoptic revision of Belonophora (Rubiaceae). Kew Bulletin 55: 63–80. https://doi.org/10.2307/4117761
Cheek M. & Tchiengué B. 2010. Argocoffeopsis fosimondi (Rubiaceae) a new cloud forest shrub species from Fosimondi, Cameroon. In: Harvey Y., Tchiengué B. & Cheek M. (eds) The Plants of the Lebialem Highlands, Cameroon: a Conservation Checklist. Royal Botanic Gardens, Kew, Richmond.
Darriba D., Taboada G., Doallo R. & Posada D. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772. https://doi.org/10.1038/nmeth.2109
Davis A.P. 2010. Six species of Psilanthus transferred to Coffea (Coffeeae, Rubiaceae). Phytotaxa 10: 41–45. https://doi.org/10.11646/phytotaxa.10.1.6
Davis A.P. & Sonké B. 2008. A new Argocoffeopsis (Coffeeae, Rubiaceae) from southern Cameroon: Argocoffeopsis spathulata. Blumea 53: 527–532. https://doi.org/10.3767/000651908X607486
Davis A.P., Bridson D. & Rakotonasolo F. 2005. A reexamination of Coffea subgenus Baracoffea and comments on the morphology and classification of Coffea and Psilanthus (Rubiaceae-Coffeea). In: Keating R.C., Hollowell V.C. & Croat T.B. (eds) A Festschrift for William G. D’arcy: the Legacy of a Taxonomist: 399–420. Missouri Botanical Garden Press, St. Louis, Missouri.
Davis A.P., Chester M., Maurin O. & Fay M.F. 2007. Searching for relatives of Coffea (Rubiaceae, Ixoroideae): circumscription and phylogeny of Coffeeae based on plastid sequence data and morphology. American Journal of Botany 94: 313–329. https://doi.org/10.3732/ajb.94.3.313
Denoeud F., Carretero-Paulet L., Dereeper A., Droc G., Guyot R., Pietrella M., Zheng C., Alberti A., Anthony F., Aprea G., Aury J.-M., Bento P., Bernard M., Bocs S., Campa C., Cenci A., Combes M.-C., Crouzillat D., Da Silva C., Daddiego L., De Bellis F., Dussert S., Garsmeur O., Gayraud T., Guignon V., Jahn K., Jamilloux V., Joët T., Labadie K., Lan T., Leclercq J., Lepelley M., Leroy T., Li L.-T., Librado P., Lopez L., Muñoz A., Noel B., Pallavicini A., Perrotta G., Poncet V., Pot D., Priyono, Rigoreau M., Rouard M., Rozas J., Tranchant-Dubreuil C., VanBuren R., Zhang Q., Andrade A.C., Argout X., Bertrand B., de Kochko A., Graziosi G., Henry R.J., Jayarama, Ming R., Nagai C., Rounsley S., Sankoff D., Giuliano G., Albert V.A., Wincker P. & Lashermes P. 2014. The coffee genome provides insight into the convergent evolution of caffeine biosynthesis. Science 345: 1181–1184. https://doi.org/10.1126/science.1255274
Doyle J.J. & Doyle J.L. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemistry Bulletin 19: 11–15.
Fischer E., Killmann D. & Dhetchuvi J.-B.M.M. 2023. The family Zingiberaceae in Rwanda with description of two new species of Renealmia. Plant Ecology and Evolution 156 (2): 225–238. https://doi.org/10.5091/plecevo.99146
GBIF.org. 2023a. GBIF occurrence download of Argocoffeopsis. Available from https://doi.org/10.15468/dl.bceknq [accessed 24 May 2023].
GBIF.org. 2023b. GBIF occurrence download of Calycosiphonia. Available from https://doi.org/10.15468/dl.qsp43h [accessed 24 May 2023].
GBIF.org. 2023c. GBIF occurrence download of Kupeantha. Available from https://doi.org/10.15468/dl.ya4bgh [accessed 24 May 2023].
GBIF.org. 2023d. Impatiens mannii in GBIF Backbone Taxonomy. Available from https://www.gbif.org/species/4936432 [accessed 22 May 2023].
Hallé F., Oldeman R.A.A. & Tomlinson P.B. 1978. Tropical Trees and Forests: an Architectural Analysis. Springer, Berlin. https://doi.org/10.1007/978-3-642-81190-6
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 (2): 518–522. https://doi.org/10.1093/molbev/msx281
IUCN Standards and Petitions Subcommittee. 2022. Guidelines for using the IUCN Red List categories and criteria. Version 15.1. Prepared by the Standards and Petitions Subcommittee.
Kainulainen K., Razafimandimbison S.G., Wikström N. & Bremer B. 2017. Island hopping, long-distance dispersal and species radiation in the Western Indian Ocean: historical biogeography of the Coffeeae alliance (Rubiaceae). Journal of Biogeography 44: 1966–1979. https://doi.org/10.1111/jbi.12981
Katoh K. & Standley D.M. 2013. MAFFT Multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30 (4): 772–780. https://doi.org/10.1093/molbev/mst010
Kilian A., Wenzl P., Huttner E., Carling J., Xia L., Blois H., Caig V., Heller-Uszynska K., Jaccoud D., Hopper C., Aschenbrenner-Kilian M., Evers M., Peng K., Cayla C., Hok P. & Uszynski G. 2012. Diversity arrays technology: a generic genome profiling technology on open platforms. In: Pompanon F. & Bonin A. (eds) Data Production and Analysis in Population Genomics. Methods in Molecular Biology 888: 67–89. Humana Press, Totowa. https://doi.org/10.1007/978-1-61779-870-2_5
Lebrun J. 1941. Recherches morphologiques et systématiques sur les caféiers du Congo. Institut Royal Colonial Belge, Section des Sciences Naturelles et Médicales, Mémoires 11 (3): 1–184.
Li H. & Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25 (14): 1754–1760. https://doi.org/10.1093/bioinformatics/btp324
Martin M. 2011. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal 17 (1): 10–12. https://doi.org/10.14806/ej.17.1.200
McKenna A., Hanna M., Banks E., Sivachenko A., Cibulskis K., Kernytsky A., Garimella K., Altshuler D., Gabriel S., Daly M. & DePristo M.A. 2010. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Research 20: 1297–1303. https://doi.org/10.1101/gr.107524.110
Minh B.Q., Schmidt H.A., Chernomor O., Schrempf D., Woodhams M.D., von Haeseler A. & Lanfear R. 2020. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution 37 (5): 1530–1534 https://doi.org/10.1093/molbev/msaa015
Moens P. 1962. La place systématique du Coffea lebruniana Germain et Kesler. Bulletin du Jardin botanique de l’État à Bruxelles 32: 129–131. https://doi.org/10.2307/3667319
Ntore S., Fischer E. & Sosef S.M. 2018. Red List of the endemic and range-restricted vascular plants of Burundi. Scripta Botanica Belgica 58: 1–215.
Persson C. 2000. Phylogeny of the Neotropical Alibertia group (Rubiaceae), with emphasis on the genus Alibertia, inferred from ITS and 5S ribosomal DNA sequences. American Journal of Botany 87 (7): 1018–1028. https://doi.org/10.2307/2657002
POWO 2023. Plants of the World Online. Facilitated by the Royal Botanic Gardens, Kew. Available from http://www.plantsoftheworldonline.org [accessed 7 Sep. 2023].
Rambaut A. 2018. FigTree ver. 1.4.4. Available from https://github.com/rambaut/figtree [accessed 7 Sep. 2023].
Rambaut A., Drummond A.J., Xie D., Baele G. & Suchard M.A. 2018. Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67 (5): 901–904. https://doi.org/10.1093/sysbio/syy032
Ranarivelo-Randriamboavonjy T., Robbrecht E., Rabakonandrianina E. & De Block P. 2007. Revision of the Malagasy species of the genus Tricalysia (Rubiaceae). Botanical Journal of the Linnean Society 155: 83–126. https://doi.org/10.1111/j.1095-8339.2007.00688.x
Robbrecht E. 1978. Sericanthe, a new African genus of Rubiaceae (Coffeeae). Bulletin du Jardin botanique national de Belgique / Bulletin van de Nationale Plantentuin van België 48: 3–78. https://doi.org/10.2307/3667918
Robbrecht E. 1979. The African genus Tricalysia A. Rich. (Rubiaceae-Coffeeae). 1. A revision of the species of subgenus Empogona. Bulletin du Jardin botanique national de Belgique / Bulletin van de Nationale Plantentuin van België 49: 239–360. https://doi.org/10.2307/3668089
Robbrecht E. 1980. Bijdragen tot de Classificatie van de Ixoroideae en tot de revisie van Tricalysia s.l. (Rubiaceae), Part 3. PhD thesis, Ghent University, Belgium.
Robbrecht E. 1981a. Studies in tropical African Rubiaceae (I). Bulletin du Jardin botanique national de Belgique / Bulletin van de Nationale Plantentuin van België 51: 165–189. https://doi.org/10.2307/3667740
Robbrecht E. 1981b. Studies in tropical African Rubiaceae (II). Bulletin du Jardin botanique national de Belgique / Bulletin van de Nationale Plantentuin van België 51: 359–378. https://doi.org/10.2307/3668069
Robbrecht E. 1982. Rubiaceae. Distributiones Plantarum Africanarum 22: maps 757–758.
Robbrecht E. 1983. The African genus Tricalysia A. Rich. (Rubiaceae). 3. Probletostemon revived as a section of subgenus Tricalysia. Bulletin du Jardin botanique national de Belgique / Bulletin van de National Plantentuin van België 53: 299–320. https://doi.org/10.2307/3667793
Robbrecht E. 1986. Studies in tropical African Rubiaceae (7–12). Bulletin du Jardin botanique national de Belgique / Bulletin van de Nationale Plantentuin van België 56: 145–162. https://doi.org/10.2307/3667762
Robbrecht E. 1987. The African genus Tricalysia A. Rich. (Rubiaceae). 4. A revision of the species of sectio Tricalysia and sectio Rosea. Bulletin du Jardin botanique national de Belgique / Bulletin van de Nationale Plantentuin van België 57: 39–208. https://doi.org/10.2307/3668317
Robbrecht E. 1988. Tropical woody Rubiaceae. Characteristic features and progressions. Contributions to a new subfamilial classification. Opera Botanica Belgica 1: 1–270.
Robbrecht E. 1996. Geography of African Rubiaceae with reference to glacial rain forest refuges. In: van der Maesen L.J.G., van der Burgt X.M. & van Medenbach de Rooy J.M. (eds) The Biodiversity of African Plants: 564–581. Springer Netherlands, Dordrecht. https://doi.org/10.1007/978-94-009-0285-5_71
Robbrecht E. & Manen J.-F. 2006. The major evolutionary lineages of the coffee family (Rubiaceae, angiosperms). Combined analysis (nDNA and cpDNA) to infer the position of Coptosapelta and Luculia, and supertree construction based on rbcL, rps16, trnL-trnF and atpB-rbcL data. A new classification in two subfamilies, Cinchonoideae and Rubioideae. Systematics and Geography of Plants 76: 85–145.
Robbrecht E. & Puff C. 1986. A survey of the Gardenieae and related tribes. Botanische Jahrbücher für Systematik, Pflanzengeschichte und Pflanzengeographie 108: 63–137.
Robbrecht E., Puff C. & Igersheim A. 1991. The genera Mitchella and Damnacanthus. Evidence for their close alliance; comments on the campylotropy in the Rubiaceae and the circumscription of the Morindeae. Blumea 35: 307–345. Available from https://repository.naturalis.nl/pub/525774 [accessed 14 Apr. 2023].
Robbrecht E., De Block P., Dessein S. & Lachenaud O. 2020. Rubiaceae, Introduction. In: Sosef M.S.M. (ed.) Flore d’Afrique centrale, nouvelle série, Spermatophyta. Jardin botanique de Meise, Meise.
Ronquist F. & Huelsenbeck J.P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574. https://doi.org/10.1093/bioinformatics/btg180
Schaumont D. 2020. GBprocesS: genotyping-by-sequencing data processing toolkit. Available from https://gitlab.com/ilvo/GBprocesS [accessed 7 Sep. 2023].
Sonké B., Djuikouo M.-N. & Robbrecht E. 2007. Calycosiphonia pentamera sp. nov. (afrotropical Rubiaceae) from the ‘Lower Guinea’ area. Nordic Journal of Botany 25: 275–280. https://doi.org/10.1111/j.0107-055X.2007.00141.x
Stoffelen P., Robbrecht E. & Smets E. 1997. Pollen morphology of Coffea and Psilanthus (Rubiaceae‐Coffeeae), mainly from Africa. Grana 36: 313–327. https://doi.org/10.1080/00173139709362625
Taylor C.M., Razafimandimbison S.G., Barrabé L., Jardim J.G. & Barbosa M.R.V. 2017. Eumachia expanded, a pantropical genus distinct from Psychotria (Rubiaceae, Palicoureeae). Candollea 72: 289–318. https://doi.org/10.15553/c2017v722a6
Thiers B. 2023. Index herbariorum. A global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. Available from https://sweetgum.nybg.org/science/ih/ [accessed 7 Sep. 2023].
Tosh J., Davis A.P., Dessein S., De Block P., Huysmans S., Fay M.F., Smets E. & Robbrecht E. 2009. Phylogeny of Tricalysia (Rubiaceae) and its relationships with allied genera based on plastid DNA data: resurrection of the genus Empogona. Annals of the Missouri Botanical Garden 96: 194–213. https://doi.org/10.3417/2006202
UNESCO. 2021. State of Conservation: Kahuzi-Biega National Park (Democratic Republic of the Congo). Available from https://whc.unesco.org/en/soc/4029 [accessed 7 Sep. 2023].
Verdcourt B. 1977. A synopsis of the genus Chazaliella (Rubiaceae-Psychotrieae). Kew Bulletin 31: 785–818. https://doi.org/10.2307/4109551
von Teichman I. & van Wyk A.E. 1994. Structural aspects and trends in the evolution of recalcitrant seeds in dicotyledons. Seed Science Research 4 (2): 225–239. https://doi.org/10.1017/S096025850000221X
White F. 1978. The Afromontane Region. In: Werger M.J.A. (ed.) Biogeography and Ecology of Southern Africa. Monographiae Biologicae. Volume 31. Springer, Dordrecht. https://doi.org/10.1007/978-94-009-9951-0_11
Wickham H. 2016. ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag, New York. https://doi.org/10.1007/978-3-319-24277-4_9
Zhang C., Rabiee M., Sayyari E. & Mirarab S. 2018. ASTRAL-III: polynomial time species tree reconstruction from partially resolved gene trees. BMC Bioinformatics 19 (Suppl 6): 153. https://doi.org/10.1186/s12859-018-2129-y
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