Phylogenetic placement of enigmatic Astianthus (Bignoniaceae) based on molecular data, wood and bark anatomy

keywords: Catalpeae, Lamiales, Plant Anatomy, Secondary phloem, Secondary xylem, Tecomeae

Abstract

Background: Astianthus is a monospecific arborescent genus of Bignoniaceae that occur in the Pacific Coast of central Mexico and northern Central America, where it grows in dense populations along riversides. Its phylogenetic placement has remained controversial since Astianthus has unusual morphological characters such as a four-loculed ovary, and simple, pulvinate, verticillate leaves.

Methods: Here we used three plastid markers ndhF, rbcL, and trnL-F, wood, and bark anatomical data to investigate the phylogenetic placement of Astianthus and assign it to one of Bignoniaceae’s main clades.

Results: Our molecular phylogenetic analyses indicated that Astianthus belongs in tribe Tecomeae s.s., where other charismatic Neotropical Bignoniaceae genera such as Campsis and Tecoma are currently placed. Wood and bark anatomy support this placement, as Astianthus reunites a unique combination of features only known from members of Tecomeae s.s., such as storied axial parenchyma, the co-occurrence of homo- and heterocellular rays, septate fibers, and scattered phloem fibers in the bark.

Conclusions: The placement of Astianthus within Tecomeae s.s. provides further support to previous proposals for the Neotropical origin of this Pantropical tribe.

Downloads

Download data is not yet available.
Phylogenetic placement of enigmatic <em>Astianthus</em> (Bignoniaceae) based on molecular data, wood and bark anatomy

References

Angyalossy V, Angeles G, Pace MR, Lima AC, Dias-Leme CL, Lohmann LG, Madero-Vega C. 2012. An overview of the anatomy, development, and evolution of the vascular system of lianas. Plant Ecology and Diversity 5: 167-182. DOI: http://dx.doi.org/10.1080/17550874.2011.615574
Angyalossy V, Pace MR, Lima AC. 2015. Liana anatomy: A broad perspective on structural evolution of the vascular system. In: Schnitzer SA, Bongers F, Burnham R, Putz FE, eds. Ecology of Lianas. Oxford: Wiley-Blackwell Publishers. pp. 253-287. DOI: 10.1002/9781118392409.
Angyalossy V, Pace MR, Evert RF, Marcati CR, Oskolski AA, Terrazas T, Kotina E, Lens F, Mazzoni-Viveiros SC, Angeles G, Machado SR, Crivellaro A, Rao KS, Junikka L, Nikolaeva N, Baas P. IAWA List of Microscopic Bark Features. IAWA J. 37: 517-615. DOI: https://doi.org/10.1163/22941932-20160151
Barbosa ACF, Pace MR, Witovsk L, Angyalossy V. 2010. A new method to obtain good anatomical slides of heterogeneous plant parts. IAWA J. 31: 373-383. DOI: https://doi.org/10.1163/22941932-90000030
Barbosa ACF, Costa GRO, Angyalossy V, Dos Santos TC, Pace MR. 2018. A simple and inexpensive method for sharpening permanent steel knives with sandpaper. IAWA J. 39: 497-503. DOI: https://doi.org/10.1163/22941932-20170212
Benson DA, Cavanaugh M, Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW. 2017. GenBank. Nucleic Acids Research. 45: D37-D42. DOI: https://doi.org/10.1093/nar/gkq1079
Bentham G, Hooker JD. 1876. Genera plantarum 2: 1026-1053. London.
Bukatsch F. 1972. Bemerkungen zur Doppelfarbung Astrablau-Safranin. Mikrokosmos 61: 255.
Callmander MW, Phillipson PB, Plunkett GM, Edwards MB, Buerki S. 2016. Generic delimitations, biogeography, and evolution in the tribe Coleeae (Bignoniaceae), endemic to Madagascar and the smaller islands od the western Indian Ocean. Molecular Phylogenetics and Evolution 96: 178-186. DOI: https://doi.org/10.1016/j.ympev.2015.11.016
Carlquist S. 1982. The use of ethylenediamine in softening hard plant structures for paraffin sectioning. Stain Technology 57: 311-317. DOI: https://doi.org/10.3109/10520298209066729
Carlquist S. 1985. Observations on functional wood histology of vines and lianas: Vessel dimorphism, tracheids, vasicentric tracheids, narrow vessels, and parenchyma. Aliso 11: 139-157.
Carlquist S. 2001. Comparative wood anatomy. ed. 2, Berlin: Springer Verlag.
Chery JG, Pace MR, Acevedo-Rodríguez P, Specht CD, Rothfels CJ. 2020. Modifications during early plant development promote the evolution of nature’s most complex woods. Current Biology 30: 1-8. DOI: https://doi.org/10.1016/j.cub.2019.11.003
Darriba D, Taboada GL, Doallo R, Posada D. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772. DOI: https://doi.org/10.1038/nmeth.2109
De Candolle AP. 1838. Revue sommaire de la famille des Bignoniacées. Tirée de la Bibliothèque Universelle de Genève 1-24.
Dos Santos GMA, Miller RB. 1992. Wood anatomy of Tecomeae. In: Gentry AH, ed. Bignoniaceae, Part II (Tribe Tecomeae). Flora Neotropic Monograph 25. pp: 336-358
Evert RF. 2006. Esau’s plant anatomy: meristems, cells, and tissues of the plant body – their structure, function, and developmental. New Jersey: John Wiley and Sons. ISBN:9780471738435
Fischer E, Theisen I, Lohmann LG. 2004. Bignoniaceae. In: Kubitzki K, Kadereit JK, eds., The families and genera of vascular plants. VII. Dicotyledons. Lamiales (except Acanthaceae including Avicenniaceae). Heidelberg: Springer-Verlag. pp. 9-38
Francisco JNC, Lohmann LG. 2020. Phylogeny and biogeography of the Amazonian Pachyptera (Bignonieae, Bignoniaceae). Systematic Botany 45: 361-374. DOI: https://doi.org/10.1600/036364420X15862837791230
Fonseca LHM, Lohmann LG. 2018. Combining high-throughput sequencing and targeted loci data to infer the phylogeny of the “Adenocalymma-Neojobertia” clade. Molecular Phylogenetics and Evolution 123: 1-15. DOI: https://doi.org/10.1016/j.ympev.2018.01.023
Fonseca LHMF, Lohmann LG. 2015. Biogeography and evolution of Dolichandra (Bignonieae, Bignoniaceae). Botanical Journal of the Linnean Society 179: 403-420. DOI: https://doi.org/10.1111/boj.12338
Gentry AH. 1980. Bignoniaceae - Part I (Crescentieae and Tourrettieae). Flora Neotropica Monograph 25: 1-130.
Gentry AH. 1992. Bignoniaceae - Part II (Tribe Tecomae). Flora Neotropica Monograph 25: 1-370.
Gerolamo CS, Angyalossy V. 2017. Wood anatomy and conductivity in lianas, shrubs and trees of Bignoniaceae. IAWA Journal 38: 412-432. DOI: https://doi.org/10.1163/22941932-20170177
Grose SO, Olmstead RG. 2007a. Evolution of a charismatic Neotropical clade: molecular phylogeny of Tabebuia s.l., Crescentieae, and allied genera (Bignoniaceae). Systematic Botany 32: 650-659. DOI: https://doi.org/10.1600/036364407782250553
Grose SO, Olmstead RG. 2007b. Taxonomic revisions in the polyphyletic genus Tabebuia s.l. (Bignoniaceae). Systematic Botany 32: 660-670. DOI: https://doi.org/10.1600/036364407782250652
Hipkins VD, Tsai CH, Strauss SH. 1990. Sequence of the gene for the large subunit of ribulose 1,5-biphosphate carboxylase from the gymnosperm, Douglas fir. Plant Mol. Biol. 15: 505–507.
IAWA Committee 1989. IAWA list of microscopic features for hardwood identification. IAWA Bulletin 10: 219-332.DOI: https://doi.org/10.1163/22941932-90000496
Kaehler M, Michelangeli FA, Lohmann LG. 2012. Phylogeny of Lundia based on molecular and morphological characters. Taxon 61: 368-380.
Kaehler M, Michelangeli FA, Lohmann LG. 2019. Fine tuning the circumscription of Fridericia (Bignonieae, Bignoniaceae). Taxon 68: 751-770. DOI:https://doi.org/10.1002/tax.12121
Kluge AG. 1989. A concern for evidence, and a phylogenetic hypothesis of relationships among Epicrates (Boidae, Serpentes). Systematic Zoology 38: 7-25.
Kraus JE, Arduin M. 1997. Manual básico de métodos em morfologia vegetal. Seropédica, Rio de Janeiro: Editora Universidade Rural.
Li J. 2008. Phylogeny of Catalpa (Bignoniaceae) inferred from sequences of chloroplast ndhF and nuclear ribosomal DNA. Journal of Systematics and Evolution 46: 341-348. DOI: https://doi.org/10.3724/SP.J.1002.2008.08025
Lohmann L. 2006. Untangling the phylogeny of neotropical lianas (Bignonieae, Bignoniaceae). American Journal of Botany 93: 304-318. DOI: https://doi.org/10.3732/ajb.93.2.304
Lohmann LG, Taylor CM. 2014. A new generic classification of tribe Bignonieae (Bignoniaceae). Annals of the Missouri Botanical Garden 99: 348-489. DOI: https://doi.org/10.3417/2003187
Maddison WP, Maddison DR. 2011 Mesquite: a modular system for evolutionary analysis. Version 2.75. http://mesquiteproject.org.
Meckes M, Garduño-Ramírez ML, Marquina S, Álvarez L. 2001. Iridoides adicionales de la planta medicinal Astianthus viminalis y su actividad hipoglucemiante y antihiperglucemiante. Revista de la Sociedad Química de México 45: 195-199.
Medeiros MC, Lohmann LG. 2015. Phylogeny and biogeography of Tynanthus Miers (Bignonieae, Bignoniaceae). Molecular Phylogenetics and Evolution 85: 3s2-40. DOI: https://doi.org/10.1016/j.ympev.2015.01.010
Miller MA, Pfeiffer W, Schwartz T. 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Gateway Computing Environment Workshop: 1-8. DOI: https://doi.org/10.1109/GCE.2010.5676129
Olmstead RG, Sweere JA. 1994. Combining data in phylogenetic systematics: an empirical approach using three molecular data sets in the Solanaceae. Systematic Biology 43: 467-481.
Olmstead RG, Zjhra ML, Lohmann LG, Grose SO, Eckert AJ. 2009. A molecular phylogeny and classification of Bignoniaceae. American Journal of Botany 96: 1731-1743. DOI: https://doi.org/10.3732/ajb.0900004
Olmstead RG. 2013. Phylogeny and biogeography in Solanaceae, Verbenaceae and Bignoniaceae: a comparison of continental and intercontinental diversification patterns. Botanical Journal of the Linnean Society 171: 80-102. DOI: https://doi.org/10.1111/j.1095-8339.2012.01306.x
Pace MR. 2019. Optimal preparation of tissue sections for light-microscopic analysis of phloem anatomy. In: Liesche J, ed., Phloem: Methods and Protocols. Methods in Molecular Biology, vol. 2014. Pp. 3-16 DOI: https://doi.org/10.1007/978-1-4939-9562-2_1
Pace MR, Angyalossy V. 2013. Wood anatomy and evolution: a case study in the Bignoniaceae. International Journal of Plant Sciences 147: 1014-1048. DOI: https://doi.org/10.1086/670258
Pace MR, Lohmann LG, Angyalossy V. 2009. The rise and evolution of the cambial variant in Bignonieae (Bignoniaceae). Evolution & Development 11: 465-479. DOI: https://doi.org/10.1111/j.1525-142X.2009.00355.x
Pace MR, Lohmann LG, Angyalossy V. 2011. Evolution of disparity between the regular and variant phloem in Bignonieae (Bignoniaceae). American Journal of Botany 98: 602-618. DOI: https://doi.org/10.3732/ajb.1000269
Pace MR, Lohmann LG, Olmstead RG, Angyalossy V. 2015a. Wood anatomy of major Bignoniaceae clades. Plant Systematics and Evolution 301: 967-995. DOI: https://doi.org/10.1007/s00606-014-1129-2
Pace MR, Lohmann LG, Alcantara S, Angyalossy V. 2015b. Secondary phloem diversity and evolution in Bignonieae (Bignoniaceae). Annals of Botany 116: 333-358. DOI: https://doi.org/10.1093/aob/mcv106
Pace MR, Zuntini AR, Lohmann LG, Angyalossy V. 2016. Phylogenetic relationships of enigmatic Sphingiphila (Bignoniaceae) based on molecular and wood anatomical data. Taxon 65:1050-1063. DOI: http://dx.doi.org/10.12705/655.7
Pérez Gutiérrez RM, Vargas Solis R, Garcia Baez E & Gallardo Navarro Y. 2009. Hypoglycemic activity of constituents from Astianthus viminalis and streptozotocin-induced diabetic mice. Journal of Natural Medicines 63: 393-401. DOI: https://doi.org/s10.1007/s11418-009-0343-7
Ragsac AC, Farias-Singer R, Freitas LB, Lohmann LG, Olmstead RG. 2019. Phylogeny of the neotropical tribe Jacarandeae (Bignoniaceae). American Journal of Botany 106: 1-13. DOI: https://doi.org/10.1002/ajb2.1399
Rasband WS. 2012. ImageJ. Program distributed by the author. U. S. National Institutes of Health. http://imagej.nih.gov/ij.
Rambaut A. 2010. FigTree v1.3.1. Institute of Evolutionary Biology, University of Edinburgh, Edinburgh. Available at: http://tree.bio.ed.ac.uk/software/figtree/ (Accessed August 25, 2018).
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA. 2018. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67: 901–904. DOI: https://doi.org/10.1093/sysbio/syy032
Record SJ & Hess RW. 1943. Timbers of the new world. New Haven: Yale University Press.
Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP. 2012. MrBayes 3.2: Efficient bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539-542. DOI: https://doi.org/10.1093/sysbio/sys029
Roth I. 1981. Structural patterns of tropical barks. In: Braun HJ, Carlquist S, Ozenda P, Roth I., eds. Encyclopedia of Plant Anatomy. Berlin: Gebrüder Bornstraeger.
Rupp P. 1964. Polyglykol als Einbettungsmedium zum Schneiden botanischer Präparate. Mikrokosmos 53: 123-128.
Schenck H. 1893. Beiträge zur Biologie und Anatomie der Lianen im Besonderen der in Brasilien einheimischen Arten. II. Theil. Beiträge zur Anatomie der Lianen. In: Schimper AFW, ed. Botanische Mittheilungen aus den Tropen. Jena: Gustav Fisher.
Spangler RE, Olmstead RG. 1999. Phylogenetic analysis of Bignoniaceae based on the cpDNA gene sequences rbcL and ndhF. Annals of the Missouri Botanical Garden 86: 33-46. DOI: https://doi.org/10.2307/2666216
Stamatakis A. 2014. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312-1313. DOI: https://doi.org/10.1093/bioinformatics/btu033
Taberlet P, Gielly L, Pautou G, Bouvet J. 1991. Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Molecular Biology 17: 1105-1109. DOI: https://doi.org/10.1007/BF00037152
Thode VA, Sanmartín I, Lohmann LG. 2019. Contrasting patterns of diversification between Amazonian and Atlantic forest clades of Neotropical lianas (Amphilophium, Bignonieae) inferred from plastid genomic data. Molecular Phylogenetics and Evolution 133: 92-106. DOI: https://doi.org/10.1016/j.ympev.2018.12.021
Zjhra ML, Sytsma KJ, Olmstead RG. 2004. Delimitation of Malagasy tribe Coleeae and implications for fruit evolution in Bignoniaceae inferred from a chloroplast DNA phylogeny. Plant Systematics and Evolution 245: 55-67. DOI: https://doi.org/10.1007/s00606-003-0025-y
Zuntini AR, Fonseca LHM, Lohmann LG. 2013. Primers for phylogeny reconstruction in Bignonieae (Bignoniaceae) using herbarium samples. Applications in Plant Sciences 1: 1300018. DOI: https://doi.org/10.3732/apps.1300018
Published
2021-02-14
How to Cite
Pace, M. R., Hernández-Hernández, B., Martínez Salas, E. M., Lohmann, L. G., & Cacho, N. I. (2021). Phylogenetic placement of enigmatic Astianthus (Bignoniaceae) based on molecular data, wood and bark anatomy. Botanical Sciences, 99(2), 398-412. https://doi.org/10.17129/botsci.2779
Section
STRUCTURAL BOTANY / BOTÁNICA ESTRUCTURAL