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Plant Systematics and Evolution

, Volume 304, Issue 6, pp 775–791 | Cite as

Systematic and phylogenetic implications of the wood anatomy of six Neotropical genera of Primulaceae

  • Bruna N. de Luna
  • Maria de F. Freitas
  • Claudia F. Barros
Original Article

Abstract

Our main goals were to identify diagnostic characters at the species, genus, and subfamily levels, find anatomical features with potential for future morphological and molecular (combined) phylogenetic analyses, and to reconstruct the evolution of wood anatomical characters in two subfamilies of Primulaceae in a molecular phylogenetic framework. We investigated twenty-seven species from the woody Myrsinoideae (4 genera) and Theophrastoideae (2 genera) using scanning electron, light, and epifluorescence microscopy. Samples were prepared using standard protocols. Based on the wood anatomical characters, we were able to identify synapomorphies and to detect evolutionary trends of interest for the genera and subfamilies. Both subfamilies share the presence of diffuse porosity, simple perforation plates, septate fibres, and scanty paratracheal axial parenchyma. Theophrastoideae species have rays > 10 cells wide and short (< 350 µm) vessel elements, and Myrsinoideae have breakdown areas in rays and longer vessel elements. Ardisia and Stylogyne have scalariform intervessel pits, Myrsine exhibit breakdown areas in rays, and two Cybianthus species from subgenus Weilgetia have distinguishing features (e.g., scalariform perforation plate in C. nemoralis and the absence of rays in C. densiflorus). Overall, when combining characters, we were able to segregate the Neotropical Primulaceae subfamilies and genera from each other and from the subfamily Maesoideae based on wood anatomy.

Keywords

Amazonia Character optimization Myrsinoideae Primuloid clade Raylessness 

Notes

Acknowledgements

We thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) for financial support. C.F.B. received grants from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq). We thank Zeiss for the opportunity to use the Axio Imager 2 equipment. We also thank anonymous reviewers for their valuable feedback.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

606_2018_1509_MOESM1_ESM.pdf (556 kb)
Online Resource 1 Matrix of wood anatomical characters used in the PCA. Data obtained from the present work and from Lens et al. (2005a). (PDF 555 kb)

References

  1. Agostini G (1980) Una nueva clasificación del género Cybianthus (Myrsinaceae). Acta Bot Venez 10:129–185Google Scholar
  2. Anderberg AA, Ståhl B (1995) Phylogenetic interrelationships in the order Primulales, with special emphasis on the family circumscriptions. Canad J Bot 73:1699–1730.  https://doi.org/10.1139/b95-184 CrossRefGoogle Scholar
  3. Anderberg AA, Ståhl B, Källersjö M (1998) Phylogenetic relationships in the Primulales inferred from rbcL sequence data. Pl Syst Evol 211:93–102.  https://doi.org/10.1007/BF00984914 CrossRefGoogle Scholar
  4. Anderberg AA, Ståhl B, Kallersjö M (2000) Maesaceae, a new primuloid family in the order Ericales s.l. Taxon 49:183–187.  https://doi.org/10.2307/1223834 CrossRefGoogle Scholar
  5. Anderberg AA, Peng CI, Trift I, Kallersjö M (2001) The Stimpsonia problem: evidence from DNA sequences of plastid genes atpB, ndhF and rbcL. Bot Jahrb Syst 123:369–376Google Scholar
  6. APG III (Angiosperm Phylogeny Group) (2009) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants. Bot J Linn Soc 161:105–161.  https://doi.org/10.1111/j.1095-8339.2009.00996.x CrossRefGoogle Scholar
  7. APG IV (Angiosperm Phylogeny Group) (2016) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Bot J Linn Soc 181:1–20.  https://doi.org/10.1111/boj.12385 CrossRefGoogle Scholar
  8. Baas P (1982) Systematic, phylogenetic, and ecological wood anatomy—history and perspectives. In: Baas P (ed) New perspectives in wood anatomy. Forestry sciences, vol. 1. Springer, Dordrecht, pp 23–58.  https://doi.org/10.1007/978-94-017-2418-0_2 CrossRefGoogle Scholar
  9. Baas P, Wheeler E, Chase M (2000) Dicotyledonous wood anatomy and the APG system of angiosperm classification. Bot J Linn Soc 134:3–17.  https://doi.org/10.1111/j.1095-8339.2000.tb02343.x CrossRefGoogle Scholar
  10. Bailey IW (1944) The development of vessels in angiosperms and its significance in morphological research. Amer J Bot 31:421–428.  https://doi.org/10.2307/2437302 CrossRefGoogle Scholar
  11. BFG (The Brazil Flora Group) (2015) Growing knowledge: an overview of Seed Plant diversity in Brazil. Rodriguésia 66:1085–1113.  https://doi.org/10.1590/2175-7860201566411 CrossRefGoogle Scholar
  12. Bukatsch F (1972) Bemerkungen zur doppelfärbung astrablau-safranin. Mikrokosmos 61:33–36Google Scholar
  13. Carlquist S (1974) Island biology. Columbia University Press, New YorkCrossRefGoogle Scholar
  14. Carlquist S (1992) Wood anatomy of sympetalous dicotyledon families: a summary, with comments on systematic relationships and evolution of the woody habit. Ann Missouri Bot Gard 79:303–332.  https://doi.org/10.2307/2399771 CrossRefGoogle Scholar
  15. Carlquist S (2001) Comparative wood anatomy, 2nd edn. Springer, Berlin.  https://doi.org/10.1007/978-3-662-04578-7 CrossRefGoogle Scholar
  16. Carlquist S (2012) How wood evolves: a new synthesis. Botany 90:901–940.  https://doi.org/10.1139/b2012-048 CrossRefGoogle Scholar
  17. Carlquist S (2013) More woodiness/less woodiness: evolutionary avenues, ontogenetic mechanisms. Int J Pl Sci 174:964–991.  https://doi.org/10.1086/670400 CrossRefGoogle Scholar
  18. Carlquist S (2015a) Living cells in wood. 1. Absence, scarcity and histology of axial parenchyma as keys to function. Bot J Linn Soc 174:291–321.  https://doi.org/10.1111/boj.12247 CrossRefGoogle Scholar
  19. Carlquist S (2015b) Living cells in wood. 2. Raylessness: histology and evolutionary significance. Bot J Linn Soc 178:529–555.  https://doi.org/10.1111/boj.12291 CrossRefGoogle Scholar
  20. Committee IAWA (1989) IAWA list of microscopic features for hardwood identification. IAWA Bull 10:219–332CrossRefGoogle Scholar
  21. Dayal R, Rao V, Sharma B (1984) Perforated ray cells in woods of Indian Myrsinaceae and Loganiaceae. IAWA Bull 5:225–228.  https://doi.org/10.1163/22941932-90000895 CrossRefGoogle Scholar
  22. Franklin GL (1945) Preparation of thin sections of synthetic resins and wood–resin composites, and a new macerating method for wood. Nature 155:51.  https://doi.org/10.1038/155051a0 CrossRefGoogle Scholar
  23. Ilic J (1987) The CSIRO family key for hardwood identification, vol. 8. Brill Archive, LeidenGoogle Scholar
  24. Johansen DA (1940) Plant microtechnique. McGraw-Hill Book Company, New YorkGoogle Scholar
  25. Källersjö M, Bergqvist G, Anderberg AA (2000) Generic realignment in primuloid families of the Ericales s.l.: a phylogenetic analysis based on DNA sequences from three chloroplast genes and morphology. Amer J Bot 87:1325–1341.  https://doi.org/10.2307/2656725 CrossRefGoogle Scholar
  26. Kukachka BF (1981) Wood Anatomy of the neotropical Sapotaceae: XX. Manilkara. US Department of Agriculture, MadisonGoogle Scholar
  27. Lens F, Jansen S, Caris P, Serlet L, Smets E (2005a) Comparative wood anatomy of the primuloid clade. Syst Bot 30:162–182.  https://doi.org/10.1600/0363644053661922 CrossRefGoogle Scholar
  28. Lens F, Dressler S, Jansen S, Van Evelghem L, Smets E (2005b) The relationships within balsaminoid Ericales: a wood anatomical approach. Amer J Bot 92:941–953.  https://doi.org/10.3732/ajb.92.6.941 CrossRefGoogle Scholar
  29. Lens F, Schönenberger J, Baas P, Jansen S, Smets E (2007) The role of wood anatomy in phylogeny reconstruction of Ericales. Cladistics 23:229–254.  https://doi.org/10.1111/j.1096-0031.2006.00142.x CrossRefGoogle Scholar
  30. Lens F, Vos R, Charrier G, van der Niet T, Merckx V, Baas P, Aguirre Gutierrez J, Jacobs B, Chacon-Dória L, Smets E, Delzon S, Janssens S (2016) Scalariform-to-simple transition in vessel perforation plates triggered by differences in climate during the evolution of Adoxaceae. Ann Bot (Oxford) 118:1043–1056.  https://doi.org/10.1093/aob/mcw151 CrossRefGoogle Scholar
  31. Ludwig JA, Reynolds JF (1988) Statistical ecology: a primer on methods and computing. Wiley, New YorkGoogle Scholar
  32. Luna BN, Defaveri ACA, Sato A, Bizzo HR, Freitas MF, Barros CF (2014) Leaf secretory tissues in Myrsine coriacea and Myrsine venosa (Primulaceae): ontogeny, morphology, and chemical composition of essential oils. Botany 92:757–766.  https://doi.org/10.1139/cjb-2014-0044 CrossRefGoogle Scholar
  33. Luna BN, Freitas MF, Baas P, De Toni KLG, Barros CF (2017) Leaf anatomy of five Neotropical genera of Primulaceae. Int J Pl Sci 178:362–377.  https://doi.org/10.1086/691213 CrossRefGoogle Scholar
  34. Maddison WP, Maddison DR (2017) Mesquite: a modular system for evolutionary analysis. Version 3.2. Available at: http://mesquiteproject.org. Accessed 4 Mar 2018
  35. Metcalfe CR, Chalk L (1950) Anatomy of the dicotyledons, vol. 2. Oxford Claredon Press, OxfordGoogle Scholar
  36. Olson ME (2005) Commentary: typology, homology, and homoplasy in comparative wood anatomy. IAWA J 26:507–522.  https://doi.org/10.1163/22941932-90000131 CrossRefGoogle Scholar
  37. Otegui MS (1994) Occurrence of perforated ray cells and ray splitting in Rapanea laetevirens and R. lorentziana (Myrsinaceae) rays. IAWA J 15:257–263.  https://doi.org/10.1163/22941932-90000605 CrossRefGoogle Scholar
  38. Otegui M, Cocucci A (1999) Flower morphology and biology of Myrsine laetevirens, structural and evolutionary implications of anemophily in Myrsinaceae. Nordic J Bot 19:71–85.  https://doi.org/10.1111/j.1756-1051.1999.tb01904.x CrossRefGoogle Scholar
  39. Otegui MS, Gaspar ML, Maldonado S, Varetti EL, Pollero R (1998) Studies on tissues associated to hydrobenzoquinone secretion in Myrsine laetevirens (Myrsinaceae). Nordic J Bot 18:447–459.  https://doi.org/10.1111/j.1756-1051.1998.tb01522.x CrossRefGoogle Scholar
  40. Pérez Olvera CP, Valdovinos TFC, Gómez MAR (1980) Estudio anatomico de la Madera de 43 especies tropicales. Instituto nacional de Investigaciones Forestales, MéxicoGoogle Scholar
  41. Pipoly JJ III (1987) A systematic revision of the genus Cybianthus subgenus Grammadenia (Myrsinaceae). Mem New York Bot Gard 43:1–76Google Scholar
  42. Schönenberger J, Anderberg AA, Sytsma KJ (2005) Molecular phylogenetics and patterns of floral evolution in the Ericales. Int J Pl Sci 166:265–288.  https://doi.org/10.1086/427198 CrossRefGoogle Scholar
  43. Sonsin JO, Gasson P, Machado SR, Caum C, Marcati CR (2014) Atlas of wood diversity in the Cerrado of São Paulo. Fundação de Estudos e Pesquisas Agrícolas e Florestais (FEPAF), BotucatuGoogle Scholar
  44. Stevens PF (2001 onwards) Angiosperm phylogeny website, version 12, July 2012. Available at: http://www.mobot.org/MOBOT/research/APweb/. Accessed 4 Mar 2018
  45. Strasburger E (1924) Handbook of practical botany, 8th edn. George Allen & Unwin, LondonGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, Diretoria de Pesquisa CientíficaRio de JaneiroBrazil

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