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Issue: Vol. 642 No. 1: 26 Mar. 2024
Type: Article
Published: 2024-03-26
DOI: 10.11646/phytotaxa.642.1.2
Page range: 21-36
Abstract views: 25
PDF downloaded: 2

Polysporangiate anthers described in Eugenia (Myrtaceae) with notes on evolutionary patterns

Faculdade de Ciências Biológicas e Ambientais, Universidade Federal da Grande Dourados, Unidade II, CEP 79804-970, Dourados, MS, Brazil
Instituto de Ciências Biológicas, Departamento de Biologia, Universidade Federal do Amazonas, Av. General Rodrigo Octávio, 6200, CEP 69080-900, Manaus, AM, Brazil
Pós-Graduação em Biotecnologia e Recursos Naturais (PPGMBT-UEA), Universidade do Estado do Amazonas, Av. Carvalho Leal, 1777, CEP 69065-001, Manaus, AM, Brazil, Museu da Amazônia, MUSA, Rua Planeta Plutão, 11, CEP 69099-415, Manaus, AM, Brazil
Universidade de São Paulo, Instituto de Biociências, Departamento de Botânica, Laboratório de Sistemática Vegetal, Rua do Matão, 277, CEP 05508-090, São Paulo, SP, Brazil
Comparative Plant and Fungal Biology Department, Herbarium, Royal Botanic Gardens, Kew TW9 3AB Richmond, Surrey, UK
Myrtales Myrteae multilocular anther polysporangiate anther sporangium stamen Eudicots

Abstract

Shifts towards compartmentalisation resulting in multilocular anthers have been described in some families of Myrtales but to date, not in Myrtaceae. In these other families sporogeneous tissue is partitioned by transverse or longitudinal septa, fitting the definition of the ‘polysporangiate anther’. Polysporangiate anther in Eugenia, a Neotropical genus of Myrtaceae is here discussed, with a detailed description of their morphology and in the context of known phylogenetic relationships within Eugenia. Anthers of Eugenia joseramosii, E. kerianthera and E. petaloidea were examined using scanning electron microscopy; E. multilocellata and E. quilombola were imaged with light microscope. Molecular sequences of five regions were used to place these species in a representative phylogenetic framework for character reconstruction analysis. Analysed anthers share dithecal organization in which each anther theca is divided in dorsal and ventral rows of sporangia. Polysporangiate anthers in Eugenia appear to have evolved independently on at least two occasions in Eugenia sect. Umbellatae. Eugenia flowers with polysporangiate anthers fit a generalist pollination pattern but Eugenia petaloidea demonstrates some unusual features that may be linked to pollination by vibration. Anthers in Eugenia is a rare condition with low systematic value. Resources should be invested to survey Myrtaceae for more species with polysporangiate anthers, to improve understanding of their evolutionary relevance and to record pollinators and modes of pollination.

References

  1. Almeda, F. & Martins, A.B. (2012) Microlicia wurdackiana (Melastomataceae: Microlicieae); a new species from Bahia, Brazil. Kew Bulletin 67: 467–470. https://doi.org/10.1007/s12225-012-9396-y
  2. Amaral, M.C.E., Bittrich, V., Endress, P.K. & Stevens, P.F. (2017) The unique morphology of resin-producing multilocellate anthers and their evolution in Clusia (Clusiaceae). Botanical Journal of the Linnean Society 184: 79–93. https://doi.org/10.1093/botlinnean/box015
  3. Amorim, B.S., Souza, M.A.D., Albuquerque, P.M., Negrão, R. & Giaretta, A. (2022) A tribute to resistance: Eugenia quilombola
  4. (Myrtaceae), a new species with multilocular anthers from the Atlantic Forest of northeastern Brazil. Phytotaxa 543 (1): 31–40. https://doi.org/10.11646/phytotaxa.543.1.3
  5. Baumgratz, J.F.A., Souza, M.L.D.R., Woodgyer, E.M. & Nic Lughadha, E.M. (1996) Polysporangiate anthers: Described for the first time in Melastomataceae. Kew Bulletin 51: 133–144. https://doi.org/10.2307/4118750
  6. Beech, E., Rivers, M., Oldfield, S. & Smith, P.P. (2017) GlobalTreeSearch: The first complete global database of tree species and country distributions. Journal of Sustainable Forestry 36: 454–489. https://doi.org/10.1080/10549811.2017.1310049
  7. Berg, O.C. (1854) Revisio Myrtacearum huc usque cognitarum s. Klotzschii “Flora Americae aequinoctialis” exhibens Myrtaceas. Linnaea 27: 1–447.
  8. Berg, O.C. (1857) Flora Brasiliensis Myrtaceae. In: K. F. P. von Martius (Ed.) Frid. Fleischer in Comm., Monachii [Munich], 1–528 pp.
  9. Brito, V.L.G., Fendrich, T.G., Smidt, E.C., Varassin, I.G. & Goldenberg, R. (2016) Shifts from specialised to generalised pollination systems in Miconieae (Melastomataceae) and their relation with anther morphology and seed number. Plant Biology 18: 585–593. https://doi.org/10.1111/plb.12432
  10. Bünger, M.O., Mazine, F.F., Forest, F., Bueno, M.L., Stehmann, J.R. & Lucas, E.J. (2016) The evolutionary history of Eugenia sect. Phyllocalyx (Myrtaceae) corroborates historically stable areas in the southern Atlantic forests. Annals of Botany 118: 1209–1223. https://doi.org/10.1093/aob/mcw209
  11. Caetano, A.P.S., Reginato, M., Goldenberg, R., Cortez, P.A., Basso-Alves, J.P., Michelangeli, F.A., Carmello-Guerreiro, S.M. & Teixeira, S.P. (2020) Structure and evolution of polysporangiate anthers in Melastomataceae. Perspectives in Plant Ecology, Evolution and Systematics 46: 125556. https://doi.org/10.1016/j.ppees.2020.125556
  12. Coutinho, K., Oliveira, M.I.U. & Funch, L.S. (2015) Four new species of Eugenia (Myrtaceae) from the Caatinga and Atlantic Forest of northeastern Brazil. Phytotaxa 234: 215–226. https://doi.org/10.11646/phytotaxa.234.3.2
  13. De Luca, P.A. & Vallejo-Marín, M. (2013) What’s the “buzz” about? The ecology and evolutionary significance of buzz-pollination. Current Opinion in Plant Biology 16: 429–435. https://doi.org/10.1016/j.pbi.2013.05.002
  14. Dickison, W.C. & Bittrich, V. (2016) Metteniusaceae (incl. Dendrobangia incert. sed.). In: Kadereit, J. & Bittrich, V. (Eds.) Flowering Plants. Eudicots. The Families and Genera of Vascular Plants, Vol. 14. Springer, Cham, pp. 263–267. https://doi.org/10.1007/978-3-319-28534-4_23
  15. Endress, K. & Stumpf, S. (1990) Non-tetrasporangiate stamens in the angiosperms: structure, systematic distribution and evolutionary aspects. Botanische Jahrbücher fur Systematik 112: 193–240.
  16. Endress, P.K. (1996) Homoplasy in Angiosperm Flowers. In: Sanderson, M.J. & Hufford, L. (Eds.) Homoplasy: the recurrence of similarity in evolution. Academic Press, San Diego, California, pp. 303–325. https://doi.org/10.1016/B978-012618030-5/50014-9
  17. Endress, P.K. (1998) Diversity and Evolutionary Biology of Tropical Flowers. Cambridge University Press, Cambridge, 582 pp.
  18. Endress, P.K. (2011) Evolutionary diversification of the flowers in angiosperms. American Journal of Botany 98: 370–396. https://doi.org/10.3732/ajb.1000299
  19. Fidalgo, A.O. & Kleinert, A.M.P. (2009) Reproductive biology of six Brazilian Myrtaceae: is there a syndrome associated with buzz-pollination? New Zealand Journal of Botany 47: 355–365. https://doi.org/10.1080/0028825x.2009.9672712
  20. Giaretta, A., Amorim, B.S., Sano, P.T., Souza, G. & Lucas, E. (2019a) Phylogenetic placement of new species with fused calyx reveals homoplastic character in Eugenia (Myrtaceae). Systematic Botany 44: 66–73. https://doi.org/10.1600/036364419X697903
  21. Giaretta, A., Lucas, E. & Sano, P.T. (2021) Taxonomic monograph of Eugenia sect. Schizocalomyrtus (Myrtaceae: Myrteae), a group within Eugenia with unusual flowers. Phytotaxa 524 (3): 135–177. https://doi.org/10.11646/phytotaxa.524.3.1
  22. Giaretta, A., Murphy, B., Maurin, O., Mazine, F.F., Sano, P. & Lucas, E. (2022) Phylogenetic relationships within the hyper-diverse genus Eugenia (Myrtaceae: Myrteae) based on target enrichment sequencing. Frontiers in Plant Science 12: 1–20. https://doi.org/10.3389/fpls.2021.759460
  23. Giaretta, A., Vasconcelos, T.N.C., Mazine, F.F., Faria, J.E.Q., Flores, R., Holst, B., Sano, P.T. & Lucas, E. (2019b) Calyx (con)fusion in a hyper-diverse genus: Parallel evolution of unusual flower patterns in Eugenia (Myrtaceae). Molecular Phylogenetics and Evolution 139: 106553. https://doi.org/10.1016/j.ympev.2019.106553
  24. González, F.A. & Rudall, P.J. (2010) Flower and fruit characters in the early-divergent lamiid family Metteniusaceae, with particular reference to the evolution of pseudomonomery. American Journal of Botany 97: 191–206. https://doi.org/10.3732/ajb.0900194
  25. Green, J.W. (1979) Corynanthera, a new genus of Myrtaceae (Subfamily Leptospermoideae, Tribe Chamelaucieae). Nuytsia 2: 368–372. https://doi.org/10.58828/nuy00050
  26. Green, J.W. (1983) Malleostemon, a new genus of Myrtaceae (subfamily Leptospermoideae, tribe Chamelaucieae) from southwestern Australia. Nuytsia 4: 295–315. https://doi.org/10.58828/nuy00079
  27. Gressler, E., Pizo, M.A. & Morellato, L.P.C. (2006) Polinização e dispersão de sementes em Myrtaceae do Brasil. Brazilian Journal of Botany 29: 509–530. https://doi.org/10.1590/S0100-84042006000400002
  28. Hooker, J.D. (1846) XVI Myrtaceae—Botany of the Antartic Voyage. Flora Antarctica, vol. 2. London, 574 pp.
  29. Hooker, W.J. (1833) Myrtaceae. Botanical Miscellany, vol. 3. London, 389 pp.
  30. Huelsenbeck, J.P., Nielsen, R. & Bollback, J.P. (2003) Stochastic mapping of morphological characters. Systematic Biology 52: 131–158. https://doi.org/10.1080/10635150390192780
  31. Judkevich, M.D., Salas, R.M. & Gonzalez, A.M. (2020) Androecium anatomy of Isertia laevis, a polysporangiate species of Rubiaceae. Protoplasma 258: 547–557. https://doi.org/10.1007/s00709-020-01582-1
  32. Kirkbride, J.H. (1985) Manipulus Rubiacearum IV. Kerianthera (Rubiaceae), a New Genus from Amazonian Brazil. Brittonia 37: 109–116. https://doi.org/10.2307/2806257
  33. Landrum, L.R. & Kawasaki, M.L. (1997) The genera of Myrtaceae in Brazil: An illustrated synoptic treatment and identification keys. Brittonia 49: 508–536. https://doi.org/10.2307/2807742
  34. Legrand, C.D. (1968) Las Mirtaceas del Uruguay III. Boletín de la Facultad de Agronomia de Universidad de Montevideo 101: 1–80.
  35. Lersten, N.R. (1971) A review of septate microsporangia in vascular plants. Iowa State Journal of Science 45: 487–497.
  36. Lima, J.F., Romero, R. & Simão, D.G. (2019) Polysporangiate anthers in Microlicia D.Don (Melastomataceae Juss.). Feddes Repertorium 130: 9–18. https://doi.org/10.1002/fedr.201800006
  37. Linnaeus, C. (1753) Species Plantarum. Impensis Laurentii Salvii, Stockholm, 471 pp.
  38. Lourenço, A.R.L., Amorim, B.S. & Alves, M. (2013) Eugenia pipensis, a new species of Eugenia sect. Umbellatae (Myrtaceae) from northeastern Brazil. Phytotaxa 104: 30–34. https://doi.org/10.11646/phytotaxa.104.1.4
  39. Lucas, E.J., Amorim, B.S., Lima, D.F., Lima-Lourenço, A.R., Nic Lughadha, E.M., Proença, C.E.B., Rosa, P.O., Rosário, A.S., Santos, L.L., Santos, M.F., Souza, M.C., Staggemeier, V.G., Vasconcelos, T.N.C. & Sobral, M. (2018) A new infra-generic classification of the species-rich Neotropical genus Myrcia s.l. Kew Bulletin 73: 1–12. https://doi.org/10.1007/s12225-017-9730-5
  40. Lucas, E.J., Harris, S.A., Mazine, F.F., Belsham, S.R., Nic Lughadha, E.M., Telford, A., Gasson, P.E. & Chase, M.W. (2007) Suprageneric phylogenetics of Myrteae, the generically richest tribe in Myrtaceae (Myrtales). Taxon 56: 1105–1128. https://doi.org/10.2307/25065906
  41. Lucas, E.J., Holst, B., Sobral, M., Mazine, F.F., Lughadha, E.M.N., Proença, C.E.B., Ribeiro, I. & Vasconcelos, T.N.C. (2019) A new subtribal classification of tribe Myrteae (Myrtaceae). Systematic Botany 44: 560–569. https://doi.org/10.1600/036364419X15620113920608
  42. Mazine, F.F., Faria, J.E.Q., Giaretta, A., Vasconcelos, T., Forest, F., Lucas, E., Faria, J.E.Q., Giaretta, A., Vasconcelos, T., Forest, F. & Lucas, E. (2018) Phylogeny and biogeography of the hyper-diverse genus Eugenia (Myrtaceae: Myrteae), with emphasis on E. sect. Umbellatae, the most unmanageable clade. Taxon 67: 752–769. https://doi.org/10.12705/674.5
  43. Mazine, F.F., Souza, V.C., Sobral, M., Forest, F. & Lucas, E. (2014) A preliminary phylogenetic analysis of Eugenia (Myrtaceae: Myrteae), with a focus on Neotropical species. Kew Bulletin 69: 9497. https://doi.org/10.1007/s12225-014-9497-x
  44. McVaugh, R. (1963) Tropical American Myrtaceae, II. Notes of generic concepts and description of previously unrecognized species. Fieldiana 29: 395–532. https://doi.org/10.5962/bhl.title.3851
  45. Nic Lughadha, E. (1998) Preferential outcrossing in Gomidesia (Myrtaceae) is maintained by a post-zygotic mechanism. In: Owens, S.J. & Rudall, P.J. (Eds.) Reproductive Biology. Royal Botanic Gardens, Kew, London, UK, pp. 363–379.
  46. Oliveira, C.T., Giacomin, L.L. & Zappi, D.C. (2011) Kerianthera longiflora (Rubiaceae), a remarkable new species from eastern Brazil, with some observations on K. preclara. Kew Bulletin 66: 143–148. https://doi.org/10.1007/s12225-011-9258-z
  47. Pacini, E., Franchi, G.G. & Hesse, M. (1985) The tapetum: Its form, function, and possible phylogeny in Embryophyta. Plant Systematics and Evolution 149: 155–185. https://doi.org/10.1007/BF00983304
  48. POWO (2024) Plants of the World Online. Facilitated by the Royal Botanic Gardens, Kew. Available from: https://powo.science.kew.org/ (accessed 15 March 2024). Facilitated by the Royal Botanic Gardens, Kew. [https://powo.science.kew.org/]
  49. Proença, C.E.B. (1992) Buzz pollination—older and more widespread than we think? Journal of Tropical Ecology 8: 115–120. https://doi.org/10.1017/S0266467400006192
  50. R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, [http://www.r-project.org]
  51. Ragsac, A.C., Farias-Singer, R., Freitas, L.B., Lohmann, L.G. & Olmstead, R.G. (2019) Phylogeny of the Neotropical tribe Jacarandeae (Bignoniaceae). American Journal of Botany 106: 1589–1601. https://doi.org/10.1002/ajb2.1399
  52. Revell, L.J. (2012) phytools: an R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution 3: 217–223. https://doi.org/10.1111/j.2041-210X.2011.00169.x
  53. RStudio Team (2019) RStudio: Integrated Development for R. RStudio, Inc., Boston, MA. [http://www.rstudio.com/]
  54. Rye, B.L. (2016) An update to the taxonomy of some Western Autralian genera of Myrtaceae tribe Chamelaucieae. 4. Malleostemon. Nuytsia 27: 103–120. https://doi.org/10.58828/nuy00778
  55. Sobral, M., Grippa, C.R., Souza, M.C., Aguiar, O.T., Bertoncello, R. & Guimarães, T.B. (2012) Fourteen new species and two taxonomic notes on Brazilian Myrtaceae. Phytotaxa 50: 19–50. https://doi.org/10.11646/phytotaxa.50.1.3
  56. Souza, M.A.D. (1996) Aspectos da biologia reprodutiva de onze espécies de Myrtaceae em floresta de terra firme na Amazônia Central. Instituto Nacional de Pesquisas da Amazônia, Amazonas, Brazil.
  57. Souza, M.A.D. (2017) Erratum for “Two new species of Eugenia (Myrtaceae) from Central Amazonia, Brazil.” Phytotaxa 298 (3): 300. https://doi.org/10.11646/phytotaxa.298.3.11
  58. Souza, M.A.D., Scudeller, V.V. & Mendonça, M.S. (2015) Three new species of Eugenia (Myrtaceae) from Brazilian Amazonia. Phytotaxa 212 (1): 87–94. https://doi.org/10.11646/phytotaxa.212.1.4
  59. Souza, M.A.D., Scudeller, V.V. & Mendonça, M.S. (2016) Two new species of Eugenia (Myrtaceae) from Central Amazonia, Brazil. Phytotaxa 289 (2): 167–174. https://doi.org/10.11646/phytotaxa.289.2.6
  60. Souza, M.A.D., Sobral, M. & Amorim, G. (2022) Six new species of Eugenia (Myrtaceae) from Amazonian Brazil. Phytotaxa 536 (3): 197–212. https://doi.org/10.11646/phytotaxa.536.3.1
  61. Suaza-Gaviria, V., Pabón-Mora, N. & González, F. (2016) Development and morphology of flowers in Loranthaceae. International Journal of Plant Sciences 177: 559–578. https://doi.org/10.1086/687280
  62. Swartz, O. (1788) Nova genera et species plantarum seu prodromus descriptionum vegetabilium. Stockholm-Uppsala, 158 pp. https://doi.org/10.5962/bhl.title.4400
  63. Thiers, B. (2024 [continuously updated]) Index Herbariorum: A global directory of public herbaria and associated staff. New york Botanical Garden’s Virtual Herbarium. Available from: http://sweetgum.nybg.org/science/ih/ (accessed 15 March 2024)
  64. Tobe, H. & Raven, P.H. (1984) The embryology and relationships of Oliniaceae. Plant Systematics and Evolution 146: 105–116. https://doi.org/10.1007/BF00984057
  65. Tobe, H. & Raven, P.H. (1986) Evolution of polysporangiate anthers in Onagraceae. American Journal of Botany 73: 475–488. https://doi.org/10.1002/j.1537-2197.1986.tb12065.x
  66. Tsou, C. & Johnson, D.M. (2003) Comparative development of aseptate and septate anthers of Annonaceae. American Journal of Botany 90: 832–848 https://doi.org/10.3732/ajb.90.6.832
  67. Valdemarin, K.S., Giaretta, A., Sobral, M., Castro, V. & Mazine, F.F. (2019) Two new species of Eugenia (Myrtaceae, Myrteae) with fused calyx from the Atlantic coastal forest, Brazil. Phytotaxa 403 (2): 99–110. https://doi.org/10.11646/phytotaxa.403.2.3
  68. Vallejo-Marín, M., Silva, E.M., Sagent, R.D. & Barret, S.C.H. (2010) Trait correlates and functional significance of heteranthery in flowering plants. New Phytologist 188: 418–425. https://doi.org/10.1111/j.1469-8137.2010.03430.x
  69. Vasconcelos, T.N.C., Lucas, E.J., Faria, J.E.Q. & Prenner, G. (2018) Floral heterochrony promotes flexibility of reproductive strategies in the morphologically homogeneous genus Eugenia (Myrtaceae). Annals of Botany 121: 161–174. https://doi.org/10.1093/aob/mcx142
  70. Vasconcelos, T.N.C., Prenner, G. & Lucas, E.J. (2019) A systematic overview of the floral diversity in Myrteae (Myrtaceae). Systematic Botany 44: 570–591. https://doi.org/10.1600/036364419X15620113920617
  71. Vasconcelos, T.N.C., Proença, C.E.B., Ahmad, B., Aguilar, D.S., Aguilar, R., Amorim, B.S., Campbell, K., Costa, I.R., De-carvalho, P.S., Faria, J.E.Q.Q., Giaretta, A., Kooij, P.W., Lima, D.F., Mazine, F.F., Peguero, B., Prenner, G., Santos, M.F., Soewarto, J., Wingler, A. & Lucas, E.J. (2017) Myrteae phylogeny, calibration, biogeography and diversification patterns: Increased understanding in the most species rich tribe of Myrtaceae. Molecular Phylogenetics and Evolution 109: 113–137. https://doi.org/10.1016/j.ympev.2017.01.002
  72. Wagner, W.L., Hoch, P.C. & Raven, P.H. (2007) Revised Classification of the Onagraceae. In: Anderson, C. (Ed.) Systematic Botany Monographs. The American Society of Plant Taxonomists, USA, p. 240.
  73. Wilson, P.G. (2011) Myrtaceae. In: Kubitzki, K. (Ed.) The families and genera of vascular plants. Flowering plants, eudicots: Sapindales, Cucurbitales, Myrtaceae. Springer-Verlag, Berlin, pp. 212–271. https://doi.org/10.1007/978-3-642-14397-7_14