Skip to main content Skip to main navigation menu Skip to site footer
Responsive image
Issue: Vol. 669 No. 2: 22 Oct. 2024
Type: Article
Published: 2024-10-22
DOI: 10.11646/phytotaxa.669.2.1
Page range: 75-86
Abstract views: 113
PDF downloaded: 94

Pollen morphology and fruit anatomy of the enigmatic monotypic genus Dicranocarpus (Coreopsideae, Asteraceae)

Biología Evolutiva, Instituto de Ecología AC, Carretera antigua a Coatepec 351, Xalapa, Veracruz 91073, México
Biología Evolutiva, Instituto de Ecología AC, Carretera antigua a Coatepec 351, Xalapa, Veracruz 91073, México
Instituto Politécnico Nacional, Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional Unidad Durango, Durango, México
Biología Evolutiva, Instituto de Ecología AC, Carretera antigua a Coatepec 351, Xalapa, Veracruz 91073, México
Compositeae cypsela anatomy Dahlia Hidalgoa Mexico phytomelanin pollen Eudicots

Abstract

Dicranocarpus is a monotypic genus endemic to the Chihuahuan Desert with atypical attributes among species of tribe Coreopsideae. Phylogenetic position of Dicranocarpus parviflorus has been controversial. A molecular phylogeny showed that the taxon was closely related to Dahlia; however, further analyses with a wider sampling of Dahlia, also including Hidalgoa, identified the genus in a more distant clade. The objective of this study is to gather anatomical attributes from the cypselae as well as palynological characters along with macromorphology to determine whether Dicranocarpus shares characters with these genera in Coreopsideae. Our results show that although the pollen of D. parviflorus does not possess attributes that distinguish it from the rest of the tribe Coreopsideae, they were useful to confirm its membership in the tribe. The cypselae anatomy identified that D. parviflorus has characters of taxonomic value that differentiate this species from the rest of the Coreopsideae. The three most significant novel characters in Dicranocarpus were in the outer mesocarp, consisting of tracheoidal-like cells forming irregular rows up to 250 μm in length, an aerenchyma in the middle mesocarp, and the lack of phytomelanin and calcium oxalate crystals. Furthermore, the results of the phytomelanin patterns in the studied taxa highlight the need for further anatomical studies of the cypselae to fully understand the evolution of phytomelanin deposition in the tribe Coreopsideae and even in the Heliantheae Alliance. Macromorphological, palynological and anatomical attributes of the cypsela in Dicranocarpus were not shared with Dahlia. Moreover, the sexual condition of the disc and ray florets shared with Hidalgoa has evolved independently in lineages of Asteraceae.

References

  1. Anderberg, A.A., Baldwin, B.G., Bayer, R.G., Breitwieser, J., Jeffrey, C., Dillon, M.O., Eldenäs, P., Funk, V., Garcia-Jacas, N., Hind, D.J.N., Karis, P.O., Lack, H.W., Nesom, G., Nordenstam, B., Oberprieler, Ch., Panero, J.L., Puttock, C., Robinson, H., Stuessy, T.F., Susanna, A., Urtubey, E., Vogt, R., Ward, J. & Watson, L.E. (2007) Compositae. In: Kadereit, J.W. & Jeffrey, C. (Eds.) Kubitzki’s The families and genera of vascular plants, vol. 8. Springer, Berlin, pp. 63–77. https://doi.org/10.1007/978-3-540-31051-8_7
  2. Arnott, G.A.W. (1836) Pugillus plantarum Indiae orientalis. Nova acta physico-medica Academiae Caesareae Leopoldino-Carolinae Naturae Curiosum 18: 319–356.
  3. Baldwin, B.G. (2009) Heliantheae alliance. In: Funk, V., Susanna, A., Stuessy, T.F. & Bayer, A. (Eds.) Systematics, evolution and biogeography of Compositae. IAPT, Vienna, pp. 689–711.
  4. Batista, M.F. & De Souza, L.A. (2017) A survey of ontogeny cypsela characters contributing to the infrafamilial characterization of Asteraceae. Journal of the Torrey Botanical Society 144: 296–302. https://doi.org/10.3159/TORREY-D-15-00035.1
  5. Beentje, H. (2016) Plant Glossary: An Illustrated Dictionary of Plant Terms, 2nd ed. Royal Botanic Gardens, Richmond.
  6. Blackmore, S., Wortley, H.A., Skvarla, J.J. & Robinson, H. (2009) Evolution of pollen in Compositae. In: Funk, V., Susanna, A., Stuessy, T.F. & Bayer, A. (Eds.) Systematics, evolution and biogeography of Compositae. IAPT, Vienna, pp. 101–126.
  7. Castro-Castro, A., Harker, M., Vargas-Amado, G. & Rodríguez, A. (2014) Análisis macromorfológico y citogenético del género Cosmos (Asteraceae, Coreopsideae), con una clave para su identificación. Botanical Sciences 92: 363–88. https://doi.org/10.17129/botsci.111
  8. Cavanilles, A.J. (1791) Icones et Descriptiones Plantarum, vol. 1. Typographia regia, Madrid, 67 pp.
  9. Crawford, D.J., Tadesse, M., Mort, M.E., Kimball, R.T. & Randle, C.P. (2009) Coreopsideae. In: Funk, V., Susanna, A., Stuessy, T.F. & Bayer, A. (Eds.) Systematics, evolution and biogeography of Compositae. IAPT, Vienna, pp. 713–727.
  10. Erdtman, G. (1960) The acetolysis method, a revised description. Svensk Botanisk Tidskrift 54: 561–564.
  11. Erdtman, G. (1969) Handbook of palynology: morphology, taxonomy, ecology; an introduction to the study of pollen grains and spores. Munksgaard, Copenhagen, 486 pp.
  12. Flora of North America Editorial Committee (Eds.) (1993 onwards) Flora of North America North of Mexico [Online], 25+ vols. New York & Oxford. Available from: http://beta.floranorthamerica.org (accessed 1 December 2023)
  13. Freitas, F.S., De-Paula, O.C., Nakajima, J.N. & Marzinek, J. (2015) Fruits of Heterocoma (Vernonieae-Lychnophorinae): Taxonomic significance and a new pattern of phytomelanin deposition in Asteraceae. Botanical Journal of the Linnean Society 179: 255–265. https://doi.org/10.1111/boj.12324
  14. Gray, A. (1853) Plantae Wrightianae Texano-Neo-Mexicanae: Part II. Smithsonian Contributions to Knowledge 5: 1–119.
  15. Gray, A. (1854) Plantae Novae Thurberianae: the characters of some new genera and species of plants in a collection made by George Thurber, of the late Mexican Boundary Commission, chiefly in New Mexico and Sonora. Memoirs of the American Academy of Arts and Sciences, ser. 2, 5: 297–328. https://doi.org/10.2307/25058183
  16. Halbritter, H., Ulrich, S., Grímsson, F., Weber, M., Zetter, R., Hesse, M., Buchner, R., Svojtka, M. & Frosch-Radivo, A. (2018) Illustrated Pollen Terminology. Springer International Publishing, 487 pp. https://doi.org/10.1007/978-3-319-71365-6
  17. Jana, B.K. & Mukherjee, S.K. (2014) Morpho-Anatomical features of cypselas in some species of the tribe Coreopsideae (Asteraceae). Journal of the Swamy Botanical Club 31: 386–393.
  18. Jana, B.K. & Mukherjee, S.K. (2018) Some Aspects and Prospects of Cypselar Features of Compositae. In: Viswanathan, M.B. (Ed.) Trends in Plant Systematics, 24th Annual Conference of Indian Association for Angiosperm Taxonomy (IAAT) and International Conference on Trends in Plant Systematics, pp. 127–143.
  19. Julio, P.G. dos Santos & Oliveira, D.M.T. (2009) Morfoanatomia comparada e ontogenese do pericarpo de Bidens gardneri Baker e B. pilosa L. (Asteraceae). Revista Brasileira de Botanica 32: 109–116. https://doi.org/10.1590/s0100-84042009000100011
  20. Kimball, R.T. & Crawford, D.J. (2004) Phylogeny of Coreopsideae (Asteraceae) using ITS sequences suggests lability in reproductive characters. Molecular Phylogenetics and Evolution 33: 127–139. https://doi.org/10.1016/j.ympev.2004.04.022
  21. La Llave, P. (1824) Novorum Vegetabilium Descriptiones, vol. 1. M. Rivera, Mexico, 32 pp.
  22. Lessing, C.F. (1830) Synanthereae Rich. Cass. In: De plantis in expeditione speculatoria Romanzoffiana observatis disserere pergunt A. de Chamisso, A. et D. de Schlechtendal. Linnaea 5: 128–164.
  23. Linnaeus, C. (1753) Species Plantarum. Salvius, Stockholm, 1200 pp.
  24. Lusa, M.G., Loeuille, B.F.P. & Apezzato-da-Glória, B. (2018) First record of phytomelanin in aerial vegetative organs and its evolutionary implications in Lychnophorinae (Vernonieae: Asteraceae). Perspectives in Plant Ecology, Evolution and Systematics 33: 18–33. https://doi.org/10.1016/j.ppees.2018.04.006
  25. Mamut, J. & Tan, D.Y. (2014) Gynomonoecy in angiosperms: phylogeny, sex expression and evolutionary significance. Chinese Journal of Plant Ecology 38: 76–90. https://doi.org/10.3724/SP.J.1258.2014.00008
  26. Marques, D., Bonfim e Cândido, J., Loeuille, B. & Marzinek, J. (2022) Comparative morphology and anatomy of cypselae in Piptolepis (Vernonieae, Asteraceae) with emphasis on the pappus systematic significance. Flora 287: 151988. https://doi.org/10.1016/j.flora.2021.151988
  27. Marques, D., Marzinek, J. & De-Paula, O.C. (2021) A new report of phytomelanin in cypselae of Vernonieae: the case of the type species of Lychnophora Mart. Anais da Academia Brasileira de Ciências 93: e20210204. https://doi.org/10.1590/0001-3765202120210204
  28. Márquez-Guzmán, J., Wong, R., Pérez, M., López, L. & Munguía, G. (2016) Técnicas de laboratorio para el estudio del desarrollo en angiospermas. Facultad de Ciencias, UMAM, México, 178 pp.
  29. Mathur, R.R. & Pandey, A.K. (2020) Development and structure of phytomelanin in Coreopsieae (Asteraceae). International Journal of Plant Reproductive Biology 12: 84–94. https://doi.org/10.14787/ijprb.202012.1
  30. Mort, M.E., Randle, C.P., Kimball, R.T., Tadesse, M. & Crawford, D.J. (2008) Phylogeny of Coreopsideae (Asteraceae) inferred from nuclear and plastid DNA sequences. Taxon 57: 109–120.
  31. Mukherjee, S.K. & Sarkar, A.K. (2001) Study of macro-morphological and anatomical structures of cypselas of eighteen taxa of the tribe Vernonieae (Asteraceae). Journal of the National Botanical Society 55: 85–104.
  32. O’Brien, T.P., Feder, N. & McCully, M.E. (1964) Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma 59: 368–373. https://doi.org/10.1007/BF01248568
  33. Pandey, A.K. & Singh, R.P. (1982) Development and structure of seeds and fruits in Compositae: Coreopsis species. Journal of the Indian Botanical Society 61: 417–425.
  34. Pandey, A.K., Stuessy, T.F. & Mathur, R.R. (2014) Phytomelanin and Systematics of the Heliantheae Alliance (Compositae). Plant Diversity and Resources 131: 145–165. https://doi.org/10.1127/1869-6155/2014/0131-0077
  35. Panero, J.L. (2007) Coreopsideae. In: Kadereit, J.W. & Jeffrey, C. (Eds.) Kubitzki’s The families and genera of vascular plants, vol. 8. Springer, Berlin, pp. 406–428.
  36. Robinson, H. (1981) A revision of the tribal and subtribal limits of the Heliantheae (Asteraceae). Smithsonian Contributions to Botany 1–102. https://doi.org/10.5479/si.0081024X.51
  37. Robinson, H. (2009) An introduction to micro-characters of Compositae. In: Funk, V., Susanna, A., Stuessy, T.F. & Bayer, A. (Eds.) Systematics, evolution and biogeography of Compositae. IAPT, Vienna, pp. 89–100.
  38. Roth, I. (1977) Fruits of angiosperms. Gebrüder Borntraeger, Berlin, 675 pp.
  39. Ryding, O. & Bremer, K. (1992) Phylogeny, distribution, and classification of the Coreopsideae (Asteraceae). Systematic Botany 17: 649–659. https://doi.org/10.2307/2419733
  40. Rzedowski, J. (1975) An Ecological and Phytogeographical Analysis of the Grasslands of Mexico. Taxon 24: 67–80. https://doi.org/10.2307/1219002
  41. Saar, D.E., Polans, N.O. & Sorensen, P.D. (2003) A phylogenetic analysis of the genus Dahlia (Asteraceae) based on internal and external transcribed spacer regions of nuclear ribosomal DNA. Systematic Botany 28: 627–639.
  42. Sánchez-Chávez, E., Rodríguez, A., Castro-Castro, A., Pérez-Farrera, M.A. & Sosa, V. (2019) Spatio-temporal evolution of climbing habit in the Dahlia-Hidalgoa group (Coreopsideae, Asteraceae). Molecular Phylogenetics and Evolution 135: 166–176. https://doi.org/10.1016/j.ympev.2019.03.012
  43. Sánchez-Chávez, E., Vovides, A.P. & Sosa, V. (2022) Pollen morphology of the genera Hidalgoa and Dahlia (Coreopsideae, Asteraceae): implications for taxonomy. PhytoKeys 199: 187–202. https://doi.org/10.3897/phytokeys.199.79501
  44. Sánchez-Chávez, E., Vovides, A.P., Castro-Castro, A. & Sosa, V. (2023) Cypselae in Dahlia and Hidalgoa (Asteraceae: Coreopsideae): anatomical and morphological differences. Flora 303: 152289. https://doi.org/10.1016/j.flora.2023.152289
  45. Sherff, E.E. (1937) Some Compositae of southeastern Polynesia (Bidens, Coreopsis, Cosmos, and Oparanthus). Occasional Papers of the Bernice Pauahi Bishop Museum of Polynesian Ethnology and Natural History 12 (19): 1–19.
  46. Souza-Filho, P.R., de Moura, Bianchessi, S.B., Yamaguchi, L.F., Kato, M.J., Coan, A.I. & Takaki, M. (2019) The role of pericarp in Bidens L. heterocarpy (Asteraceae). Flora 257: 151426. https://doi.org/10.1016/j.flora.2019.151426
  47. Stuessy, T.F. (1973) Systematic Review of the Subtribe Melampodiinae (Compositae. Heliantheae). Contributions from the Gray Herbarium of Harvard University 203: 65–80. https://doi.org/10.5962/p.336432
  48. Stuessy, T.F. (1975) A revision of Moonia (Compositae, Heliantheae, Coreopsidinae). Brittonia 27 (2): 97–102. https://doi.org/10.2307/2805467
  49. Stuessy, T.F. (1977) Heliantheae: Systematic Review. In: Heywood, V.H., Harborne, J.B. & Turner, B.L. (Eds.) The Biology and Chemistry of the Compositae. London and New York. Academic Press, pp. 621–671.
  50. Tadesse, M. (1984) The genus Bidens (Compositae) in NE Tropical Africa. Symbolae Botanicae Upsalienses 24: 1–138.
  51. Tadesse, M. (1986) The Morphological basis for the inclusion of African species of Coreopsis L. in Bidens L. (Compositas—Heliantheae). Symbolae Botanicae Upsalienses 26: 189–203.
  52. Tadesse, M. & Crawford, D.J. (2014) The phytomelanin layer in traditional members of Bidens and Coreopsis and phylogeny of the Coreopsideae (Compositae). Nordic Journal of Botany 32: 80–91. https://doi.org/10.1111/j.1756-1051.2011.001714.x
  53. Tadesse, M., Crawford, D.J. & Smith, E.B. (1995a) Comparative capitular morphology and anatomy of Coreopsis L. and Bidens L. (Compositae), including a review of generic boundaries. Brittonia 47: 61–91. https://doi.org/10.2307/2807249
  54. Tadesse, M., Crawford, D.J. & Smith, E.B. (1995b) Pollen morphology of North American Coreopsis (Compositae—Heliantheae). Grana 34: 21–27. https://doi.org/10.1080/00173139509429029
  55. Tellería, M.C. (2017) Spines vs. microspines: An overview of the sculpture exine in selected basal and derived Asteraceae with focus on Asteroideae. Journal of Plant Research 130: 1023–1033. https://doi.org/10.1007/s10265-017-0956-y
  56. Turner, B.L. (1978) New Species and Combinations in the Genera Sigesbeckia and Trigonospermum (Compositae: Melampodiinae). Brittonia 30: 64–68. https://doi.org/10.2307/2806460
  57. Turner, B.L. (2010) The Comps of Mexico. A systematic account of the family Asteraceae (Chapter 10: Subfamily Coreopsideae). Phytologia Memoirs 1: 1–224.
  58. Turner, B.L. & Johnston, M.C. (1956) Chromosome numbers and geographic distribution of Lindheimera, Engelmannia, and Berlandiera (Compositae-Heliantheae-Melampodinae). Southwestern Naturalist 1: 125–132. https://doi.org/10.2307/3669135
  59. Turner, B.L. & King, R.M. (1962) A cytotaxonomic survey of Melampodium (Compositae-Heliantheae). American Journal of Botany 49: 263–269. https://doi.org/10.2307/2439548
  60. Wodehouse, R.P. (1930) The origin of the six-furrowed configuration of Dahlia pollen grains. Bulletin of the Torrey Botanical Club 57: 371–380. https://doi.org/10.2307/2480640