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The Botanical Review

, Volume 84, Issue 3, pp 203–241 | Cite as

Evolution of Stem and Leaf Structural Diversity: a Case Study in Lychnophorinae (Asteraceae)

  • Makeli Garibotti Lusa
  • Benoit Francis Patrice Loeuille
  • Daniela Ciccarelli
  • Beatriz Appezzato-da-Glória
Article
  • 105 Downloads

Abstract

Lychnophorinae occurs mainly in campos rupestres and cerrados of the Cerrado Domain (Brazil) and are species subject to fire occurrences and intense solar radiation, occupying acid and well-drained soils. Informative characters on the taxonomy of this subtribe were studied considering the leaf and stem morphology and anatomy. In addition, putative synapomorphies and features that probably determined the success of these species in occupying these habitats were identified. Samples of leaves and stems of 52 species were analyzed using usual techniques in plant anatomy. The reconstruction of ancestral states of characters was made in parsimony analysis using the phylogeny established for Lychnophorinae. The analyses indicated two distinct types of stems and a wide variation in foliar features, with the possible occurrence of three synapomorphies for the stems and 11 for the leaves. Adaptive pressures of restricted environments, where most species live, probably directed the evolution of morphological and anatomical diversity in Lychnophorinae.

Keywords

Synapomorphies Morphology Anatomy Campos rupestres Cerrados 

Notes

Acknowledgements

We thank the IEF, MG, Brazil, for granting permission and facilities to collect plant material for this study. This work was supported by the National Council for Scientific and Technological Development (CNPq) - grants [Proc. n° 302776/2010-9] and the São Paulo Council for Research (FAPESP) - financial support [Thematic Project Proc. no. 2010/51454-3] and grants for the first author [Proc. no. 2010/02085-5].

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Literature Cited

  1. Alcorn, S. M. & P. A. Ark . 1953. Softening paraffin-embedded plant tissues. Stain Technology 28: 55–56.Google Scholar
  2. Alves, R. J. & N. G. Silva . 2011. O fogo é sempre um vilão nos campos rupestres? Biodiversidade Brasileira 1:120–127.Google Scholar
  3. Baruch, Z. 1979. Elevation differentiation in Espeletia schultzii (Compositae), a giant rosette plant of the venezuelan Paramos. Ecology 60: 85–98.Google Scholar
  4. ——— & A. P. Smith . 1979. Morphological and physiological correlates of niche breadth in two species of Espeletia (Compositae) in the Venezuelan Andes. Oecologia 38: 71–82.Google Scholar
  5. Beierkuhnlein, C. & A. Jentsch . 2005. Ecological importance of species diversity. In: R. J. Henry (ed.). Diversity and evolution genotypic and phenotypic variation in higher plants. Wallingford: CABI publishing, 249–285.Google Scholar
  6. Coile, N. C. & S. B. Jones Jr . 1981. Lychnophora (Compositae: Vernonieae), a genus endemic to the brazilian planalto. Brittonia 33: 528–542.Google Scholar
  7. Cox, G., C. R. Hawes, L. Van der Lubbe & B. E. Juniper . 1987. High-voltage electron microscopy of whole, critical-point dried plant cells. 2. Cytoskeletal structures and plastid motility in Selaginella. Protoplasma 140: 173–186.Google Scholar
  8. Cuatrecasas, J. 1933. Plantae colombianae novae. Trabajos del Museo de Ciencias Naturales - Serie Botanica 33: 1–158.Google Scholar
  9. ——— 2013. A systematic study of the subtribe Espeletiinae (Heliantheae, Asteraceae). New York, New York Botanical Garden Press.Google Scholar
  10. Dantas, V. L. & M. A. Batalha . 2011. Vegetation structure: fine scale relationships with soil in a cerrado site. Flora 206: 341–346.Google Scholar
  11. De Pinna, M. C. C . 1991. Concepts and tests of homology in the cladistic paradigm. Cladistics 7: 367–394.Google Scholar
  12. Echternacht, L., M. Trovó, C. T. Oliveira & J. R. Pirani . 2011. Areas of endemism in the Espinhaço range in Minas Gerais, Brazil. Flora 206:782–791.Google Scholar
  13. Fahn, A. & D. F. Cutler. 1992. Xerophytes. Berlin/Stuttgart, Gebrüder Borntraeger.Google Scholar
  14. Fujinami, R., I. Yoshihama & R. Imaichi . 2011. Dimorphic chloroplasts in the epidermis of Podostemoideae, a subfamily of the unique aquatic angiosperm family Podostemaceae. Journal of Plant Research 124: 601–605.Google Scholar
  15. Funk, V. A., A. Susanna, T. F. Stuessy & H. Robinson . 2009. Classification of Compositae. In: V. A. Funk, A. Susanna, T. F. Stuessy & R. J. Bayer (eds). Systematics, Evolution and Biogeography of Compositae. Vienna, Austria: International Association for Plant Taxonomy (IAPT), 171–189.Google Scholar
  16. Gardoni, L. C. P., R. M. S. Isaias & F. H. A. Vale . 2007. Morfologia e anatomia foliar de três morfotipos de Marcetia taxifolia (A. St.-Hil.) DC. (Melastomataceae) na Serra do Cipó, MG. Revista Brasileira de Botânica 30: 487–500.Google Scholar
  17. Giulietti, A. M., J. R. Pirani & R. M. Harley . 1997. Espinhaço Range Region. In: S. D. Davis, V. H. Heywood, O. Herrera-MacBride, J. Villa-Lobos & A. C. Hamilton (eds). Centres of Plant Diversity: a guide and strategy for their conservation. Vol. 3: The Americas. Cambridge, WWF-IUCN, 397–404.Google Scholar
  18. Givnish, T. J., R. W. McDiarmid & W. R. Buck . 1986. Fire adaptation in Neblinaria celiae (Theaceae), a high-elevation rosette shrub endemic to a wet equatorial tepui. Oecologia 70: 481–485.Google Scholar
  19. Goodland, R. & M. G. Ferri . 1979. Ecologia do Cerrado. São Paulo, Editora da Universidade de São Paulo.Google Scholar
  20. Gregory, M. & P. Baas. 1989. A survey of mucilage cells in vegetative organs of the dicotyledons. Israel Journal of Botany 38:125–174.Google Scholar
  21. Hughes, J. & M. E. McCull . 1975. The use of an optical brightener in the study of plant structure. Stain Technology 50: 319–329.Google Scholar
  22. Jensen, W. A. 1962. Botanical histochemistry: principle and practice. San Francisco, W. H. Freeman.Google Scholar
  23. Karnovsky, M. J. 1965. A Formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. The Journal of cell Biology 27: 137a-138a.Google Scholar
  24. Keeley, S. C. & H. Robinson. 2009. Vernonieae. In: V. A. Funk, A. Susanna, T. F. Stuessy & R. J. Bayer (eds). Systematics, evolution and biogeography of compositae. Michigan, Sheridan books, 439–469.Google Scholar
  25. ———, Z. H. Forsman & R. Chan . 2007. A phylogeny of the “evil tribe” (Vernonieae: Compositae) reveals old/new world long distance dispersal: support from separate and combined congruent datasets (trnL-F, ndhF, ITS). Molecular Phylogenetics and Evolution 44: 89–103.Google Scholar
  26. Kriebel, R., F. A. Michelangeli & L. M. Kelly . 2015. Discovery of unusual anatomical and continuous characters in the evolutionary history of Conostegia (Miconieae: Melastomataceae). Molecular Phylogenetics and Evolution 82: 289–313.Google Scholar
  27. Loeuille, B. 2011. Towards a phylogenetic classification of Lychnophorinae (Asteraceae: Vernonieae). Tese. Universidade de São Paulo, São Paulo, Brasil.Google Scholar
  28. ———, S. C. Keeley & J. R. Pirani. 2015a. Systematics and evolution of syncephaly in American Vernonieae (Asteraceae) with emphasis on the Brazilian subtribe Lychnophorinae. Systematic Botany 40: 286–298.Google Scholar
  29. ———, J. Semir, L. G. Lohmann & J. R. Pirani . 2015b. A phylogenetic analysis of Lychnophorinae (Asteraceae: Vernonieae) based on molecular and morphological data. Systematic Botany 40: 299–315.Google Scholar
  30. Luque, R. & N. L. Menezes . 2003. Anatomia foliar de Lychnophora Mart.(Vernonieae: Asteraceae). Plantula 3: 117–128Google Scholar
  31. ———, ——— & J. Semir. 1999. Estructura primaria del tallo de Lychnophora Mart.(Vernonieae: Asteraceae). Plantula 2: 141–152Google Scholar
  32. Lusa, M. G., B. Appezzato-da-Glória, B. Loeuille, G. Bartoli & D. Ciccarelli . 2014. Functional groups in Lychnophorinae (Asteraceae: Vernonieae) based on morphological and anatomical traits. Australian Journal of Botany 62: 150–163.Google Scholar
  33. ———, E. C. Cardoso, S. R. Machado & B. Appezzato-da-Glória . 2015. Trichomes related to an unusual method of water retention and protection of the stem apex in an arid zone perennial species. AoB PLANTS 7: plu088.Google Scholar
  34. ———, M. E. P. Martucci, B. Loeuille, L. Gobbo-Neto, B. Appezzato-da-Glória & F. B. Da Costa . (2016). Characterization and evolution of secondary metabolites in Brazilian Vernonieae (Asteraceae) assessed by LC-MS fingerprinting. The Botanical Journal of the Linnean Society 182(3): 594–611. Google Scholar
  35. Maddison, W. P. & D. R. Maddison. 2014. Mesquite: a modular system for evolutionary analysis. http://mesquiteproject.org.
  36. Mello-Silva, R . 1990. Morphological and anatomical differentiation of Vellozia hirsuta populations (Velloziaceae). Plant Systematics and Evolution 173: 197–208.Google Scholar
  37. Melo-de-Pinna, G. F. A. 2004. Anatomia foliar de Richterago Kuntze (Mutisieae, Asteraceae). Acta botanica brasilica 18: 591–600.Google Scholar
  38. Minelli, A . 1993. Biological systematics: the state of the art. London, Chapman & Hall, 3–43.Google Scholar
  39. Nakajima, J. N., A. M. Teles, M. Ritter, C. A. Mondin, M. Dematteis, G. Heiden, X. B. Borges, V. L. Rivera, J. B. A. Bringer Jr, M. Saavedra, R. de-Cássia-Araújo-Pereira & M. R. C. Sales-de-Melo . 2009. Asteraceae. In: A. M. Giulietti, (ed). Plantas raras do Brasil: Conservação Internacional. Belo Horizonte. Universidade Estadual de Feira de Santana, 76–89.Google Scholar
  40. ———, M. Dematteis, B. Loeuille, et al. 2013. Asteraceae. In: G. Martinelli & M. A. Moraes (eds). Livro vermelho da flora do Brasil. Rio de Janeiro, Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, 203–286.Google Scholar
  41. Nogueira, A., J. H. L. El Ottra, E. Guimarães, S. R. Machado & L. G. Lohmann . 2013. Trichome structure and evolution in Neotropical lianas. Annals of Botany 112: 1331–1350.Google Scholar
  42. Oliveira, R. S., A. Abrahão, C. Pereira, G. S. Teodoro, M. Brum, S. Alcantara & H. Lambers . 2016. Ecophysiology of Campos Rupestres plants. In: G.W. Fernandes (ed). Ecology and conservation of mountaintop grasslands in Brazil. Cham, Springer International Publishing Switzerland, 227–272.Google Scholar
  43. Pace, M. R. & V. Angyalossy . 2013. Wood anatomy and evolution: a case study in the Bignoniaceae. International Journal of Plant Sciences 174: 1014–1048.Google Scholar
  44. ———, L. G. Lohmann & V. Angyalossy . 2011. Evolution of disparity between the regular and variant phloem in Bignonieae (Bignoniaceae). American Journal of Botany 98: 602–618.Google Scholar
  45. Panero, J. L., S. E. Freire, L. A. Espinar, B. S. Crozier, G. E. Barboza & J. J. Cantero . 2014. Resolution of deep nodes yields an improved backbone phylogeny and a new basal lineage to study early evolution of Asteraceae. Molecular phylogenetics and evolution 80: 43–53.Google Scholar
  46. Rapini, A., P. L. Ribeiro, S. Lambert & J. R. Pirani . 2008. A flora dos campos rupestres da Cadeia do Espinhaço. Megadiversidade 4: 15–23.Google Scholar
  47. Ratter, J. A., J. F. Ribeiro & S. Bridgewater . 1997. The Brazilian cerrado vegetation and threats to its biodiversity. Annals of Botany 80: 223–230.Google Scholar
  48. Sajo, M. G., M. G. L. Wanderley & L. M. Carvalho . 1995. Caracterização anatômica foliar para 14 espécies de Xyris L. (Xyridaceae) da Serra do Cipó, MG, Brasil. Acta Botanica Brasilica 9: 101–114.Google Scholar
  49. Sakai, W. S . 1973. Simple method for differential staining of paraffin embedded plant material using toluidine blue O. Stain Technology 48: 247–249.Google Scholar
  50. Sakurai, N., K. Domoto & S. Takagi . 2005. Blue-light-induced reorganization of the actin cytoskeleton and the avoidance response of chloroplasts in epidermal cells of Vallisneria gigantea. Planta 221: 66–74.Google Scholar
  51. Scatena, V., A. Giulietti, E. Borba & C. van den Berg . 2005. Anatomy of Brazilian Eriocaulaceae: correlation with taxonomy and habitat using multivariate analyses. Plant Systematics and Evolution 253: 1–22.Google Scholar
  52. Scotland, R. & R. T. Pennington . 2000. Homology and systematics: Coding characters for phylogenetic analysis. Systematics association special volumes. Boca Raton: CRC Press.Google Scholar
  53. Simon, M. F. & T. Pennington . 2012. Evidence for adaptation to fire regimes in the tropical savannas of the Brazilian Cerrado. International Journal of Plant Sciences 173:711–23.Google Scholar
  54. ———, R. Grether, L. P. Queiroz, C. Skema, R. T. Pennington & C. E. Hughes. 2009. Recent assembly of the cerrado, a neotropical plant diversity hotspot, by in situ evolution of adaptations to fire. Proceedings of the National Academy of science 106: 20.359–20.364.Google Scholar
  55. Skelton, R. P., J. J. Midgley, J. M. Nyaga, S. D. Johnson & M. D. Cramer. 2012. Is leaf pubescence of Cape Proteaceae a xeromorphic or radiation-protective trait? Australian Journal of Botany 60: 104–113.Google Scholar
  56. Smith, A. & T. Young . 1987. Tropical alpine plant ecology. Annual Review of Ecology and Systematics 18: 137–158.Google Scholar
  57. Turner, I. M . 1994. Sclerophylly - primarily protective? Functional Ecology 8: 669–675.Google Scholar
  58. Werker, E . 2000. Trichome diversity and development: Advances in botanical research incorporating advances in Plant Pathology 31: 1–35.Google Scholar
  59. Zwieniecki M. A. & C. K. Boyce . 2014. Evolution of a unique anatomical precision in angiosperm leaf venation lifts constraints on vascular plant ecology. Proceedings of the Royal Society of London B: Biological Sciences 281: 20132829.Google Scholar

Copyright information

© The New York Botanical Garden 2017

Authors and Affiliations

  • Makeli Garibotti Lusa
    • 1
    • 2
  • Benoit Francis Patrice Loeuille
    • 3
  • Daniela Ciccarelli
    • 4
  • Beatriz Appezzato-da-Glória
    • 1
  1. 1.Departamento de Botânica, Centro de Ciências BiológicasUniversidade Federal de Santa CatarinaFlorianópolisBrazil
  2. 2.Programa de Pós-graduação em Biologia Vegetal, Instituto de BiologiaUniversidade Estadual de CampinasSão PauloBrazil
  3. 3.Departamento de Botânica, Centro de Ciências BiológicasUniversidade Federal do PernambucoPernambucoBrazil
  4. 4.Dipartimento di BiologiaUniversità di PisaPisaItaly

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