Functional role and evolutionary contributions of floral gland morphoanatomy in the Paleotropical genus Acridocarpus (Malpighiaceae)
Autoři:
Isabel Reis Guesdon aff001; André Márcio Amorim aff002; Renata Maria Strozi Alves Meira aff001
Působiště autorů:
Universidade Federal de Viçosa, UFV, Departamento de Biologia Vegetal, Viçosa, Minas Gerais, Brazil
aff001; Universidade Estadual de Santa Cruz, UESC, Departamento de Ciências Biológicas, Ilhéus, Bahia, Brazil
aff002; Herbário Centro de Pesquisas do Cacau, CEPEC, Itabuna, Bahia, Brazil
aff003
Vyšlo v časopise:
PLoS ONE 14(9)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0222561
Souhrn
The stereotyped floral morphology of Neotropical Malpighiaceae species—zygomorphic and calyx with oil glands—is correlated with oil-bee pollination. In contrast, the floral trends of the Paleotropical lineages are actinomorphy and lack of calyx glands, probably due to the absence of oil-collecting bees. The Paleotropical genus Acridocarpus is an exception because of its zygomorphic, gland-bearing flowers. Glands throughout Acridocarpus inflorescences were morphoanatomically evaluated to verify the occurrence of patterns related to species and geographic distribution. Herbarium (25 species) and fresh samples of A. longifolius were processed according to standard anatomical techniques. To verify the presence of glucose and protein, strip tests were applied to the exudate. Fresh samples were fixed and submitted to histochemical tests. Based on the occurrence, number and placement of glands, three distribution patterns were recognized on the bracteole and ten on the calyx. Bract, bracteole and sepal glands have a typical nectary structure with a palisade-like epidermis and vascularized parenchyma. Glands were classified as short-stalked, sessile or immersed. Histochemical tests performed on bract and sepal glands of A. longifolius were positive for proteins, polysaccharides and phenolic compounds, and negative for oil compounds. Glucose and protein were detected in the exudate. These results allow us to recognize the glands in Acridocarpus inflorescences as nectaries. This comprehensive morphoanatomical study helps to clarify the correlation between patterns of floral morphology and secretion consumers, as well as to better understand floral evolution in Malpighiaceae across their dispersal events.
Klíčová slova:
Biology and life sciences – Plant science – Anatomy – Integumentary system – Skin – Epidermis – Medicine and health sciences – Physiology – Physiological processes – Earth sciences – Plant anatomy – Secretion – Paleontology – Paleobiology – Flower anatomy – Sepals – Calyx – Petals – Nectaries – Inflorescences
Zdroje
1. Vogel S. History of the Malpighiaceae in the light of Pollination Ecology. Memoirs of the New York Botanical Garden. 1990; 55: 130–142.
2. Anderson WR. Floral conservation in Neotropical Malpighiaceae. Biotropica. 1979; 11: 219–223.
3. Davis CC, Anderson WR. A complete generic phylogeny of Malpighiaceae inferred from nucleotide sequence data and morphology. American Journal of Botany. 2010; 97: 2031–2048. doi: 10.3732/ajb.1000146 21616850
4. Anderson WR. Malpighiaceae. In: Berry PE, Yatskievych K, Holst BK editors. Flora of the Venezuelan Guayana. Saint Louis: Missouri Botanical Garden; 2001. pp. 82–185.
5. Anderson WR. Malpighiaceae. In: Smith N et al. editors. Flowering Plants of the Neotropics. New Jersey: Princeton; 2004. pp. 229–232.
6. Davis CC, Bell CD, Mathews S, Donoghue MJ. Laurasian migration explains Gondwanan disjunctions: evidence from Malpighiaceae. Proceedings of the National Academy of Sciences. 2002; 99: 6833–6837.
7. Davis CC, Bell CD, Fritsch PW, Mathews S. Phylogeny of Acridocarpus—Brachylophon (Malpighiaceae): implications for Tertiary tropical floras and Afroasian biogeography. Evolution. 2002; 56: 2395–2405. 12583580
8. Davis CC, Schaefer H, Xi Z, Baum DA, Donoghue MJ, Harmon LJ. Long-term morphological stasis maintained by a plant–pollinator mutualism. Proceedings of the National Academy of Sciences. 2014; 111: 5914–5919.
9. Anderson WR. The origin of the Malpighiaceae-The evidence from morphology. Memoirs of the New York Botanical Garden.1990; 64: 210–224.
10. Raven PH, Axelrod DI. Angiosperm biogeography and past continental movements. Annals of the Missouri Botanical Garden.1974; 61: 39–637.
11. Lobreau-Callen D. Les Malpighiaceae et leurs pollinisateurs. Coadaptation ou coevolution. Bulletin du Muséum National d'Histoire Naturelle, Adansonia. 1989; 1: 79–94.
12. Ren M, Zhong Y, Song X. Mirror-image flowers without buzz pollination in the Asian endemic Hiptage benghalensis (Malpighiaceae). Botanical Journal of the Linnean Society. 2013; 173: 764–774.
13. Michener CD. The bees of the world. Baltimore: The John Hopkins University Press; 2000.
14. Anderson WR. Malpighiaceae. The Botany of the Guayana Highland, part XI. Memoirs of the New York Botanical Garden.1981; 32: 137–147.
15. Buchmann SL. The ecology of oil flowers and their bees. Annual Review of Ecology and Systematics. 1987; 18: 343–369.
16. Endress PK. Diversity and evolutionary biology of tropical flowers. Cambridge: University Press.; 1996.
17. Sigrist MR, Sazima M. Pollination and reproductive biology of twelve species of neotropical Malpighiaceae: stigma morphology and its implications for the breeding system. Annals of Botany. 2004; 94: 33–41. doi: 10.1093/aob/mch108 15194562
18. Simpson BB, Neff JL. Floral rewards: alternatives to pollen and nectar. Annals of the Missouri Botanical Garden. 1981; 68: 301–322.
19. Vinson SB, Williams HJ, Frankie GW, Shrum G. Floral lipid chemistry of Byrsonima crassifolia (Malpighiaceae) and a use of floral lipid by Centris bees (Hymenopotera: Apidae). Biotropica. 1997; 29: 76–83.
20. Zhang W, Kramer EM, Davis CC. Floral symmetry genes and the origin and maintenance of zygomorphy in a plant-pollinator mutualism. Proceedings of the National Academy of Sciences. 2010; 107: 6388–6393.
21. Niedenzu F. De genere Acridocarpo. Arbeiten aus dem botanischen Institut der Staatlichen Akademie (vorm. Kgl. Lyceum hosianum). Braunsberg: Ostpreussen; 1921.
22. Niedenzu F. Malpighiaceae. In: Engler A. editor. Das Pflanzenreich. Leipzig: Verlag von Wilhelm Engelmann; 1928. pp. 1–870.
23. Launert E. Malpighiaceae. In: Edwards S. et al. editor. Flora of Ethiopia and Eritrea. Uppsala: The National Herbarium, Addis Ababa and the Department of Systematic Botany; 1995. pp. 257–263.
24. Johansen DA. Plant Microtechnique. New York: Mc Graw-Hill Book Co. Inc.; 1940.
25. Smith FH, Smith EC. Anatomy of the inferior ovary of Darbya. American Journal of Botany. 1942; 29: 464–471.
26. O’Brien TP, Feder N, McCully ME. Polycromatic staining of plant cell walls by toluidina blue O. Protoplasma. 1964; 59: 368–373.
27. Clark SG. Staining procedures. Baltimore: Williams and Wilkins; 1981.
28. Fisher DB. Protein staining of ribboned epon sections for light microscopy. Histochemistry and Cell Biology.1968; 16: 92–96.
29. McManus JFA. Histological and histochemical uses of periodic acid. Stain Technology. 1948; 23: 99–108. doi: 10.3109/10520294809106232 18867618
30. Pearse AGE. Histochemistry Theoretical and Applied, 4th ed. Edinburgh: Churchill Livingston; 1980.
31. Arènes J. Malpighiacées. In: Flore de Madagascar et des Comores. Catalogue of Vascular Plants of Madagascar, Tropicos.org, Missouri, Portland. 1950. vol. 108: 1–176.
32. Arènes J. Un Acridocarpus nouveau de Madagascar. Notulae Systematicae. 1955 ["1954"]; 15: 4–5.
33. Launert E. Malpighiaceae. Flora of tropical East Africa. British Museum (Natural History). 1968; 1–26.
34. Wilczek R. Malpighiaceae. In: Robyns W, Staner P, Demaret F, Germain R, Gilbert G, Hauman L. et al. editors. Flore du Congo-Belge et du Ruanda-Urundi. Bruxelles: Institut National pour l´Etude Agronomique du Congo belge; 1958. 214–234.
35. Hutchinson J, Dalziel JM. Malpighiaceae In: Keay RWJ, Hepper FN editors. Flora of West tropical Africa, London: Crown Agents; 1958. pp. 350–354.
36. Oliver D. Malpighiaceae. In: Oliver D editor. Flora of tropical Africa. London: L. Reeve and Co.; 1868. pp. 276–282.
37. Launert E. Malpighiaceae. In: Exell AW et al. editors. Flora zambesiaca. London: Crow Agentes; 1963. pp. 109–225.
38. Birnbaum P, Florence J. Validation d'Acridocarpus monodii Arènes & Jaeger ex Birnbaum & J. Florence, sp. nov. (Malpighiaceae). Notes sur biologie. Adansonia. 2005; 27: 235–241.
39. Guillemin JA, Perrottet S, Richard A. Malpighiaceae. Acridocarpus. Florae Senegambiae tentamen, Paris, vol. 29: 123–124. 1831.
40. Doorn-Hoekman H. van. Rhinopteryx Niedenzu and Acridocarpus (G.Don) Guill. et. Perr. (Malpighiaceae) united. Acta Botanica Neerlandica. 1975; 24: 69–82.
41. Wilczek R. Novitates africanae I (Malpighiaceae et Linaceae). Bulletin du Jardin botanique de l'état Bruxelles. 1955; 25: 303–313.
42. Thulin M. Malpighiaceae. In: Thulin M editor. Flora of Somalia. Kew: Royal Botanic Gardens; 1993. pp. 260–264
43. Vogel S. Ölblumen und ölsammelnde Bienen. Tropische und subtropische Pflanzenwelt. 1974; 7: 283–547.
44. Possobom CCF, Guimarães E, Machado SR. Structure and secretion mechanisms of floral glands in Diplopterys pubipetala (Malpighiaceae) and a Neotropical species. Flora. 2015; 211: 36–39.
45. Araújo JS, Meira RMSA. Comparative anatomy of calyx and foliar glands of Banisteriopsis C. B. Rob. (Malpighiaceae). Acta Botanica Brasilica. 2016; 30: 112–123.
46. Possobom CCF, Machado SR. Elaiophores in three Neotropical Malpighiaceae species: a comparative study. Plant Systematics and Evolution. 2017; 304: 15–32.
47. Guesdon IR. Estruturas secretoras em linhagens Neo e Paleotropicais de Malpighiaceae: morfoanatomia, evidências funcionais e contribuições taxonômicas e evolutivas. Doctoral thesis. Universidade Federal de Viçosa. 2017.
48. Arumugasamy K, Inamdar JA, Subramanian RB. Structure, ontogeny and secretion of oil secreting glands in Hiptage acuminate. Current Science. 1989; 58: 260–261.
49. Arumugasamy K, Udaiyan K, Manian S, Sugavanam V. Ultrastructure and oil secretion in Hiptage sericeae Hook. Acta Societatis Botanicorum Poloniae.1993; 62: 17–20.
50. Subramanian RB, Arumugasamy K, Inamdar JS. Studies in secretory glands of Hiptage sericea (Malpighiaceae). Nordic Journal of Botany. 1990; 10: 57–62.
51. Almeida RF, Guesdon IR, Pace MR, Meira RMSA. Taxonomic revision of Mcvaughia W.R.Anderson (Malpighiaceae): notes on vegetative and reproductive anatomy and the description of a new species. PhytoKeys. 2019; 117: 45–72.
52. Guesdon IR, Amorim AMA, Meira RMSA. The hydrochorous Amazonian genus Glandonia (Malpighiaceae): New records, morphoanatomy update, and taxonomic contributions. Phytotaxa. 2018; 345: 13–25.
53. Castro MA, Veja AS, Mulgura ME. Structure and ultrastructure of leaf and calyx glands in Galphimia brasiliensis (Malpighiaceae). American Journal of Botany. 2001; 88: 1935–1944. 21669626
54. Possobom CCF, Guimarães E, Machado SR. Leaf glands act as nectaries in Diplopterys pubipetala (Malpighiaceae). Plant Biology. 2010; 12: 863–870. doi: 10.1111/j.1438-8677.2009.00304.x 21040301
55. Cocucci AA, Holgado AM, Anton AM. Estudio morfologico y anatomico de los eleoforos pedicelados de Dinemandra ericoides, Malpighiacea endemica del desierto de Atacama, Chile. Darwiniana. 1996; 34: 183–192.
56. Elias TS. Foliar nectaries of unusual structure in Leonardoxa africana (Leguminosae) an African obligate myrmecophyte. American Journal of Botany. 1980; 67: 423–425.
57. Gonzalez AM, Marazzi B. Extrafloral nectaries in Fabaceae: filling gaps in structural and anatomical diversity in the family. Botanical Journal of the Linnean Society. 2018; 20: 1–20.
58. Lanza J. Response of fire ants (Formicidae: Solenopsis invicta and S. geminata) to artificial nectars with amino acids. Ecological Entomology. 1991; 16: 203–210.
59. González-Teuber M, Heil M. The role of extrafloral nectar amino acids for the preferences of facultative and obligate ant mutualists. Journal of Chemical Ecology. 2009; 35:459–68. doi: 10.1007/s10886-009-9618-4 19370376
60. Ness JH, Morris W, Bronstein JL. For ant-protected plants, the best defense is a hungry offense. Ecology. 2009; 90: 2823–2831. doi: 10.1890/08-1580.1 19886490
61. Sudd JH, Sudd ME. Seasonal changes in the response of wood-ants (Formica lugubris) to sucrose baits. Ecological Entomology. 1985; 10: 89–97.
62. Baker-Méio B, Marquis RJ. Context-dependent benefits from ant–plant mutualism in three sympatric varieties of Chamaecrista desvauxii. Journal of Ecology. 2012; 100: 242–252.
63. Nicolson SW, Thornburg RW. Nectar chemistry. In: Nicolson SW, Nepi M, Pacini E. editors. Nectaries and Nectar. Dordrecht: Springer; 2007. pp. 215–63.
64. Fahn A. Plant Anatomy, 4 ed. Oxford: Pergamon Press; 1990.
65. Nery LA, Vieira MF, Ventrella MC. Leaf glands of Banisteriopsis muricata (Malpighiaceae): distribution, secretion composition, anatomy and relationship to visitor. Acta Botanica Brasilica. 2017; 31: 459–467.
66. McKey D. The distribution of secondary compounds within plants. In: Rosenthal G.A. & Janzen D.H. [eds.], Herbivores: Their Interactions with Secondary Plant Metabolites, 55–133. New York: Academic Press.; 1979.
67. Teixeira LAG, Machado IC. Sistemas de polinização e reprodução de Byrsonima sericea DC (Malpighiaceae). Acta Botanica Brasilica. 2000; 14: 347–357.
68. Anderson C. Revision of Galphimia (Malpighiaceae). Contribution from University Michigan Herbarium. 2007; 25: 1–82.
69. Anderson WR, Corso S. Psychopterys, a new genus of Malpighiaceae from Mexico and Central America. Contribution from University Michigan Herbarium. 2007; 25: 113–135.
70. Chen S, Funston M. Malpighiaceae. Flora of China, 2008; 11: 132–138. http://flora.huh.harvard.edu/china/mss/volume11/Malpighiaceae.pdf (Accessed 23 May. 2019).
71. Sazima M, Sazima I. Oil-gathering bees visit flowers of eglandular morphs of the oil-producing Malpighiaceae. Botanica Acta. 1989; 102: 106–111.
72. Carvalho PD, Borba EL, Lucchese AM. Variação no número de glândulas e produção de óleo em flores de Stigmaphyllon paralias A. Juss. (Malpighiaceae). Acta Botanica Brasilica. 2005; 19: 209–214.
73. Souto LS, Oliveira DMT. Evaluation of the floral vasculature of the Janusia, Mascagnia and Tetrapterys species as a tool to explain the decrease of floral organs in Malpighiaceae. Flora. 2013; 208: 351–359.
Článok vyšiel v časopise
PLOS One
2019 Číslo 9
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Těžké menstruační krvácení může značit poruchu krevní srážlivosti. Jaký management vyšetření a léčby je v takovém případě vhodný?
- Fixní kombinace paracetamol/kodein nabízí synergické analgetické účinky
Najčítanejšie v tomto čísle
- Graviola (Annona muricata) attenuates behavioural alterations and testicular oxidative stress induced by streptozotocin in diabetic rats
- CH(II), a cerebroprotein hydrolysate, exhibits potential neuro-protective effect on Alzheimer’s disease
- Comparison between Aptima Assays (Hologic) and the Allplex STI Essential Assay (Seegene) for the diagnosis of Sexually transmitted infections
- Assessment of glucose-6-phosphate dehydrogenase activity using CareStart G6PD rapid diagnostic test and associated genetic variants in Plasmodium vivax malaria endemic setting in Mauritania