ACTUAL STATE OF CARPOLOGICAL STUDIES IN THE CAMPANULACEAE JUSS. WITH REGARD TO ITS SYSTEMATICS

R. Andreychuk, A. Odintsova


DOI: http://dx.doi.org/10.30970/sbi.1402.616

Abstract


The systems of the Campanulaceae Juss. introduced by the end of the 20th century used external morphological characteristics of the fruit. However, they significantly differed one from another by the number of subfamilies and tribes. In the system of Campanulaceae s. str. A. Kolakovsky (1995) distinguished four subfamilies, 22 tribes, and 49 genera on the basis of carpological features. Due to this fact, his system is “artificial” and does not correlate with other treatments of this family. The carpological system of Campanulaceae s. str. resulted from the detailed classification of fruits proposed by A. Kolakovsky that reflected the tiniest differences in the mode of formation of openings in the capsule, the location of lignified tissues (axicorns) and the shape of the axicorns. A. Kolakovsky distinguished 43 types of fruits, combined into two groups: non-axicorn-type and axicorn-type. Unfortunately, this classification proposed essential fragmentation of genera and establishment of many new taxa that are not acceptable at present. Molecular and complex studies have led to the integration of Campanulaceae s. str. with related families and the recognition of Campanulaceae s. l. consisting of five subfamilies: Campanuloideae Burnett, Cyphioideae (A. DC.) Walp., Cyphocarpoideae Miers, Lobelioideae Burnett and Nemacladoideae Lammers. The most primitive and diverse in carpological aspect is Campanuloideae that is characterized by superior and inferior, isomerous and oligomerous, dry and fleshy, dehiscent and indehiscent fruits. The fruits in the other four subfamilies are mostly dimerous, superior or semi-inferior, low-seeded, loculicidal capsules with apical valves. Researchers of the Campanulaceae use inconsistent fruit classifications, therefore, only several examples of applying the carpological data to taxonomy are known at generic and infrageneric level. Some features of the Campanulaceae have not been properly studied, in particular: vertical zonation of the gynoecium, placentation, the ovary position and anatomy of the fruit wall. Therefore, the state of knowledge on the evolutionary carpology of Campanulaceae is unsatisfactory. For possible usage of the carpological information in systematics of the Campanulaceae family, it is important to conduct complex studies of fruits as the terminal stage of the flower morphogenesis.


Keywords


bellflower family, subfamily, tribe, axicorn, capsule, fruit dehiscence

References


1. Andreychuk R., Odintsova A. Morphological and anatomical structure of Campanula latifolia L. fruits. Studia Biologica, 2019; 13(1): 95-105.
Crossref ● Google Scholar

2. Angiosperm Phylogeny Group. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical Journal of the Linnean Society, 2016; 181(1): 1-20.
Crossref ● Google Scholar

3. Antonelli A. Higher level phylogeny and evolutionary trends in Campanulaceae subfam. Lobelioideae: Molecular signal overshadows morphology. Molecular Phylogenetics and Evolution, 2008; 46: 1-18.
Crossref ● PubMed ● Google Scholar

4. Bobrov A.V., Melikian A.P., Romanov M.S. Morphogenesis of fruits of Magnoliophyta. Moscow: Librokom, 2009. 400 p. (In Russian)

5. Bobrov A.V., Romanov M.S. Morphogenesis of fruits and types of fruit of angiosperms. Bota­ny Letters, 2019; 166(3): 366-399.
Crossref ● Google Scholar

6. Borsch T., Korotkova N., Raus T., Lobin W., Löhne C. The petD group II intron as a species level marker: utility for tree inference and species identification in the diverse genus Campanula (Campanulaceae). Willdenowia, 2009; 39: 7-33.
Crossref ● Google Scholar

7. Candolle A. de. Monographie des Сampanulées. Paris: Veuve Desray, 1830. 384 p.
Crossref

8. Candolle A. Pyramo de. Prodromus systematis naturalis regni vegetabilis. 1839; Vol. 7(2): 801 p.

9. Clausing G., Meyer K., Renner S.S. Correlations among fruit traits and evolution of different fruits within Melastomataceae. Bot. Journal Linn. Soc., 2000; 133: 303-326.
Crossref ● Google Scholar

10. Crowl A.A., Miles N.W., Visger C.J., Hansen K., Ayers T., Haberle R., Cellinese N. A global perspective on Campanulaceae: Biogeographic, genomic, and floral evolution. Amer. J. Bot., 2016; 103(2): 1-13.
Crossref ● PubMed ● Google Scholar

11. Cupido C.N., Weitz F.M. Kericodon (Campanulaceae s. s.), a new monotypic wahlenbergioid genus from South Africa. Kew Bull., 2016. 10 p.
Crossref ● Google Scholar

12. Dremliuga N.G. An overview of taxonomic studies of the genus Campanula L. Ukr. Bot. J., 2009; 66(6): 805-813. (In Ukrainian)

13. Dremliuga N.G. Morphological peculiarities of fruits of the species from subgenus Rapunculus (Fourr.) Boiss. of genus Campanula L. in the flora of Ukraine. Mod. Phytomorphol., 2013; 4: 321-324. (In Ukrainian)

14. Dremliuga N.G. The fruіts' morphological peculiarities of species from section Medium DC. of genus Campanula L. in the flora of Ukraine. Chornomors'k. bot. z., 2013; 9(1): 24-29. (In Ukrainian)
Crossref ● Google Scholar

15. Eddie W.M.M., Shulkina T., Gaskin J., Haberle R.C., Jansen R.K. Phylogeny of Campanulaceae s. str. inferred from ITS sequences of nuclear ribosomal DNA. Annals of the Missouri Botanical Garden, 2003; 90(4): 554-575.
Crossref ● Google Scholar

16. Eddie W.M.M., Cupido C.N. Hesperocodon, a new genetic name for Wahlenbergia hederacea (Campanulaceae): phylogeny and capsule dehiscence. Edinburgh Journal of Botany, 2014; 71(1): 63-74.
Crossref ● Google Scholar

17. Fagundes N.F., Araujo Mariath J.E. de. Morphoanatomy and ontogeny of fruit in Bromeliaceae species. Acta bot. Bras., 2010; 24(3): 765-779.
Crossref ● Google Scholar

18. Fedorov A.A. Family Campanulaceae Juss. In: Komarov V.L. (ed.). Flora of USSR. Moskow; Leningrad: Academy of Sciences of USSR, 1957. Vol. 24: 162-450. (In Russian)

19. Fedorov A.A. Family Campanulaceae Juss. In: Fedorov A.A. (ed.). Flora partis europaeae USSR. Leningrad: Nauka, 1978. Vol. 3: 213-238. (In Russian)

20. Givnish T.J., Millam K.C., Mast A.R., Paterson T.B., Theim T.J., Hipp A.L., Henss J.M., Smith J.F., Wood K.R., Sytsma K.J. Origin, adaptive radiation and diversification of the Hawaiian lobeliads (Asterales: Campanulaceae). Proc. R. Soc. B., 2009; 276: 407-416.
Crossref ● PubMed ● Google Scholar

21. Graham S.A., Graham A. Ovary, fruit, and seed morphology of the Lythraceae. International Journal of Plant Sciences, 2014; 175(2): 202-240.
Crossref ● Google Scholar

22. Haberle R.C., Dang A., Lee T., Peñaflor C., Cortes-Burns H., Oestreich A., Raubeson L., Cellinese N., Edwards E.J., Kim S.-T., Eddie W.M.M., Jansen R.K. Taxonomic and biogeogra­phic implications of a phylogenetic analysis of the Campanulaceae based on three chloroplast genes. Taxon, 2009; 58(3): 715-734.
Crossref ● Google Scholar

23. Herrera F., Mitchell J.D., Pell S.K., Collinson M.E., Daly D.C., Manchester S.R. Fruit morpho­logy and anatomy of the spondioid Anacardiaceae. Bot. Rev., 2018; 84(4): 315-393.
Crossref ● PubMed ● Google Scholar

24. Hong D.-Y., Wang Q. A new taxonomic system of the Campanulaceae s.s. J. Syst. Evol., 2015; 53: 203-209.
Crossref ● Google Scholar

25. Jiménez-Mejías P., Vargas P. Taxonomy of the tribe Apieae (Apiaceae) revisited as revealed by molecular phylogenies and morphological characters. Phytotaxa, 2015; 212(1): 57-79.
Crossref ● Google Scholar

26. Jussieu A. L. de. Genera plantarum secundum ordines naturales disposita. 1789. 499 p.
Crossref ● Google Scholar

27. Kaden N.N. The fruit types of plants inhabiting the middle zone of the European part of the U.S.S.R. Botanicheskii Zhurnal, 1965; 50(6): 775-787. (In Russian)

28. Kaplan D.R. Floral morphology, organogenesis and interpretation of the inferior ovary in Downingia bacigalupii. Amer. J. Bot., 1967; 54(10): 1274-1290.
Crossref ● Google Scholar

29. Kolakovsky A.A. New data in morphology of the flower and fruit in the family Campanulaceae. Bulletin of the Academy of Sciences of the Georgian SSR, 1990; 139(2): 381-384. (In Russian)

30. Kolakovsky A.A. Family Campanulaceae. Мoscow, 1995. 92 р. (In Russian)

31. Kravtsova T.I. Comparative carpology of the Urticaceae Juss. Moscow: KMK Scientific Press Ltd, 2009. 400 p. (In Russian)

32. Lagomarsino L., Antonelli A., Muchhala N., Timmermann A., Mathews S., Davis C.C. Phylo­geny, classification, and fruit evolution of the species-rich Neotropical bellflowers (Campanulaceae: Lobelioideae). Amer. J. Bot., 2014; 101(12): 2097-2112.
Crossref ● PubMed ● Google Scholar

33. Lakoba P.V. Towards the anatomy of axicorn: an organ of Campanulaceae. Bulletin of the Academy of Sciences of the Georgian SSR, 1986; 123(1): 141-143. (In Russian)

34. Lammers T.G. Campanulaceae. The families and genera of vascular plants. Ed. by K. Kubitzki. VIII, Flowering plants - Еudicots: Asterales / volume editors J.W. Kadereit, C. Jeffrey. Berlin: Springer, 2007. P 26-56.

35. Leinfellner W. Der Bauplan des synkarpen Gynözeums. Österr. bot. Z., 1950; 97: 403-436.
Crossref ● Google Scholar

36. Leins P., Erbar C. Flower and fruit: Morphology, ontogeny, phylogeny, function and ecology. Stuttgart: Schweizerbart, 2010. 439 p.
Google Scholar

37. Levina R.E. Methods of dispersal of seeds and fruits. Mosсow: Nauka, 1957. 358 p. (In Russian)

38. Levina R.E. Morphology and ecology of fruits. Leningrad: Nauka, 1987. 160 p. (In Russian)

39. Liveri E., Crowl A.A., Cellinese N. Past, present, and future of Campanula (Campanulaceae) systematics - a review. Bot. Chron., 2019; 22: 209-222.
Google Scholar

40. Mairal M., Pokorny L., Aldasoro J.J., Alarcon M., Sanmartin I. Ancient vicariance and climate-driven extinction explain continental-wide disjunctions in Africa: the case of the Rand Flora genus Canarina (Campanulaceae). Mol. Biol., 2015; 24: 1335-1354.
Crossref ● PubMed ● Google Scholar

41. Mansion G., Parolly G., Crowl A.A., Mavrodiev E., Cellinese N., Oganesian M., Fraunhofer K., Kamari G., Phitos D., Haberle R., Akaydin G., Ikinci N., Raus T., Borsch T. How to handle speciose clades? Mass Taxon-Sampling as a strategy towards illuminating the natural history of Campanula (Campanuloideae). PLoS ONE, 2012; 7(11): 23 p.
Crossref ● PubMed ● Google Scholar

42. Miroshnichenko N.N. Some aspects of the reproductive biology of Campanula sibirica L., C. taurica Juz. and C. talievii Juz. in Crimea. Studia Biologica, 2014; 8(1): 161-170. (In Ukrainian)
Crossref ● Google Scholar

43. Mosyakin S.L. Families and orders of Angiosperms of the flora of Ukraine: a pragmatic classification and position in the phylogenetic system. Ukr. Bot. J., 2013; 70(3): 289-307. (In Ukrainian)
Crossref ● Google Scholar

44. Pabón-Mora N., Litt A. Comparative anatomical and developmental analysis of dry and fleshy fruits of Solanaceae. Amer. J. Bot., 2011; 98(9): 1415-1436.
Crossref ● PubMed ● Google Scholar

45. Pijl L. van der. Principles of dispersal in higher plants. 3nd ed., Berlin; Heidelberg; New York: Springer, 1982. 214 p.
Crossref ● Google Scholar

46. Roquet C., Sáez L., Aldasoro J.J., Alfonso S., Alarcón M. L., Núria G.-J. Natural delineation, molecular phylogeny and floral evolution in Campanula. Syst. Bot., 2008; 33: 203-217.
Crossref ● Google Scholar

47. Roquet C., Sanmartín I., Garcia-Jacas N., Sáez L., Susanna A., Wikström N., Aldasoro J.J. Reconstructing the history of Campanulaceae with a Bayesian approach to molecular dating and dispersal-vicariance analyses. Molecular Phylogenetics and Evolution, 2009; 52: 575-587.
Crossref ● PubMed ● Google Scholar

48. Roth I. Fruits of Angiosperms. In: Encyclopedia of Plant Anatomy. Eds. W. Zimmermann, S. Carlquist, P. Ozenda, H.D. Wulff. Berlin: G. Borntraeger, 1977; 10(1): 200-675.

49. Schönland S. Campanulaceae. In: Engler, A., Prantl, K. (Eds.), Die Natürlichen Pflanzenfamilien, Teil IV, Abt. 5. Leipzig: Engelmann, 1894. S. 40-70.

50. Shulkina T.V., Gaskin J.F., Eddie W.M.M. Morphological studies toward an improved classification of Campanulaceae s. str. Annals of the Missouri Botanical Garden, 2003; 90(4): 576-591.
Crossref ● Google Scholar

51. Spjut R.W. A systematic treatment of fruit types. Mem. New York Bot. Gard., 1994; (70): 1-182.

52. Stevens P.F. (2001 onwards). Angiosperm Phylogeny Website. Version 14, July 2017 [and more or less continuously updated since]. http://www.mobot.org/MOBOT/research/APweb/. [Accessed 01.02.2019]

53. Takhtajan A. Foundations of evolutionary morphology of the Angiosperms. Moskow: Nauka, 1964. 236 p. (In Russian)

54. Takhtajan A. Systema et phylogenia Magnoliophytorum. Leningrad: Nauka, 1966. 612 p. (In Russian)

55. Takhtajan A. Systema Magnoliophytorum. Leninopoli: Nauka, 1987. 439 p. (In Russian).

56. Takhtajan A. Flowering Plants. 2nd ed. Springer, 2009. 871 p.
Crossref ● Google Scholar

57. The Plant List. А working list of all plant species. Version 1.1. (2013). Published on the Internet; http://www.theplantlist.org/ [Accessed 01.01.2020]

58. Visyulina O.D. Family Campanulaceae Juss. Flora of Ukrainian SSR. Kyiv: Academy of Sciences of USSR, 1961. Vol. 10. P. 401-435. (In Ukrainian)

59. Wang Q., Wang X.-Q., Sun H., Yu Y., He X.-J., Hong D.-Y. Evolution of the platycodonoid group with particular references to biogeography and character evolution. Journal of Integrative Plant Biology, 2014; 56(10): 995-1008.
Crossref ● PubMed ● Google Scholar

60. Yoo K.-O., Crowl A.A., Kim K.-A., Cheon K.-S., Cellinese N. Origins of East Asian Campanuloideae (Campanulaceae) diversity. Molecular Phylogenetics and Evolution, 2018, 1-7.
Crossref ● PubMed ● Google Scholar

61. Zhuo Z., Wen J., Li G. Phylogenetic assessment and biogeographic analyses of tribe Peracarpeae (Campanulaceae). Plant Syst. Evol., 2011, 14 p.
Crossref ● Google Scholar


Refbacks

  • There are currently no refbacks.


Copyright (c) 2020 Studia biologica

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.