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Sympodial Model of Bulb Growth in Amaryllidaceae: A Comparative Morphological Approach

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Abstract

For a long time, Amaryllidaceae were a textbook example of monopodially growing bulbs. The position of the first leaf of the innovation bud in Galanthus, which is not adaxial in relation to the inflorescence, was the main argument in favor of this. The discussion about the type of bulb innovation continued over 150 years and was completed with the approval of a sympodial innovation model. The relevance of this study is due to the fact that no satisfactory explanation of the variability of phyllotaxis in the innovation bud of Amaryllidaceae has been found. We have carried out a homologization of innovation-bud prophylls in different clades of this family. Using the methods of comparative structural morphology, we have detected the universality of sympodial model of bulb innovation for the Amaryllidaceae family. Our study proves that the prophyll of the innovation bud can undergo a reduction from a well-developed green leaf through lower scales to completely ablasted (phantom) organs. We have established that the traits of prophyll structure are synapomorphies for large geographic clades of Amaryllidaceae allocated according to molecular phylogenetic data. We register the highest variability of the prophyll structure for African Amaryllidaceae. It is important to note that a row of morphological reduction of the prophyll (that we identify) cannot be considered evolutionary. Apparently, a polymorphic state with different degree of the prophyll development can be taken as ancestral, while the fixation of the prophyll traits has occurred in the course of further evolution for most large clades (except for African). Thus, in our study the fairness of the sympodial model of bulb innovation has finally been proven for the whole Amaryllidaceae family.

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REFERENCES

  1. Afanas’eva, N.N., Morphological and anatomic features and systematic of Haemanthus (Amaryllidaceae), Bot. Zh., 1995, vol. 80, no. 3, pp. 30–40.

    Google Scholar 

  2. APG II, An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants, Bot. J. Linn. Soc., 2003, vol. 141, pp. 399–436.

  3. APG IV, An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants, Bot. J. Linn. Soc., 2016, vol. 181, no. 1, pp. 1–20.

  4. Artyushenko, Z.T., Amarillisovye (Amaryllidaceae Jaume St.-Hilaire) SSSR. Morfologiya, sistematika i ispol’zovanie. Monografiya (Amaryllis (Amaryllidaceae Jaume St.-Hilaire) of USSR: Morphology, Systematics, and Use. Monograph), Leningrad: Nauka, 1970.

  5. Artyushenko, Z.T. and Shchepak, A.V., Shoot branching of the members of family Amaryllidaceae, Bot. Zh., 1982, vol. 67, no. 8, pp. 1074–1082.

    Google Scholar 

  6. Asatryan, M.Ya., Lower chaffs of bulbs of some members of family Amaryllidaceae, Bot. Zh., 1993, vol. 78, no. 3, pp. 52–57.

    Google Scholar 

  7. Blaauw, A.H., De orgaanvorming und periodiciteit van Hippeastrum hybridum, Verh.-K. Ned. Akad. Wet., Afd. Natuurkd.,Derde Reeks, 1931, vol. 29, no. 1, pp. 1–90.

    Google Scholar 

  8. Brunaud, A. and Turlier, M.F., Monopodial and sympodial structures: some instances under discussion, Bull. Soc. Bot. Fr., 1971, vol. 118, nos. 7–8, pp. 543–560.

    Article  Google Scholar 

  9. Chase, M.W., Reveal, J.L., and Fay, M.F., A subfamilial classification for the expanded asparagalean families Amaryllidaceae, Asparagaceae, and Xanthorrhoeaceae, Bot. J. Linn. Soc., 2009, vol. 161, pp. 132–136.

    Article  Google Scholar 

  10. Choob, V.V., Phantom leaves: a new look to the old problem of branching in Galanthus (Amaryllidaceae), Syst. Geogr. Plants, 1999, vol. 68, pp. 67–72.

    Article  Google Scholar 

  11. Choob, V.V., Rol’ pozitsionnoi informatsii v regulyatsii razvitiya organov tsvetka i listovykh serii pobegov (Role of Position Information in Regulation of Development of Flower Organs and Leaf Series of Shoots), Moscow: BINOM. Laboratoriya Znanii, 2010.

  12. Choob, V.V. and Kozhevnikova, A.D., Bulb structure of dwarf daffodils (Narcissus bulbocodium L. and N. triandrus L., Amaryllidaceae), Byull. Mosk. O-va. Ispyt. Prir., Otd.Biol., 2000, vol. 105, no. 4, pp. 53–59.

    Google Scholar 

  13. Chub, V.V. and Kozhevnikova, A.D., A comparative analysis of the monopodial and sympodial models of bulb branching in Galanthus L., Biol. Bull. (Moscow), 2000, vol. 27, no. 3, pp. 241–248.

    Google Scholar 

  14. Dahlgren, R.M.T., Clifford, H.T., and Yeo, P.F., The Families of the Monocotyledons: Structure, Evolution, and Taxonomy, Berlin: Springer-Verlag, 1985.

    Book  Google Scholar 

  15. Dzidziguri, L.K., Shoot branching of Zephyranthes Herb. (Amaryllidaceae), Bot. Zh., 1979, vol. 64, no. 1, pp. 64–68.

    Google Scholar 

  16. Eichler, A.W., Blütendiagramme, Leipzig: W. Engelmann, 1875, vol. 1.

    Google Scholar 

  17. García, N., Meerow, A.W., Arroyo-Leuenberger, S., Oliveira, R.S., Dutilh, J.H., Soltis, P.S., and Judd, W.S. Generic classification of Amaryllidaceae tribe Hippeastreae, Taxon, 2019, vol. 68, no. 3, pp. 481–498.

    Article  Google Scholar 

  18. García, N., Meerow, A.W., Soltis, D.E., and Soltis, P.S., Testing deep reticulate evolution in Amaryllidaceae tribe Hippeastreae (Asparagales) with ITS and chloroplast sequence data, Syst. Bot., 2014, vol. 39, no. 1, pp. 75–89.

    Article  Google Scholar 

  19. Hartsema, A.M. and Leupen, F.F., Orgaanvorming en periodicitet van Amaryllis belladonna, Meded. Landbouwgewassen, Wageningen, 1942, vol. 46, no. 4.

  20. Huisman, E. and Hartsema, A.M., De periodike Ontwikkeling van Narcissus pseudonarcissus L., Meded. Landbouwgewassen, Wageningen, 1933, vol. 37, no. 1.

  21. Irmisch, T., Zur Morphologie der monokotylischen Knollen- und Zwiebelgewächse, Berlin: G. Reimer, 1850.

    Book  Google Scholar 

  22. Irmisch, T., Beiträge zur Morphologie der Amaryllideen, Berlin: G. Fischer, 1860.

    Google Scholar 

  23. Kapinos, G.E., Biologicheskie zakonomernosti razvitiya lukovichnykh i klubnelukovichnykh rastenii na Apsherone (Biological Features of Development of Bulbous and Bulbotuberiferous Plants of the Absheron), Baku: Akad. Nauk AzSSR, 1965.

  24. Levacher, P.M., La croissance sympodique du perce-neige (Galanthus nivalis L.), et la position superposee de la prefeuille du bourgeon de replacement, C. R. Hebd. Seances Acad. Sci., D, 1970, vol. 217, no. 13, pp. 1079–1082.

  25. Luiten, I. and van Waveren, J.M., De orgaanvorming van Leucojum aestivum L., Meded. Landbouwgewassen, Wageningen, 1938, vol. 42, no. 1.

  26. Luiten, I. and van Waveren, J.M., De orgaanvorming van Galanthus nivalis L., Meded.Landbouwgewassen, Wageningen, 1952, vol. 52, no. 4, pp. 105–124.

    Google Scholar 

  27. Meerow, A.W., Systematics of the Amazon lilies, Eucharis and Caliphruria (Amaryllidaceae), Ann. Mo. Bot. Gard., 1989, vol. 76, pp. 136–220.

    Article  Google Scholar 

  28. Meerow, A. and Clayton, J., Generic relationships among the baccate-fruited Amaryllidaceae (tribe Haemantheae) inferred from plastid and nuclear non-coding DNA sequences, Plant Syst. Evol., 2004, vol. 244, pp. 141–155.

    Article  CAS  Google Scholar 

  29. Meerow, A.W. and Snijman, D.A., The never-ending story: multigene approaches to the phylogeny of Amaryllidaceae, Aliso, 2006, vol. 22, pp. 355–366.

    Article  Google Scholar 

  30. Meerow, A.W., Guy, C.L., Li, Q.-B., and Yang, S.-L., Phylogeny of the American Amaryllidaceae based on nrDNA ITS sequences, Syst. Bot., 2000, vol. 25, no. 4, pp. 708–726.

    Article  Google Scholar 

  31. Mori, G. and Sakanishi, Y., Studies on the growth and flowering of bulbous plants of Amaryllidaceae, Engei-Gakkai Zasshi, 1976, vol. 45, no. 4, pp. 389–396.

    Article  Google Scholar 

  32. Mori, G., Kawabata, H., Imanishi, H., and Sakanishi, Y., Growth and flowering of Leucojum aestivum L. and L. autumnale L. grown outdoors, Engei-Gakkai Zasshi, 1990, vol. 59, pp. 815–821.

    Article  Google Scholar 

  33. Müller-Doblies, D., Galanthus ist doch sympodial gebaut! Ber. Dtsch. Bot. Ges., 1971, vol. 84, no. 11, pp. 665–682.

    Google Scholar 

  34. Müller-Doblies, D. and Müller-Doblies, U., Zum Bauplan von Ungernia, der einzigen endemischen Amaryllidaeen-Gattung Zentralasiens, Bot. Jahrb. Syst., 1978, vol. 99, nos. 2–3, pp. 249–263.

    Google Scholar 

  35. Paula, C.B., Morphological analysis of tropical bulbs and environmental effects on flowering and bulb development of Habranthus robustus and Zephyranthes spp., PhD Thesis, Gainesville, FL: Univ. of Florida, 2006.

  36. Pax, F., Amarylidaceae, in Die Natürlichen Pflanzenfamilien von A. Engler und K. Prantl, Leipzig: W. Engelmann, 1889, part 1, pp. 97–124.

  37. Rees, A.R., The initiation and growth of Narcissus bulbs, Ann. Bot., 1969, vol. 33, no. 130, pp. 277–288.

    Article  Google Scholar 

  38. Saint-Hilaire, J., Les Amaryllidées, in Exposition Des Familles Naturelles et De La Germination Des Plantes, Vol. 1: Treuttel et Würtz, Paris, 1805, pp. 134–142.

    Google Scholar 

  39. Saint-Hilaire, A., Leçons de Botanique, Comprenant Principalement la Morphologie Végétale, la Terminologie, la Botanique Comparée, l’Examen de la Valeur des Caractères dans les Diverses Familles Naturelles, etc., Paris: P.-J. Loss, 1840.

    Google Scholar 

  40. Schumann, K., Neue Untersuchungen über den Blütenanschluss, Leipzig: W. Engelmann, 1890.

    Book  Google Scholar 

  41. Serebryakov, I.G., Morfologiya vegetativnykh organov vysshikh rastenii (Morphology of Vegetative Organs of Higher Plants), Moscow: Sovetskaya Nauka, 1952.

  42. Slabbert, M.M., Inflorescence initiation and development in Cyrtanthus elatus (Jacq.) Traub, Sci. Hortic., 1997, vol. 69, pp. 61–71.

    Article  Google Scholar 

  43. Theron, K.I. and Jacobs, G., Periodicity of inflorescence initiation and development in Nerine bowdenii W. Watson (Amaryllidaceae), J. Am. Soc. Hort. Sci., 1994, vol. 119, no. 6. P.1121–1126.

    Article  Google Scholar 

  44. Troll, W., Praktische Einführung in die Pflanzenmorphologie, Part 1: Der Vegetative Aufbau, Jena: Gustav Fischer, 1954.

  45. Vogel, S. and Müller-Doblies, D., Eine nachtblütige Herbst-Narzisse. Zwiebelbau und Blütenökologie von Narcissus viridiflorus Shoesboe, Bot. Jahrb. Syst., 1975, vol. 96, nos. 1–4, pp. 427–447.

    Google Scholar 

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  1. Botanical Garden, Department of Biology, Moscow State University, 119991, Moscow, Russia

    V. V. Choob

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Choob, V.V. Sympodial Model of Bulb Growth in Amaryllidaceae: A Comparative Morphological Approach. Contemp. Probl. Ecol. 13, 237–247 (2020). https://doi.org/10.1134/S199542552003004X

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