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Ukr. Bot. J. 2022, 79(3): 169–183
https://doi.org/10.15407/ukrbotj79.03.169
Structural Botany

Morphogenesis of fruit as a subject matter for the carpological studies

Odintsova A.V.
Abstract

In this review, the concept of fruit morphogenesis is treated in the context of implementation of the evo-devo approach in carpology. A new viewpoint on the fruit morphogenesis is proposed and justified, comprising the pre-anthetic, as well as post-anthetic periods of fruit development, id est, development of the gynoecium, and development of the fruit itself. It is proposed to recognize ontogenetical (individual) and evolutionary (historical) aspects of fruit morphogenesis, the first of them we can study directly, while the second aspect can be only hypothesized or treated as a theoretical model of fruit evolution in consequence of some presumed changes in the individual fruit morphogenesis. In this article these aspects are named as "ontomorphogenesis" and "phylomorphogenesis" of the fruit, correspondingly. Our concept of ontomorphogenesis of the fruit involves four components that could not be brought together, such as changes in the morphological structure of the gynoecium, abscission of the extragynecial floral parts and the style, histogenesis of the fruit wall and other fruit parts, and terminal stages of the fruit morphogenesis (dehiscence, splitting, or abscission). The current state of studies of these components in the individual and evolutionary contexts is discussed. By examining the patterns of fruit evolution, we should consider factors acting at both the post-anthetic and pre-anthetic periods of fruit ontomorphogenesis.

Keywords: flower, fruit dehiscence, fruit wall, gynoecium, histogenesis

Full text: PDF (Ukr) 1.21M

References
  1. Almeida O.J.G., de Souza L.A., Paoli A.A.S., Davis A.R., Cota-Sanchez J.H. 2018. Pericarp development in fruit of epiphytic cacti: implications for fruit classification and macro-morphology in the Cactaceae. Botany (Ottawa), 96(9): 621–635. https://doi.org/10.1139/cjb-2018-0074
  2. Andreychuk R., Odintsova A. 2021. Morpho-anatomy of the gynoecium and fruit in three ornamental members of Campanuloideae (Campanulaceae). Acta Agrobotanica, 74(4): Article 7415. https://doi.org/10.5586/aa.7415
  3. Andreychuk R.R., Kolomiychuk V.P., Odintsova A.V. 2020. Morpho-anatomical structure and development of fruit in Asyneuma canescens (Campanulaceae). Regulatory Mechanisms in Biosystems, 11(4): 513–519. https://doi.org/10.15421/022078
  4. Arab R., Majd A., Tajadod G., Rezanejad F., Mirzaei M. 2019. The morphological and anatomical studies of inflorescence, flower, embryo and fruit development in Maclura pomifera (Moraceae). Cogent Biology, 5: 1663698. https://doi.org/10.1080/23312025.2019.1663698
  5. Areces-Berazain F., AckermanJ. D. 2017. Diversification and fruit evolution in eumalvoids (Malvaceae). Botanical Journal of the Linnean Society, 184: 401–417. https://doi.org/10.1093/botlinnean/box035
  6. Arnaud N., Girin T., Sorefan K., Fuentes S., Wood T. A., Lawrenson T., Sablowski R., Østergaard L. 2010. Gibberellins control fruit patterning in Arabidopsis thaliana. Genes & Development, 24: 2127–2132. https://doi.org/10.1101/gad.593410
  7. Artyushenko Z.T., Fedorov Al.A. 1986. Atlas po opisatelnoy morfologii vysshikh rasteniy. Plod. Leningrad: Nauka, 392 pp.
  8. Bacci L.F., Michelangeli F.A., Goldenberg R. 2019. Revisiting the classification of Melastomataceae: implications for habit and fruit evolution. Botanical Journal of the Linnean Society, 190: 1–24. https://doi.org/10.1093/botlinnean/boz006
  9. Barna M.M. 2013. Botany. Terms. Concepts. Personalities. 2nd ed. Ternopil: Terno-Graf, 360 pp.
  10. Beaulieu J.M., Donoghue M.J. 2013. Fruit evolution and diversification in campanulid angiosperms. Evolution, 67(11): 3132–3144. https://doi.org/10.1111/evo.12180
  11. Biologicheskiy entsiklopedicheskiy slovar. 1989. Ed. M.S. Gilyarov. 2nd ed. Moscow: Sovetskaya entsiklopediya, 863 pp.
  12. Bobrov A.V., Romanov M.S. 2019. Morphogenesis of fruits and types of fruit of angiosperms. Botany Letters, 166(3): 366–399. https://doi.org/10.1080/23818107.2019.1663448
  13. Bobrov A.V., Melikian A.P., Romanov M.S. 2009. Morphogenesis of fruits of Magnoliophyta. Moscow: Librokom, 400 pp.
  14. Bobrov A.V., Romanov M.S., Melikian A.P. 2012. Byulleten Glavnogo Botanicheskogo Sada, 198(2): 46–60.
  15. Casoti R., Manfrona M.P., Oliveira J.M.S. 2016. Ovary and fruit morphology and anatomy of Amphilophium crucigerum. Revista Brasileira de Farmacognosia, 26(1): 15–22. https://doi.org/10.1016/j.bjp.2015.08.006
  16. Clausing G., Meyer K., Renner S.S. 2000. Correlations among fruit traits and evolution of different fruits within Melastomataceae. Botanical Journal of the Linnean Society, 133: 303–326. https://doi.org/10.1111/j.1095-8339.2000.tb01548.x
  17. Cruden R.W. 1977. Pollen-Ovule ratios: a conservative indicator of breeding systems in flowering plants. Evolution, 31(1): 32–46. https://doi.org/10.2307/2407542
  18. Dardick C., Callahan A. M. 2014. Evolution of the fruit endocarp: molecular mechanisms underlying adaptations in seed protection and dispersal strategies. Frontiers in Plant Science, 5, Article 284: 1–10. https://doi.org/10.3389/fpls.2014.00284
  19. Delaux P.-M., Hetherington A.J., Coudert Y., Delwiche C., Dunand C., Gould S., Kenrick P., Li F.-W., Philippe H., Rensing S.A., Rich M., Strullu-Derrien C., de Vries J. 2019. Reconstructing trait evolution in plant evo-devo studies. Current Biology, 29(21): R1110–R1118. https://doi.org/10.1016/j.cub.2019.09.044
  20. Deniz İ., Yildiz K., Cirpici A. 2018. Taxonomical study of seeds and fruit micromorphology of the Geranium (Geraniaceae) species in the Thrace region of Turkey (Europe). Phytologia Balcanica, 24(1): 35–43.
  21. Doweld A.B. 1998. Carpology, seed anatomy and taxonomic relationships of Tetracentron (Tetracentraceae) and Trochodendron (Trochodendraceae). Annals of Botany, 82: 413–443. https://doi.org/10.1006/anbo.1998.0679
  22. Eames A.J. 1961. Morphology of the angiosperms. New-York; Toronto: McGraw-Hill, 498 pp. https://doi.org/10.5962/bhl.title.5986
  23. Ebeed H., El-helely A.A. 2021. Programmed Cell Death in Plants: insights into developmental and stress-induced cell death. Current Protein & Peptide Science, 22(12): 873–889. http://dx.doi.org/10.2174/1389203722666211109102209
  24. Eldridge T., Łangowski Ł., Stacey N., Jantzen F., Moubayidin L., Sicard A., Southam P., Kennaway R., Lenhard M., Coen E. S., Østergaard L. 2016. Fruit shape diversity in the Brassicaceae is generated by varying patterns of anisotropy. Development, 143: 3394–3406. https://doi.org/10.1242/dev.135327
  25. Endress P.K. 2003. Morphology and angiosperm systematics in the molecular era. The Botanical Review, 68(4): 545–570. https://doi.org/10.1663/0006-8101(2002)068[0545:MAASIT]2.0.CO;2
  26. Endress P.K. 2011. Changing views of flower evolution and new questions. In: Flowers on the Tree of Life. Eds. L. Wanntorp, L.P. Ronse De Craene. Cambridge: Cambridge University Press, pp. 120–141. https://doi.org/10.1017/CBO9781139013321.005
  27. Erbar C. 2007. Current opinions in flower development and the evo-devo approach in plant phylogeny. Plant Systematics and Evolution, 269(1/2): 107–132. https://doi.org/10.1007/s00606-007-0579-1
  28. Erbar C., Langlotz M. 2005. Pollen to ovule ratios: standard or variation – a compilation. Botanische Jahrbücher fur Systematik, Pflanzengeschichte und Pflanzengeographie, 126(1): 71–132. https://doi.org/10.1127/0006-8152/2005/0126-0071
  29. Erbar C., Leins P. 1996. Distribution of the character states "early sympetaly" and "late sympetaly" within the "Sympetalae Tetracyclicae" and presumably allied groups. Botanica Acta: Berichte der Deutschen Botanischen Gesellschaft, Journal of the German Botanical Society, 109(5): 427–440. https://doi.org/10.1111/j.1438-8677.1996.tb00593.x
  30. Fagundes N.F., de Mariath A.J.E. 2010. Morphoanatomy and ontogeny of fruit in Bromeliaceae species. Acta Botanica Brasilica, 24(3): 765–779. https://doi.org/10.1590/S0102-33062010000300020
  31. Fan K.-Y., Bain A., Tzeng H.-Y., Chiang Y.-P., Chou L.-S., Kuo-Huang L.-L. 2019. Comparative anatomy of the fig wall (Ficus, Moraceae). Botany, 97: 417–426. https://doi.org/10.1139/cjb-2018-0192
  32. Ferrándiz C. 2002. Regulation of fruit dehiscence in Arabidopsis. Journal of Experimental Botany, 53(377): 2031–2038. https://doi.org/10.1093/jxb/erf082
  33. Ferrándiz C., Fourquin C. 2014. Role of the FUL–SHP network in the evolution of fruit morphology and function. Journal of Experimental Botany, 65(16): 4505–4513. https://doi.org/10.1093/jxb/ert479
  34. Ferrándiz C., Pelaz S., Yanofsky M.F. 1999. Control of carpel and fruit development in Arabidopsis. Annual Review of Biochemistry, 68: 321–354. https://doi.org/10.1146/annurev.biochem.68.1.321
  35. Fishchuk O., Odintsova A. 2021. Flower and fruit micromorphology and anatomy in Hippeastrum vittatum (L'Hér.) Herb. (Amaryllidaceae). Wulfenia, 28: 129–140.
  36. Fleming T.H. 1991. Fruiting plant-frugivore mutualism: the evolutionary theater and the ecological play. In: Plant-animal interactions: Evolutionary ecology in tropical and temperate regions. Eds. P.W. Price, T.M. Lewinsohn, G.W. Fernandes, W.W. Benson. New York: Wiley, pp. 119–144.
  37. Forlani S., Mizzotti Ch., Masiero S. 2021. The NAC side of the fruit: tuning of fruit development and maturation. BMC Plant Biology, 21(238): 1–14. https://doi.org/10.1186/s12870-021-03029-y
  38. Gagliardi K.B., Souza L.A., Albiero A.L.M. 2014. Comparative fruit development in some Euphorbiaceae and Phyllanthaceae. Plant Systematics and Evolution, 300: 775–782. https://doi.org/10.1007/s00606-013-0918-3
  39. Gao H., Li J., Wang L., Zhang J., He C. 2020. Transcriptomic variation of the flower–fruit transition in Physalis and Solanum. Planta, 252: 1–28. https://doi.org/10.1007/s00425-020-03434-x
  40. Graham S.A., Graham A. 2014. Ovary, fruit, and seed morphology of the Lythraceae. International Journal of Plant Sciences, 175(2): 202–240. https://doi.org/10.1086/674316
  41. Guzicka M., Zieliński J., Tomaszewski D., Gawlak M. 2012. Anatomical study on the developing pericarp of selected Rosa species (Rosaceae). Dendrobiology, 68: 77–87.
  42. Hautegem T.V., Waters A.J., Goodrich J., Nowack M.K. 2015. Only in dying, life: Programmed cell death during plant development. Trends in Plant Science, 20(2): 102–113. https://doi.org/10.1016/j.tplants.2014.10.003
  43. Havel L., Durzan D. 1996. Apoptosis in plants. Botanica Acta, 109: 268–277. https://doi.org/10.1111/j.1438-8677.1996.tb00573.x
  44. Herrera F., Mitchell J.D., Pel S.K., Collinson M.E., Daly D.C., Manchester S.R. 2018. Fruit morphology and anatomy of the spondioid Anacardiaceae. The Botanical Review, 84(4): 315–393. https://doi.org/10.1007/s12229-018-9201-1
  45. Herrera-Ubaldo H., de Folter S. 2022. Gynoecium and fruit development in Arabidopsis. Development, 149(5): dev200120. https://doi.org/10.1242/dev.200120
  46. Horbens M., Gao J., Neinhuis C. 2014. Cell differentiation and tissue formation in the unique fruits of devil's claws (Martyniaceae). American Journal of Botany, 101(6): 914–924. https://doi.org/10.3732/ajb.1400006
  47. Ickert-Bond S.M., Gerrath J., Wen J. 2014. Gynoecial structure of Vitales and implications forthe evolution of placentation in the Rosids. International Journal of Plant Sciences, 175(9): 998–1032. https://doi.org/10.1086/678086
  48. Kaden N.N. 1947. Vestnik Moskovskogo universiteta, 12: 31–42.
  49. Kaden N.N. 1961. Botanicheskiy Zhurnal, 46(4): 498–504.
  50. Kaden N.N. 1962. Botanicheskiy Zhurnal, 47(4): 495–504.
  51. Kaden N.N. 1964a. Botanicheskiy Zhurnal, 49(7): 966–973.
  52. Kaden N.N. 1964b. Botanicheskiy Zhurnal, 49(12): 1776–1779.
  53. Kaden N.N. 1968. Bulletin of Moscow Society of Naturalists. Biological series, 73(2): 127–135.
  54. Kordyum E.L. 2010. Ukrainian Botanical Journal, 67(6): 789–801.
  55. Kordyum E.L., Kravets H. A. 2021. Evolutionary patterns of the internal structures of generative organs in angiosperm plants. In: Plant Reproductive Ecology – Recent Advances. Eds. A. Rustagi, B. Chaudhry. IntechOpen. https://doi.org/10.5772/intechopen.100593
  56. Kravtsova T.I. 2009. Comparative carpology of the family Urticaceae Juss. Moscow: KMK Scientific Press Ltd., 400 pp.
  57. Kuriyama H., Fukuda H. 2003. Developmental programmed cell death in plants. Current opinion in plant biology, 5(6): 568–573. https://doi.org/10.1016/S1369-5266(02)00305-9
  58. Laczkó-Zöld E., Komlósi A., Varga E., Papp N. 2019. Comparative histological evaluation of the fruit of Ribes nigrum and Ribes rubrum. Acta Biologica Marisiensis, 2(2): 5–14. https://doi.org/10.2478/abmj-2019-0006
  59. Lagomarsino L.P., Antonelli A., Muchhala N., Timmermann A., Mathews S., Davis C.C. 2014. Phylogeny, classification, and fruit evolution of the species-rich Neotropical bellflowers (Campanulaceae: Lobelioideae). American Journal of Botany, 101(12): 2097–2112. https://doi.org/10.3732/ajb.1400339
  60. Leinfellner W. 1950. Der Bauplan des synkarpen Gynözeums. Österreichishe Botanische Zeitschrift, 97: 403–436. https://doi.org/10.1007/BF01763317
  61. Leins P. 1964. Das zentripetale und zentrifugale Androeceum. Berichte der Deutschen Botanischen Gesellschaft, 77: 22–26.
  62. Leins P. 1975. Die Beziegungen zwischen multistaminalen und einfachen Androceen. Botanische Jahrbücher fur Systematik, Pflanzengeschichte und Pflanzengeographie, 96: 231–237.
  63. Leins P., Erbar C. 2010. Flower and fruit: Morphology, ontogeny, phylogeny, function and ecology. Stuttgart: Schweizerbart, 439 pp.
  64. Levina R.E. 1951. Botanicheskiy Zhurnal, 46(4): 488–495.
  65. Levina R.E. 1974. Bulletin of Moscow Society of Naturalists. Biological series, 79(1): 89–99.
  66. Levina R.E. 1987. Morphology and ecology of fruit. Leningrad: Nauka, 160 pp.
  67. Locato V., De Gara L. 2018. Programmed cell death in plants: an overview. Methods in Molecular Biology, 1743: 1–8. https://doi.org/10.1007/978-1-4939-7668-3_1
  68. Luna M.L., Giudice G.E. Grossi M.A., Gutiérrez D.G. 2017. Development and morphology of the fruit and seed of the hemiparasite genus Jodina (Cervantesiaceae). Anales del Jardin Botanico de Madrid, 74(1): e051. https://doi.org/10.3989/ajbm.2444
  69. Marcussen Th., Meseguer A.S. 2017. Species-level phylogeny, fruit evolution and diversification history of Geranium (Geraniaceae). Molecular Phylogenetics and Evolution, 110: 134–149. https://doi.org/10.1016/j.ympev.2017.03.012
  70. Motley T.J., Wurdack K.J., Delprete P.G. 2005. Molecular systematics of the Catesbaeeae-Chiococceae complex (Rubiaceae): flower and fruit evolution and biogeographic implications. American Journal of Botany, 92(2): 316– 329. https://doi.org/10.3732/ajb.92.2.316
  71. Muehlhausen A., Lenser T., Mummenhoff K., Theissen G. 2013. Evidence that an evolutionary transition from dehiscent to indehiscent fruits in Lepidium (Brassicaceae) was caused by a change in the control of valve margin identity genes. Plant Journal, 73(5): 824–835. https://doi.org/10.1111/tpj.12079
  72. Mysyura V.P., Zakorko N.H. 2014. In: Natural science. Issue 11. Sumy: Sumy State Pedagogical University named after A.S. Makarenko, pp. 58–62. Available at: http://repository.sspu.sumy.ua/handle/123456789/3333 (Accessed 2 April 2022).
  73. Novikov A., Barabasz-Krasny B. 2015. Modern plant systematics: General topics: hand-book. Lviv: Liga-Pres, 686 pp. http://dx.doi.org/10.13140/RG.2.1.4745.6164
  74. Nuraliev M.S., Sokoloff D.D. 2014. Botanicheskii Zhurnal, 99(2): 129–158.
  75. Odintsova A.V. 2012. Modern Phytomorphology, 1: 71–75.
  76. Odintsova A.V. 2016. Studia Biologica, 10(3–4): 129–140. https://doi.org/10.30970/sbi.1003.504
  77. Odintsova A., Honcharenko V. 2020. In: Status and biodiversity of ecosystems of Shatskyi National Nature Park and other protected areas: proceedings of the International scientific conference (Lviv, 10–13 September 2020). Lviv: SPOLOM, pp. 71–74.
  78. Odintsova A., Klimovych N. 2017. Ukrainian Botanical Journal, 74(6): 582–593. https://doi.org/10.15407/ukrbotj74.06.582
  79. Oyama S.O., Souza L.A. 2011. Morphology and anatomy of the developing fruit of Maclura tinctoria, Moraceae. Revista Brasileira de Botanica, 34(2): 187–195. https://doi.org/10.1590/S0100-84042011000200006
  80. Oyama S.O., Souza L.A., Muneratto J.C., Albiero A.L.M. 2010. Morphological and anatomical features of the flowers and fruits during the development of Chamissoa altissima (Jacq.) Kunth (Amaranthaceae). Brazilian Archives of Biology and Technology, 53(6): 1425–1432. https://doi.org/10.1590/S1516-89132010000600019
  81. Pabón-Mora N., Litt A. 2011. Comparative anatomical and developmental analysis of dry fleshy fruits of Solanaceae. American Journal of Botany, 98(9): 1415–1436. https://doi.org/10.3732/ajb.1100097
  82. Paschoalini G.O., Pirani J.R., Demarco D., El Ottra J.H.L. 2022. Revisiting pericarp structure, dehiscence and seed dispersal in Galipeeae (Zanthoxyloideae, Rutaceae). Brazilian Journal of Botany, 45(1): 415–429. https://doi.org/10.1007/s40415-021-00779-9
  83. Payer J.-B. 1857. Traité d'organogénie comparée de la fleur. Texte et Atlas. Paris: Victor Masson, viii + 749 pp. https://archive.org/details/bub_gb_0bAMVvUSFEkC
  84. Polli A., Souza L.A., Almeida O.J.G. 2016. Structural development of the fruits and seeds in three mistletoe species of Phoradendron (Visceae: Santalaceae). Rodriguesia, 67(3): 649–659. https://doi.org/10.1590/2175-7860201667309
  85. Robles P., Pelaz S. 2005. Flower and fruit development in Arabidopsis thaliana. International Journal of Developmental Biology, 49: 633–643. https://doi.org/10.1387/ijdb.052020pr
  86. Rogers H. J. 2006. Programmed cell death in floral organs: how and why do flowers die? Annals of Botany, 97(3): 309–315. https://doi.org/10.1093/aob/mcj051
  87. Romanov M.S., Bobrov A.V., Romanova E.S., Zdravchev N.S., Sorokin A.N. 2021. Fruit development, structure and histology in Nelumbo (Nelumbonaceae: Proteales). Botanical Journal of the Linnean Society, boab067. https://doi.org/10.1093/botlinnean/boab067
  88. Romanov M.S., Endress P.K., Bobrov A.V., Yurmanov A.A., Romanova E. 2018. Fruit structure of Calycanthaceae (Laurales): histology and development. International Journal of Plant Sciences, 179(8): 616–634. https://doi.org/10.1086/699281
  89. Rosa-Osman S.M., Rodrigues R., Mendonça M.S., Souza L.A., Piedade M.T.F. 2011. Morphology of flower, fruit and seedling of Victoria amazonica (Poepp.) J.C.Sowerby (Nymphaeaceae). Acta Amazonica, 41(1): 21–28. http://dx.doi.org/10.1590/S0044-59672011000100003
  90. Roth I. 1977. Fruits of Angiosperms. In: Encyclopedia of Plant Anatomy. Vol. 10, part 1. Eds. W. Zimmermann, S. Carlquist, P. Ozenda, H.D. Wulff. Berlin: Borntraeger, XVI+675 pp.
  91. Rutishauser R. 2020. EvoDevo: Past and future of continuum and process plant morphology. Philosophies, 5: 41. https://doi.org/10.3390/philosophies5040041
  92. Rutishauser R., Grob V., Pfeifer E. 2008. Plants are used to having identity crises. In: Evolving pathways: key themes in evolutionary developmental biology. Eds. A. Minelli, G. Fusco. Cambridge: Cambridge University Press, pp. 194– 213. https://doi.org/10.1017/CBO9780511541582.015
  93. Santos-Silva F., Mastroberti A.A., Mariath J.E.A. 2015. Capsule structure in three species of Dyckia (Bromeliaceae): ontogenetic and taxonomic issues. Journal of the Torrey Botanical Society, 142(3): 249–257. https://doi.org/10.3159/TORREY-D-14-00002.1
  94. Shamrov I.I. 2020. Structure and development of the coenocarpous gynoecium in angiosperms. Wulfenia, 27: 145–182.
  95. Sinnott E.W. 1960. Plant morphogenesis. New-York; Toronto; London: McGraw Hill, 550 pp. https://doi.org/10.5962/bhl.title.4649
  96. Sinnott-Armstrong M.A., Lee Ch., Clement W.L., Donoghue M.J. 2020. Fruit syndromes in Viburnum: correlated evolution of color, nutritional content, and morphology in bird-dispersed fleshy fruits. BMC Evolutionary Biology, 20(7): 1–19. https://doi.org/10.1186/s12862-019-1546-5
  97. Skrypets K., Odintsova A. 2020. Ukrainian Botanical Journal, 77(3): 210–224. https://doi.org/10.15407/ukrbotj77.03.210
  98. Sokoloff D.D., Nuraliev M.S., Oskolski A.A., Remizowa M.V. 2017. Vestnik Moskovskogo universiteta. Seriya 16. Biologiya, 72(3): 115–127.
  99. Sousa-Baena M.S., Menezes N.L. 2019. Comparative developmental anatomy of ovary and fruit in Brazilian Velloziaceae. Botanical Journal of the Linnean Society, 191(2): 236–260. https://doi.org/10.1093/botlinnean/boz040
  100. Souza L.A. 2021. Structural diversity of fruits: conceptual reflexions and taxonomic implications. Brazilian Journal of Development, Curitiba, 7(7): 69342–69354. https://doi.org/10.34117/bjdv7n7-218
  101. Takhtajan A.L. 1948. Morfologicheskaya evolyutsiya pokrytosemennykh. Moscow: Izd-vo MOIP, 301 pp.
  102. Takhtajan A. 1950. Teoriya filembriogeneza A.N. Severtsova i evolyutsionnaya morfologiya rasteniy. In: Problemy botaniki. Issue 1. Moscow; Leningrad: Izd-vo AN SSSR, pp. 222–231.
  103. Takhtajan A.L. 1964. Osnovy evolyutsionnoy morfologii pokrytosemennykh. Moscow; Leningrad: Nauka, 236 pp.
  104. Takhtajan A.L. 1966. Sistema i filogeniya tsvetkovykh rasteniy. Moscow; Leningrad: Nauka, 611 pp.
  105. Takhtajan A. 2009. Flowering Plants. Springer Science+Business Media. 2nd ed., 870 pp. https://doi.org/10.1007/978-1-4020-9609-9
  106. Thadeo M., Hampilos K.E., Stevenson D.W. 2015. Anatomy of fleshy fruits in the Monocots. American Journal of Botany, 102(11): 1–23. https://doi.org/10.3732/ajb.1500204
  107. The Tomato Genome Consortium. 2012. The tomato genome sequence provides insights into fleshy fruit evolution. Nature, 485: 635–641. https://doi.org/10.1038/nature11119
  108. Tieghem van M.Ph. 1875. Recherches sur la structure du pistil et sur l'anatomie comparée de la fleur. In: Mémoires Présentés par Divers Savants à l'Académie des Sciences. Série. 2. Vol. 21. Paris: Inst. Impérial France, 261 pp.
  109. Vasile M.-A., Luebert F. Jeiter J., Weigend M. 2021. Fruit evolution in Hydrophyllaceae. American Journal of Botany, 108(6): 1–21. https://doi.org/10.1002/ajb2.1691
  110. Wefferling K.M., Hoot S.B., Neves S.S. 2013. Phylogeny and fruit evolution in Menispermaceae. American Journal of Botany, 100(5): 883–905. https://doi.org/10.3732/ajb.1200556
  111. Whitney K.D. 2009. Comparative evolution of flower and fruit morphology. Proceedings of the Royal Society B, 276: 2941–2947. https://doi.org/10.1098/rspb.2009.0483
  112. Xiang Y., Huang Ch.-H., Hu Y., Wen J., Li Sh., Yi T., Chen H., Xiang J., Ma H. 2017. Evolution of Rosaceae fruit types based on nuclear phylogeny in the context of geological times and genome duplication. Molecular Biology and Evolution, 34(2): 262–281. https://doi.org/10.1093/molbev/msw242
  113. Zhmylev P.Yu., Alekseev Yu.E., Karpukhina E.A., Balandin S.A. 2005. Biomorfologiya rasteniy: illyustrirovannyy slovar. 2nd ed. Moscow: MGU, 256 pp.
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