Ботанический журнал, 2023, T. 108, № 9, стр. 785-820
Структурные и регуляторные аспекты морфогенеза Equisetum sylvaticum и Equisetum fluviatile в связи с гомологией листьев хвощовых и других папоротниковидных
М. А. Романова 1, *, В. В. Домашкина 1, 2, Н. А. Бортникова 2
1 Санкт-Петербургский государственный университет
199034 Санкт-Петербург,
Университетская наб., 7–9, Россия
2 Ботанический институт им. В.Л. Комарова РАН
197376 Санкт-Петербург, ул. Проф. Попова, 2, Россия
* E-mail: m.romanova@spbu.ru
Поступила в редакцию 14.08.2023
После доработки 30.08.2023
Принята к публикации 19.09.2023
- EDN: RBKVVF
- DOI: 10.31857/S0006813623090065
Полные тексты статей выпуска доступны в ознакомительном режиме только авторизованным пользователям.
Аннотация
Изучены строение апикальной меристемы побега, ультраструктура ее клеток и заложение в ней зачатков органов у хвощовых Equisetum sylvaticum и E. fluviatile. Выявлены относительно невысокая степень вакуолизации и структурная однородность клеток зоны поверхностных инициалей, наличие в их пластидах единичных крахмальных зерен и единичных липидных капель в цитоплазме. Эти черты более сходны с таковыми в моноплексной апикальной меристеме плауновидных, чем папоротниковидных. Инициация листьев E. sylvaticum и E. fluviatile сходна с таковой у других растений с моноплексной апикальной меристемой, а основная особенность органогенеза хвощовых – заложение мутовки листьев как единой структуры. Прекращение функционирования апикальной меристемы листа, обусловленное вакуолизацией его апикальной инициали, приводит к отсутствию в листовой пластинке маргинальной меристемы и проводящих тканей. Осуществлен поиск гомологов генов, кодирующих известные для цветковых регуляторы развития адаксиального и абаксиального доменов листа в транскриптомах хвощовых и сравнение их с таковыми в геномах моховидных, папоротниковидных и голосеменных. У хвощовых выявлено по одному регулятору адаксиального (C3HDZ) и абаксиального (KANADI) доменов, как у других папоротниковидных. Это подтверждает вероятную утерю регуляторов адаксиального (ARP) и абаксиального (YABBY) доменов у общего предка Polypodiophyta. Филогенетический анализ белков WOX позволил предположить, что T3 клада, включающая регуляторы маргинальной (WOX3) и пластинчатой (WOX1) меристем листа возникла у общего предка Polypodiophyta, также указывая на сходство в молекулярно-генетической регуляции листьев всех папоротниковидных.
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Список литературы
Bierhorst D.W. 1971. Morphology of vascular plants. New York. 560 p.
Bower F.O. 1935. Primitive land plants-also known as the Archegoniatae. London. 658 p.
Bowman J.L., Briginshaw L.N., Florent S.N. 2019. Evolution and co-option of developmental regulatory networks in early land plants. – Curr. Top. Dev. Biol. 131: 35–53. https://doi.org/10.1016/bs.ctdb.2018.10.001
Bowman J.L., Kohchi T., Yamato K.T., Jenkins J., Shu S., Ishizaki K., Yamaoka S., Nishihama R., Nakamura Y., Berger F., Adam C., Aki S.S., Althoff F., Araki T., Arteaga-Vazquez M.A., Balasubrmanian S., Barry K., Bauer D., Boehm C.R., Briginshaw L., Caballero-Perez J., Catarino B., Chen F., Chiyoda S., Chovatia M., Davies K.M., Delmans M., Demura T., Dierschke T., Dolan L., Dorantes-Acosta A.E., Eklund D.M., Florent S.N., Flores-Sandoval E., Fujiyama A., Fukuzawa H., Galik B., Grimanelli D., Grimwood J., Grossniklaus U., Hamada T., Haseloff J., Hethe-rington A.J., Higo A., Hirakawa Y., Hundley H.N., Ikeda Y., Inoue K., Inoue S., Ishida S., Jia Q., Kakita M., Kanazawa T., Kawai Y., Kawashima T., Kennedy M., Kinose K., Kinoshita T., Kohara Y., Koide E., Komat-su K., Kopischke S., Kubo M., Kyozuka J., Lagercrantz U., Lin S.-S., Lindquist E., Lipzen A.M., Lu C.-W., De Luna E., Martienssen R.A., Minamino N., Mizutani Masaharu, Mizutani Miya, Mochizuki N., Monte I., Mosher R., Nagasaki H., Nakagami H., Naramoto S., Nishitani K., Ohtani M., Okamoto T., Okumura M., Phillips J., Pollak B., Reinders A., Rövekamp M., Sano R., Sawa S., Schmid M.W., Shirakawa M., Solano R., Spunde A., Suetsugu N., Sugano S., Sugiyama A., Sun R., Suzuki Y., Takenaka M., Takezawa D., Tomogane H., Tsuzuki M., Ueda T., Umeda M., Ward J.M., Watanabe Y., Yazaki K., Yokoyama R., Yoshitake Y., Yotsui I., Zachgo S., Schmutz J. 2017. Insights into land plant evolution garnered from the Marchantia polymorpha genome. – Cell. 171: 287–304.e15. https://doi.org/10.1016/j.cell.2017.09.030
Briginshaw L.N., Flores-Sandoval E., Dierschke T., Alvarez J.P., Bowman J.L. 2022. KANADI promotes thallus differentiation and FR-induced gametangiophore formation in the liverwort Marchantia. – New Phytol. 234 (4): 1377–1393. https://doi.org/10.1111/nph.18046
Byrne M.E., Barley R., Curtis M., Arroyo J.M., Dunham M., Hudson A., Martienssen R.A. 2000. Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis. – Nature. 408: 967–971. https://doi.org/10.1038/35050091
Caggiano M.P., Yu X., Bhatia N., Larsson A., Ram H., Ohno C.K., Sappl P., Meyerowitz E.M., Jönsson H., Heisler M.G. 2017. Cell type boundaries organize plant development. – eLife 6: e27421. https://doi.org/10.7554/eLife.27421
Chen H., Fang Y., Zwaenepoel A., Huang S., Van de Peer Y., Li Z. 2023. Revisiting ancient polyploidy in leptosporangiate ferns. New Phytol. Feb; 237 (4): 1405–1417. https://doi.org/. Epub 2022 Dec 7. PMID: 36349406; PMCID: PMC7614084.https://doi.org/10.1111/nph.18607
Cooke T.D., Tilney M.S., Tilney L.G. 1996. Plasmodesmatal networks in apical meristems and mature structures: geometric evidence for both primary and secondary formation of plasmodesmata. – In: Membranes: specialized functions in plants. Cambridge. P. 471–488.
Croxdale J.G. 1978. Salvinia leaves. I. Origin and early differentiation of floating and submerged leaves. – Can. J. Botany. 56 (16): 1982–1991.
Donoghue P.C.J., Harrison C.J., Paps J., Schneider H. 2021. The evolutionary emergence of land plants. – Curr. Biol. 31 (19): R1281–R1298. https://doi.org/10.1016/j.cub.2021.07.038
Du F., Guan C., Jiao Y. 2018. Molecular mechanisms of leaf morphogenesis. – Mol. Plant. 11 (9): 1117–1134. https://doi.org/10.1016/j.molp.2018.06.006
Du H., Ran J., Feng Y., Wang X. 2020. The flattened and needlelike leaves of the pine family (Pinaceae) share a conserved genetic network for adaxial-abaxial polarity but have diverged for photosynthetic adaptation. – BMC Evol. Biol. 20:131. https://doi.org/10.1186/s12862-020-01694-5
Emery J.F., Floyd S.K., Alvarez J., Eshed Y., Hawker N.P., Izhaki A., Baum S.F., Bowman J.L. 2003. Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. – Curr. Biol. 13 (20): 1768–1774. https://doi.org/10.1016/j.cub.2003.09.035
[Esau] Эсау К. 1969. Анатомия растений. М. 564 с.
Eshed Y., Izhaki A., Baum S.F., Floyd S.K., Bowman J.L. 2004. Asymmetric leaf development and blade expansion in Arabidopsis are mediated by KANADI and YABBY activities. – Development. 131 (12): 2997–3006. https://doi.org/10.1242/dev.01186
Evkaikina A.I., Berke L., Romanova M.A., Proux-Wéra E., Ivanova A.N., Rydin C., Pawlowski K., Voitsekhovskaja O.V. 2017. The Huperzia selago shoot tip transcriptome sheds new light on the evolution of leaves. – Genome Biol. Evol. 9 (9): 2444–2460. https://doi.org/10.1093/gbe/evx169
Finet C., Floyd S.K., Conway S.J., Zhong B., Scutt C.P., Bowman J.L. 2016. Evolution of the YABBY gene family in seed plants. – Evol. Dev. 18: 116–126. https://doi.org/10.1111/ede.12173
Floyd S.K., Bowman J.L. 2006. Distinct developmental mechanisms reflect the independent origins of leaves in vascular plants. – Curr. Biol. 16 (19): 1911–1917. https://doi.org/10.1016/j.cub.2006.07.067
Floyd S.K., Zalewski C.S., Bowman J.L. 2006. Evolution of class III homeodomain-leucine zipper genes in Streptophytes. – Genetics. 173(1): 373–388.https://doi.org/10.1534/genetics.105.054239
Frank M.H., Edwards M.B., Schultz E.R., McKain M.R., Fei Z., Sørensen I., et al. 2015. Dissecting the molecular signatures of apical cell-type shoot meristems from two ancient land plant lineages. – New Phytol. 207: 893–904. https://doi.org/10.1111/nph.13407
Gifford E.M., Foster A.S. 1989. Morphology and evolution of vascular plants. New York. 626 p.
Golub S.J., Wetmore R.H. 1948a. Studies of development in the vegetative shoot of Equisetum arvense L. I. The Shoot Apex. – Am. J. Bot. 35 (10): 755–767. https://doi.org/10.2307/2438157
Golub S.J., Wetmore R.H. 1948b. Studies of development in the vegetative shoot of Equisetum arvense L. II. The Mature Shoot. – Am. J. Bot. 35 (10): 767–781. https://doi.org/10.2307/2438158
Goodstein D.M., Shu S., Howson R., Neupane R., Hayes R.D., Fazo J., Mitros T., Dirks W., Hellsten U., Putnam N., Rokhsar D.S. 2012. Phytozome: a comparative platform for green plant genomics. – Nucleic Acids Res. 40 (D1): D1178–D1186. https://doi.org/10.1093/nar/gkr944
Gouy M., Guindon S., Gascuel O. 2010. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. – Mol. Biol. Evol. 27 (2): 221–224. https://doi.org/10.1093/molbev/msp259
Harrison C.J., Corley S.B., Moylan E.C., Alexander D.L., Scotland R.W., Langdale J.A. 2005. Independent recruitment of a conserved developmental mechanism during leaf evolution. – Nature. 434: 509–514. https://doi.org/10.1038/nature03410
Harrison C.J., Morris J.L. 2018. The origin and early evolution of vascular plant shoots and leaves. – Philos. T. Roy. Soc. B. 373 (1739): 20160496. https://doi.org/10.1098/rstb.2016.0496
Harrison C.J., Rezvani M., Langdale J.A. 2007. Growth from two transient apical initials in the meristem of Selaginella kraussiana. – Development. 134 (5): 881–889. https://doi.org/10.1242/dev.001008
Hedman H., Zhu T., von Arnold S., Sohlberg J.J. 2013. Analysis of the WUSCHEL-RELATED HOMEOBOX gene family in the conifer Picea abies reveals extensive conservation as well as dynamic patterns. – BMC Plant Biol. 13: 89. https://doi.org/10.1186/1471-2229-13-89
Hernández-Hernández B., Tapia-López R., Ambrose B.A., Vasco A. 2021. R2R3-MYB gene evolution in plants, incorporating ferns into the story. – Int. J. Plant. Sci. 182 (1): 1–8. https://doi.org/10.1086/710579
Hirakawa Y. 2022. Evolution of meristem zonation by CLE gene duplication in land plants. – Nature Plants. 8: 735–740. https://doi.org/10.1038/s41477-022-01199-7
HmmerWeb 2.43. 19 May 2023. https://www.ebi.ac.uk/Tools/hmmer/search/hmmsearch
Hornwort genomes. 19 May 2023. https://www.hornworts.uzh.ch/en/hornwort-genomes.html
Hou G.C., Hill J.P. 2004. Developmental anatomy of the fifth shoot-borne root in young sporophytes of Ceratopteris richardii. – Planta. 219 (2): 212–20. https://doi.org/10.1007/s00425-004-1225-6
Huang X., Wang W., Gong T., Wickell D., Kuo L.-Y., Zhang X., Wen J., Kim H., Lu F., Zhao H., Chen Song, Li H., Wu W., Yu C., Chen Su, Fan W., Chen Shuai, Bao X., Li L., Zhang D., Jiang L., Yan X., Liao Z., Zhou G., Guo Y., Ralph J., Sederoff R.R., Wei H., Zhu P., Li F.-W., Ming R., Li Q. 2022. The flying spider-monkey tree fern genome provides insights into fern evolution and arborescence. – Nat. Plants. 8: 500–512. https://doi.org/10.1038/s41477-022-01146-6
Imaichi R., Hiratsuka R. 2007. Evolution of shoot apical meristem structures in vascular plants with respect to plasmodesmatal network. – Am. J. Bot. 94 (12): 1911–1921. https://doi.org/10.3732/ajb.94.12.1911
Jackson D., Veit B., Hake S. 1994. Expression of maize KNOTTED1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot. – Development. 120 (2): 405–413.
Kaplan D.R. 2001. The science of plant morphology: definition, history, and role in modern biology. – Am. J. Bot. 88 (10): 1711–1741. https://doi.org/10.2307/3558347
Kenrick P., Crane P. 1997. The origin and early diversification of land plants: a cladistic study. Washington. 441 p.
[Koteeva] Котеева Н.К. 1997. Изменение ультраструктуры клеток апикальной меристемы побега Pinus sylvestris (Pinaceae) в годичном цикле. – Бот. журн. 82 (6): 10–23.
Li F.-W., Nishiyama T., Waller M., Frangedakis E., Keller J., Li Z., Fernandez-Pozo N., Barker M.S., Bennett T., Blázquez M.A., Cheng S., Cuming A.C., de Vries J., de Vries S., Delaux P.-M., Diop I.S., Harrison C.J., Hauser D., Hernández-García J., Kirbis A., Meeks J.C., Monte I., Mutte S.K., Neubauer A., Quandt D., Robison T., Shimamura M., Rensing S.A., Villarreal J.C., Weijers D., Wicke S., Wong G.K.-S., Sakakibara K., Szövényi P. 2020. Anthoceros genomes illuminate the origin of land plants and the unique biology of hornworts. – Nat. Plants. 6: 259–272. https://doi.org/10.1038/s41477-020-0618-2
Liu H., Wang Q.F., Taylor W.C. 2006. Morphological and anatomical variation in sporophylls of Isoetes sinensis Palmer (Isoetaceae), an endangered quillwort in China. – Am. Fern J. 96 (3): 67–74. https://doi.org/10.1640/0002-8444
Lumpkin T.A., Plucknett D.L. 1980. Azolla: Botany, physiology, and use as a green manure. – Econ. Bot. 34: 111–153. https://doi.org/10.1007/BF02858627
Lyons E., Freeling M. 2008. How to usefully compare homologous plant genes and chromosomes as DNA sequences. – Plant J. 53 (4): 661–673. https://doi.org/10.1111/j.1365-313X.2007.03326.x
Morris J.L., Puttick M.N., Clark J.W., Edwards D., Kenrick P., Pressel S., Wellman C.H., Yang Z., Schneider H., Donoghue P. 2018. The timescale of early land plant evolution. – PNAS. 115 (10): 2274–2283. https://doi.org/10.1073/pnas.1719588115
Mueller R.J. 1983. Indeterminate growth and ramification of the climbing leaves of Lygodium japonicum (Schizaeaceae). – Am. J. Bot. 70 (5): 682–690.
Nakata M., Matsumoto N., Tsugeki R., Rikirsch E., Laux T., Okada K. 2012. Roles of the middle domain-specific WUSCHEL-RELATED HOMEOBOX genes in early development of leaves in Arabidopsis. – Plant Cell. 24: 519–535. https://doi.org/10.1105/tpc.111.092858
Napp-Zinn K. 1966. Anatomie des Blattes. Blattanatomie der Gymnospermen. Berlin.
Nardmann J., Werr W. 2012. The invention of WUS-like stem cell-promoting functions in plants predates leptosporangiate ferns. – Plant Mol. Biol. 78: 123–134. https://doi.org/10.1007/s11103-011-9851-4
Nardmann J., Werr W. 2013. Symplesiomorphies in the WUSCHEL clade suggest that the last common ancestor of seed plants contained at least four independent stem cell niches. – New Phytol. 199: 1081–1092. https://doi.org/10.1111/nph.12343
National Center for Biotechnology Information (NCBI). 19 May 2023. https://www.ncbi.nlm.nih.gov/
[Naumenko, Romanova] Науменко А.Н., Романова М.А. 2008. Апикальный морфогенез Psilotum nudum (Psilotaceae) и Botrychium lunaria (Ophioglossaceae). – Вестн. С.-Петерб. ун-та. Сер. 3. 2: 15–27.
Newman I.V. 1965. Pattern in the meristems of vascular plants: III. Pursuing the patterns in the apical meristem where no cell is a permanent cell. – J. Linn. Soc. Lond. Bot. 59: 185–214. https://doi.org/10.1111/j.1095-8339.1965.tb00057.x
Nystedt B., Street N.R., Wetterbom A., Zuccolo A., Lin Y.-C., Scofield D.G., Vezzi F., Delhomme N., Giacomello S., Alexeyenko A., Vicedomini R., Sahlin K., Sherwood E., Elfstrand M., Gramzow L., Holmberg K., Hällman J., Keech O., Klasson L., Koriabine M., Kucukoglu M., Käller M., Luthman J., Lysholm. F, Niittylä T., Olson Å., Rilakovic N., Ritland C., Ros-selló J.A., Sena J., Svensson T., Talavera-López C., Theißen G., Tuominen H., Vanneste K., Wu Z-Q., Zhang B., Zerbe P., Arvestad L., Bhalerao R., Bohlmann J., Bousquet J., Gil R.G., Hvidsten T.R., de Jong P., MacKay J., Morgante M., Ritland K., Sundberg B., Thompson S.L., Van de Peer Y., Andersson B., Nilsson O., Ingvarsson P.K., Lundeberg J., Jansson S. 2013. The Norway spruce genome sequence and conifer genome evolution. – Nature. 497: 579–584. https://doi.org/10.1038/nature12211
One Thousand Plant Transcriptomes Initiative. 2019. One thousand plant transcriptomes and the phylogenomics of green plants. – Nature. 574 (7780): 679–685. https://doi.org/10.1038/s41586-019-1693-2
Owens I.N. 1968. Initiation and development of leaves in Douglas fir. – Can. J. Bot. 46 (3): 271–278.
Paysan-Lafosse T., Blum M., Chuguransky S., Grego T., Pinto B.L., Salazar G.A., Bileschi M.L., Bork P., Bridge A., Colwell L., Gough J., Haft D.H., Letunić I., Marchler-Bauer A., Mi H., Natale D.A., Orengo C.A., Pandurangan A.P., Rivoire C., Sigrist C.J.A., Sillitoe I., Thanki N., Thomas P.D., Tosatto S.C.E, Wu C.H., Bateman A. 2022. InterPro in 2022. – Nucleic Acids Res. 51 (D1): D418-D427. https://doi.org/10.1093/nar/gkac993
PPG I. 2016. A community-derived classification for extant lycophytes and ferns. – J. Syst. Evol. 54: 563–603. https://doi.org/10.1111/jse.12229
Romani F., Reinheimer R., Florent S.N., Bowman J.L., Moreno J.E. 2018. Evolutionary history of HOMEODOMAIN LEUCINE ZIPPER transcription factors during plant transition to land. – New Phytol. 219 (1): 408–421. https://doi.org/10.1111/nph.15133
Romanova M., Jernstedt J. 2005. Morphogenetic events in the Ceratopteris richardii shoot apex. – Fern. Gaz. 17: 204.
[Romanova, Borisovskaya] Романова М.А., Борисовская Г.М. 2004. Принципы структурной организации вегетативного тела папоротников: онтогенетический подход. – Бот. журн. 89 (5): 705–717.
[Romanova et al.] Романова М.А., Науменко А.Н., Евкайкина А.И. 2010. Особенности апикального морфогенеза в разных таксонах несеменных растений. – Вестн. С.-Петерб. ун-та. Сер. 3. 3: 29–41.
Romanova M.A., Domashkina V.V., Maksimova A.I., Pawlowski K., Voitsekhovskaja O.V. 2023. All together now: Cellular and molecular aspects of leaf development in lycophytes, ferns, and seed plants. – Front. Ecol. Evol. 11. https://doi.org/10.3389/fevo.2023.1097115
[Romanova et al.] Романова М.А., Яковлева О.В., Максимова А.И., Иванова А.Н., Домашкина В.В. 2022. Строение апикальных меристем побегов и особенности ультраструктуры их клеток у плауновидных и папоротниковидных. – Бот. журн. 107 (9): 65–85. https://doi.org/10.31857/S0006813622090095
Ruzin S.E. 1999. Plant microtechnique and microscopy. Oxford. 322 p.
Sakakibara K., Reisewitz P., Aoyama T., Friedrich T., Ando S., Sato Y. 2014. WOX13-like genes are required for reprogramming of leaf and protoplast cells into stem cells in the moss Physcomitrella patens. – Development. 141 (8): 1660–1670. https://doi.org/10.1242/dev.097444
Sarojam R., Sappl P.G., Goldshmidt A., Efroni I., Floyd S.K., Eshed Y., Bowman J.L. 2010. Differentiating Arabidopsis shoots from leaves by combined YABBY activities. – Plant Cell. 22 (7): 2113–2130. https://doi.org/10.1105/tpc.110.075853
Sarvepalli K., Das Gupta M., Challa K.R., Nath U. 2019. Molecular cartography of leaf development – role of transcription factors. – Curr. Opin. Plant Biol. 47: 22–31. https://doi.org/10.1016/j.pbi.2018.08.002
Sawa S., Watanabe K., Goto K., Kanaya E., Morita E.H., Okada K. 1999. FILAMENTOUS FLOWER, a meristem and organ identity gene of Arabidopsis, encodes a protein with a zinc finger and HMG-related domains. – Genes Dev. 13 (9): 1079–1088. https://doi.org/10.1101/gad.13.9.1079
Schneider H., Pryer K.M., Cranfill R., Smith A.R., Wolf P.G. 2002. Evolution of vascular plant body plans: a phylogenetic perspective. – In: Developmental Genetics and Plant Evolution. P. 330–364. https://doi.org/10.1201/9781420024982.ch17
[Skupchenko] Скупченко В.Б. 2019. Клеточный рост основной паренхимы стебля в морфогенезе побега Piceа abies (Pinaceae). – Раст. ресурсы. 55: 195–212. https://doi.org/10.1134/S0033994619020092
[Skupchenko, Ladanova] Скупченко В.Б., Ладанова Н.В. 1984. Структура однолетней хвои в кроне Picea obovata (Pinaceae). – Бот. журн. 69 (7): 203–206.
Spencer V., Venza Z.N., Harrison C.J. 2021. What can lycophytes teach us about plant evolution and development? Modern perspectives on an ancient lineage. – Evol. Dev. 23: 174–196. https://doi.org/10.1111/ede.12350
Steeves T.A., Sussex I.M. 1989. Patterns in plant development. Cambridge. 388 p.
Stöver B.C., Müller K.F. 2010. TreeGraph 2: Combining and visualizing evidence from different phylogenetic analyses. – BMC Bioinformatics. 11: 7. https://doi.org/10.1186/1471-2105-11-7
Sundell D., Mannapperuma C., Netotea S., Delhomme N., Lin Y.C., Sjödin A., Van de Peer Y., Jansson S., Hvidsten T.R., Street N.R. 2015. The Plant Genome Integrative Explorer Resource: PlantGenIE.org. – New Phytol. 208 (4): 1149–1156. https://doi.org/10.1111/nph.13557
Szövényi P., Waller M., Kirbis A. 2019. Evolution of the plant body plan. Curr. Top. Devel. Biol. 131: 1–34. https://doi.org/10.1186/1471-2105-11-7
Timothy L., Bailey T., Elkan C. 1994. Fitting a mixture model by expectation maximization to discover motifs in biopolymers. – Proc. Int. Conf. Intell. Syst. Mol. Biol. 2: 28–36. https://doi.org/7584402
Tomescu A.M.F. 2009. Megaphylls, microphylls and the evolution of leaf development. – Trends in Plant Science. 14 (1): 5–12. https://doi.org/10.1016/j.tplants.2008.10.008
Tomescu A.M.F., Escapa I.H., Rothwell G.W., Elgorriaga A., Cúneo N.R. 2017. Developmental programmes in the evolution of Equisetum reproductive morphology: a hierarchical modularity hypothesis. – Ann. Bot. 119 (4): 489–505. https://doi.org/10.1093/aob/mcw273
Trifinopoulos J., Nguyen L.-T., von Haeseler A., Minh B.Q. 2016. W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. – Nucleic Acids Res. 44 (W1): W232–W235. https://doi.org/10.1093/nar/gkw256
Tsukaya H. 2021. The leaf meristem enigma: The relationship between the plate meristem and the marginal meristem. – The Plant Cell. 33 (10): 3194–3206. https://doi.org/10.1093/plcell/koab190
van der Graaff E., Laux T., Rensing S. 2009. The WUS homeobox-containing (WOX) protein family. – Genome Biology. 10 (12): 248. pmid:20067590
Vanneste K., Sterck L., Myburg A.A., Van de Peer Y., Mizrachi E. 2015. Horsetails Are Ancient Polyploids: Evidence from Equisetum giganteum. – Plant Cell. 27 (6): 1567–78. Epub 2015 May 22. PMID; PMCID: PMC4498207.https://doi.org/10.1105/tpc.15.0015726002871
Vasco A., Ambrose B.A. 2020. Simple and divided leaves in ferns: exploring the genetic basis for leaf morphology differences in the genus Elaphoglossum (Dryopteridaceae). – Int. J. Mol. Sci. 21 (15): 5180. https://doi.org/10.3390/ijms21155180
Vasco A., Moran R.C., Ambrose B.A. 2013. The evolution, morphology and development of fern leaves. – Front. Plant Sci. 4: 345. https://doi.org/10.3389/fpls.2013.00345
Vasco A., Smalls T.L., Graham S.W., Cooper E.D., Wong G.K., Stevenson D.W., Moran R.C., Ambrose B.A. 2016. Challenging the paradigms of leaf evolution: Class III HD-Zips in ferns and lycophytes. – New Phytol. 212 (3): 745–758. https://doi.org/10.1111/nph.14075
Wang B., Yeun L.H., Xue J.Y., Liu Y., Ané J. M., Qiu Y.L. 2010. Presence of three mycorrhizal genes in the common ancestor of land plants suggests a key role of mycorrhizas in the colonization of land by plants. – The New Phytol. 186 (5): 514–525. https://doi.org/10.1111/j.1469-8137.2009.03137.x
Wardlaw C.W. 1949. Experimental and analytical studies of pteridophytes: XIV. Leaf formation and phyllotaxis in Dryopteris aristata Druce. – Ann. Bot. 13 (2): 163–198.
White R., Turner M. 1995. Anatomy and development of the fern sporophyte. – Bot. Rev. 61 (4): 281–305. https://doi.org/10.1007/BF02912620
Wickell D., Kuo L.Y., Yang H.P. et al. 2021. Underwater CAM photosynthesis elucidated by Isoetes genome. – Nat Commun. 12: 6348. https://doi.org/10.1038/s41467-021-26644-7
Wu C.C., Li F.W., Kramer E.M. 2019. Large-scale phylo-genomic analysis suggests three ancient superclades of the WUSCHEL-RELATED HOMEOBOX transcription factor family in plants. – PloS One. 14 (10): e0223521. https://doi.org/10.1371/journal.pone.0223521
Xia Z., Liu L., Wei Z., Wang F., Shen H., Yan Y. 2022. Analysis of comparative transcriptome and positively selected genes reveal adaptive evolution in leaf-less and root-less whisk ferns. – Plants. 11 (9): 1198. https://doi.org/10.3390/plants11091198
Yamaguchi T., Nukazuka A., Tsukaya H. 2012. Leaf adaxial-abaxial polarity specification and lamina outgrowth: evolution and development. – Plant Cell Physiol. 53 (7): 1180–1194. https://doi.org/10.1093/pcp/pcs074
Yang M., You W., Wu S., Fan Z., Xu B., Zhu M., Li X., Xiao Y. 2017. Global transcriptome analysis of Huperzia serrata and identification of critical genes involved in the biosynthesis of huperzine A. – BMC Genomics. 18 (1): 245. https://doi.org/10.1186/s12864-017-3615-8
Yip H.K., Floyd S.K., Sakakibara K., Bowman J.L. 2016. Class III HD-Zip activity coordinates leaf development in Physcomitrella patens. – Dev. Biol. 419 (1): 184–197. https://doi.org/10.1016/j.ydbio.2016.01.012
Zimmerman W. 1952. Main results of the “Telome Theory”. – Paleobotanist. 1: 456–470.
Zumajo-Cardona C., Ambrose B. A. 2020. Phylogenetic analyses of key developmental genes provide insight into the complex evolution of seeds. – Mol. Phylogenet. Evol. 147: 106778. https://doi.org/10.1016/j.ympev.2020.106778
Zumajo-Cardona C., Vasco A., Ambrose B.A. 2019. The evolution of the KANADI gene family and leaf development in lycophytes and ferns. – Plants (Basel). 8 (9): 313. https://doi.org/10.3390/plants8090313
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