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Zygnematophyceae

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Zygnematophyceae
Conjugation in Spirogyra.
Scientific classification Edit this classification
Clade: Viridiplantae
(unranked): Charophyta
Class: Zygnematophyceae
Round, 1971
Subclasses
Synonyms[1]
  • Akontae Blackman & Tansley, 1902
  • Conjugatophyceae Engler, 1892
  • 'Conjugatae' Engler, 1892
  • Gamophyceae
  • Saccodermae Pascher ex Kossinskaja, 1952
  • Zygnemaphyceae Round 1971
  • Zygophyceae Widder, 1960

Zygnematophyceae (or Conjugatophyceae) is a class of green algae in the paraphylum streptophyte algae, also referred to as Charophyta,[2] consisting of more than 4000 described species.[3] The Zygnematophyceae are the sister clade of the Embryophyta (land plants).[4][5][6]

Common members of the Zygnematophyceae include the filamentous algae Spirogyra and Mougeotia, as well as desmids, which are microscopic algae characterized by symmetrical and elaborately ornate cells.[7]

Morphology

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The body plan of Zygnematophyceae is simple, and the group appears to have gone through a secondary loss of morphological complexity.[8] The most basal members are unicellular, but filamentous species have evolved at least five times,[9] and a few species form colonies.[7] Each cell contains a single nucleus.[7]

The chloroplasts of the Zygnematophyceae are large, typically axile but sometimes parietally located, and contain one or several pyrenoids. One or several chloroplasts may be present in a single cell. The shape of the chloroplast may be star-shaped (in Zygnema), ribbon-shaped (in Spirogyra), or elaborately lobed and dissected. In some taxa, particularly Mougeotia, the chloroplast is able to move in response to different light conditions.[7]

In the Zygnematophyceae, cell walls are composed of three layers: one outer layer consisting of mucus, a primary wall consisting of microfibrils, and an innermost layer of cellulosic microfibrils. Some species shed their primary wall and retain only the innermost layer. The cell wall may be variously decorated with striations, granules, or spines. In the Desmidiales, there are pores in the cell wall which allow the cell to extrude a layer of mucilage for protection.[7]

Several Zygnematophyceae contain genes involved in protection from desiccation that appear to have been derived by horizontal gene transfer from bacteria; the genes are found in plants, Zygnematophyceae, and bacteria, but no other organisms. The genes may have helped to enable plants to make the transition to life on land.[10][11]

A new subclass called Spirogloeophycidae, represented by the species Spirogloea muscicola, was established after the unicellular subaerial algae, resembling a "gelatinous blob", was rediscovered on a rock close to a river bank near Cologne in 2006, after first being discovered in France in 1845.[12]

Reproduction

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The Zygnematophyceae are able to reproduce both asexually and sexually. Asexual reproduction takes place via fragmentation, cell division, akinete formation, or parthenospores.[7]

Sexual reproduction in the Zygnematophyceae takes place through a process called conjugation.[13] Unusually, the gametes lack flagella,[7] and they also lack centrioles which suggest that flagella were not secondarily lost. This lack of flagella sets the Zygnematophyceae apart from nearly all groups of algae, except for red algae and cyanobacteria (also known as blue-green algae, if they are classified as such).[1] The gametes are scarcely differentiated from vegetative cells.[7]

In conjugation, cells or filaments of opposite sex line up, and tubes form between corresponding cells. The male cells then become amoeboid and crawl across the female, or sometimes both cells crawl into the connecting tube. The cells then meet and fuse to form a zygote, which later undergoes meiosis to produce new cells or filaments. As in land plants, only the female passes its chloroplasts on to the offspring.[14]

Taxonomy

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The Zygnematophyceae is monophyletic. Traditionally, it has been known to contain two orders, the Zygnematales and Desmidiales.[7] However, the Zygnematales were found to be paraphyletic with respect to the Desmidiales, and so it was split up. As of 2023, five orders and two subclasses are recognized: the Spirogloeales in Spirogloeophycidae, and the Serritaeniales, the Zygnematales, the Spirogyrales, and the Desmidiales in Zygnematophycidae.[9]

Class Zygnematophyceae[15]

Phylogeny

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A phylogeny of the families of Zygnematophyceae is presented below:[16][11]

Zygnematophyceae

Habitat

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Members of the Zygnematophyceae are common in nearly all freshwater habitats, particularly filamentous genera such as Spirogyra and Mougeotia. Some Spirogyra species can tolerate disturbed habitats. On the other hand, desmids (the Desmidiales) often prefer bogs, peatlands, and lakes.[17]

Fossil record

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Vegetative cells of the Zygnematophyceae are fragile and usually not preserved, but the zygospores are resistant to decay and can become fossilized. The Zygnematophyceae have been recorded from at least the middle Devonian period, and before the Carboniferous period, all the major groups had diverged. Fossils of zygospores are indicators of warming spring conditions and shallow, stagnant mesotrophic habitats.[7]

Genomes

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The first genomes published for Zygnematophyceae were Mesotaenium endlicherianum and Spirogloea muscicola.[11] Since then, genomes have been published on Penium margaritaceum,[18] Zygnema spp.,[19] and the Closterium peracerosum–strigosum–littorale complex.[20] Furthermore, the gene models of Mesotaenium endlicherianum have been updated.[21]

References

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  1. ^ a b Guiry, Michael D. (15 March 2013). "Taxonomy and nomenclature of the Conjugatophyceae (= Zygnematophyceae)". Algae. 28 (1): 1–29. doi:10.4490/algae.2013.28.1.001. hdl:10379/11755.
  2. ^ Gontcharov, A. A.; Marin, B; Melkonian, M (5 December 2003). "Are Combined Analyses Better Than Single Gene Phylogenies? A Case Study Using SSU rDNA and rbcL Sequence Comparisons in the Zygnematophyceae (Streptophyta)". Molecular Biology and Evolution. 21 (3): 612–624. doi:10.1093/molbev/msh052. PMID 14739253.
  3. ^ Pichrtová, Martina; Holzinger, Andreas; Kulichová, Jana; Ryšánek, David; Šoljaková, Tereza; Trumhová, Kateřina; Nemcova, Yvonne (8 October 2018). "Molecular and morphological diversity of Zygnema and Zygnemopsis (Zygnematophyceae, Streptophyta) from Svalbard (High Arctic)". European Journal of Phycology. 53 (4): 492–508. doi:10.1080/09670262.2018.1476920. PMC 6235541. PMID 30487730.
  4. ^ Wickett, Norman J.; Mirarab, Siavash; Nguyen, Nam; Warnow, Tandy; Carpenter, Eric; Matasci, Naim; Ayyampalayam, Saravanaraj; Barker, Michael S.; Burleigh, J. Gordon; Gitzendanner, Matthew A.; Ruhfel, Brad R.; Wafula, Eric; Der, Joshua P.; Graham, Sean W.; Mathews, Sarah; Melkonian, Michael; Soltis, Douglas E.; Soltis, Pamela S.; Miles, Nicholas W.; Rothfels, Carl J.; Pokorny, Lisa; Shaw, A. Jonathan; DeGironimo, Lisa; Stevenson, Dennis W.; Surek, Barbara; Villarreal, Juan Carlos; Roure, Béatrice; Philippe, Hervé; dePamphilis, Claude W.; Chen, Tao; Deyholos, Michael K.; Baucom, Regina S.; Kutchan, Toni M.; Augustin, Megan M.; Wang, Jun; Zhang, Yong; Tian, Zhijian; Yan, Zhixiang; Wu, Xiaolei; Sun, Xiao; Wong, Gane Ka-Shu; Leebens-Mack, James (11 November 2014). "Phylotranscriptomic analysis of the origin and early diversification of land plants". Proceedings of the National Academy of Sciences. 111 (45): E4859–E4868. Bibcode:2014PNAS..111E4859W. doi:10.1073/pnas.1323926111. PMC 4234587. PMID 25355905.
  5. ^ de Vries, Jan; Stanton, Amanda; Archibald, John M.; Gould, Sven B. (June 2016). "Streptophyte Terrestrialization in Light of Plastid Evolution". Trends in Plant Science. 21 (6): 467–476. doi:10.1016/j.tplants.2016.01.021. PMID 26895731.
  6. ^ Gitzendanner, Matthew A.; Soltis, Pamela S.; Wong, Gane K.-S.; Ruhfel, Brad R.; Soltis, Douglas E. (March 2018). "Plastid phylogenomic analysis of green plants: A billion years of evolutionary history". American Journal of Botany. 105 (3): 291–301. doi:10.1002/ajb2.1048. PMID 29603143.
  7. ^ a b c d e f g h i j Hall, John D.; McCourt, Richard M. (2017). "Zygnematophyta". Handbook of the Protists. pp. 135–163. doi:10.1007/978-3-319-28149-0_41. ISBN 978-3-319-28149-0.
  8. ^ Nishiyama, Tomoaki; Sakayama, Hidetoshi; de Vries, Jan; Buschmann, Henrik; Saint-Marcoux, Denis; Ullrich, Kristian K.; Haas, Fabian B.; Vanderstraeten, Lisa; Becker, Dirk; Lang, Daniel; Vosolsobě, Stanislav; Rombauts, Stephane; Wilhelmsson, Per K.I.; Janitza, Philipp; Kern, Ramona; Heyl, Alexander; Rümpler, Florian; Villalobos, Luz Irina A. Calderón; Clay, John M.; Skokan, Roman; Toyoda, Atsushi; Suzuki, Yutaka; Kagoshima, Hiroshi; Schijlen, Elio; Tajeshwar, Navindra; Catarino, Bruno; Hetherington, Alexander J.; Saltykova, Assia; Bonnot, Clemence; Breuninger, Holger; Symeonidi, Aikaterini; Radhakrishnan, Guru V.; Van Nieuwerburgh, Filip; Deforce, Dieter; Chang, Caren; Karol, Kenneth G.; Hedrich, Rainer; Ulvskov, Peter; Glöckner, Gernot; Delwiche, Charles F.; Petrášek, Jan; Van de Peer, Yves; Friml, Jiri; Beilby, Mary; Dolan, Liam; Kohara, Yuji; Sugano, Sumio; Fujiyama, Asao; Delaux, Pierre-Marc; Quint, Marcel; Theißen, Günter; Hagemann, Martin; Harholt, Jesper; Dunand, Christophe; Zachgo, Sabine; Langdale, Jane; Maumus, Florian; Van Der Straeten, Dominique; Gould, Sven B.; Rensing, Stefan A. (July 2018). "The Chara Genome: Secondary Complexity and Implications for Plant Terrestrialization". Cell. 174 (2): 448–464.e24. doi:10.1016/j.cell.2018.06.033. PMID 30007417. S2CID 206569169.
  9. ^ a b Hess, Sebastian; Williams, Shelby K.; Busch, Anna; Irisarri, Iker; Delwiche, Charles F.; Vries, Sophie de; Darienko, Tatyana; Roger, Andrew J.; Archibald, John M.; Buschmann, Henrik; Schwartzenberg, Klaus von; Vries, Jan de (2022-09-01). "A phylogenomically informed five-order system for the closest relatives of land plants". Current Biology. 32 (20): 4473–4482.e7. doi:10.1016/j.cub.2022.08.022. ISSN 0960-9822. PMC 9632326. PMID 36055238.
  10. ^ Zimmer, Carl (14 November 2019). "How Did Plants Conquer Land? These Humble Algae Hold Clues". The New York Times.
  11. ^ a b c d Cheng, Shifeng; Xian, Wenfei; Fu, Yuan; Marin, Birger; Keller, Jean; Wu, Tian; Sun, Wenjing; Li, Xiuli; Xu, Yan; Zhang, Yu; Wittek, Sebastian; Reder, Tanja; Günther, Gerd; Gontcharov, Andrey; Wang, Sibo; Li, Linzhou; Liu, Xin; Wang, Jian; Yang, Huanming; Xu, Xun; Delaux, Pierre-Marc; Melkonian, Barbara; Wong, Gane Ka-Shu; Melkonian, Michael (2019). "Genomes of Subaerial Zygnematophyceae Provide Insights into Land Plant Evolution". Cell. 179 (5): 1057–1067.e14. doi:10.1016/j.cell.2019.10.019. PMID 31730849.
  12. ^ Ancient plants learned to survive on land by stealing other species' DNA
  13. ^ Kapraun, D. F. (30 November 2006). "Nuclear DNA Content Estimates in Green Algal Lineages: Chlorophyta and Streptophyta". Annals of Botany. 99 (4): 677–701. doi:10.1093/aob/mcl294. PMC 2802934. PMID 17272304.
  14. ^ Permann C, Píchrtová M, Šoljaková T, Herburger K, Jouneau PH, Uwizeye C, Falconet D, Marechai E, Holzinge A (August 23, 2023). Pfeifer L (ed.). "3D-reconstructions of zygospores in Zygnema vaginatum (Charophyta) reveal details of cell wall formation, suggesting adaptations to extreme habitats". Physiologia Plantarum. 175 (4): e13988. doi:10.1111/ppl.13988. PMID 37616005.
  15. ^ Guiry, M.D.; Guiry, G.M. "Zygnematophyceae". AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. Retrieved 2023-04-30.
  16. ^ Stancheva, Rosalina; Hall, John D.; Herburger, Klaus; Lewis, Louise A.; Mccourt, Richard M.; Sheath, Robert; Holzinger, Andreas (July 2014). "Phylogenetic position of Zygogonium ericetorum (Zygnematophyceae, Charophyta) from a high alpine habitat and ultrastructural characterization of unusual aplanospores". Journal of Phycology. 50 (5): 790–803. doi:10.1111/jpy.12229. PMC 4370237. PMID 25810560.
  17. ^ Hall, John D.; McCourt, Richard M. (2014). "Chapter 9. Conjugating Green Algae Including Desmids". In Wehr, John D.; Sheath, Robert G.; Kociolek, J. Patrick (eds.). Freshwater Algae of North America: Ecology and Classification (2 ed.). Elsevier Inc. ISBN 978-0-12-385876-4.
  18. ^ Jiao, Chen; Sørensen, Iben; Sun, Xuepeng; Sun, Honghe; Behar, Hila; Alseekh, Saleh; Philippe, Glenn; Palacio Lopez, Kattia; Sun, Li; Reed, Reagan; Jeon, Susan; Kiyonami, Reiko; Zhang, Sheng; Fernie, Alisdair R.; Brumer, Harry (May 2020). "The Penium margaritaceum Genome: Hallmarks of the Origins of Land Plants". Cell. 181 (5): 1097–1111.e12. doi:10.1016/j.cell.2020.04.019. PMID 32442406. S2CID 218763002.
  19. ^ Feng, Xuehuan; Zheng, Jinfang; Irisarri, Iker; Yu, Huihui; Zheng, Bo; Ali, Zahin; De Vries, Sophie; Keller, Jean; Fürst-Jansen, Janine M.R. (2023-02-01). Chromosome-level genomes of multicellular algal sisters to land plants illuminate signaling network evolution (Report). Evolutionary Biology. doi:10.1101/2023.01.31.526407. PMC 9915684. PMID 36778228.
  20. ^ Sekimoto, Hiroyuki; Komiya, Ayumi; Tsuyuki, Natsumi; Kawai, Junko; Kanda, Naho; Ootsuki, Ryo; Suzuki, Yutaka; Toyoda, Atsushi; Fujiyama, Asao; Kasahara, Masahiro; Abe, Jun; Tsuchikane, Yuki; Nishiyama, Tomoaki (March 2023). "A divergent RWP‐RK transcription factor determines mating type in heterothallic Closterium". New Phytologist. 237 (5): 1636–1651. doi:10.1111/nph.18662. ISSN 0028-646X. PMID 36533897. S2CID 254918679.
  21. ^ Dadras, Armin; Fürst-Jansen, Janine M. R.; Darienko, Tatyana; Krone, Denis; Scholz, Patricia; Sun, Siqi; Herrfurth, Cornelia; Rieseberg, Tim P.; Irisarri, Iker; Steinkamp, Rasmus; Hansen, Maike; Buschmann, Henrik; Valerius, Oliver; Braus, Gerhard H.; Hoecker, Ute (2023-08-28). "Environmental gradients reveal stress hubs pre-dating plant terrestrialization". Nature Plants. 9 (9): 1419–1438. doi:10.1038/s41477-023-01491-0. ISSN 2055-0278. PMC 10505561. PMID 37640935.
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