Expanding the molecular toolbox for Zygnematophyceae – transient genetic transformation of the desmid Micrasterias radians var. evoluta

References

• Abe, J., Hiwatashi, Y., Ito, M., Hasebe, M. & Sekimoto, H. (2008). Expression of exogenous genes under the control of endogenous HSP70 and CAB promoters in the Closterium peracerosum-strigosum-littorale complex. Plant and Cell Physiology, 49: 625–632.
   PubMed Web of Science ®Google Scholar
• Abe, J., Hori, S., Tsuchikane, Y., Kitao, N., Kato, M. & Sekimoto, H. (2011). Stable nuclear transformation of the Closterium peracerosum-strigosum-littorale complex. Plant and Cell Physiology, 52: 1676–1685.
   PubMed Web of Science ®Google Scholar
• Affenzeller, M.J., Darehshouri, A., Andosch, A., Lütz, C. & Lütz-Meindl, U. (2009). Salt stress-induced cell death in the unicellular green alga Micrasterias denticulata. Journal of Experimental Botany, 60: 939–954.
   PubMed Web of Science ®Google Scholar
• Cheng, S., Xian, W., Fu, Y., Marin, B., Keller, J., Wu, T., Sun, W., Li, X., Xu, Y., Zhang, Y., Wittek, S., Reder, T., Günther, G., Gontcharov, A., Wang, S., Li, L., Liu, X., Wang, J., Yang, H., Xu, X., Delaux, P.M., Melkonian, B., Wong, G.K.-S. & Melkonian, M. (2019). Genomes of subaerial Zygnematophyceae provide insights into land plant evolution. Cell, 179: 1057–1067.
   PubMed Web of Science ®Google Scholar
• Christensen, A.H. & Quail, P.H. (1996). Ubiquitin promoter-based vectors for high-level expression of selectable and/or screenable marker genes in monocotyledonous plants. Transgenic Research, 5: 213–218.
   PubMed Web of Science ®Google Scholar
• Dallmeier, K. & Neyts, J. (2013). Simple and inexpensive three-step rapid amplification of cDNA 5’ ends using 5’ phosphorylated primers. Analytical Biochemistry, 434: 1–3.
   PubMed Web of Science ®Google Scholar
• Delwiche, C.F. & Cooper, E.D. (2015). The evolutionary origin of a terrestrial flora. Current Biology, 25: R899–R910.
   PubMed Web of Science ®Google Scholar
• Domozych, D.S., Popper, Z.A. & Sørensen, I. (2016). Charophytes: evolutionary giants and emerging model organisms. Frontiers in Plant Science, 7: 1470.
   PubMed Web of Science ®Google Scholar
• Droop, M.R. (1967). A procedure for routine purification of algal cultures with antibiotics. British Phycological Bulletin, 3: 295–297.
   Google Scholar
• Gontcharov, A.A. & Melkonian, M. (2011). A study of conflict between molecular phylogeny and taxonomy in the Desmidiaceae (Streptophyta, Viridiplantae): analyses of 291 rbcL sequences. Protist, 162: 253–267.
   PubMed Web of Science ®Google Scholar
• Hirano, N., Marukawa, Y., Abe, J., Hashiba, S., Ichikawa, M., Tanabe, Y., Ito, M., Nishii, I., Tsuchikane, Y. & Sekimoto, H. (2015). A receptor-like kinase, related to cell wall sensor of higher plants, is required for sexual reproduction in the unicellular charophycean alga, Closterium peracerosum-strigosum-littorale complex. Plant and Cell Physiology, 56: 1456–1462.
   PubMed Web of Science ®Google Scholar
• Hori, K., Maruyama, F., Fujisawa, T., Togashi, T., Yamamoto, N., Seo, M., Sato, S., Yamada, T., Mori, H., Tajima, N., Moriyama, T., Ikeuchi, M., Watanabe, M., Wada, H., Kobayashi, K., Saito, M., Masuda, T., Sasaki-Sekimoto, Y., Mashiguchi, K., Awai, K., Shimojima, M., Masuda, S., Iwai, M., Nobusawa, T., Narise, T., Kondo, S., Saito, H., Sato, R., Murakawa, M., Ihara, Y., Oshima-Yamada, Y., Ohtaka, K., Satoh, M., Sonobe, K., Ishii, M., Ohtani, R., Kanamori-Sato, M., Honoki, R., Miyazaki, D., Mochizuki, H., Umetsu, J., Higashi, K., Shibata, D., Kamiya, Y., Sato, N., Nakamura, Y., Tabata, S., Ida, S., Kurokawa, K. & Ohta, H. (2014). Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nature Communications, 5: 3978.
   PubMed Web of Science ®Google Scholar
• Ichimura, T. (1971). Sexual cell division and conjugation-papilla formation in sexual reproduction of Closterium strigosum. In Proceedings of the 7th International Seaweed Symposium, 1971, 208–214. University of Tokyo Press.
   Google Scholar
• Jiao, C., Sørensen, I., Sun, X., Sun, H., Behar, H., Alseekh, S., Philippe, G., Palacio Lopez, K., Sun, L., Reed, R., Jeon, S., Kiyonami, R., Zhang, S., Fernie, A.R., Brumer, H., Domozych, D.S., Fei, Z. & Rose, J.K.C. (2020). The genome of the charophyte alga Penium margaritaceum bears footprints of the evolutionary origins of land plants. Cells. https://doi.org/10.1016/j.cell.2020.04.019.
   Google Scholar
• Kanda, N., Ichikawa, M., Ono, A., Toyoda, A., Fujiyama, A., Abe, J., Tsuchikane, Y., Nishiyama, T. & Sekimoto, H. (2017). CRISPR/Cas9-based knockouts reveal that CpRLP1 is a negative regulator of the sex pheromone PR-IP in the Closterium peracerosum-strigosum-littorale complex. Scientific Reports, 7: 17873.
   PubMed Web of Science ®Google Scholar
• Kiermayer, O. (1968). The distribution of microtubules in differentiating cells of Micrasterias denticulata bréb. Planta, 83: 223–236.
   PubMed Web of Science ®Google Scholar
• Lacalli, T. (1975). Morphogenesis in Micrasterias: I. Tip growth. Development, 33: 95–115.
   Google Scholar
• Lindner, A.C., Lang, D., Seifert, M., Podlesakova, K., Novak, O., Strnad, M., Reski, R. & von Schwartzenberg, K. (2014). Isopentenyltransferase-1 (IPT1) knockout in Physcomitrella together with phylogenetic analyses of IPTs provide insights into evolution of plant cytokinin biosynthesis. Journal of Experimental Botany, 65: 2533–2543.
   PubMed Web of Science ®Google Scholar
• Liu, Y.G. & Chen, Y. (2007). High-efficiency thermal asymmetric interlaced PCR for amplification of unknown flanking sequences. Biotechniques, 43: 649–650, 652, 654.
   Google Scholar
• Liu, Y.G., Mitsukawa, N., Oosumi, T. & Whittier, R.F. (1995). Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. The Plant Journal, 8: 457–463.
   PubMed Web of Science ®Google Scholar
• Liu, Y.G. & Whittier, R.F. (1995). Thermal asymmetric interlaced PCR: automatable amplification and sequencing of insert end fragments from PI and YAC clones for chromosome walking. Genomics, 25: 674–681.
   PubMed Web of Science ®Google Scholar
• Lutz-Meindl, U. (2016). Micrasterias as a model system in plant cell biology. Frontiers in Plant Science, 7: 999.
   PubMed Web of Science ®Google Scholar
• Masani, M.Y., Noll, G.A., Parveez, G.K., Sambanthamurthi, R. & Prufer, D. (2014). Efficient transformation of oil palm protoplasts by PEG-mediated transfection and DNA microinjection. PLoS ONE, 9: e96831.
   PubMed Web of Science ®Google Scholar
• McElroy, D., Zhang, W., Cao, J. & Wu, R. (1990). lsolation of an efficient actin promoter for use in rice transformation. Plant Cell, 2: 163–171.
   PubMed Web of Science ®Google Scholar
• Meindl, U. (1993). Micrasterias cells as a model cystem for research on morphogenesist. Microbiology Reviews, 57: 415–433.
   PubMedGoogle Scholar
• Meindl, U. & Lütz, C. (1996). Effects of UV irradiation on cell development and ultrastructure of the green alga Micrasterias. Journal of Photochemistry and Photobiology B: Biology, 36: 285–292.
   Google Scholar
• Meindl, U., Zhang, D., & Hepler, P.K. (1994). Actin microfilaments are associated with the migrating nucleus and the cell cortex in the green alga Micrasterias: studies on living cells. Journal of Cell Science, 107: 1929–1934.
   PubMed Web of Science ®Google Scholar
• Melak, M., Plessner, M. & Grosse, R. (2017). Correction: actin visualization at a glance. Journal of Cell Science, 130: 1688.
   PubMed Web of Science ®Google Scholar
• Murray, M.G. & Thompson, W.F. (1980). Rapid isolation of high molecular weight plant DNA. Nucleic Acids Research, 8: 4321–4326.
   PubMed Web of Science ®Google Scholar
• Nishiyama, T., Sakayama, H., de Vries, J., Buschmann, H., Saint-Marcoux, D., Ullrich, K.K., Haas, F.B., Vanderstraeten, L., Becker, D., Lang, D., Vosolsobe, S., Rombauts, S., Wilhelmsson, P.K.I., Janitza, P., Kern, R., Heyl, A., Rumpler, F., Villalobos, L., Clay, J.M., Skokan, R., Toyoda, A., Suzuki, Y., Kagoshima, H., Schijlen, E., Tajeshwar, N., Catarino, B., Hetherington, A.J., Saltykova, A., Bonnot, C., Breuninger, H., Symeonidi, A., Radhakrishnan, G.V., Van Nieuwerburgh, F., Deforce, D., Chang, C., Karol, K.G., Hedrich, R., Ulvskov, P., Glockner, G., Delwiche, C.F., Petrasek, J., Van de Peer, Y., Friml, J., Beilby, M., Dolan, L., Kohara, Y., Sugano, S., Fujiyama, A., Delaux, P.M., Quint, M., Theissen, G., Hagemann, M., Harholt, J., Dunand, C., Zachgo, S., Langdale, J., Maumus, F., Van Der Straeten, D., Gould, S.B. & Rensing, S.A. (2018). The Chara genome: secondary complexity and implications for plant terrestrialization. Cell, 174: 448–464.
   PubMed Web of Science ®Google Scholar
• Ohiwa, T. (1977). Preparation and culture of Spirogyra and Zygnema protoplasts. Cell Structure and Function, 2: 249–255
   Web of Science ®Google Scholar
• Oñate-Sánchez, L. & Vicente-Carbajosa, J. (2008). DNA-free RNA isolation protocols for Arabidopsis thaliana, including seeds and siliques. BMC Research Notes, 1: 93.
   PubMedGoogle Scholar
• Regensdorff, M., Deckena, M., Stein, M., Borchers, A., Scherer, G., Lammers, M., Hansch, R., Zachgo, S. & Buschmann, H. (2018). Transient genetic transformation of Mougeotia scalaris (Zygnematophyceae) mediated by the endogenous alpha-tubulin1 promoter. Journal of Phycology, 54: 840–849.
   PubMed Web of Science ®Google Scholar
• Rensing, S.A. (2017). Why we need more non-seed plant models. New Phytologist, 216: 355–360.
   PubMed Web of Science ®Google Scholar
• Riedl, J., Crevenna, A.H., Kessenbrock, K., Yu, J.H., Neukirchen, D., Bista, M., Bradke, F., Jenne, D., Holak, T.A., Werb, Z., Sixt, M. & Wedlich-Soldner, R. (2008). Lifeact: a versatile marker to visualize F-actin. Nature Methods, 5: 605–607.
   PubMed Web of Science ®Google Scholar
• Schaefer, D. (1994). Molecular genetic approaches to the biology of the moss Physcomitrella patens. PhD Thesis, University of Lausanne.
   Google Scholar
• Schaefer, D., Zryd, J.P., Knight, C.D. & Cove, D.J. (1990). Stable transformation of the moss Physcomitrella patens. Molecular and General Genetics MGG, 226: 418–424.
   Google Scholar
• Schneider-Poetsch, T., Ju, J., Eyler, D.E., Dang, Y., Bhat, S., Merrick, W.C., Green, R., Shen, B. & Liu, J.O. (2010). Inhibition of eukaryotic translation elongation by cycloheximide and lactimidomycin. Nature Chemical Biology, 6: 209–217.
   PubMed Web of Science ®Google Scholar
• Sheen, J. (2001). Signal transduction in maize and Arabidopsis mesophyll protoplasts. Plant Physiology, 127: 1466–1475.
   PubMed Web of Science ®Google Scholar
• Škaloud, P., Nemjova, K., Vesela, J., Cerna, K. & Neustupa, J. (2011). A multilocus phylogeny of the desmid genus Micrasterias (Streptophyta): evidence for the accelerated rate of morphological evolution in protists. Molecular Phylogenetics and Evolution, 61: 933–943.
   PubMed Web of Science ®Google Scholar
• Sørensen, I., Fei, Z., Andreas, A., Willats, W.G., Domozych, D.S. & Rose, J.K. (2014). Stable transformation and reverse genetic analysis of Penium margaritaceum: a platform for studies of charophyte green algae, the immediate ancestors of land plants. The Plant Journal, 77: 339–351.
   PubMed Web of Science ®Google Scholar
• Vannerum, K., Abe, J., Sekimoto, H., Inzé, D. & Vyverman, W. (2010). Intracellular localization of an endogenous cellulose synthase of Micrasterias denticulata (Desmidiales, Chlorophyta) by means of transient genetic transformation. Journal of Phycology, 46: 839–845.
   Web of Science ®Google Scholar
• Vannerum, K., De Rycke, R., Pollier, J., Goossens, A., Inze, D. & Vyverman, A.W. (2012). Characterization of a RABE (RAS gene from rat brain e) gtpase expressed during morphogenesis in the unicellular green alga Micrasterias denticulata (Zygnematophyceae, Streptophyta). Journal of Phycology, 48: 682–692.
   PubMed Web of Science ®Google Scholar
• Vannerum, K., Huysman, M.J., De Rycke, R., Vuylsteke, M., Leliaert, F., Pollier, J., Lütz-Meindl, U., Gillard, J., De Veylder, L. & Goossens, A. (2011). Transcriptional analysis of cell growth and morphogenesis in the unicellular green alga Micrasterias (Streptophyta), with emphasis on the role of expansin. BMC Plant Biology, 11: 128.
   PubMed Web of Science ®Google Scholar
• Volland, S., Bayer, E., Baumgartner, V., Andosch, A., Lütz, C., Sima, E. & Lütz-Meindl, U. (2014). Rescue of heavy metal effects on cell physiology of the algal model system Micrasterias by divalent ions. Journal of Plant Physiology, 171: 154–163.
   PubMed Web of Science ®Google Scholar
• von Schwartzenberg, K., Nunez, M.F., Blaschke, H., Dobrev, P.I., Novak, O., Motyka, V. & Strnad, M. (2007). Cytokinins in the bryophyte Physcomitrella patens: analyses of activity, distribution, and cytokinin oxidase/dehydrogenase overexpression reveal the role of extracellular cytokinins. Plant Physiology, 145: 786–800.
   PubMed Web of Science ®Google Scholar
• von Schwartzenberg, K., Bornfleth, S., Lindner, A.-C. & Hanelt, D. (2013). The Microalgae and Zygnematophyceae Collection Hamburg (MZCH) – living cultures for research on rare streptophytic algae. Algological Studies, 142: 77–107.
   Google Scholar
• Watanabe, Y. & Saiki, H. (1997). Development of a photobioreactor incorporating Chlorella sp. for removal of CO2 in stack gas. Energy Conversion and Management, 38: S499–S503.
   Web of Science ®Google Scholar
• Zeidler, M., Hartmann, E. & Hughes, J. (1999). Transgene expression in the moss Ceratodon purpureus. Journal of Plant Physiology, 154: 641–650.
   Web of Science ®Google Scholar
• Zhou, H. & von Schwartzenberg, K. (2020). Zygnematophyceae – from living algae collections to the establishment of future models. Journal of Experimental Botany, 71: 3296–3304, 10.1093/jxb/eraa09.
   Google Scholar