Freezing and desiccation tolerance in the Antarctic bangiophyte Pyropia endiviifolia (Rhodophyta): a chicken and egg problem?

References

• Archibald, J.M. & Keeling, P.J. (2002). Recycled plastids: A “green movement” in eukaryotic evolution. Trends in Genetics, 18: 577–584.
   PubMed Web of Science ®Google Scholar
• Ballesteros, D., Pritchard, H.W. & Walters, C. (2020). Dry architecture: towards the understanding of the variation of longevity in desiccation- tolerant germplasm. Seed Science Research, 30: 142–155.
   Web of Science ®Google Scholar
• Barker, P.F., Diekmann, B. & Escutia, C. (2007). Onset of Cenozoic Antarctic glaciation. Deep-Sea Research Part II: Topical Studies in Oceanography, 54: 2293–2307.
   Web of Science ®Google Scholar
• Becker, B. (2013). Snow ball earth and the split of Streptophyta and Chlorophyta. Trends in Plant Science, 18: 180–183.
   PubMed Web of Science ®Google Scholar
• Becker, S., Walter, B. & Bischof, K. (2009). Freezing tolerance and photosynthetic performance of polar seaweeds at low temperatures. Botanica Marina, 52: 609–616.
   Web of Science ®Google Scholar
• Bengtson, S., Sallstedt, T., Belivanova, V. & Whitehouse, M. (2017). Three dimensional preservation of cellular and subcellular structures suggests 1.6 billion-year-old crown-group red algae. PLoS Biology, 15: e2000735.
   PubMed Web of Science ®Google Scholar
• Blouin, N., Calder, B.L., Perkins, B. & Brawley, S.H. (2006). Sensory and fatty acid analyses of two Atlantic species of Porphyra (Rhodophyta). Journal of Applied Phycology, 18: 79–85.
   Web of Science ®Google Scholar
• Blouin, N.A., Brodie, J.A., Grossman, A.C., Xu, P., & Brawley, S.H. (2011). Porphyra: a marine crop shaped by stress. Trends in Plant Science, 16: 29–37.
   PubMed Web of Science ®Google Scholar
• Bose, S., Herbert, S.K. & Fork, D.C. (1988). Fluorescence characteristics of photoinhibition and recovery in a sun and a shade species of the red algal genus Porphyra. Plant Physiology, 86: 946–950.
   PubMed Web of Science ®Google Scholar
• Butterfield, N.J. (2000). Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes. Paleobiology, 26: 386–404.
   Web of Science ®Google Scholar
• Brawley, S.H., Blouin, N.A., Ficko-Blean, E., Wheeler, G., Lohr, M., Goodson, H.V., Jenkins, J., Blaby-Haas, C.E., Helliwell, K., Chan, C.X., Marriage, T., Bhattacharya, D., Klein, A., Badis, Y., Brodie, J., Cao, Y., Collen, J., Dittami, S., Gachon, C., Green, B., Karpowicz, S., Kim, J., Lin, S., Michel, G., Mittag, M., Olson, B., Pangilinan, J., Peng, Y., Qiu, H., Riek, S.Z., Shu, S.Q., Singer, J., Smith, A., Sprecher, B., Wagner, V., Wang, W., Wang, Z., Yan, Z., Yarish, C., Zhuang, Y.Y., Zou, Y., Lindquist, E., Grimwood, J., Barry, K., Rokshar, D., Schumtz, J., Gantt, E., Stiller, J., Grossman, A. & Prochnik, S. (2017). Insights into the red algae and eukaryotic evolution from the genome of Porphyra umbilicalis (Bangiophyceae, Rhodophyta). Proceedings of the National Academy of Sciences, 114: E6361–E6370.
   Google Scholar
• Celis-Plá, P.S.M., Moenne, F., Rodríguez-Rojas, F., Pardo, D., Lavergne, C., Moenne, A., Brown, M.T., Huovinen, P., Gómez, I., Navarro, N. & Sáez, C.A. (2020). Antarctic intertidal macroalgae under predicted increased temperatures mediated by global climate change: Would they cope? Science of the Total Environment, 740: 1–12.
   Web of Science ®Google Scholar
• Contreras-Porcia, L., López-Cristoffanini, C., Meynard, A. & Kumar, M. (2017). Tolerance pathways to desiccation stress in seaweeds. In Systems Biology of Marine Ecosystems. (Kumar M. & Ralph P., eds.), 13–33.
   Google Scholar
• Contreras-Porcia, L., Thomas, D., Flores, V. & Correa, J.A. (2011). Tolerance to oxidative stress induced by desiccation in Porphyra columbina (Bangiales, Rhodophyta). Journal of Experimental Botany, 62: 1815–1829.
   PubMed Web of Science ®Google Scholar
• Dautermann, O. & Lohr, M. (2017). A functional zeaxanthin epoxidase from red algae shedding light on the evolution of light-harvesting carotenoids and the xanthophyll cycle in photosynthetic eukaryotes. Plant Journal, 92: 879–891.
   PubMed Web of Science ®Google Scholar
• Esteban, R., Martínez, B., Fernández-Marín, B., Becerril, J.M. & García-Plazaola, J.I. (2009). Carotenoid composition in Rhodophyta: Insights into xanthophyll regulation in Corallina elongata. European Journal of Phycology, 44: 221–230.
   Web of Science ®Google Scholar
• Fernández-Marín, B., Holzinger, A. & García-Plazaola, J.I. (2016). Photosynthetic strategies of desiccation-tolerant organisms. In Handbook of Photosynthesis, Third Edition. (Pessarakli, M. editor), 663–681. CRC Press, Boca Raton.
   Google Scholar
• Fernández-Marín, B., Kranner, I., Sebastián, M.S., Artetxe, U., Laza, J.M., Vilas, J.L., Pritchard, H.W., Nadajaran, J., Miguez, F., Becerril, J.M. & García-Plazaola, J.I. (2013). Evidence for the absence of enzymatic reactions in the glassy state. A case study of xanthophyll cycle pigments in the desiccation-tolerant moss Syntrichia ruralis. Journal of Experimental Botany, 64: 3033–3043.
   PubMed Web of Science ®Google Scholar
• Fernández-Marín, B., López-pozo, M., Perera-Castro, A. V, Arzac, M.I., Sáenz-ceniceros, A., Colesie, C., de los Ríos, A., Sancho, L.G., Pintado, A., Laza, J.M., Pérez-Ortega, S. & García-Plazaola, J.I. (2019). Symbiosis at its limits: ecophysiological consequences of lichenization in the genus Prasiola in Antarctica. Annals of Botany. 124: 1211–1226.
   Web of Science ®Google Scholar
• Ferraces-Casais, P., Lage-Yusty, M.A., de Quirós, A.R.B. & López-Hernández, J. (2012). Evaluation of bioactive compounds in fresh edible seaweeds. Food Analytical Methods, 5: 828–834.
   Web of Science ®Google Scholar
• Fierro, C., López-Cristoffanini, C., Meynard, A., Lovazzano, C., Castañeda, F., Guajardo, E. & Contreras-Porcia, L. (2017). Expression profile of desiccation tolerance factors in intertidal seaweed species during the tidal cycle. Planta, 245: 1149–1164.
   PubMed Web of Science ®Google Scholar
• Flores-Molina, M.R., Thomas, D., Lovazzano, C., Núñez, A., Zapata, J., Kumar M., Correa, J.A. & Contreras-Porcia, L. (2014). Desiccation stress in intertidal seaweeds: Effects on morphology, antioxidant responses and photosynthetic performance. Aquatic Botany, 113: 90–99.
   Web of Science ®Google Scholar
• Furbino, L.E., Godinho, V.M., Santiago, I.F., Pellizari, F.M., Alves, T.M.A., Zani, C.L., Junior, P.A.S., Romanha, A.J., Carvalho, G.O., Gil, L.H.V.G., Rosa, C.A., Minnis, A.M. & Rosa, L.H. (2014). Diversity patterns, ecology and biological activities of fungal communities associated with the endemic macroalgae across the Antarctic Peninsula. Microbial Ecology, 67: 775–787.
   PubMed Web of Science ®Google Scholar
• Gaff, D.F. & Oliver, M. (2013). The evolution of desiccation tolerance in angiosperm plants: a rare yet common phenomenon. Functional Plant Biology, 40: 315–328.
   PubMed Web of Science ®Google Scholar
• García-Plazaola, J.I. & Becerril, J.M. (1999). A rapid high-performance liquid chromatography method to measure lipophilic antioxidants in stressed plants: simultaneous determination of carotenoids and tocopherols. Phytochemical Analysis, 10: 307–313.
   Web of Science ®Google Scholar
• García-Plazaola, J.I. & Becerril, J.M. (2001). Seasonal changes in photosynthetic pigments and antioxidants in beech (Fagus sylvatica) in a Mediterranean climate: implications for tree decline diagnosis. Australian Journal of Plant Physiology, 28: 225–232.
   Google Scholar
• Genty, B., Briantais, J.M. & Baker, N.R. (1989). The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta - General Subjects, 990: 87–92.
   Web of Science ®Google Scholar
• Goudriaan, J. (1982). Potential production processes. In Simulation of plant growth and crop production. (Penning de Vries, F. & van Laar, H., editors), 98–113. Pudoc, Wageningen.
   Google Scholar
• Green, L.A. & Neefus, C.D. (2014). The effects of short- and long-term freezing on Porphyra umbilicalis Kützing (Bangiales, Rhodophyta) blade viability. Journal of Experimental Marine Biology and Ecology, 461: 499–503.
   Web of Science ®Google Scholar
• Guiry, M.D. & Guiry, G.M. (2021). AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. https://www.algaebase.org; searched on September 14, 2022.
   Google Scholar
• Herbert, S.K. (1990). Photoinhibition resistance in the red alga Porphyra perforata: The role of photoinhibition repair. Plant Physiology, 92: 514–519.
   PubMed Web of Science ®Google Scholar
• Jassby, A.D., Platt, T. & Jassbyl, A.D. (1976). Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnology and Oceanography, 21: 540–547.
   Web of Science ®Google Scholar
• Kanwisher, J. (1957). Freezing and drying in intertidal algae. The Biological Bulletin, 113: 275–285.
   Web of Science ®Google Scholar
• Koizumi, J., Takatani, N., Kobayashi, N., Mikami, K., Miyashita, K., Yamano, Y., Wada, A., Maoka, T. & Hosokawa, M. (2018). Carotenoid profiling of a red seaweed Pyropia yezoensis: Insights into biosynthetic pathways in the order bangiales. Marine Drugs, 16: 426.
   PubMed Web of Science ®Google Scholar
• Krall, J.P. & Edwards, G.E. (1992). Relationship between photosystem II activity and CO2 fixation in leaves. Physiologia Plantarum, 86: 180–187.
   Web of Science ®Google Scholar
• Lin, A.P., Wang, G.C., Shen, S.D., Yang, F. & Pan, G.H. (2010). Two specific causes of cell mortality in freeze-thaw cycle of young thalli of Porphyra yezoensis (Bangiales, Rhodophyta). Journal of Phycology, 46: 773–779.
   Web of Science ®Google Scholar
• Lobo, F. de A., de Barros, M.P., Dalmagro, H.J., Dalmolin, Â.C., Pereira, W.E., de Souza, É.C., Vourlitis, G.L. & Rodríguez Ortíz, C.E. (2013). Fitting net photosynthetic light-response curves with Microsoft Excel - a critical look at the models. Photosynthetica, 51: 445–456.
   Web of Science ®Google Scholar
• López-Pozo, M., Flexas, J., Gulías, J., Carriquí, M., Nadal, M., Perera-Castro, A.V., Clemente-Moreno, M.J., Gago, J., Núñez-Oliveira, E., Martínez-Abaigar, J., Hernández, A., Artetxe, U., Bentley, J., Farrant, J.M., Verhoeven, A.V., García-Plazaola, J.I. & Fernández-Marín, B. (2019). A field portable method for semi-quantitative estimation of dehydration tolerance of photosynthetic tissues across distantly related land plants. Physiologia Plantarum, 167: 540–555.
   PubMed Web of Science ®Google Scholar
• Lundheim, R. (1997). Ice nucleation in seaweeds in relation to vertical zonation. Journal of Phycology, 33: 739–742.
   Web of Science ®Google Scholar
• Marcías, M.L., Deregibus, D., Saravia, L.A., Campana, G.L. & Quartino, M.L. (2017). Life between tides: Spatial and temporal variations of an intertidal macroalgal community at Potter Peninsula, South Shetland Islands, Antarctica. Estuarine, Coastal and Shelf Science, 187: 193–203.
   Web of Science ®Google Scholar
• Na, Y., Lee, H.N., Wi, J., Jeong, W.J. & Choi, D.W. (2018). PtDRG1, a desiccation response gene from Pyropia tenera (Rhodophyta), exhibits chaperone function and enhances abiotic stress tolerance. Marine Biotechnology, 20: 584–593.
   PubMed Web of Science ®Google Scholar
• Oliveira, E., Absher, T., Pellizzari, F. & Oliveira, M. (2009). The seaweed flora of Admiralty Bay, King George Island, Antarctic. Polar Biology, 32: 1639–1647.
   Web of Science ®Google Scholar
• Oliver, M.J., Farrant, J.M., Hilhorst, H.W.M., Mundree, S., Williams, B. & Bewley, J.D. (2020). Desiccation tolerance: avoiding cellular damage during drying and rehydration. Annual Review of Plant Biology, 71: 435–460.
   PubMed Web of Science ®Google Scholar
• Pearson, G. & Davison, R. (1994). Freezing stress and osmotic dehydration in Fucus distichus (Phaeophyta): evidence for physiological similarity. Journal of Phycology, 30: 257–267.
   Web of Science ®Google Scholar
• Peat, H.J., Clarke, A. & Convey, P. (2007). Diversity and biogeography of the Antarctic flora. Journal of Biogeography, 34: 132–146.
   Web of Science ®Google Scholar
• Perera-Castro, A.V., Nadal, M. & Flexas, J. (2020a). What drives photosynthesis during desiccation? Mosses and other outliers from the photosynthesis-elasticity trade-off. Journal of Experimental Botany, 71: 6460–6470.
   PubMed Web of Science ®Google Scholar
• Perera-Castro, A.V., Waterman, M.J., Turnbull, J.D., Ashcroft, M.B., McKinley, E., Watling, J.R., Bramley-Alvez, J., Casanova-Katny, A., Zuniga, G. & Robinson, S.A. (2020b). It is hot in the sun: Antarctic mosses have high temperature optima for photosynthesis despite cold climate. Frontiers in Plant Science, 11: 1178.
   PubMed Web of Science ®Google Scholar
• Qian, F., Luo, Q., Yang, R., Zhu, Z., Chen, H. & Yan, X. (2015). The littoral red alga Pyropia haitanensis uses rapid accumulation of floridoside as the desiccation acclimation strategy. Journal of Applied Phycology, 27: 621–632.
   Web of Science ®Google Scholar
• Ritchie, R.J. & Prvan, T. (1996a). Current staistical methods for estimating the Km and Vmax of Michaelis-Menten kinetics. Biochemical Education, 24: 196–206.
   Google Scholar
• Ritchie, R.J. & Prvan, T. (1996b). A simulation study on designing experiments to measure the Km of Michaelis-Menten kinetics curves. Journal of Theoretical Biology, 178: 239–254.
   Web of Science ®Google Scholar
• Santos, M.A.Z., Colepicolo, P., Pupo, D., Fujii, M.T., de Pereira, C.M.P. & Mesko, M.F. (2017). Antarctic red macroalgae: a source of polyunsaturated fatty acids. Journal of Applied Phycology, 29: 759–767.
   Web of Science ®Google Scholar
• Smith, E. (1936). Photosynthesis in relation to light and carbon dioxide. Proceedings of the National Academy of Sciences of the United States of America, 22: 504–511.
   Google Scholar
• Sutherland, J.E., Lindstrom, S., Nelson, W., Brodie, J., Lynch, M., Hwang, M.S., Choi, H.-G., Miyata, M., Kikuchi, N., Oliveira, M., Farr, T., Neefus, C., Mortensen, A., Milstein, D. & Muller, K. (2011). A new look at an ancient order: generic revision of the Bangiales. Journal of Phycology, 47: 1131–1151.
   PubMed Web of Science ®Google Scholar
• Ursi, S., Pedersén, M., Plastino, E. & Snoeijs, P. (2003). Intraspecific variation of photosynthesis, respiration and photoprotective carotenoids in Gracilaria birdiae (Gracilariales: Rhodophyta). Marine Biology, 142: 997–1007.
   Web of Science ®Google Scholar
• Verhoeven, A., García-Plazaola, J.I. & Fernández-Marín, B. (2018). Shared mechanisms of photoprotection in photosynthetic organisms tolerant to desiccation or to low temperature. Environmental and Experimental Botany, 154: 66–79.
   Web of Science ®Google Scholar
• Wang, W.J., Sun, X.T., Liu, F.L., Liang, Z.R., Zhang, J.H. & Wang, F.J. (2016). Effect of abiotic stress on the gameophyte of Pyropia katadae var. hemiphylla (Bangiales, Rhodophyta). Journal of Applied Phycology, 28: 469–479.
   Web of Science ®Google Scholar
• Wisniewski, M., Gusta, L. & Neuner, G. (2014). Adaptive mechanisms of freeze avoidance in plants: A brief update. Environmental and Experimental Botany, 99: 133–140.
   Web of Science ®Google Scholar
• Wolfe, J. & Bryant, G. (1999). Freezing, drying, and/or vitrification of membrane–solute–water systems. Cryobiology, 129: 103–129.
   Google Scholar
• Yang, L.-I., Zhoua, W., Denga, Y.-Y., Xua, Chuan-Ming Hua, C.-M., Zhang, T., Russell, S., Zhua, J.-Y., Lua, Q-Q. & Brodie, J. (2018). A molecular phylogeny of the bladed Bangiales (Rhodophyta) in China provides insights into biodiversity and biogeography of the genus Pyropia. Molecular Phylogenetics and Evolution, 120: 94–102.
   PubMed Web of Science ®Google Scholar
• Xie, X., Lu, X., Wang, L., He, L. & Wang, G. (2020). High light intensity increases the concentrations of β-carotene and zeaxanthin in marine red macroalgae. Algal Research, 47: 101852.
   Google Scholar
• Zacher, K., Rautenberger, R., Hanelt, D., Wulff, A. & Wiencke, C. (2009). The abiotic environment of polar marine benthic algae. Botanica Marina, 52: 483–490.
   Web of Science ®Google Scholar