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Can genomics tools assist in gaining insights from the aquatic angiosperms to transform crop plants with multiple carbon concentrating mechanisms to adapt and yield better in challenging environment?

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Abstract

Studies on the speciation and diversification events in plants that are often associated with adaptations acquired through the long-term interaction with the earth’s geological factors can throw insights on the key driving factors of adaptation in those plants. One such important adaptive trait is the oxygenic photosynthesis, evolved initially in cyanobacteria. The CO2 concentration mechanisms (CCMs), four well-known biochemical types, were evolved independently in multiple lineages of plants in response to the earth’s environmental influences. The carboxysomes and pyrenoids were the earliest known biophysical type CCM, evolved respectively in the cyanobacteria and algae around 400 million years ago (Ma.). Additionally, vascular plants were known to possess CCMs as early as 300 Ma. Aquatic angiosperms though represent only 2% of the flowering plants, they have evolved for multiple CCMs to overcome various environmental issues with reference to aquatic environment like: the lesser rate (104 times) of diffusion for CO2 in water when compared to air, altered pH due to acidification in waterbodies, marine and freshwater environment. The Hydrocharitaceae is one of the most diverse family of aquatic angiosperms known to possess multiple CCMs of preliminary nature for its survival and photosynthesis in the much difficult aquatic environment. The present review gives an overview on the importance of this taxa to gain novel insights especially on their photosynthetic and multiple CCMs trait for its implications in crop plants to attain better productivity in changing climate scenario. The genomics research drive required in such special aquatic taxa are highlighted for its utility in the crop improvement programs.

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References

  • Adler, L., Díaz-Ramos, A., Mao, Y., Pukacz, K. R., Fei, C., & McCormick, A. J. (2022). New horizons for building pyrenoid-based CO2-concentrating mechanisms in plants to improve yields. Plant Physiology.https://doi.org/10.1093/plphys/kiac373

  • Amaral Zettler, L. A., Gómez, F., Zettler, E., Keenan, B. G., Amils, R., & Sogin, M. L. (2002). Eukaryotic diversity in Spain’s River of Fire. Nature, 417, 137.

    Article  CAS  Google Scholar 

  • Arora, L., & Narula, A. (2017). Gene editing and crop improvement using CRISPR-Cas9 system. Frontiers in Plant Science, 8, 1932.

    Article  Google Scholar 

  • Badger, M. (2003). The roles of carbonic anhydrases in photosynthetic CO2 concentrating mechanisms. Photosynthesis Research, 77, 83–94.

    Article  CAS  Google Scholar 

  • Badger, M. R., Hanson, D., & Price, G. D. (2002). Evolution and diversity of CO2 concentrating mechanisms in cyanobacteria. Functional Plant Biology, 29, 161–173.

    Article  CAS  Google Scholar 

  • Badger, M. R., Kaplan, A., & Berry, J. A. (1980). Internal inorganic carbon pool of Chlamydomonas reinhardtii: Evidence for a carbon dioxide-concentrating mechanism. Plant Physiology, 66, 407–413.

    Article  CAS  Google Scholar 

  • Badger, M. R., & Price, G. D. (2003). CO2 concentrating mechanisms in cyanobacteria: Molecular components, their diversity and evolution. Journal of experimental botany, 54, 609–622.

    Article  CAS  Google Scholar 

  • Beer, S. (1989). Photosynthesis and photorespiration of marine angiosperms. Aquatic Botany, 34, 153–166.

    Article  CAS  Google Scholar 

  • Beer, S., Sand-Jensen, K., Madsen, T. V., & Nielsen, S. L. (1991). The carboxylase activity of Rubisco and the photosynthetic performance in aquatic plants. Oecologia, 87, 429–434.

    Article  CAS  Google Scholar 

  • Beerling, D. J., & Royer, D. L. (2011). Convergent cenozoic CO2 history. Nature Geoscience, 4, 418–420.

    Article  CAS  Google Scholar 

  • Bekker, A., Holland, H., Wang, P. L., Rumble, D., Stein, H., Hannah, J., Coetzee, L., & Beukes, N. (2004). Dating the rise of atmospheric oxygen. Nature, 427, 117–120.

    Article  CAS  Google Scholar 

  • Benedict, C. R., & Scott, J. R. (1976). Photosynthetic carbon metabolism of a marine grass. Plant Physiology, 57, 876–880.

    Article  CAS  Google Scholar 

  • Bindeman, I., Zakharov, D., Palandri, J., Greber, N. D., Dauphas, N., Retallack, G., Hofmann, A., Lackey, J., & Bekker, A. (2018). Rapid emergence of subaerial landmasses and onset of a modern hydrologic cycle 2.5 billion years ago. Nature, 557, 545–548.

    Article  CAS  Google Scholar 

  • Blank, C. E. (2013). Origin and early evolution of photosynthetic eukaryotes in freshwater environments: Reinterpreting proterozoic paleobiology and biogeochemical processes in light of trait evolution. Journal of Phycology, 49, 1040–1055.

    Article  CAS  Google Scholar 

  • Blankenship, R. E. (2010). Early evolution of photosynthesis. Plant physiology, 154, 434–438.

    Article  CAS  Google Scholar 

  • Blikstad, C., Dugan, E. J., Laughlin, T. G., Liu, M. D., Shoemaker, S. R., Remis, J. P., & Savage, D. F. (2021). Discovery of a carbonic anhydrase-Rubisco supercomplex within the alpha-carboxysome. bioRxiv: https://doi.org/10.1101/2021.1111.1105.467472

  • Block, J. E. (2022). Life of Govindjee, known as Mister Photosynthesis. Journal of Plant Science Research, 38, 1–22.

    Google Scholar 

  • Bose, J. C. (1924). Photosynthetic evolution of oxygen in the complete absence of Carbon dioxide. The Physiology of Photosynthesis (pp. 122–131). London: Longmans Green and Co.

    Google Scholar 

  • Bowes, G., Holaday, A. S., Van, T. K., & Haller, W. T. (1978). Photosynthetic and photorespiratory carbon metabolism in aquatic plants. In Hall, D.,, Coombs, J., Goodwin, T. (eds.) Proceedings of the Fourth International Congress on Photosynthesis (pp. 289–298). The Biochemical Society, London.

  • Bowes, G., Rao, S. K., Estavillo, G. M., & Reiskind, J. B. (2002). C4 mechanisms in aquatic angiosperms: Comparisons with terrestrial C4 systems. Functional Plant Biology, 29, 379–392.

    Article  CAS  Google Scholar 

  • Bowes, G., & Salvucci, M. E. (1989). Plasticity in the photosynthetic carbon metabolism of submersed aquatic macrophytes. Aquatic Botany, 34, 233–266.

    Article  CAS  Google Scholar 

  • Brock, T. D. (1967). Micro-organisms adapted to high temperatures. Nature, 214, 882–885.

    Article  CAS  Google Scholar 

  • Burlacot, A., Dao, O., Auroy, P., Cuiné, S., Li-Beisson, Y., & Peltier, G. (2022). Alternative photosynthesis pathways drive the algal CO2-concentrating mechanism. Nature, 605, 366–371.

    Article  CAS  Google Scholar 

  • Cabello-Yeves, P. J., Scanlan, D. J., Callieri, C., Picazo, A., Schallenberg, L., Huber, P., Roda-Garcia, J. J., Bartosiewicz, M., Belykh, O. I., & Tikhonova, I. V. (2022). α-cyanobacteria possessing form IA RuBisCO globally dominate aquatic habitats. The ISME Journal, 16, 2421–2432.

    Article  CAS  Google Scholar 

  • Capó-Bauçà, C. (2022). Correlative adaptation between Rubisco and CO2-concentrating mechanisms in seagrasses. Nature Plants, 8, 706–716.

    Article  Google Scholar 

  • Cardona, T., Sánchez-Baracaldo, P., Rutherford, A. W., & Larkum, A. W. (2019). Early Archean origin of photosystem II. Geobiology, 17, 127–150.

    Article  CAS  Google Scholar 

  • Carr, G. M., Duthie, H. C., & Taylor, W. D. (1997). Models of aquatic plant productivity: A review of the factors that influence growth. Aquatic Botany, 59, 195–215.

    Article  Google Scholar 

  • Casati, P., Lara, M. V., & Andreo, C. S. (2000). Induction of a C4-Like Mechanism of CO2Fixation in Egeria densa, a Submersed Aquatic Species. Plant Physiology, 123, 1611–1622.

    Article  CAS  Google Scholar 

  • Catallo, W. J., Shupe, T. F., & Eberhardt, T. L. (2008). Hydrothermal processing of biomass from invasive aquatic plants. Biomass and Bioenergy, 32, 140–145.

    Article  CAS  Google Scholar 

  • Cavalier-Smith, T. (2000). Membrane heredity and early chloroplast evolution. Trends in Plant Science, 5, 174–182.

    Article  CAS  Google Scholar 

  • Chan, C. X., & Bhattacharya, D. (2010). The origin of plastids. Nature Education, 3, 84.

    Google Scholar 

  • Chen, J., Li, S., He, Y., Li, J., & Xia, L. (2022a). An update on precision genome editing by homology-directed repair in plants. Plant Physiology, 188, 1780–1794.

    Article  CAS  Google Scholar 

  • Chen, L. Y., Chen, J. M., Gituru, R. W., & Wang, Q. F. (2012). Generic phylogeny, historical biogeography and character evolution of the cosmopolitan aquatic plant family Hydrocharitaceae. BMC Evolutionary Biology, 12, 30.

    Article  CAS  Google Scholar 

  • Chen, L. Y., Lu, B., Morales-Briones, D. F., Moody, M. L., Liu, F., Hu, G. W., Huang, C. H., Chen, J. M., & Wang, Q. F. (2022b). Phylogenomic analyses of Alismatales shed light into adaptations to aquatic environments. Molecular Biology and Evolution, 39, msac079.

    Article  CAS  Google Scholar 

  • Chen, L., Les, D. H., Xu, L., Yao, X., Kang, M., & Huang, H. (2006). Isolation and characterization of a set of microsatellite loci in the submerged macrophyte, Vallisneria spinulosa Yan (Hydrocharitaceae). Molecular Ecology Notes, 6, 1243–1245.

    Article  CAS  Google Scholar 

  • Christenhusz, M. J., & Byng, J. W. (2016). The number of known plants species in the world and its annual increase. Phytotaxa, 261, 201–217.

    Article  Google Scholar 

  • Clement, R., Dimnet, L., Maberly, S. C., & Gontero, B. (2016). The nature of the CO 2-concentrating mechanisms in a marine diatom, Thalassiosira pseudonana. New Phytologist, 209, 1417–1427.

    Article  CAS  Google Scholar 

  • da Cunha, N. L., Xue, H., Wright, S. I., & Barrett, S. C. (2022). Genetic variation and clonal diversity in floating aquatic plants: Comparative genomic analysis of water hyacinth species in their native range. Molecular Ecology. https://doi.org/10.1111/mec.16664

  • Degroote, D., & Kennedy, R. A. (1977). Photosynthesis in Elodea canadensis Michx: Four-carbon acid synthesis. Plant Physiology, 59, 1133–1135.

    Article  CAS  Google Scholar 

  • Dima, O., Heyvaert, Y., & Inzé, D. (2022). Interactive database of genome editing applications in crops and future policy making in the European Union. Trends in Plant Science.

  • DiMario, R. J., Machingura, M. C., Waldrop, G. L., & Moroney, J. V. (2018). The many types of carbonic anhydrases in photosynthetic organisms. Plant Science, 268, 11–17.

    Article  CAS  Google Scholar 

  • Dinakar, C., & Bartels, D. (2013). Desiccation tolerance in resurrection plants: New insights from transcriptome, proteome and metabolome analysis. Frontiers in plant science, 4, 482.

    Article  Google Scholar 

  • Doohan, M. E., & Newcomb, E. H. (1976). Leaf ultrastructure and δ13C values of three seagrasses from the Great Barrier Reef. Functional Plant Biology, 3, 9–23.

    Article  Google Scholar 

  • Dusenge, M. E., Duarte, A. G., & Way, D. A. (2019). Plant carbon metabolism and climate change: Elevated CO 2 and temperature impacts on photosynthesis, photorespiration and respiration. New Phytologist, 221, 32–49.

    Article  CAS  Google Scholar 

  • Eaton-Rye, J. J. (2007). Celebrating Govindjee’s 50 years in photosynthesis research and his 75th birthday. Photosynthesis Research, 93, 1–5.

    Article  CAS  Google Scholar 

  • Eaton-Rye, J. J. (2013). Govindjee at 80: More than 50 years of free energy for photosynthesis. Photosynthesis Research, 116, 111–144.

    Article  CAS  Google Scholar 

  • Falcón, S., & Castillo, A. (2010). Dating the cyanobacterial ancestor of the chloroplast. ISME Journal , 4: 777–783

  • Falkowski, P. G., & Godfrey, L. V. (2008). Electrons, life and the evolution of Earth’s oxygen cycle. Philosophical Transactions of the Royal Society B: Biological Sciences, 363, 2705–2716.

    Article  CAS  Google Scholar 

  • Figge, R., Cassier-Chauvat, C., Chauvat, F., & Cerff, R. (2001). Characterization and analysis of an NAD (P) H dehydrogenase transcriptional regulator critical for the survival of cyanobacteria facing inorganic carbon starvation and osmotic stress. Molecular Microbiology, 39, 455–469.

    Article  CAS  Google Scholar 

  • Fiz-Palacios, O., Schneider, H., Heinrichs, J., & Savolainen, V. (2011). Diversification of land plants: Insights from a family-level phylogenetic analysis. BMC Evolutionary Biology, 11, 341.

    Article  Google Scholar 

  • Fukuzawa, H., Miura, K., Ishizaki, K., & Kucho, K. (2001). -i, Saito T, Kohinata T, Ohyama K Ccm1, a regulatory gene controlling the induction of a carbon-concentrating mechanism in Chlamydomonas reinhardtii by sensing CO2 availability. Proceedings of the National Academy of Sciences 98: 5347–5352

  • 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.

    Article  Google Scholar 

  • Gechev, T. S., Dinakar, C., Benina, M., Toneva, V., & Bartels, D. (2012). Molecular mechanisms of desiccation tolerance in resurrection plants. Cellular and Molecular Life Sciences, 69, 3175–3186.

    Article  CAS  Google Scholar 

  • Giordano, M., Beardall, J., & Raven, J. A. (2005). CO2 concentrating mechanisms in algae: Mechanisms, environmental modulation, and evolution. Annual Review of Plant Biology, 56, 99–131.

    Article  CAS  Google Scholar 

  • Goudet, M. M., Orr, D. J., Melkonian, M., Müller, K. H., Meyer, M. T., Carmo-Silva, E., & Griffiths, H. (2020). Rubisco and carbon‐concentrating mechanism co‐evolution across chlorophyte and streptophyte green algae. New Phytologist, 227, 810–823.

    Article  CAS  Google Scholar 

  • Govindjee, G., Shevela, D., & Björn, L. O. (2017). Evolution of the Z-scheme of photosynthesis: A perspective. Photosynthesis Research, 133, 5–15.

    Article  CAS  Google Scholar 

  • Gray, M. W. (1992). The endosymbiont hypothesis revisited. International Review of Cytology, 141, 233–357.

    Article  CAS  Google Scholar 

  • Green, W. (2010). The function of the aerenchyma in arborescent lycopsids: Evidence of an unfamiliar metabolic strategy. Proceedings of the Royal Society B: Biological Sciences 277: 2257–2267

  • Gunning, B., & Pate, J. (1969). “Transfer cells” plant cells with wall ingrowths, specialized in relation to short distance transport of solutes—their occurrence, structure, and development. Protoplasma, 68, 107–133.

    Article  Google Scholar 

  • Guo, J., Xue, J., Hua, J., Xuan, L., & Yin, Y. (2022). Research status and trends of underwater photosynthesis. Sustainability, 14, 4644.

    Article  CAS  Google Scholar 

  • Hagemann, M., Song, S., & Brouwer, E. M. (2021). Inorganic carbon assimilation in cyanobacteria: Mechanisms, regulation, and engineering. In P. Hudson, S. Y. Lee, & J. Nielsen (Eds.), Cyanobacteria Biotechnology (pp. 1–31). Weinheim, Germany: Wiley-Blackwell. In.

    Google Scholar 

  • Han, S., Maberly, S. C., Gontero, B., Xing, Z., Li, W., Jiang, H., & Huang, W. (2020). Structural basis for C4 photosynthesis without Kranz anatomy in leaves of the submerged freshwater plant Ottelia alismoides. Annals of Botany, 125, 869–879.

    Article  CAS  Google Scholar 

  • Harrison, J. P., Gheeraert, N., Tsigelnitskiy, D., & Cockell, C. S. (2013). The limits for life under multiple extremes. Trends in Microbiology, 21, 204–212.

    Article  CAS  Google Scholar 

  • Helder, R. (1982). Carbon assimilation pattern in the submerged leaves of the aquatic angiosperm: Vallisneria spiralis L. Acta Botánica Neerlandica, 31, 281–295. Van Harmelen M.

    Article  CAS  Google Scholar 

  • Hennacy, J. H., & Jonikas, M. C. (2020). Prospects for engineering biophysical CO2 concentrating mechanisms into land plants to enhance yields. Annual Review of Plant Biology, 71, 461–485.

    Article  CAS  Google Scholar 

  • Henry, R. J. (2020). Innovations in plant genetics adapting agriculture to climate change. Current Opinion in Plant Biology, 56, 168–173.

    Article  Google Scholar 

  • Henry, R. J., Rangan, P., & Furtado, A. (2016). Functional cereals for production in new and variable climates. Current Opinion in Plant Biology, 30, 11–18.

    Article  Google Scholar 

  • Henry, R. J., Rangan, P., Furtado, A., Busch, F. A., & Farquhar, G. D. (2017). Does C4 photosynthesis occur in wheat seeds? Plant Physiology, 174, 1992–1995.

    Article  CAS  Google Scholar 

  • Hershner, C., & Havens, K. J. (2008). Managing invasive aquatic plants in a changing system: Strategic consideration of ecosystem services. Conservation Biology, 22, 544–550.

    Article  Google Scholar 

  • Heyduk, K., Moreno-Villena, J. J., Gilman, I. S., Christin, P. A., & Edwards, E. J. (2019). The genetics of convergent evolution: Insights from plant photosynthesis. Nature Reviews Genetics, 20, 485–493.

    Article  CAS  Google Scholar 

  • Holaday, A. S., & Bowes, G. (1980). C4 acid metabolism and dark CO2 fixation in a submersed aquatic macrophyte (Hydrilla verticillata). Plant Physiology, 65, 331–335.

    Article  CAS  Google Scholar 

  • Hori, H., Lim, B. L., & Osawa, S. (1985). Evolution of green plants as deduced from 5S rRNA sequences. Proceedings of the National Academy of Sciences 82: 820–823

  • Hu, S., Li, G., Yang, J., & Hou, H. (2017). Aquatic plant genomics: Advances, applications, and prospects. International Journal of Genomics, 2017, 6347874.

    Article  Google Scholar 

  • Huang, G., Peng, S., & Li, Y. (2022). Variation of photosynthesis during plant evolution and domestication: Implications for improving crop photosynthesis. Journal of Experimental Botany, 73, 4886–4896.

    Article  Google Scholar 

  • Hussner, A. (2009). Growth and photosynthesis of four invasive aquatic plant species in Europe. Weed Research, 49, 506–515.

    Article  Google Scholar 

  • Hussner, A., Stiers, I., Verhofstad, M., Bakker, E., Grutters, B., & Haury, J. (2017). Management and control methods of invasive alien freshwater aquatic plants: A review. Aquatic Botany, 136, 112–137. Van Valkenburg JBrundu G, Newman J, Clayton J.

    Article  Google Scholar 

  • Iwan Jones, J., Hardwick, K., & Eaton, J. W. (1996). Diurnal carbon restrictions on the photosynthesis of dense stands of Elodea nuttallii. (Planch) St John Hydrobiologia, 340, 11–16.

    Article  Google Scholar 

  • Jiang, K., Shi, Y. S., Zhang, J., & Xu, N. N. (2011). Microsatellite primers for vulnerable seagrass Halophila beccarii (Hydrocharitaceae). American Journal of Botany, 98, e155–e157.

    Article  CAS  Google Scholar 

  • Jin, S., Sun, J., Wunder, T., Tang, D., Cousins, A. B., Sze, S. K., Mueller-Cajar, O., & Gao, Y. G. (2016). Structural insights into the LCIB protein family reveals a new group of β-carbonic anhydrases. Proceedings of the National Academy of Sciences 113: 14716–14721

  • Kaplan, A., Badger, M. R., & Berry, J. A. (1980). Photosynthesis and the intracellular inorganic carbon pool in the bluegreen alga Anabaena variabilis: Response to external CO2 concentration. Planta, 149, 219–226.

    Article  CAS  Google Scholar 

  • Keeley, J. E. (1998). CAM photosynthesis in submerged aquatic plants. The Botanical Review, 64, 121–175.

    Article  Google Scholar 

  • Keeley, J. E. (1999). Photosynthetic pathway diversity in a seasonal pool community. Functional Ecology, 13, 106–118.

    Article  Google Scholar 

  • Kenrick, P., & Crane, P. R. (1997). The origin and early evolution of plants on land. Nature, 389, 33–39.

    Article  CAS  Google Scholar 

  • Klavsen, S. K., & Maberly, S. C. (2010). Effect of light and CO2 on inorganic carbon uptake in the invasive aquatic CAM-plant Crassula helmsii. Functional Plant Biology, 37, 737–747.

    Article  CAS  Google Scholar 

  • Krabel, D., Eschrich, W., Gamalei, Y. V., Fromm, J., & Ziegler, H. (1995). Acquisition of carbon in Elodea canadensis Michx. Journal of Plant Physiology, 145, 50–56.

    Article  CAS  Google Scholar 

  • Kromdijk, J., & McCormick, A. J. (2022). Genetic variation in photosynthesis: Many variants make light work. Journal of Experimental Botany, 73, 3053–3056.

    Article  CAS  Google Scholar 

  • Kumar, A., Block, J. E., & Nonomura, A. M. (2021). Mister Photosynthesis of the 21st Century, Govindjee. International Journal of Life Sciences, 10, 61–80.

    Article  Google Scholar 

  • Les, D. H., Cleland, M. A., & Waycott, M. (1997). Phylogenetic studies in Alismatidae, II: Evolution of marine angiosperms (seagrasses) and hydrophily. Systematic Botany, 22, 443–463.

    Article  Google Scholar 

  • Les, D. H., Moody, M. L., & Soros, C. L. (2006). A reappraisal of phylogentic relationships in the monocotyledon family Hydrocharitaceae (Alismatidae). Aliso: A Journal of Systematic and Floristic Botany 22: 211–230

  • Lewis, L. A., & McCourt, R. M. (2004). Green algae and the origin of land plants. American Journal of Botany, 91, 1535–1556.

    Article  Google Scholar 

  • Li, B., Lopes, J. S., Foster, P. G., Embley, T. M., & Cox, C. J. (2014). Compositional biases among synonymous substitutions cause conflict between gene and protein trees for plastid origins. Molecular Biology and Evolution, 31, 1697–1709.

    Article  CAS  Google Scholar 

  • Li, Z. Z., Lehtonen, S., Gichira, A. W., Martins, K., Efremov, A., Wang, Q. F., & Chen, J. M. (2022). Plastome phylogenomics and historical biogeography of aquatic plant genus Hydrocharis (Hydrocharitaceae). BMC Plant Biology, 22, 106.

    Article  Google Scholar 

  • Li, Z. Z., Lehtonen, S., Martins, K., Gichira, A. W., Wu, S., Li, W., Hu, G. W., Liu, Y., Zou, C. Y., & Wang, Q. F. (2020). Phylogenomics of the aquatic plant genus Ottelia (Hydrocharitaceae): Implications for historical biogeography. Molecular Phylogenetics and Evolution, 152, 106939.

    Article  Google Scholar 

  • Liu, L. N. (2022). Advances in the bacterial organelles for CO2 fixation. Trends in Microbiology, 30, 567–580.

    Article  CAS  Google Scholar 

  • Long, B. M., Rae, B. D., Rolland, V., Förster, B., & Price, G. D. (2016). Cyanobacterial CO2-concentrating mechanism components: Function and prospects for plant metabolic engineering. Current Opinion in Plant Biology, 31, 1–8.

    Article  CAS  Google Scholar 

  • Lyons, T. W., Reinhard, C. T., & Planavsky, N. J. (2014). The rise of oxygen in Earth’s early ocean and atmosphere. Nature, 506, 307–315.

    Article  CAS  Google Scholar 

  • Maberly, S. C., Berthelot, S. A., Stott, A. W., & Gontero, B. (2015). Adaptation by macrophytes to inorganic carbon down a river with naturally variable concentrations of CO2. Journal of Plant Physiology, 172, 120–127.

    Article  CAS  Google Scholar 

  • Maberly, S. C., & Madsen, T. V. (2002). Freshwater angiosperm carbon concentrating mechanisms: Processes and patterns. Functional Plant Biology, 29, 393–405.

    Article  CAS  Google Scholar 

  • Mackinder, L. C. (2018). The Chlamydomonas CO2-concentrating mechanism and its potential for engineering photosynthesis in plants. New Phytologist, 217, 54–61.

    Article  CAS  Google Scholar 

  • Magnin, N. C., Cooley, B. A., Reiskind, J. B., & Bowes, G. (1997). Regulation and localization of key enzymes during the induction of Kranz-less, C4-type photosynthesis in Hydrilla verticillata. Plant Physiology, 115, 1681–1689.

    Article  CAS  Google Scholar 

  • Mantovani, O., Reimann, V., Haffner, M., Herrmann, F. P., Selim, K. A., Forchhammer, K., Hess, W. R., & Hagemann, M. (2022). The impact of the cyanobacterial carbon-regulator protein SbtB and of the second messengers cAMP and c‐di‐AMP on CO2‐dependent gene expression. New Phytologist, 234, 1801–1816.

    Article  CAS  Google Scholar 

  • McFadden, G. I. (2001). Chloroplast origin and integration. Plant Physiology, 125, 50–53.

    Article  CAS  Google Scholar 

  • McGrath, J. M., & Long, S. P. (2014). Can the cyanobacterial carbon-concentrating mechanism increase photosynthesis in crop species? A theoretical analysis. Plant Physiology, 164, 2247–2261.

    Article  CAS  Google Scholar 

  • Melkozernov, A. N., & Blankenship, R. E. (2006). Photosynthetic functions of chlorophylls. In B. Grimm, R. J. Porra, W. Rudiger, & H. Scheer (Eds.), Chlorophylls and bacteriochlorophylls: Biochemistry, biophysics, functions and applications (25 vol., pp. 397–412). Dordrecht, The Netherlands: Springer. In.

    Chapter  Google Scholar 

  • Meyer, M., & Griffiths, H. (2013). Origins and diversity of eukaryotic CO2-concentrating mechanisms: Lessons for the future. Journal of experimental botany, 64, 769–786.

    Article  CAS  Google Scholar 

  • Meyer, M. T. (2022). Rubisco microcompartments: The function of carboxysomes and pyrenoids in aquatic CO 2-concentrating mechanisms. In S. C. Maberly, & B. Gontero (Eds.), Blue Planet, red and green photosynthesis: Productivity and carbon cycling in aquatic ecosystems (pp. 197–224). USA: John Wiley and Sons Inc. In.

    Chapter  Google Scholar 

  • Meyer, M. T., Genkov, T., Skepper, J. N., Jouhet, J., Mitchell, M. C., Spreitzer, R. J., & Griffiths, H. (2012). Rubisco small-subunit α-helices control pyrenoid formation in Chlamydomonas. Proceedings of the National Academy of Sciences 109: 19474–19479

  • Moore, K. R., Magnabosco, C., Momper, L., Gold, D. A., Bosak, T., & Fournier, G. P. (2019). An expanded ribosomal phylogeny of cyanobacteria supports a deep placement of plastids. Frontiers in Microbiology, 10, 1612.

    Article  Google Scholar 

  • Morden, C. W., Delwiche, C. F., Kuhsel, M., & Palmer, J. D. (1992). Gene phylogenies and the endosymbiotic origin of plastids. Biosystems, 28, 75–90.

    Article  CAS  Google Scholar 

  • Nishimura, T., Takahashi, Y., Yamaguchi, O., Suzuki, H., & Maeda Si, Omata, T. (2008). Mechanism of low CO2-induced activation of the cmp bicarbonate transporter operon by a LysR family protein in the cyanobacterium Synechococcus elongatus strain PCC 7942. Molecular microbiology, 68, 98–109.

    Article  CAS  Google Scholar 

  • Nölke, G., Barsoum, M., Houdelet, M., Arcalís, E., Kreuzaler, F., Fischer, R., & Schillberg, S. (2019). The integration of algal carbon concentration mechanism components into tobacco chloroplasts increases photosynthetic efficiency and biomass. Biotechnology journal, 14, 1800170.

    Article  Google Scholar 

  • Nutbeam, A. R., & Duffus, C. M. (1976). Evidence for C4 photosynthesis in barley pericarp tissue. Biochemical and Biophysical Research Communications, 70, 1198–1203.

    Article  CAS  Google Scholar 

  • Omata, T., Price, G. D., Badger, M. R., Okamura, M., Gohta, S., & Ogawa, T. (1999). Identification of an ATP-binding cassette transporter involved in bicarbonate uptake in the cyanobacterium Synechococcus sp. strain PCC 7942. Proceedings of the National Academy of Sciences, 96: 13571–13576

  • Osmond, C., Valaane, N., Haslam, S., Uotila, P., & Roksandic, Z. (1981). Comparisons of δ13C values in leaves of aquatic macrophytes from different habitats in Britain and Finland; some implications for photosynthetic processes in aquatic plants. Oecologia, 50, 117–124.

    Article  CAS  Google Scholar 

  • Pagani, M., Zachos, J. C., Freeman, K. H., Tipple, B., & Bohaty, S. (2005). Marked decline in atmospheric carbon dioxide concentrations during the Paleogene. Science, 309, 600–603.

    Article  CAS  Google Scholar 

  • Pedersen, O., Colmer, T. D., & Sand-Jensen, K. (2013). Underwater photosynthesis of submerged plants–recent advances and methods. Frontiers in plant science, 4 140.

    Article  Google Scholar 

  • Phadwal, K., & Singh, P. (2003). Isolation and characterization of an indigenous isolate of Dunaliella sp. for β-carotene and glycerol production from a hypersaline lake in India. Journal of Basic Microbiology: An International Journal on Biochemistry Physiology Genetics Morphology and Ecology of Microorganisms, 43, 423–429.

    Article  Google Scholar 

  • Prančl, J., Kaplan, Z., Trávníček, P., & Jarolimova, V. (2014). Genome size as a key to evolutionary complex aquatic plants: Polyploidy and hybridization in Callitriche (Plantaginaceae). PLoS One, 9, e105997.

    Article  Google Scholar 

  • Price, G. D., Badger, M. R., & von Caemmerer, S. (2011). The prospect of using cyanobacterial bicarbonate transporters to improve leaf photosynthesis in C3 crop plants. Plant Physiology, 155, 20–26.

    Article  CAS  Google Scholar 

  • Price, G. D., Badger, M. R., Woodger, F. J., & Long, B. M. (2008). Advances in understanding the cyanobacterial CO2-concentrating-mechanism (CCM): Functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants. Journal of Experimental Botany, 59, 1441–1461.

    Article  CAS  Google Scholar 

  • Price, G. D., Pengelly, J. J., Forster, B., Du, J., Whitney, S. M., von Caemmerer, S., Badger, M.R., Howitt, S.M. & Evans, J.R. (2013). The cyanobacterial CCM as a source of genes for improving photosynthetic CO2 fixation in crop species. Journal of Experimental Botany, 64, 753–768.

    Article  CAS  Google Scholar 

  • Pucker, B., Irisarri, I., de Vries, J., & Xu, B. (2022). Plant genome sequence assembly in the era of long reads: Progress, challenges and future directions. Quantitative Plant Biology, 3, e5.

    Article  Google Scholar 

  • Rae, B. D., Long, B. M., Förster, B., Nguyen, N. D., Velanis, C. N., Atkinson, N., Hee, W. Y., Mukherjee, B., Price, G. D., & McCormick, A. J. (2017). Progress and challenges of engineering a biophysical CO2-concentrating mechanism into higher plants. Journal of Experimental Botany, 68, 3717–3737.

    Article  CAS  Google Scholar 

  • Rangan, P., Furtado, A., & Henry, R. J. (2016). New evidence for grain specific C4 photosynthesis in wheat. Scientific Reports, 6, 1–12.

    Article  Google Scholar 

  • Rangan, P., Wankhede, D. P., Subramani, R., Chinnusamy, V., Malik, S. K., Baig, M. J., Singh, K., & Henry, R. (2022). Evolution of an intermediate C4 photosynthesis in the non-foliar tissues of the Poaceae. Photosynthesis Research, 153, 125–134.

    Article  CAS  Google Scholar 

  • Rao, S. K., Magnin, N. C., Reiskind, J. B., & Bowes, G. (2002). Photosynthetic and Other Phospho enol pyruvate Carboxylase Isoforms in the Single-Cell, Facultative C4 System of Hydrilla verticillata. Plant Physiology, 130, 876–886.

    Article  CAS  Google Scholar 

  • Raven, J. (1968). The mechanism of photosynthetic use of bicarbonate by Hydrodictyon africanum. Journal of Experimental Botany, 19, 193–206.

    Article  CAS  Google Scholar 

  • Raven, J. (1970). Exogenous inorganic carbon sources in plant photosynthesis. Biological Reviews, 45, 167–220.

    Article  CAS  Google Scholar 

  • Raven, J. A., & Beardall, J. (2014). CO2 concentrating mechanisms and environmental change. Aquatic Botany, 118, 24–37.

    Article  CAS  Google Scholar 

  • Raven, J. A., & Beardall, J. (2016). The ins and outs of CO2. Journal of Experimental Botany, 67, 1–13.

    Article  CAS  Google Scholar 

  • Raven, J. A., & Cockell, C. S. (2008). The evolution of inorganic carbon concentrating mechanisms in photosynthesis. Philosophical Transactions of the Royal Society B: Biological Sciences, 363, 2641–2650. De La Rocha CL.

    Article  CAS  Google Scholar 

  • Reiskind, J. B., & Maberly, S. C. (2014). A tribute to George Bowes: Linking terrestrial and aquatic botany. Aquatic Botany, 118, 1–3.

    Article  Google Scholar 

  • Riding, R. (2006). Cyanobacterial calcification, carbon dioxide concentrating mechanisms, and Proterozoic–Cambrian changes in atmospheric composition. Geobiology, 4, 299–316.

    Article  CAS  Google Scholar 

  • Riis, T., Olesen, B., Clayton, J. S., Lambertini, C., Brix, H., & Sorrell, B. K. (2012). Growth and morphology in relation to temperature and light availability during the establishment of three invasive aquatic plant species. Aquatic Botany, 102, 56–64.

    Article  Google Scholar 

  • Sage, R. F., & Coleman, J. R. (2001). Effects of low atmospheric CO2 on plants: More than a thing of the past. Trends in plant science, 6, 18–24.

    Article  CAS  Google Scholar 

  • Salvucci, M. E., & Bowes, G. (1981). Induction of reduced photorespiratory activity in submersed and amphibious aquatic macrophytes. Plant Physiology, 67, 335–340.

    Article  CAS  Google Scholar 

  • Sánchez-Baracaldo, P., Raven, J. A., Pisani, D., & Knoll, A. H. (2017). Early photosynthetic eukaryotes inhabited low-salinity habitats. Proceedings of the National Academy of Sciences 114: E7737-E7745

  • Sánchez-Baracaldo, P., & Cardona, T. (2020). On the origin of oxygenic photosynthesis and Cyanobacteria. New Phytologist, 225, 1440–1446.

    Article  Google Scholar 

  • Sand-Jensen, K. (1997). Broad-scale comparison of photosynthesis in terrestrial and aquatic plant communities. Oikos: 203–208

  • Scheer, H. (2006). An overview of chlorophylls and bacteriochlorophylls: Biochemistry, biophysics, functions and applications. In Grimm, B., Porra, R. J., Rudiger, W. & Scheer H. (Eds.) Chlorophylls and bacteriochlorophylls: Biochemistry, Biophysics, functions and applications (25 vol., pp. 1–26). Dordrecht, The Netherlands: Springer.

    Chapter  Google Scholar 

  • Servais, T., Cascales-Miñana, B., Cleal, C. J., Gerrienne, P., Harper, D. A., & Neumann, M. (2019). Revisiting the Great Ordovician Diversification of land plants: Recent data and perspectives. Palaeogeography, Palaeoclimatology, Palaeoecology 534: 109280

  • Shevela, D., Bjorn, L. O., & Govindjee, G. (2019). Photosynthesis: Solar energy for life. World Scientific Publishing.

    Google Scholar 

  • Simkin, A. J., Faralli, M., Ramamoorthy, S., & Lawson, T. (2020). Photosynthesis in non-foliar tissues: Implications for yield. The Plant Journal, 101, 1001–1015.

    Article  CAS  Google Scholar 

  • Smit, M. A., & Mezger, K. (2017). Earth’s early O2 cycle suppressed by primitive continents. Nature Geoscience, 10, 788–792.

    Article  CAS  Google Scholar 

  • Stirbet, A., Shevela, D., Pareek, A., Naithani, S., Björn, L. O., Eaton-Rye, J. J., & Nonomura, A. (2022). Govindjee’s 90th birthday: A life dedicated to photosynthesis. Plant Physiology Reports. https://doi.org/10.1007/s40502-022-00690-9

  • Sültemeyer, D., Schmidt, C., & Fock, H. P. (1993). Carbonic anhydrases in higher plants and aquatic microorganisms. Physiologia Plantarum, 88, 179–190.

    Article  Google Scholar 

  • Tabita, F. R., Satagopan, S., Hanson, T. E., Kreel, N. E., & Scott, S. S. (2008). Distinct form I, II, III, and IV Rubisco proteins from the three kingdoms of life provide clues about Rubisco evolution and structure/function relationships. Journal of Experimental botany, 59, 1515–1524.

    Article  CAS  Google Scholar 

  • Tanaka, H., Kitamura, M., Nakano, Y., Katayama, M., Takahashi, Y., Kondo, T., Manabe, K., Omata, T., & Kutsuna, S. (2012). CmpR is important for circadian phasing and cell growth. Plant and Cell Physiology, 53, 1561–1569.

    Article  CAS  Google Scholar 

  • Tanaka, N., Setoguchi, H., & Murata, J. (1997). Phylogeny of the family hydrocharitaceae inferred fromrbcL andmatK gene sequence data. Journal of Plant Research, 110, 329–337.

    Article  CAS  Google Scholar 

  • Tashiro, T., Ishida, A., Hori, M., Igisu, M., Koike, M., Méjean, P., Takahata, N., Sano, Y., & Komiya, T. (2017). Early trace of life from 3.95 Ga sedimentary rocks in Labrador. Canada Nature, 549, 516–518.

    Article  Google Scholar 

  • Tay Fernandez, C. G., Nestor, B. J., Danilevicz, M. F., Marsh, J. I., Petereit, J., Bayer, P. E., Batley, J., & Edwards, D. (2022). Expanding Gene-Editing Potential in Crop Improvement with Pangenomes. International Journal of Molecular Sciences, 23, 2276.

    Article  CAS  Google Scholar 

  • Walker, J., Geissman, J., Bowring, S., & Babcock, L. (2018). GSA Geologic time scale v.5.0 (,5ed, Ed 5 vol.). USA: Geological Society of America. https://www.geosociety.org/documents/gsa/timescale/timescl.pdfIn.

    Google Scholar 

  • Wang, S., Li, P., Liao, Z., Wang, W., Chen, T., Yin, L., Jiang, H. S., & Li, W. (2022). Adaptation of inorganic carbon utilization strategies in submerged and floating leaves of heteroblastic plant Ottelia cordata. Environmental and Experimental Botany, 196, 104818.

    Article  CAS  Google Scholar 

  • Whibley, A., Kelley, J. L., & Narum, S. R. (2021). The changing face of genome assemblies: Guidance on achieving high-quality reference genomes. Molecular Ecology Resources, 21, 641–652.

    Article  CAS  Google Scholar 

  • Xiong, J., Fischer, W. M., Inoue, K., Nakahara, M., & Bauer, C. E. (2000). Molecular evidence for the early evolution of photosynthesis. Science, 289, 1724–1730.

    Article  CAS  Google Scholar 

  • Xu, N. N., Yu, S., Zhang Jg, Tsang, P. K. E., & Chen, X. Y. (2010). Microsatellite primers for Halophila ovalis and cross-amplification in H. minor (Hydrocharitaceae). American Journal of Botany, 97, e56–e57.

    Article  CAS  Google Scholar 

  • Yin, L., Li, W., Madsen, T. V., Maberly, S. C., & Bowes, G. (2017). Photosynthetic inorganic carbon acquisition in 30 freshwater macrophytes. Aquatic Botany, 140, 48–54.

    Article  CAS  Google Scholar 

  • Zhang, Y., Massel, K., Godwin, I. D., & Gao, C. (2018). Applications and potential of genome editing in crop improvement. Genome Biology, 19, 1–11.

    Article  Google Scholar 

  • Zhang, Y., Yin, L., Jiang, H. S., Li, W., Gontero, B., & Maberly, S. C. (2014). Biochemical and biophysical CO2 concentrating mechanisms in two species of freshwater macrophyte within the genus Ottelia (Hydrocharitaceae). Photosynthesis research, 121, 285–297.

    Article  CAS  Google Scholar 

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Acknowledgements

The research Grant 16113160001-1006976 funded by the Indian Council of Agricultural Research, New Delhi through the ‘Incentivizing research in Agriculture’ scheme is gratefully acknowledged.

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  1. Division of Genomic Resources, ICAR-National Bureau of Plant Genetic Resources, 110012, New Delhi, India

    Parimalan Rangan

  2. Queensland Alliance for Agriculture and Food Innovation, University of Queensland, 4072, St Lucia, QLD, Australia

    Parimalan Rangan

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This article is dedicated to Prof. Govindjee, dearly known as Mister Photosynthesis, for his outstanding contributions that gave the world a better understanding on the photosynthesis, and in addition he had transformed many students to world leaders in photosynthesis research.

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Rangan, P. Can genomics tools assist in gaining insights from the aquatic angiosperms to transform crop plants with multiple carbon concentrating mechanisms to adapt and yield better in challenging environment?. Plant Physiol. Rep. 27, 580–589 (2022). https://doi.org/10.1007/s40502-022-00700-w

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