Photosynthetica 2020, 58(5):1090-1097 | DOI: 10.32615/ps.2020.064

The carbon reactions of photosynthesis: role of lectins and glycoregulation

A.M. NONOMURA1, D. SHEVELA2,3, S.S. KOMATH5, K.Y. BIEL6,7, G. GOVINDJEE5,†
Carbon Reactions of Photosynthesis Sector, BRANDT iHammer, Powell, Ohio, USA1
2 Department of Chemistry, Chemical Biological Centre, Umeå University, Umeå, Sweden
3 ShevelaDesign AB, Umeå, Sweden
5 School of Life Sciences, Jawaharlal Nehru University, New Delhi, India
6 Institute of Basic Biological Problems, Russian Academy of Sciences, Pushchino, Russia
7 Biosphere Systems International Foundation, Tucson, Arizona, USA
Department of Plant Biology, Department of Biochemistry, and Center of Biophysics & Quantitative Biology, University of Illinois at Urbana-Champaign, Urbana, Illinois, USA†

Modulation of glycoregulation in agriculture is reviewed here with emphasis on the elucidation of previously unknown pathways involving vacuolar lectins as well as a bypass of lectins that direct free sugars toward productivity. The reversible binding sequences of the endogenous lectin cycle are compared to an induced lectin bypass, as follows. (1) In the cycle, carbohydrate ligands, with similar binding specificities that compete for binding sites on lectins, are involved in the natural cycle of sugar exchanges. (2) For the bypass, tightly bound ligands that occupy lectins prevent free sugars from binding, making them available for productivity. This bypass is induced by methyl-α-D-mannopyranoside, a biochemical plant growth regulator for photosynthesis. Integration of this novel technology, with structural elements crucial for ligand binding by the lectins and with nitrogen assimilation, provides the basis for successful modulation of glycoregulation in crops for enhancement of quality and quantity.

Additional key words: agglutinin; Benson-Bassham-Calvin cycle; concanavalin A; dark reactions; mannose-binding specificity; α-D-mannoside.

Received: July 26, 2020; Revised: July 26, 2020; Accepted: September 1, 2020; Prepublished online: September 24, 2020; Published: December 8, 2020  Show citation

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NONOMURA, A.M., SHEVELA, D., KOMATH, S.S., BIEL, K.Y., & GOVINDJEE, G. (2020). The carbon reactions of photosynthesis: role of lectins and glycoregulation. Photosynthetica, 58(5), 1090-1097. doi: 10.32615/ps.2020.064
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    References

    1. Aleksidze G. Ya., Litvinov A.I., Vyskrebentseva E.I.: The model of Calvin cycle enzyme organization on thylakoid membranes with the involvement of the Photosystem I lectin. - Russ. J. Plant Physl+ 49: 137-141, 2002. Go to original source...
    2. Aluri S., Büttner M.: Identification and functional expression of the Arabidopsis thaliana vacuolar glucose transporter 1 and its role in seed germination and flowering. - P. Natl. Acad. Sci. USA 104: 2537-2542, 2007. Go to original source...
    3. Armbruster U., Strand D.D.: Regulation of chloroplast primary metabolism. - Photosynth. Res. 145: 1-3, 2020. Go to original source...
    4. Aubert S., Choler P., Pratt J. et al.: Methyl-β-D-glucopyranoside in higher plants: Accumulation and intracellular localization in Geum montanum L. leaves and in model systems studied by 13C nuclear magnetic resonance. - J. Exp. Bot. 55: 2179-2189, 2004. Go to original source...
    5. Barre A., Bourne Y., Van Damme E.J.M. et al.: Mannose-binding plant lectins: different structural scaffolds for a common sugar-recognition process. - Biochimie 83: 645-651, 2001. Go to original source...
    6. Barre A., Bourne Y., Van Damme E.J.M., Rougé P.: Overview of the structure-function relationships of mannose-specific lectins from plants, algae and fungi. - Int. J. Mol. Sci. 20: 254, 2019. Go to original source...
    7. Bassham J.A.: Mapping the carbon reduction cycle: a personal retrospective. - Photosynth. Res. 76: 35-52, 2003. Go to original source...
    8. Benson A.A.: Following the path of carbon in photosynthesis: a personal story. - Photosynth. Res. 73: 29-49, 2002. Go to original source...
    9. Benson A.A., Nonomura A.M.: The path of carbon in photosyn-thesis: methanol inhibition of glycolic acid accumulation. - In: Murata N. (ed.): Research in Photosynthesis, Proceedings of the IX International Congress on Photosynthesis. P-522. Kluwer, Dordrecht 1992. Go to original source...
    10. Benson A.A., Nonomura A.M., Gerard V.A.: The path of carbon in photosynthesis. XXV. Plant and algal growth responses to glycopyranosides. - J. Plant Nutr. 32: 1185-1200, 2009. Go to original source...
    11. Biel K.Y., Fomina I.R.: Benson-Bassham-Calvin cycle contribu-tion to the organic life on our planet. - Photosynthetica 53: 161-167, 2015. Go to original source...
    12. Biel K.Y., Nonomura A.M., Benson A.A., Nishio J.N.: The path of carbon in photosynthesis. XXVI. Uptake and transport of methylglucopyranoside throughout plants. - J. Plant Nutr. 33: 902-913, 2010. Go to original source...
    13. Bloemen J., McGuire M.A., Aubrey D.P. et al.: Transport of root-respired CO2 via the transpiration stream affects aboveground carbon assimilation and CO2 efflux in trees. - New Phytol. 197: 555-565, 2013. Go to original source...
    14. Bloom A.J.: Photorespiration and nitrate assimilation: a major intersection between plant carbon and nitrogen. - Photosynth. Res. 123: 117-128, 2015. Go to original source...
    15. Bloom A.J., Smart D.R., Nguyen D.T., Searles P.S.: Nitrogen assimilation and growth of wheat under elevated carbon dioxide. - P. Natl. Acad. Sci. USA 99: 1730-1735, 2002. Go to original source...
    16. Buchanan B.B.: The carbon (formerly dark) reactions of photosynthesis. - Photosynth. Res. 128: 215-217, 2016. Go to original source...
    17. Calvin M., Benson A.A.: The path of carbon in photosynthesis. - Science 107: 476-480, 1948. Go to original source...
    18. Casset F., Hamelryck T., Loris R. et al.: NMR, molecular modeling, and crystallographic studies of lentil lectin-sucrose interaction. - J. Biol. Chem. 270: 25619-25628, 1995. Go to original source...
    19. Dam T.K., Brewer C.F.: Fundamentals of lectin-carbohydrate interactions. - In: Kamerling J.P., Boons G.J., Lee Y.C. et al. (ed.): Comprehensive Glycoscience. Pp. 397-452. Elsevier, Oxford 2007. Go to original source...
    20. Edelman G.M., Wang J.L.: Binding and functional properties of concanavalin A and its derivatives. III. Interactions with indoleacetic acid and other hydrophobic ligands. - J. Biol. Chem. 253: 3016-3022, 1978. Go to original source...
    21. Fageria N.K., Baligar V.C., Li Y.C.: The role of nutrient efficient plants in improving crop yields in the twenty first century. - J. Plant Nutr. 31: 1121-1157, 2008. Go to original source...
    22. Fageria N.K., Barbosa Filho M.P., Moreira A., Guimarães C.M.: Foliar fertilization of crop plants. - J. Plant Nutr. 32: 1044-1064, 2009. Go to original source...
    23. Fomina I.R., Biel K.Y.: Photosynthetic carbon metabolism: strategy of adaptation over evolutionary history. - In: Allakhverdiev S.I. (ed.): Photosynthesis: New Approaches to the Molecular, Cellular, and Organismal Levels. Pp. 233-326. Scrivener Publishing, Austin 2016. Go to original source...
    24. Gout E., Aubert S., Bligny R. et al.: Metabolism of methanol in plant cells. Carbon-13 nuclear magnetic resonance studies. - Plant Physiol. 123: 287-296, 2000. Go to original source...
    25. Govindjee G., Nonomura A., Lichtenthaler H.K.: Remembering Melvin Calvin (1911-1997), a highly versatile scientist of the 20th century. - Photosynth. Res. 143: 1-11, 2020. Go to original source...
    26. Hincha D.K., Bakaltcheva I., Schmitt J.M.: Galactose-specific lectins protect isolated thylakoids against freeze-thaw damage. - Plant Physiol. 103: 59-65, 1993. Go to original source...
    27. Hoagland D.R., Arnon D.I.: The water-culture method for growing plants without soil. California Agricultural Experiment Station Circular 347. The College of Agriculture, University of California, Berkeley 1950.
    28. Hymus G.J., Baker N.R., Long S.P.: Growth in elevated CO2 can both increase and decrease photochemistry and photoinhibition of photosynthesis in a predictable manner. Dactylis glomerata grown in two levels of nitrogen nutrition. -Plant Physiol. 127: 1204-1211, 2001. Go to original source...
    29. Jin X., Yang G., Tan C., Zhao C.: Effects of nitrogen stress on the photosynthetic CO2 assimilation, chlorophyll fluorescence, and sugar-nitrogen ratio in corn. - Sci. Rep.-UK 5: 9311, 2015. Go to original source...
    30. Kiba T., Kudo T., Kojima M., Sakakibara H.: Hormonal control of nitrogen acquisition: roles of auxin, abscisic acid, and cytokinin. - J. Exp. Bot. 62: 1399-1409, 2011. Go to original source...
    31. Komath S.S., Kavitha M., Swamy M.J.: Beyond carbohydrate binding: new directions in plant lectin research. - Org. Biomol. Chem. 4: 973-988, 2006. Go to original source...
    32. Kovalchuk N.V., Melnykova N.M., Musatenko L.: Role of phytolectin in the life cycle of plants. - Biopolym. Cell 28: 171-180, 2012. Go to original source...
    33. Lambin J., Asci S.D., Dubiel M. et al.: OsEUL lectin gene expression in rice: stress regulation, subcellular localization and tissue specificity. - Front. Plant Sci. 11: 185, 2020. Go to original source...
    34. Lannoo N., Van Damme E.J.M.: Nucleocytoplasmic plant lectins. - BBA-Gen. Subjects 1800: 190-201, 2010. Go to original source...
    35. Lannoo N., Van Damme E.J.M.: Lectin domains at the frontiers of plant defense. - Front. Plant Sci. 5: 397, 2014. Go to original source...
    36. Laus M.C., Logman T.J., Lamers G.E. et al.: A novel polar surface polysaccharide from Rhizobium leguminosarum binds host plant lectin. - Mol. Microbiol. 59: 1704-1713, 2006. Go to original source...
    37. Law S.R., Kellgren T., Björk R. et al.: Centralization within sub-experiments enhances the biological relevance of gene co-expression networks: a plant mitochondrial case study. - Front. Plant Sci. 11: 524, 2020. Go to original source...
    38. Loris R., Hamelryck T., Bouckaert J., Wyns L.: Legume lectin structure. - BBA-Protein Struct. Mol. Enzymol. 1383: 9-36, 1998. Go to original source...
    39. Marty F.: Plant Vacuoles. - Plant Cell 11: 587-599, 1999. Go to original source...
    40. Naismith J.H., Emmerich C., Habash J. et al.: Refined structure of concanavalin A complexed with methyl α-D-mannopyranoside at 2.0 Å resolution and comparison with the saccharide-free structure. - Acta Crystallogr. D 50: 847-858, 1994. Go to original source...
    41. Naismith J.H., Field R.A.: Structural basis of trimannoside recognition by concanavalin A. - J. Biol. Chem. 271: 972-976, 1996. Go to original source...
    42. Nilsson C.L.: Lectins: Analytical Technologies. Pp. 442. Elsevier, Amsterdam 2007.
    43. Nonomura A.M., Benson A.A.: The path of carbon in photosynthesis. XXIV. Improved crop yields with methanol. - P. Natl. Acad. Sci. USA 89: 9794-9798, 1992a. Go to original source...
    44. Nonomura A.M., Benson A.A.: The path of carbon in photosyn-thesis. Methanol and light. - In: Murata N. (ed.): Research in Photosynthesis, Proceedings of the IX International Congress on Photosynthesis. P-589. Kluwer, Dordrecht 1992b. Go to original source...
    45. Nonomura A.M., Benson A.A.: The path of carbon in photosyn-thesis. XXIX. Glass microbeads. - J. Plant Nutr. 35: 1896-1909, 2012. Go to original source...
    46. Nonomura A.M., Benson A.A.: The path of carbon in photosynthesis. XXX. α-Mannosides. - In: Dubinsky Z. (ed.): Photosynthesis. Pp. 3‑22. InTech, Rijeka 2013.
    47. Nonomura A.M., Benson A.A.: The path of carbon in photosynthesis. XXXI. The role of lectins. - J. Plant Nutr. 37: 785-794, 2014. Go to original source...
    48. Nonomura A.M., Benson A.A., Biel K.Y.: The path of carbon in photosynthesis. XXVII. Sugar-conjugated plant growth regulators enhance general productivity. - J. Plant Nutr. 34: 653-664, 2011. Go to original source...
    49. Nonomura A.M., Biel K.Y., Fomina I.R. et al.: Benson's protocol. -In: Fomina I.R., Biel K.Y., Soukhovolsk V.G. (ed.): Complex Biological Systems: Adaptation and Tolerance to Extreme Environments. 2nd Edition, extended. Pp. 463-508. John Wiley & Sons, Inc., Hoboken 2018a. doi: 10.1002/9781119510390.ch11. Go to original source...
    50. Nonomura A.M., Cullen B.A., Benson A.A.: The path of carbon in photosynthesis. XXVIII. Responses of plants to polyalkyl-glycopyranose and polyacylglycopyranose. - In: Najafpour M.M. (ed.): Advances in Photosynthesis: Fundamental Aspects. Pp. 259-271. InTech, Rijeka 2012.
    51. Nonomura A.M., Holtz B., Biel K.Y. et al.: The paths of Andrew A. Benson: a radio-autobiography. - Photosynth. Res. 134: 93-105, 2017. Go to original source...
    52. Nonomura A.M., Pedersen A., Brummel D.P. et al.: Brandt iH026a plant growth regulator. - Photosynthetica 56: 411-417, 2018b. Go to original source...
    53. Nonomura A.M., Shevela D., Komath S.S. et al.: A plant growth regulator for photosynthesis. Govindjee's Educational Poster Series, 2020. doi: 10.13140/RG.2.2.30634.44480. Go to original source...
    54. Pier J., Barlow D. (ed.): Western Fertilizer Handbook. 3rd Edition. Western Plant Health Association. Pp. 400. Waveland Press, Long Grove 2018. ISBN: 1-4786-3846-x.
    55. Roberts D.D., Goldstein I.J.: Adenine binding sites of the lectin from lima beans (Phaseolus lunatus). - J. Biol. Chem. 258: 13820-13824, 1983. Go to original source...
    56. Schröder W.P., Petit P.X.: Flow cytometry of spinach chloro-plasts. - Plant Physiol. 100: 1092-1102, 1992. Go to original source...
    57. Schwarz F.P., Puri K.D., Bhat R.G., Surolia A.: Thermodynamics of monosaccharide binding to concanavalin A, pea (Pisum sativum) lectin, and lentil (Lens culinaris) lectin. - J. Biol. Chem. 268: 7668-7677, 1993. Go to original source...
    58. Sekhar K.M., Kota V.R., Reddy T.P. et al.: Amelioration of plant responses to drought under elevated CO2 by rejuvenating photosynthesis and nitrogen use efficiency: implications for future climate-resilient crops. - Photosynth. Res., 2020. doi: 10.1007/s11120-020-00772-5. Go to original source...
    59. Sharkey T.D.: Discovery of the canonical Calvin-Benson cycle. -Photosynth. Res. 140: 235-252, 2019. Go to original source...
    60. Sharon N., Lis H.: Lectins. 2nd Edition. Pp. 454. Springer, Dordrecht 2007. Go to original source...
    61. Shevela D., Björn L.O., Govindjee G.: Photosynthesis: Solar Energy for Life. Pp. 204. World Scientific Publishing, Singapore 2018. doi: 10.1142/10522. Go to original source...
    62. Shevela D., Do H.-N., Fantuzzi A. et al.: Bicarbonate-mediated CO2 formation on both sides of Photosystem II. - Biochemistry 59: 2442-2449, 2020. Go to original source...
    63. Shevela D., Eaton-Rye J.J., Shen J.R., Govindjee: Photosystem II and unique role of bicarbonate: a historical perspective. - BBA-Bioenergetics 1817: 1134-1151, 2012. Go to original source...
    64. Smeets K., Van Damme E.J.M., Verhaert P. et al.: Isolation, characterization and molecular cloning of the mannose-binding lectins from leaves and roots of garlic (Allium sativum L.). - Plant Mol. Biol. 33: 223-234, 1997. Go to original source...
    65. ten Veldhuis M.C., Ananyev G., Dismukes G.C.: Symbiosis extended: exchange of photosynthetic O2 and fungal-respired CO2 mutually power metabolism of lichen symbionts. - Photosynth. Res. 143: 287-299, 2020. Go to original source...
    66. Thompson M., Gamage D., Hirotsu N. et al.: Effects of elevated carbon dioxide on photosynthesis and carbon partitioning: a perspective on root sugar sensing and hormonal crosstalk. - Front. Physiol. 8: 578, 2017. Go to original source...
    67. Van Damme E.J.M., Lannoo N., Peumans W.: Plant lectins. - Adv. Bot. Res. 48: 107-209, 2008. Go to original source...
    68. Van Damme E.J.M., Peumans W.J., Pusztai A., Bardocz S.: Handbook of Plant Lectins: Properties and Biomedical Applications. Pp. 466. John Wiley & Sons, New York 1998. ISBN: 978-0-471-96445-2.
    69. Van Holle S., Van Damme E.J.M.: Messages from the past: new insights in plant lectin evolution. - Front. Plant Sci. 10: 36, 2019. Go to original source...
    70. Zhang C., Hicks G.R., Raikhel N.V.: Molecular composition of plant vacuoles: important but less understood regulations and roles of tonoplast lipids. - Plants-Basel 4: 320-333, 2015. Go to original source...
    71. Zhang J., Wang N., Miao Y. et al.: Identification of SLAC1 anion channel residues required for CO2/bicarbonate sensing and regulation of stomatal movements. - P. Natl. Acad. Sci. USA 115: 11129-11137, 2018. Go to original source...

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