Ferulic acid in C4 grasses.

Volume 7, Issue 3, June 2022     |     PP. 82-97      |     PDF (325 K)    |     Pub. Date: August 14, 2022
DOI: 10.54647/biology18191    75 Downloads     5489 Views  

Author(s)

Marco Antônio Menezes Neto, Institute of Biological Sciences, Federal University of Pará, Belém, Pará, Brazil.
Miguel Pedro Guerra, Graduate Program in Plant Genetic Resources, Federal University of Santa Catarina, Florianópolis, SC, P.O. Box 476, 88040-900, Brazil; Graduate Program in Agricultural and Natural Ecosystems, Federal University of Santa Catarina, Curitibanos, Campus Ulysses Gaboardi Road, Km 3, 89520-000, Curitibanos, SC, Brazil

Abstract
In order to identify the phenolic substance that is responsive in a new C4-safranin histochemical test for determination of the photosynthetic pathway in grasses, we developed a fluorescence microscopy aided protocol for extraction and quantification of the target substance, with subsequent mass spectrometry analysis for molecular identification. The results indicate the target phenolic substance in C4 grasses' bundle sheath cells is ferulic acid. In addition, we observed differences in distribution and compartmentalization of ferulic acid depending on the plants’ photosynthetic pathway. In C3 grasses, ferulic acid is restricted to mesophyll cells and concentrated on cell walls, while in C4 grasses it is restricted to bundle sheath cells, and concentrated in the membrane adjacent to radial and tangential walls. Taken together these results indicate that ferulic acid may have an important function related to the C4 photosynthetic pathway in grasses. Such function may be unprecedented and different from any other previously ascribed to this substance.

Keywords
C4 grasses, fluorescence microscopy, ferulic acid.

Cite this paper
Marco Antônio Menezes Neto, Miguel Pedro Guerra, Ferulic acid in C4 grasses. , SCIREA Journal of Biology. Volume 7, Issue 3, June 2022 | PP. 82-97. 10.54647/biology18191

References

[ 1 ] Neto, M.A.M., Mardegan, S.F. and Barbosa, S.M. Determinação da via fotossintética em gramíneas. In: Filho A P da S S, (ed). Poaceae Barnhart. Marques Editora: Belém, Pará, 103-122, (2017).
[ 2 ] Lewis, N.G. and Yamamoto, E. Lignin: ocorrence, biogenesis and biodegradation. Annual Review Plant Physiology.141: 455-496 (1999).
[ 3 ] Neto, M.A.M. and Guerra, M.P. A new method for determination of the photosynthetic pathway in grasses. Photosynthesis Research 140: 1-6 (2019). https://doi.org/10.1007/s11120-019-00646-5
[ 4 ] Das, A.K. and Singh, V. Antioxidative free and bound phenolic constituents in pericarp, germ and endosperm of Indian dent (Zea mays var. indentara) and flint (Zea mays var. indurate) maize. Journal of Functional Foods. 13: 363-374. 2015.
[ 5 ] Das, A.K. and Singh, V. Antioxidative free and bound phenolic constituents in botanical fractions of Indian specialty maiz (Zea mays L.) genotypes. Food Chemistry. 201: 298-306. (2016).
[ 6 ] Guo, W. and Beta, T. Phenolic acid composition and antioxidant potential of insoluble and soluble dietary fibre extracts derived from select whole-grain cereals. Food Research International. 51: 518-525. (2013).
[ 7 ] Roberts, K. Handbook of plants science. Vol.1. Chichester: JohnWiley & Sons, Ltd. (2007).
[ 8 ] Van Hung, P. Phenolic compounds of cereals and their antioxidant capacity. Critical Reviews in Food Science and Nutrition. 56: 25-35. (2016).
[ 9 ] Buanafina, M.M. de O, Langdon, T., Hauck, B., et al. Manipulating the phenolic acid content and digestibility of Italian ryegrass (Lolium multiflorum) by vacuolar-targeted expression of a ferulic acid esterase. Applied Biochemistry and Biotechnology 130: 416-426 (2006).
[ 10 ] Mathew, S. and Abraham, T.E. ferulic acid: An antioxidant found naturally in plant cell walls and feruloyl esterases involved in its release and their applications. Critical Reviews in Biotechnology. 24: 59-83. (2004).
[ 11 ] Santiago, R. and Malvar, R.A. Role of ehydrodiferuletes im maize resistance to pests and diseases. International Journal of Molecular Sciences. 11: 691-703. (2010).
[ 12 ] Saulnier, L. Vigouroux, J. and Thilbault, J.F. Isolation and partial characterization of eruloylated oligosaccharides from maize bran. Crbohydrate Research. 272: 241-253. (1995).
[ 13 ] Zhao, Z. and Moghadasian, M.H. Chemistry, natural sources, dietary intake and pharmacokinetic properties of ferulic acid: A review. Food Chemistry. 109: 691-702. (2008).
[ 14 ] Faulds, C.B. and Williamson G. The role of hydroxycinnamates in the plant cell wall. J. Sci. Food and Agric. 79:393–395 (1999).
[ 15 ] Lambert, N., Kroon, P.A., Faulds, C.B., Plumb, G.W., McLauchlan, W.R., et al. Purification of cytosolic beta-glucosidase from pig liver and its reactivity towards flavonoid glycosides. Biochim. Biophys. Acta. 1435: 110–116 (1999).
[ 16 ] Harris, P.J. and Hartley, R.D. Detection of bound ferulic acid in cell walls of the Gramineae by ultraviolet fluorescence microscopy. Nature. 259: 508–510 (1976).
[ 17 ] Carpita, N.C. Structure and biogenesis of the cell walls of grasses. Ann Rev Plant Physiol Plant Mol Biol. 47: 445-476 (1996).
[ 18 ] Buanafina, M.M. de O, Langdon, T., Hauck, B, et al. Expression of a fungal ferulic acid esterase increases cell wall digestibility of tall fescue (Festuca arundinaceae). Plant Biotechnology Journal. 6: 264-280 (2008)
[ 19 ] Buanafina, M.M. de O Feruloylation in grasses: current and future perspectives. Molecular Plant. 5: 861-872 (2009).
[ 20 ] Ibrahim, R.K., and Barron, D. Phenylpropanoids. In: Dey PM, Harbornej B (eds) Methods in Plant biochemistry, Vol 1. Plant phenolics. Academic Press, New York, 197-235 (1989).
[ 21 ] Veit, M., Geiger, H., Wray, V., Abou-Mandour, A.A., Rozdzinski, W., Witte, L., Strack, D. and Czygan, F.C. Equisetum pyrone, a styrylpyrone glucoside in gametophytes from Equisetum arvense. Phytochemistry. 32: 1029-1032 (1993).
[ 22 ] Gorham, J. The biochemistry of the stilbenoids. Chapman & Hall, London (1995).
[ 23 ] Treutter, D. Chemical reaction detection of catechins and proanthocyanins with 4-dimethylamino-cinnamaldehyde. Journal of Chromatography. 467: 185-193 (1989).
[ 24 ] Ibrahim, R.K. Immunolocalization of flavonoid conjugates and their enzymes. In: Stafford HA, Ibrahim RK, eds. Phenolic metabolism in plants. Plenum Press, New York, 25-61 (1992).
[ 25 ] Grandmaison, J. and Ibrahim, R.K. Evidence for nuclear binding of flavonol sulphate esters in Flaveria chloraefolia. Journal of Plant Physiology. 147: 653-660 (1996).
[ 26 ] Vogt, T., Pollak, P., Tarlyn, N. and Taylor, L.P. Pollination or wound-induced kaempferol accumulation in petunia stigmas enhances seed production. Plant cell. 6: 11-23(1994).
[ 27 ] Schnitzler, J.P., Junggblut, T.P., Heller, W., Hutzler, P., Heinzmann, U., Schmelzer, E., Ernst, D., Langebartels, C. and Sandermann, H. Tissue localization of UV-B screening pigments and chalcone synthase mRNA in Scots pine (Pinus sylvestris L.) needles. New phythologist. 132: 247-258 (1996).
[ 28 ] Reinold, S. and Hahlbrock, K. In situ localization of phenylpropanoid biosynthetic mRNAs and proteins in parsley (Petroselinum crispum). Botanica Acta. 110: 431-443 (1997).
[ 29 ] Lichtenthaler, H.K. and Schweiger, J. Cell wall bound ferulic acid, the major substance of the blue-green fluorescence emission of plants. Journal of Plant Physiology. 152: 272-282 (1997).
[ 30 ] Harborne, J. Introduction to ecological biochemistry. Academic Press, London (1993).
[ 31 ] Hutzler, P., Fischbach, R., Heller, W., Jungblut, T.P., Reuber, S., Schmitz, R., Veit, M., Weissenbock, G. and Schnitzler, J.P. Tissue localization of phenolic compounds in plants by confocal laser scanning microscopy. Journal of Experimental Botany. 4: 953–965 (1998).
[ 32 ] Saulnier, L. and Thilbault, J.F. Ferulic acid and diferulic acids as components of sugar beet pectins and maize bran heteroxylans. Journal of the Science of Food and Agriculture. 79: 396-402. (1999).
[ 33 ] Zhang, Z., Smith, C., & Li, W. Extraction and modification technology of arabinoxylans from cereal by-products: A critical review. Food Research International. 65: 423-436 (2014).
[ 34 ] Pedersen, M.B., Bunzel, M., Schafer, J., Knudsen, K.E.B., Sørensen, J.F., Yu, S. & Lærke, H.N. Frulic acid dehydrodimer and dehydrotrimer profiles of distiller’s dried grains with solubles from different cereal species. Journal of Agricultural and Food Chemistry. 63: 2006-2012. (2015).
[ 35 ] Hartley, R.D. and Ford, C.W. Phenolic constituents of plant-cell walls and wall biodegradability. Acs Symposium Series 399: 137-145 (1989).
[ 36 ] Ralph, J. and Helm. R.F. Lignin/hydroxynnamic acid/polysaccharide complexes: synthetic models for region chemical characterization. In Forage Cell Wall: Structure and Digestibility, Jung JHG Buxton DR and Hartley RD, (eds) (Madison: ASA-CSSA-SSSA), pp 201-246 (1993).
[ 37 ] Wende, G. and Fry, S.C. 2-O-beta-D-xylopiranosyl-(5-O-feruloyl)-L-arabinose, a widespread component of grass cell walls. Phytochemistry. 44: 1019-1030 (1997).
[ 38 ] Ou, S.Y. and Kwok, K.C. Ferulic acid: pharmaceutical functions, preparation and applications in foods. Journal of the Science of Food and Agriculture. 84: 1261-1269 (2004).
[ 39 ] Knogge, W. and Weissenböck, G. Tissue-distribution of secondary phenolic biosynthesis in developing leaves of Avena sativa L. Planta 2: 196-205 (1986).
[ 40 ] Schmelzer, E., Jahnen, W. and Hahlbrock, K. In situ localization of light-induced chalcone synthase mRNA, chalcone synthase and flavonoid end products in epidermal cells of parsley leaves. Proceedings of the National Academy of Sciences, USA 85: 2989-2993 (1988).
[ 41 ] Haussühl, K., Rohde, W. and Weissenböck, G. Expression of chalcone synthase genes in coleoptiles and primary leaves of Secale cereal L. after induction by UV radiation: evidence for a UV-protective role for the coleoptile. Botanica Acta. 109: 229-238 (1996).
[ 42 ] Moskowitz, A.H. and Hradzima, G. Vacuolar contents of fruit sub epidermal cells from Vitis sp. Plant Physiology. 68: 686-692 (1981).
[ 43 ] Weissenböck, G., Hedrich, R. and Sachs, H. Secondary phenolic products in isolated guard cell, epidermal cell and mesophyll cell protoplasts- distribution and determination. Protoplasma. 134: 141-148 (1986).
[ 44 ] Schnabl, H., Weissenböck, G. and Scharf, H. In vivo micro spectrophotometric characterization of flavonol glycosides in Vicia faba guard and epidermal cells. Journal of Experimental Botany. 37: 61-72 (1986).
[ 45 ] Schnabl, H., Weissenböck, G. and Scharf, H. Cellular distribution of UV-absorbing compounds in guard and subsidiary cells of Zea mays L. Journal of Plant Physiology. 135: 249-252 (1989).
[ 46 ] Ozimina, I.I. Flavonoids of Spartium junceum. 1. Flavones and flavonoids. Chemistry of Natural Compounds. 16 (3): 763-764 (1979).
[ 47 ] Geldner, N. The endodermes. Annual Review Plant Biology. 64: 531-558 (2013).
[ 48 ] Nelson, T. and Dengler, N. Leaf vascular pattern formation. The Plant Cell. 9: 1121-1135 (1997).
[ 49 ] Slewinski, T.L. Non-structural carbohydrate partitioning in grass stems: a target to increase yield stability, stress tolerance, and biofuel production. Journal of Experimental Botany. 63: 4647-4670 (2012).
[ 50 ] Naseer, S., Lee, Y., Lapierre, C, Franke, R., Nawrath, C. and Geldner, N. Casparian strip diffusion barrier in Arabidopsis is made of a lignin polymer without suberin. Proceedings of the National Academy of Sciences of the United States of America. 25:10101-10106 (2012).
[ 51 ] Slewinski, T.L. Using evolution as a guide to engineer Kranz-type C4 photosynthesis. Frontiers in Plant Science. 4:1-13 (2013).
[ 52 ] Smith, M.M. and Hartley, R.D. Occurrence and nature of ferulic acid substituition of cell-wall polysaccharides in graminaceous plants. Carbohydrate Research. 118: 65-80. (1983).
[ 53 ] Sun, R., Sun, X., Wang, S. Zhu, W. Wang, X. Ester and ether linkages between hydroxycinnamic acids and lignins from wheat, rice, rye, and barley straws, maize stems, and fast-growing poplar wood. Industrial Crops and Products. 15: 179-188. (2002).
[ 54 ] Levigne, S.V., Ralet, M.C.J., Quéméner, B.C., Pollet, B.N.L., Lapierre, C. and Thibault, J.F.J. Isolation from sugar beet cell walls of arabinan oligosaccharides esterified by two ferulic acid monomers. Plant Physiology. 134: 1173-1180. (2004).
[ 55 ] Schatz, P.F., Ralph, J., Lu, F., Guzel, I.A. and Bunzel, M. Synthesis and identification of 2, 5-bis (4-hidroxy-3-methoxyphenyl)-tetrahydrofuran-3, 4-dicarboxylic acid, an unanticipated ferulate 8-8-coupling product acylating cereal plant cell walls. Organic & Biomeolecular Chemistry. 4: 2801-2806. (2006).
[ 56 ] Lopez-Martinez, L.X. Oliart-Ros, R.M., Valerio-Alfaro, G. Lee, C.H., Parkin, K.L. and Garcia, H.S. Antioxidant activity, phenolic compounds and anthocyanins content of eighteen strains of Mexicam maize. LWT-Food Science and Technology. 42: 1187-1192. (2009).
[ 57 ] Dobberstein, D. and Bunzel, M. Separation and detection of cell wall-bound ferulic acid dehydrodimers and dehydrotrimers in cereals and outher plant materials by reversed phase high-performance liquid chromatography with ultraviolet detection. Journal of Agricultural and Food Chemistry 58: 8927-8935 (2010).
[ 58 ] Sun, X.F., Fowler, P., Rajaratam, M. and Zhang, G. Extraction and characterization of hemicelluloses from maize stem. Phytochemical Analysis. 21: 406-415. (2010).
[ 59 ] Uddin, M.N. Hanstein, S., Faust, F., Eitenmüller, P.T., Pitann, B. and Schubert, S. Diferulic acids in the cell wall may contribute to the suppression of shoot growth in the first phase of salt stress in maize. Phytochemistry. 102: 126-136. (2014).
[ 60 ] Dynkowska, W.M. Cyran, M.R. and Ceglinska, A. Soluble and cell wall-bound phenolic acids and ferulic acid Dehydrodimers in rye flour and five bread model systems: Insight into mechanisms of improved availability. Journal of the Science of Food and Agriculture. 965: 1103-1115. (2015).
[ 61 ] Malunga, L.N. and Beta, T. Isolation and identification of feruloylated arabinoxylan mono and oligosaccharides from undigested and digested maize and wheat. Heliyon. E00106. (2016).