The novel features of Plantago ovata seed mucilage accumulation, storage and release
Jana L Phan, James M Cowley, Kylie A Neumann, Lina Herliana, Lisa A O'Donovan, Rachel A Burton, Jana L Phan, James M Cowley, Kylie A Neumann, Lina Herliana, Lisa A O'Donovan, Rachel A Burton
Abstract
Seed mucilage polysaccharide production, storage and release in Plantago ovata is strikingly different to that of the model plant Arabidopsis. We have used microscopy techniques to track the development of mucilage secretory cells and demonstrate that mature P. ovata seeds do not have an outer intact cell layer within which the polysaccharides surround internal columellae. Instead, dehydrated mucilage is spread in a thin homogenous layer over the entire seed surface and upon wetting expands directly outwards, away from the seed. Observing mucilage expansion in real time combined with compositional analysis allowed mucilage layer definition and the roles they play in mucilage release and architecture upon hydration to be explored. The first emergent layer of hydrated mucilage is rich in pectin, extremely hydrophilic, and forms an expansion front that functions to 'jumpstart' hydration and swelling of the second layer. This next layer, comprising the bulk of the expanded seed mucilage, is predominantly composed of heteroxylan and appears to provide much of the structural integrity. Our results indicate that the synthesis, deposition, desiccation, and final storage position of mucilage polysaccharides must be carefully orchestrated, although many of these processes are not yet fully defined and vary widely between myxospermous plant species.
Figures
References
- Phan JL, Burton RA. New insights into the composition and structure of seed mucilage. Annu. Plant Rev. Online. 2018;1:1–41.
- Macquet A, Ralet M-C, Kronenberger J, Marion-Poll A, North HM. Insitu, chemical and macromolecular study of the composition of Arabidopsisthaliana seed coat mucilage. Plant Cell Physiol. 2007;48:984–999.
- Harpaz-Saad S, et al. Cellulose synthesis via the FEI2 RLK/SOS5 pathway and CELLULOSE SYNTHASE 5 is required for the structure of seed coat mucilage in Arabidopsis. Plant J. 2011;68:941–953.
- Yang B, et al. TRM 4 is essential for cellulose deposition in Arabidopsis seed mucilage by maintaining cortical microtubule organization and interacting with CESA 3. New Phytol. 2019;221:881–895.
- Yu L, et al. CELLULOSE SYNTHASE-LIKE A2, a glucomannan synthase, is involved in maintaining adherent mucilage structure in Arabidopsis seed. Plant Physiol. 2014;164:1842–1856.
- Voiniciuc C, Günl M, Schmidt MH-W, Usadel B. MUCI10 produces galactoglucomannan that maintains pectin and cellulose architecture in Arabidopsis seed mucilage. Plant Physiol. 2015;169:403–420.
- Hu R, et al. Xylan synthesized by Irregular Xylem 14 (IRX14) maintains the structure of seed coat mucilage in Arabidopsis. J. Exp. Bot. 2016;67:1243–1257.
- Hu R, et al. Irregular xylem 7 (IRX7) is required for anchoring seed coat mucilage in Arabidopsis. Plant Mol. Biol. 2016;92:25–38.
- Yu L, et al. Multi-layer mucilage of Plantagoovata seeds: Rheological differences arise from variations in arabinoxylan side chains. Carbohydr. Polym. 2017;165:132–141.
- Cowley JM, et al. A small-scale fractionation pipeline for rapid analysis of seed mucilage characteristics. Plant Methods. 2020;16:1–12.
- Phan JL, et al. Differences in glycosyltransferase family 61 accompany variation in seed coat mucilage composition in Plantago spp. J. Exp. Bot. 2016;67:6481–6495.
- Fischer MH, et al. The gel-forming polysaccharide of psyllium husk (Plantagoovata Forsk) Carbohydr. Res. 2004;339:2009–2017.
- Ren Y, Yakubov GE, Linter BR, Macnaughtan W, Foster TJ. Temperature fractionation, physicochemical and rheological analysis of psyllium seed husk heteroxylan. Food Hydrocoll. 2020 doi: 10.1016/j.foodhyd.2020.105737.
- Jensen JK, Johnson NR, Wilkerson CG. Arabidopsisthaliana IRX10 and two related proteins from psyllium and Physcomitrellapatens are xylan xylosyltransferases. Plant J. 2014;80:207–215.
- Urbanowicz BR, Peña MJ, Moniz HA, Moremen KW, York WS. Two Arabidopsis proteins synthesize acetylated xylan in vitro. Plant J. 2014;80:197–206.
- Chiniquy D, et al. XAX1 from glycosyltransferase family 61 mediates xylosyltransfer to rice xylan. Proc. Natl. Acad. Sci. USA. 2012;109:17117–17122.
- Anders N, et al. Glycosyl transferases in family 61 mediate arabinofuranosyl transfer onto xylan in grasses. Proc. Natl. Acad. Sci. USA. 2012;109:989–993.
- Voiniciuc C, Gunl M, Schmidt MH-W, Usadel B. Highly branched Xylan made by IRREGULAR XYLEM14 and MUCILAGE-RELATED21 Links mucilage to. Plant Physiol. 2015;169:2481–2495.
- Ralet M-C, et al. Xylans provide the structural driving force for mucilage adhesion to the Arabidopsis seed coat. Plant Physiol. 2016;171:165–178.
- Jensen JK, Johnson N, Wilkerson CG. Discovery of diversity in xylan biosynthetic genes by transcriptional profiling of a heteroxylan containing mucilaginous tissue. Front. Plant Sci. 2013;4:20.
- Marlett JA, Kajs TM, Fischer MH. An unfermented gel component of psyllium seed husk promotes laxation as a lubricant in humans. Am. J. Clin. Nutr. 2000;72:784–789.
- McRorie JW, et al. Psyllium is superior to docusate sodium for treatment of chronic constipation. Aliment. Pharmacol. Ther. 1998;12:491–497.
- Anderson JW, et al. Cholesterol-lowering effects of psyllium intake adjunctive to diet therapy in men and women with hypercholesterolemia: Meta-analysis of 8 controlled trials. Am. J. Clin. Nutr. 2000;71:472–479.
- Cappa C, Lucisano M, Mariotti M. Influence of Psyllium, sugar beet fibre and water on gluten-free dough properties and bread quality. Carbohydr. Polym. 2013;98:1657–1666.
- Mancebo CM, San Miguel MÁ, Martínez MM, Gómez M. Optimisation of rheological properties of gluten-free doughs with HPMC, psyllium and different levels of water. J. Cereal Sci. 2015;61:8–15.
- Fratelli C, Muniz DG, Santos FG, Capriles VD. Modelling the effects of psyllium and water in gluten-free bread: An approach to improve the bread quality and glycemic response. J. Funct. Foods. 2018;42:339–345.
- Haque A, Morris ER. Combined use of ispaghula and HPMC to replace or augment gluten in breadmaking. Food Res. Int. 1994;27:379–393.
- Bahrani, A. S. Processes for dehusking psyllium seeds. USPat.Number5020732 (1991).
- Kumar, J. Goodagriculturalpracticesforisabgol. (2015).
- Francoz E, Ranocha P, Burlat V, Dunand C. Arabidopsis seed mucilage secretory cells: Regulation and dynamics. Trends Plant Sci. 2015;20:515–524.
- Schneitz K, Huiskamp M, Pruitt RE. Wild-type ovule development in Arabidopsisthaliana: A light microscope study of cleared whole-mount tissue. Plant J. 1995;7:731–749.
- Windsor JB, Symonds VV, Mendenhall J, Lloyd AM. Arabidopsis seed coat development: Morphological differentiation of the outer integument. Plant J. 2000;22:483–493.
- Beeckman T, Rycke RD, Viane R, Inzé D. Histological study of seed coat development in Arabidopsisthaliana. J. Plant Res. 2000;113:139–148.
- Western TL, Skinner DJ, Haughn GW. Differentiation of mucilage secretory cells of the Arabidopsis seed coat. Plant Physiol. 2000;122:345–356.
- Voiniciuc C, Yang B, Schmidt MH-W, Gunl M, Usadel B. Starting to gel: How Arabidopsis seed coat epidermal cells produce specialized secondary cell walls. Int. J. Mol. Sci. 2015;16:3452–3473.
- Miart F, et al. Cytological approaches combined with chemical analysis reveals the layered nature of flax mucilage. Front. Plant Sci. 2019;10:1–16.
- Witzum A. Mucilaginous plate pells in the nutlet epidermis of Coleusblumei Benth. (Labiatae) Bot. Gaz. 1978;139:430–435.
- Muñoz LA, Cobos A, Diaz O, Aguilera JM. Chia seeds: Microstructure, mucilage extraction and hydration. J. Food Eng. 2012;108:216–224.
- Hyde BB. Mucilage-producing cells in the seed coat of Plantagoovata: Developmental fine structure. Am. J. Bot. 1970;57:1197–1206.
- Ruprecht C, et al. A synthetic glycan microarray enables epitope mapping of plant cell wall glycan-directed antibodies. Plant Physiol. 2017;175:00737.
- Verhertbruggen Y, Marcus SE, Haeger A, Ordaz-Ortiz JJ, Knox JP. An extended set of monoclonal antibodies to pectic homogalacturonan. Carbohydr. Res. 2009;344:1858–1862.
- Ruel K, Nishiyama Y, Joseleau JP. Crystalline and amorphous cellulose in the secondary walls of Arabidopsis. Plant Sci. 2012;193–194:48–61.
- Tucker MR, et al. Dissecting the genetic basis for seed coat mucilage heteroxylan biosynthesis in plantago ovata using gamma irradiation and infrared spectroscopy. Front. Plant Sci. 2017;8:326.
- Voiniciuc C, et al. Flying saucer1 is a transmembrane RING E3 ubiquitin ligase that regulates the degree of pectin methylesterification in Arabidopsis seed mucilage. Plant Cell. 2013;25:944–959.
- Boesewinkel FD. Development of ovule and testa of Linumusitatssimum L. Acta Bot. Neerl. 1980;29:17–32.
- Madgulkar A, Rao M, Warrier D. Characterization of Pysillium (Plantagoovata) polysaccharide and its uses. Polysaccharides. 2014 doi: 10.1007/978-3-319-03751-6_49-1.
- Garcia D, FitzGerald JN, Berger F. Maternal control of integument cell elongation and zygotic control of endosperm growth are coordinated to determine seed size in Arabidopsis. Plant Cell. 2005;17:52–60.
- Cooper GO. Development of the ovule and the formation of the seed in Plantagolanceolata. Am. J. Bot. 1942;29:577–581.
- Mikesell J. Anatomy of terminal haustoria in the ovule of Plantain (Plantagomajor L.) with taxonomic comparison to other angiosperm taxa. Bot. Gaz. 1990;151:452–464.
- Johri B, Ambegaokar K, Srivastava P. Plantaginales. Comparative Embryology of Angiosperms. Berlin: Springer; 1992. pp. 777–779.
- Saez-Aguayo S, et al. PECTIN METHYLESTERASE INHIBITOR6 promotes Arabidopsis mucilage release by limiting methylesterification of homogalacturonan in seed coat epidermal cells. Plant Cell. 2013;25:308–323.
- Macquet A, et al. A naturally occurring mutation in an Arabidopsis accession affects a β-d-galactosidase that increases the hydrophilic potential of rhamnogalacturonan I in seed mucilage. Plant Cell. 2007;19:3990–4006.
- Walker M, et al. The transcriptional regulator LEUNIG_HOMOLOG regulates mucilage release from the Arabidopsis testa. Plant Physiol. 2011;156:46–60.
- Atmodjo MA, Hao Z, Mohnen D. Evolving views of pectin biosynthesis. Annu. Rev. Plant Biol. 2013;64:747–779.
- Guo Q, Cui SW, Wang Q, Christopher Young J. Fractionation and physicochemical characterization of psyllium gum. Carbohydr. Polym. 2008;73:35–43.
- Sullivan S, et al. CESA5 is required for the synthesis of cellulose with a role in structuring the adherent mucilage of Arabidopsis seeds. Plant Physiol. 2011;156:1725–1739.
- Burton RA, et al. Over-expression of specific HvCslF cellulose synthase-like genes in transgenic barley increases the levels of cell wall (1,3;1,4)-β-d-glucans and alters their fine structure. Plant Biotechnol. J. 2011;9:117–135.
- Guillon F, et al. Brachypodium distachyon grain: Characterization of endosperm cell walls. J. Exp. Bot. 2011;62:1001–1015.
- Hassan AS, et al. A Genome Wide Association Study of arabinoxylan content in 2-row spring barley grain. PLoS One. 2017;12:1–19.
Source: PubMed