The Source of Inorganic Nitrogen Has Distinct Effects on Cell Wall Composition in Brachypodium Distachyon

Overview

Journal J Exp Bot

Publisher Oxford University Press

Specialty Biology

Date 2019 Sep 11

PMID 31504748

Citations 7

Authors

Sylwia Glazowska

Laetitia Baldwin

Jozef Mravec

Christian Bukh

Jonathan U Fangel

William Gt Willats

Jan K Schjoerring

Affiliations

Soon will be listed here.

Abstract

Plants have evolved different strategies to utilize various forms of nitrogen (N) from the environment. While regulation of plant growth and development in response to application of inorganic N forms has been characterized, our knowledge about the effect on cell wall structure and composition is quite limited. In this study, we analysed cell walls of Brachypodium distachyon supplied with three types of inorganic N (NH4NO3, NO3-, or NH4+). Cell wall profiles showed distinct alterations in both the quantity and structures of individual polymers. Nitrate stimulated cellulose, but inhibited lignin deposition at the heading growth stage. On the other hand, ammonium supply resulted in higher concentration of mixed linkage glucans. In addition, the chemical structure of pectins and hemicelluloses was strongly influenced by the form of N. Supply of only NO3- led to alteration in xylan substitution and to lower esterification of homogalacturonan. We conclude that the physiological response to absorption of different inorganic N forms includes pleotropic remodelling of type II cell walls.

Citing Articles

Inositol pyrophosphate catabolism by three families of phosphatases regulates plant growth and development.

Laurent F, Bartsch S, Shukla A, Rico-Resendiz F, Couto D, Fuchs C PLoS Genet. 2024; 20(11):e1011468.

PMID: 39531477 PMC: 11611267. DOI: 10.1371/journal.pgen.1011468.

Natural variation in the adjustment of primary metabolism determines ammonium tolerance in the model grass Brachypodium distachyon.

De la Pena M, Poucet T, Montardit-Tarda F, Urmeneta L, Urbano-Gamez J, Cassan C J Exp Bot. 2024; 75(22):7237-7253.

PMID: 39292826 PMC: 11629996. DOI: 10.1093/jxb/erae382.

Variation of mesophyll conductance mediated by nitrogen form is related to changes in cell wall property and chloroplast number.

Cao Y, Pan Y, Yang Y, Liu T, Wang M, Li Y Hortic Res. 2024; 11(6):uhae112.

PMID: 38919556 PMC: 11197310. DOI: 10.1093/hr/uhae112.

Ammonium treatment inhibits cell cycle activity and induces nuclei endopolyploidization in Arabidopsis thaliana.

Burian M, Podgorska A, Kryzheuskaya K, Gieczewska K, Sliwinska E, Szal B Planta. 2024; 259(5):94.

PMID: 38509428 DOI: 10.1007/s00425-024-04372-8.

Reproducible growth of in EcoFAB 2.0 reveals that nitrogen form and starvation modulate root exudation.

Novak V, Andeer P, Bowen B, Ding Y, Zhalnina K, Hofmockel K Sci Adv. 2024; 10(1):eadg7888.

PMID: 38170767 PMC: 10776018. DOI: 10.1126/sciadv.adg7888.

References

Carlisle E, Myers S, Raboy V, Bloom A . The Effects of Inorganic Nitrogen form and CO(2) Concentration on Wheat Yield and Nutrient Accumulation and Distribution. Front Plant Sci. 2012; 3:195. PMC: 3432492. DOI: 10.3389/fpls.2012.00195. View

Scheller H, Ulvskov P . Hemicelluloses. Annu Rev Plant Biol. 2010; 61:263-89. DOI: 10.1146/annurev-arplant-042809-112315. View

Moller I, Sorensen I, Bernal A, Blaukopf C, Lee K, Obro J . High-throughput mapping of cell-wall polymers within and between plants using novel microarrays. Plant J. 2007; 50(6):1118-28. DOI: 10.1111/j.1365-313X.2007.03114.x. View

Scholthof K, Irigoyen S, Catalan P, Mandadi K . : A Monocot Grass Model Genus for Plant Biology. Plant Cell. 2018; 30(8):1673-1694. PMC: 6139682. DOI: 10.1105/tpc.18.00083. View

Draper J, Mur L, Jenkins G, Bablak P, Hasterok R, Routledge A . Brachypodium distachyon. A new model system for functional genomics in grasses. Plant Physiol. 2001; 127(4):1539-55. PMC: 133562. View

Willats W, Orfila C, Limberg G, Buchholt H, Van Alebeek G, Voragen A . Modulation of the degree and pattern of methyl-esterification of pectic homogalacturonan in plant cell walls. Implications for pectin methyl esterase action, matrix properties, and cell adhesion. J Biol Chem. 2001; 276(22):19404-13. DOI: 10.1074/jbc.M011242200. View

Wu Z, Zhang M, Wang L, Tu Y, Zhang J, Xie G . Biomass digestibility is predominantly affected by three factors of wall polymer features distinctive in wheat accessions and rice mutants. Biotechnol Biofuels. 2013; 6(1):183. PMC: 3878626. DOI: 10.1186/1754-6834-6-183. View

Bevan M, Garvin D, Vogel J . Brachypodium distachyon genomics for sustainable food and fuel production. Curr Opin Biotechnol. 2010; 21(2):211-7. DOI: 10.1016/j.copbio.2010.03.006. View

Smith-Moritz A, Hao Z, Fernandez-Nino S, Fangel J, Verhertbruggen Y, Holman H . Structural characterization of a mixed-linkage glucan deficient mutant reveals alteration in cellulose microfibril orientation in rice coleoptile mesophyll cell walls. Front Plant Sci. 2015; 6:628. PMC: 4539472. DOI: 10.3389/fpls.2015.00628. View

10.

Nasholm T, Kielland K, Ganeteg U . Uptake of organic nitrogen by plants. New Phytol. 2009; 182(1):31-48. DOI: 10.1111/j.1469-8137.2008.02751.x. View

11.

Camargo E, Nascimento L, Soler M, Salazar M, Lepikson-Neto J, Marques W . Contrasting nitrogen fertilization treatments impact xylem gene expression and secondary cell wall lignification in Eucalyptus. BMC Plant Biol. 2014; 14:256. PMC: 4189757. DOI: 10.1186/s12870-014-0256-9. View

12.

Bloom A . The increasing importance of distinguishing among plant nitrogen sources. Curr Opin Plant Biol. 2015; 25:10-6. DOI: 10.1016/j.pbi.2015.03.002. View

13.

Caffall K, Mohnen D . The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydr Res. 2009; 344(14):1879-900. DOI: 10.1016/j.carres.2009.05.021. View

14.

Fernandes J, Goulao L, Amancio S . Regulation of cell wall remodeling in grapevine (Vitis vinifera L.) callus under individual mineral stress deficiency. J Plant Physiol. 2016; 190:95-105. DOI: 10.1016/j.jplph.2015.10.007. View

15.

Oliveira D, Finger-Teixeira A, Mota T, Salvador V, Moreira-Vilar F, Molinari H . Ferulic acid: a key component in grass lignocellulose recalcitrance to hydrolysis. Plant Biotechnol J. 2014; 13(9):1224-32. DOI: 10.1111/pbi.12292. View

16.

Britto D, Kronzucker H . Ecological significance and complexity of N-source preference in plants. Ann Bot. 2013; 112(6):957-63. PMC: 3783226. DOI: 10.1093/aob/mct157. View

17.

Willats W, McCartney L, Mackie W, Knox J . Pectin: cell biology and prospects for functional analysis. Plant Mol Biol. 2001; 47(1-2):9-27. View

18.

Rydahl M, Hansen A, Kracun S, Mravec J . Report on the Current Inventory of the Toolbox for Plant Cell Wall Analysis: Proteinaceous and Small Molecular Probes. Front Plant Sci. 2018; 9:581. PMC: 5943554. DOI: 10.3389/fpls.2018.00581. View

19.

Cosgrove D . Growth of the plant cell wall. Nat Rev Mol Cell Biol. 2005; 6(11):850-61. DOI: 10.1038/nrm1746. View

20.

Smith P, Wang H, York W, Pena M, Urbanowicz B . Designer biomass for next-generation biorefineries: leveraging recent insights into xylan structure and biosynthesis. Biotechnol Biofuels. 2017; 10:286. PMC: 5708106. DOI: 10.1186/s13068-017-0973-z. View