Cell wall remodeling under salt stress: Insights into changes in polysaccharides, feruloylation, lignification, and phenolic metabolism in maize

Although cell wall polymers play important roles in the tolerance of plants to abiotic stress, the effects of salinity on cell wall composition and metabolism in grasses remain largely unexplored. Here, we conducted an in‐depth study of changes in cell wall composition and phenolic metabolism induce...

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Veröffentlicht in:Plant, cell and environment cell and environment, 2020-09, Vol.43 (9), p.2172-2191
Hauptverfasser: Oliveira, Dyoni M., Mota, Thatiane R., Salatta, Fábio V., Sinzker, Renata C., Končitíková, Radka, Kopečný, David, Simister, Rachael, Silva, Mariana, Goeminne, Geert, Morreel, Kris, Rencoret, Jorge, Gutiérrez, Ana, Tryfona, Theodora, Marchiosi, Rogério, Dupree, Paul, del Río, José C., Boerjan, Wout, McQueen‐Mason, Simon J., Gomez, Leonardo D., Ferrarese‐Filho, Osvaldo, dos Santos, Wanderley D.
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container_issue 9
container_start_page 2172
container_title Plant, cell and environment
container_volume 43
creator Oliveira, Dyoni M.
Mota, Thatiane R.
Salatta, Fábio V.
Sinzker, Renata C.
Končitíková, Radka
Kopečný, David
Simister, Rachael
Silva, Mariana
Goeminne, Geert
Morreel, Kris
Rencoret, Jorge
Gutiérrez, Ana
Tryfona, Theodora
Marchiosi, Rogério
Dupree, Paul
del Río, José C.
Boerjan, Wout
McQueen‐Mason, Simon J.
Gomez, Leonardo D.
Ferrarese‐Filho, Osvaldo
dos Santos, Wanderley D.
description Although cell wall polymers play important roles in the tolerance of plants to abiotic stress, the effects of salinity on cell wall composition and metabolism in grasses remain largely unexplored. Here, we conducted an in‐depth study of changes in cell wall composition and phenolic metabolism induced upon salinity in maize seedlings and plants. Cell wall characterization revealed that salt stress modulated the deposition of cellulose, matrix polysaccharides and lignin in seedling roots, plant roots and stems. The extraction and analysis of arabinoxylans by size‐exclusion chromatography, 2D‐NMR spectroscopy and carbohydrate gel electrophoresis showed a reduction of arabinoxylan content in salt‐stressed roots. Saponification and mild acid hydrolysis revealed that salinity also reduced the feruloylation of arabinoxylans in roots of seedlings and plants. Determination of lignin content and composition by nitrobenzene oxidation and 2D‐NMR confirmed the increased incorporation of syringyl units in lignin of maize roots. Salt stress also induced the expression of genes and the activity of enzymes enrolled in phenylpropanoid biosynthesis. The UHPLC–MS‐based metabolite profiling confirmed the modulation of phenolic profiling by salinity and the accumulation of ferulate and its derivatives 3‐ and 4‐O‐feruloyl quinate. In conclusion, we present a model for explaining cell wall remodeling in response to salinity. We demonstrate the modulations induced by salt stress in the amounts of crystalline cellulose, matrix polysaccharides and lignin in roots of maize seedlings and roots, stems and leaves of maize plants. Salt stress reduced the feruloylation of arabinoxylan, increased the incorporation of syringyl lignin, and induced the biosynthesis and accumulation of ferulic acid and its derivatives. Based on these findings, we propose a model of grass cell wall remodeling in response to salinity.
doi_str_mv 10.1111/pce.13805
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Here, we conducted an in‐depth study of changes in cell wall composition and phenolic metabolism induced upon salinity in maize seedlings and plants. Cell wall characterization revealed that salt stress modulated the deposition of cellulose, matrix polysaccharides and lignin in seedling roots, plant roots and stems. The extraction and analysis of arabinoxylans by size‐exclusion chromatography, 2D‐NMR spectroscopy and carbohydrate gel electrophoresis showed a reduction of arabinoxylan content in salt‐stressed roots. Saponification and mild acid hydrolysis revealed that salinity also reduced the feruloylation of arabinoxylans in roots of seedlings and plants. Determination of lignin content and composition by nitrobenzene oxidation and 2D‐NMR confirmed the increased incorporation of syringyl units in lignin of maize roots. Salt stress also induced the expression of genes and the activity of enzymes enrolled in phenylpropanoid biosynthesis. The UHPLC–MS‐based metabolite profiling confirmed the modulation of phenolic profiling by salinity and the accumulation of ferulate and its derivatives 3‐ and 4‐O‐feruloyl quinate. In conclusion, we present a model for explaining cell wall remodeling in response to salinity. We demonstrate the modulations induced by salt stress in the amounts of crystalline cellulose, matrix polysaccharides and lignin in roots of maize seedlings and roots, stems and leaves of maize plants. Salt stress reduced the feruloylation of arabinoxylan, increased the incorporation of syringyl lignin, and induced the biosynthesis and accumulation of ferulic acid and its derivatives. 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Here, we conducted an in‐depth study of changes in cell wall composition and phenolic metabolism induced upon salinity in maize seedlings and plants. Cell wall characterization revealed that salt stress modulated the deposition of cellulose, matrix polysaccharides and lignin in seedling roots, plant roots and stems. The extraction and analysis of arabinoxylans by size‐exclusion chromatography, 2D‐NMR spectroscopy and carbohydrate gel electrophoresis showed a reduction of arabinoxylan content in salt‐stressed roots. Saponification and mild acid hydrolysis revealed that salinity also reduced the feruloylation of arabinoxylans in roots of seedlings and plants. Determination of lignin content and composition by nitrobenzene oxidation and 2D‐NMR confirmed the increased incorporation of syringyl units in lignin of maize roots. Salt stress also induced the expression of genes and the activity of enzymes enrolled in phenylpropanoid biosynthesis. The UHPLC–MS‐based metabolite profiling confirmed the modulation of phenolic profiling by salinity and the accumulation of ferulate and its derivatives 3‐ and 4‐O‐feruloyl quinate. In conclusion, we present a model for explaining cell wall remodeling in response to salinity. We demonstrate the modulations induced by salt stress in the amounts of crystalline cellulose, matrix polysaccharides and lignin in roots of maize seedlings and roots, stems and leaves of maize plants. Salt stress reduced the feruloylation of arabinoxylan, increased the incorporation of syringyl lignin, and induced the biosynthesis and accumulation of ferulic acid and its derivatives. 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Mota, Thatiane R. ; Salatta, Fábio V. ; Sinzker, Renata C. ; Končitíková, Radka ; Kopečný, David ; Simister, Rachael ; Silva, Mariana ; Goeminne, Geert ; Morreel, Kris ; Rencoret, Jorge ; Gutiérrez, Ana ; Tryfona, Theodora ; Marchiosi, Rogério ; Dupree, Paul ; del Río, José C. ; Boerjan, Wout ; McQueen‐Mason, Simon J. ; Gomez, Leonardo D. ; Ferrarese‐Filho, Osvaldo ; dos Santos, Wanderley D.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3885-c3fa99a4b1a2fade5c2e50be12141d4bc92770f9e70843749ba4dc46fd6b7d8b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Abiotic stress</topic><topic>Arabinoxylans</topic><topic>Biosynthesis</topic><topic>Carbohydrates</topic><topic>cell wall</topic><topic>Cell walls</topic><topic>Cellulose</topic><topic>Composition</topic><topic>Corn</topic><topic>Electrophoresis</topic><topic>ferulic acid</topic><topic>Gel electrophoresis</topic><topic>Gene expression</topic><topic>lignification</topic><topic>Lignin</topic><topic>Magnetic resonance spectroscopy</topic><topic>Metabolism</topic><topic>Metabolites</topic><topic>Nitrobenzene</topic><topic>NMR</topic><topic>NMR spectroscopy</topic><topic>Nuclear magnetic resonance</topic><topic>Oxidation</topic><topic>Phenolic compounds</topic><topic>Phenols</topic><topic>Plant extracts</topic><topic>Plant roots</topic><topic>Polymers</topic><topic>Polysaccharides</topic><topic>p‐coumaric acid</topic><topic>Roots</topic><topic>Saccharides</topic><topic>Salinity</topic><topic>Salinity effects</topic><topic>Salts</topic><topic>Seedlings</topic><topic>Stress</topic><topic>xylan</topic><topic>Zea mays</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Oliveira, Dyoni M.</creatorcontrib><creatorcontrib>Mota, Thatiane R.</creatorcontrib><creatorcontrib>Salatta, Fábio V.</creatorcontrib><creatorcontrib>Sinzker, Renata C.</creatorcontrib><creatorcontrib>Končitíková, Radka</creatorcontrib><creatorcontrib>Kopečný, David</creatorcontrib><creatorcontrib>Simister, Rachael</creatorcontrib><creatorcontrib>Silva, Mariana</creatorcontrib><creatorcontrib>Goeminne, Geert</creatorcontrib><creatorcontrib>Morreel, Kris</creatorcontrib><creatorcontrib>Rencoret, Jorge</creatorcontrib><creatorcontrib>Gutiérrez, Ana</creatorcontrib><creatorcontrib>Tryfona, Theodora</creatorcontrib><creatorcontrib>Marchiosi, Rogério</creatorcontrib><creatorcontrib>Dupree, Paul</creatorcontrib><creatorcontrib>del Río, José C.</creatorcontrib><creatorcontrib>Boerjan, Wout</creatorcontrib><creatorcontrib>McQueen‐Mason, Simon J.</creatorcontrib><creatorcontrib>Gomez, Leonardo D.</creatorcontrib><creatorcontrib>Ferrarese‐Filho, Osvaldo</creatorcontrib><creatorcontrib>dos Santos, Wanderley D.</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium &amp; 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Here, we conducted an in‐depth study of changes in cell wall composition and phenolic metabolism induced upon salinity in maize seedlings and plants. Cell wall characterization revealed that salt stress modulated the deposition of cellulose, matrix polysaccharides and lignin in seedling roots, plant roots and stems. The extraction and analysis of arabinoxylans by size‐exclusion chromatography, 2D‐NMR spectroscopy and carbohydrate gel electrophoresis showed a reduction of arabinoxylan content in salt‐stressed roots. Saponification and mild acid hydrolysis revealed that salinity also reduced the feruloylation of arabinoxylans in roots of seedlings and plants. Determination of lignin content and composition by nitrobenzene oxidation and 2D‐NMR confirmed the increased incorporation of syringyl units in lignin of maize roots. Salt stress also induced the expression of genes and the activity of enzymes enrolled in phenylpropanoid biosynthesis. The UHPLC–MS‐based metabolite profiling confirmed the modulation of phenolic profiling by salinity and the accumulation of ferulate and its derivatives 3‐ and 4‐O‐feruloyl quinate. In conclusion, we present a model for explaining cell wall remodeling in response to salinity. We demonstrate the modulations induced by salt stress in the amounts of crystalline cellulose, matrix polysaccharides and lignin in roots of maize seedlings and roots, stems and leaves of maize plants. Salt stress reduced the feruloylation of arabinoxylan, increased the incorporation of syringyl lignin, and induced the biosynthesis and accumulation of ferulic acid and its derivatives. 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source Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Access via Wiley Online Library; Wiley Online Library (Open Access Collection)
subjects Abiotic stress
Arabinoxylans
Biosynthesis
Carbohydrates
cell wall
Cell walls
Cellulose
Composition
Corn
Electrophoresis
ferulic acid
Gel electrophoresis
Gene expression
lignification
Lignin
Magnetic resonance spectroscopy
Metabolism
Metabolites
Nitrobenzene
NMR
NMR spectroscopy
Nuclear magnetic resonance
Oxidation
Phenolic compounds
Phenols
Plant extracts
Plant roots
Polymers
Polysaccharides
p‐coumaric acid
Roots
Saccharides
Salinity
Salinity effects
Salts
Seedlings
Stress
xylan
Zea mays
title Cell wall remodeling under salt stress: Insights into changes in polysaccharides, feruloylation, lignification, and phenolic metabolism in maize
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