Gabriela Ellen Barreto Bossoni , Matt Stata , Aline Marengoni Almeida , Rodrigo Polimeni Constantin , Rogério Marchiosi , Osvaldo Ferrarese-Filho , Rowan F. Sage , Wanderley Dantas dos Santos
{"title":"Assessing the cell wall nitrogen use efficiency – Can the differences between cell wall architectures contribute to the nitrogen economy of plants?","authors":"Gabriela Ellen Barreto Bossoni , Matt Stata , Aline Marengoni Almeida , Rodrigo Polimeni Constantin , Rogério Marchiosi , Osvaldo Ferrarese-Filho , Rowan F. Sage , Wanderley Dantas dos Santos","doi":"10.1016/j.plaphy.2025.110548","DOIUrl":null,"url":null,"abstract":"<div><div>C4 plants exhibit greater nitrogen use efficiency (NUE) than C3 plants, primarily due to lower ribulose-1,5-bisphosphate carboxylase/oxygenase requirements. However, plant NUE also varies among C4 species, suggesting that other factors, such as cell wall composition, contribute to nitrogen economy. To investigate the contribution of cell wall architecture to nitrogen economy, we compared plant species with distinct cell wall types: eudicots with type I cell walls (T1CW) and grasses with type II cell walls (T2CW), under four nitrogen regimes: deficit, low, medium, and normal. Species with different photosynthetic metabolisms were compared to confirm known differences in photosynthetic nitrogen use efficiency (pNUE), while species with similar metabolism but distinct cell wall types were compared assessing the influence of cell wall on nitrogen economy. The pNUE of C4 grasses was higher than that of C4 eudicots, increasing from +54 % in normal nitrogen to +81 % in nitrogen deficit. C4 grasses presented lower structural nitrogen (−26 %) in normal nitrogen supply, which decreased to −58 % in nitrogen deficit, in comparison to C4 eudicots. An exploratory parameter <em>cwpNUE</em> (photosynthetic rate/structural nitrogen) resulted in a much higher value in C4 grasses (∼1.1 μmol CO<sub>2</sub> s<sup>−1</sup> mmol<sup>−1</sup> cell wall nitrogen) than in the other groups (∼0.5 μmol CO<sub>2</sub> s<sup>−1</sup> mmol<sup>−1</sup> cell wall nitrogen). In turn, the ester-linked ferulic acid increased from +177 % in C4 grasses in normal nitrogen to +362 % in nitrogen deficit, when compared to C4 eudicots. Data supports the hypothesis that in hot, humid tropical environments, nitrogen became a major limiting nutrient for C4 plant growth and development. The overlap between extensins and FA-GAX in crosslinking CW polymers observed in T2CW suggest that nitrogen scarcity may have exerted a selection pressure for adaptations in C4 grasses to contribute to NUE.</div></div>","PeriodicalId":20234,"journal":{"name":"Plant Physiology and Biochemistry","volume":"229 ","pages":"Article 110548"},"PeriodicalIF":5.7000,"publicationDate":"2025-09-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Plant Physiology and Biochemistry","FirstCategoryId":"99","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S0981942825010769","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"PLANT SCIENCES","Score":null,"Total":0}
引用次数: 0
Abstract
C4 plants exhibit greater nitrogen use efficiency (NUE) than C3 plants, primarily due to lower ribulose-1,5-bisphosphate carboxylase/oxygenase requirements. However, plant NUE also varies among C4 species, suggesting that other factors, such as cell wall composition, contribute to nitrogen economy. To investigate the contribution of cell wall architecture to nitrogen economy, we compared plant species with distinct cell wall types: eudicots with type I cell walls (T1CW) and grasses with type II cell walls (T2CW), under four nitrogen regimes: deficit, low, medium, and normal. Species with different photosynthetic metabolisms were compared to confirm known differences in photosynthetic nitrogen use efficiency (pNUE), while species with similar metabolism but distinct cell wall types were compared assessing the influence of cell wall on nitrogen economy. The pNUE of C4 grasses was higher than that of C4 eudicots, increasing from +54 % in normal nitrogen to +81 % in nitrogen deficit. C4 grasses presented lower structural nitrogen (−26 %) in normal nitrogen supply, which decreased to −58 % in nitrogen deficit, in comparison to C4 eudicots. An exploratory parameter cwpNUE (photosynthetic rate/structural nitrogen) resulted in a much higher value in C4 grasses (∼1.1 μmol CO2 s−1 mmol−1 cell wall nitrogen) than in the other groups (∼0.5 μmol CO2 s−1 mmol−1 cell wall nitrogen). In turn, the ester-linked ferulic acid increased from +177 % in C4 grasses in normal nitrogen to +362 % in nitrogen deficit, when compared to C4 eudicots. Data supports the hypothesis that in hot, humid tropical environments, nitrogen became a major limiting nutrient for C4 plant growth and development. The overlap between extensins and FA-GAX in crosslinking CW polymers observed in T2CW suggest that nitrogen scarcity may have exerted a selection pressure for adaptations in C4 grasses to contribute to NUE.
期刊介绍:
Plant Physiology and Biochemistry publishes original theoretical, experimental and technical contributions in the various fields of plant physiology (biochemistry, physiology, structure, genetics, plant-microbe interactions, etc.) at diverse levels of integration (molecular, subcellular, cellular, organ, whole plant, environmental). Opinions expressed in the journal are the sole responsibility of the authors and publication does not imply the editors'' agreement.
Manuscripts describing molecular-genetic and/or gene expression data that are not integrated with biochemical analysis and/or actual measurements of plant physiological processes are not suitable for PPB. Also "Omics" studies (transcriptomics, proteomics, metabolomics, etc.) reporting descriptive analysis without an element of functional validation assays, will not be considered. Similarly, applied agronomic or phytochemical studies that generate no new, fundamental insights in plant physiological and/or biochemical processes are not suitable for publication in PPB.
Plant Physiology and Biochemistry publishes several types of articles: Reviews, Papers and Short Papers. Articles for Reviews are either invited by the editor or proposed by the authors for the editor''s prior agreement. Reviews should not exceed 40 typewritten pages and Short Papers no more than approximately 8 typewritten pages. The fundamental character of Plant Physiology and Biochemistry remains that of a journal for original results.