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The Molecular Basis of Carbon and Nitrogen Metabolism in Plants

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A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Plant Sciences".

Deadline for manuscript submissions: closed (30 September 2020) | Viewed by 47900

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Special Issue Editors

Prof. Dr. Takuji Ohyama

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1. Department of Agricultural Chemistry, Faculty of Applied Biosciences, Tokyo University of Agriculture, Tokyo, Japan
2. Graduate School of Science and Technology, Niigata University, Niigata, Japan
Interests: nitrogen metabolism; nitrogen fixation; nodule; carbon metabolism; isotope tracer experiment; soybean; nitrogen fertilizer; flower bulb
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Dr. Kuni Sueyoshi

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Guest Editor

Graduate School of Science and Technology, Niigata University, Niigata, Japan
Interests: plant nutrition; nitrogen metabolism; nitrogen absorption; nitrogen transport; nitrate assimilation

Dr. Toshiaki Mitsui

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Department of Applied Biological Chemistry, Faculty of Agriculture, Niigata University, Niigata 951-8510, Japan
Interests: starch breakdown; carbon metabolism; high temperature; high CO₂; organelle biology; plant biochemistry

Dr. Marouane Baslam

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Guest Editor

Laboratory of Biochemistry, Faculty of Agriculture, Niigata University, Niigata 950-2181, Japan
Interests: plant–microorganism interactions, -omics; climate change; yield; sustainability
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Carbon and nitrogen are the most important essential elements constituting the organic compounds in plants. Carbohydrates (i.e., sugars, starches, and cell wall polysaccharides) are mostly composed of C, H, and O; and proteins and nucleic acids consist of C, H, O, and N. Terrestrial plants are photoautotrophs turn carbon dioxide into sugar by using light energy and water in the leaves. At the same time, plants absorb nitrogen from the soil, mainly in the form of nitrate or ammonium for their posterior incorporation into amino acids, and hence for the synthesis of protein. Several microorganisms fix nitrogen symbiotically by partnering with a host plant. The shoots and roots depend on each other by exchanging the C and N through xylem and phloem transport systems. C and N metabolism are regulated by complex mechanisms in order to optimize plant growth, agricultural crop production, and the maintenance of agro- and natural-ecosystem. The up-to-date review articles are welcomed as well as original regular papers.

This Special Issue aims to shed light on cutting-edge research of:

The molecular basis of carbon and nitrogen metabolism and their regulation.
Integrated networks using multiple omics for understanding C and N metabolisms under normal and/or biotic and abiotic stresses in plants. Only-omics approaches providing further insights into C and N regulation will be considered for review.
The interaction of C and N metabolism, transport, and storage.
Insights into the interaction and regulation of carbon and nitrogen metabolisms within the plant–microorganism communication.
The signal transductions related to phytohormones, signal peptide, and non-coding RNA.
Agricultural and ecological aspects based on molecular approaches will be welcome.

Prof. Dr. Takuji Ohyama
Dr. Kuni Sueyoshi
Dr. Toshiaki Mitsui
Dr. Marouane Baslam
Guest Editors

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Keywords

carbon metabolism
nitrogen metabolism
nitrogen absorption
carbon and nitrogen transport
carbon and nitrogen storage
interactions with other organisms
multi-omics
signal transduction

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Published Papers (8 papers)

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Research

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27 pages, 4690 KiB

Open AccessArticle

Application of Nitrate, Ammonium, or Urea Changes the Concentrations of Ureides, Urea, Amino Acids and Other Metabolites in Xylem Sap and in the Organs of Soybean Plants (Glycine max (L.) Merr.)

by Yuki Ono, Masashige Fukasawa, Kuni Sueyoshi, Norikuni Ohtake, Takashi Sato, Sayuri Tanabata, Ryo Toyota, Kyoko Higuchi, Akihiro Saito and Takuji Ohyama

Int. J. Mol. Sci. 2021, 22(9), 4573; https://doi.org/10.3390/ijms22094573 - 27 Apr 2021

Cited by 13 | Viewed by 3622

Abstract

Soybean (Glycine max (L.) Merr.) plants form root nodules and fix atmospheric dinitrogen, while also utilizing the combined nitrogen absorbed from roots. In this study, nodulated soybean plants were supplied with 5 mM N nitrate, ammonium, or urea for 3 days, and the changes in metabolite concentrations in the xylem sap and each organ were analyzed. The ureide concentration in the xylem sap was the highest in the control plants that were supplied with an N-free nutrient solution, but nitrate and asparagine were the principal compounds in the xylem sap with nitrate treatment. The metabolite concentrations in both the xylem sap and each organ were similar between the ammonium and urea treatments. Considerable amounts of urea were present in the xylem sap and all the organs among all the treatments. Positive correlations were observed between the ureides and urea concentrations in the xylem sap as well as in the roots and leaves, although no correlations were observed between the urea and arginine concentrations, suggesting that urea may have originated from ureide degradation in soybean plants, possibly in the roots. This is the first finding of the possibility of ureide degradation to urea in the underground organs of soybean plants. Full article

(This article belongs to the Special Issue The Molecular Basis of Carbon and Nitrogen Metabolism in Plants)

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18 pages, 3285 KiB

Open AccessArticle

Nitrogen Regulating the Expression and Localization of Four Glutamine Synthetase Isoforms in Wheat (Triticum aestivum L.)

by Yihao Wei, Xiaochun Wang, Zhiyong Zhang, Shuping Xiong, Xiaodan Meng, Jie Zhang, Lulu Wang, Xiaojiao Zhang, Meiqin Yu and Xinming Ma

Int. J. Mol. Sci. 2020, 21(17), 6299; https://doi.org/10.3390/ijms21176299 - 31 Aug 2020

Cited by 18 | Viewed by 2592

Abstract

Glutamine synthetase (GS), the key enzyme in plant nitrogen assimilation, is strictly regulated at multiple levels, but the most relevant reports focus on the mRNA level. Using specific antibodies as probes, the effects of nitrogen on the expression and localization of individual wheat GS (TaGS) isoforms were studied. In addition to TaGS2, TaGS1;1 with high affinity to substrate and TaGS1;3 with high catalytic activity were also localized in mesophyll, and may participate in cytoplasmic assimilation of ammonium (NH₄⁺) released from photorespiration or absorbed by roots; TaGS1;2 was localized in xylem of leaves. In roots, although there were hundreds of times more TaGS1;1 than TaGS1;2 transcripts, the amount of TaGS1;1 subunit was not higher than that of TaGS1;2; NH₄⁺ inhibited TaGS1;1 expression but stimulated TaGS1;3 expression. In root tips, nitrate stimulated TaGS1;1, TaGS1;3, and TaGS2 expression in meristem, while NH₄⁺ promoted tissue differentiation and TaGS1;2 expression in endodermis and vascular tissue. Only TaGS1;2 was located in vascular tissue of leaves and roots, and was activated by glutamine, suggesting a role in nitrogen transport. TaGS1;3 was induced by NH₄⁺ in root endodermis and mesophyll, suggesting a function in relieving NH₄⁺ toxicity. Thus, TaGS isoforms play distinct roles in nitrogen assimilation for their different kinetic properties, tissue locations, and response to nitrogen regimes. Full article

(This article belongs to the Special Issue The Molecular Basis of Carbon and Nitrogen Metabolism in Plants)

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16 pages, 3666 KiB

Open AccessArticle

Functional Analysis of Rice Long-Chain Acyl-CoA Synthetase 9 (OsLACS9) in the Chloroplast Envelope Membrane

by Aya Kitajima-Koga, Marouane Baslam, Yuuki Hamada, Namiko Ito, Tomoko Taniuchi, Takeshi Takamatsu, Kazusato Oikawa, Kentaro Kaneko and Toshiaki Mitsui

Int. J. Mol. Sci. 2020, 21(6), 2223; https://doi.org/10.3390/ijms21062223 - 23 Mar 2020

Cited by 13 | Viewed by 4372

Abstract

The long-chain acyl-CoA synthetases (LACSs) are involved in lipid synthesis, fatty acid catabolism, and the transport of fatty acids between subcellular compartments. These enzymes catalyze the critical reaction of fatty acyl chains to fatty acyl-CoAs for the triacylglycerol biosynthesis used as carbon and energy reserves. In Arabidopsis, LACSs are encoded by a family of nine genes, with LACS9 being the only member located in the chloroplast envelope membrane. However, the comprehensive role of LACS9 and its contribution to plant metabolism have not been explored thoroughly. In this study, we report on the identification and characterization of LACS9 mutants in rice plants. Our results indicate that the loss-of-function mutations in OsLACS9 affect the architecture of internodes resulting in dwarf plants with large starch granules in the chloroplast, showing the suppression of starch degradation. Moreover, the plastid localization of α-amylase I-1 (AmyI-1)—a key enzyme involved in starch breakdown in plastids—was suppressed in the lacs9 mutant line. Immunological and confocal laser scanning microscopy analyses showed that OsLACS9-GFP is located in the chloroplast envelope in green tissue. Microscopic analysis showed that OsLACS9s interact with each other in the plastid envelope membrane. Furthermore, OsLACS9 is also one of the proteins transported to plastids without a transit peptide or involvement of the Toc/Tic complex system. To identify the plastid-targeting signal of OsLACS9, the transient expression and localization of a series of N-terminal truncated OsLACS9-green fluorescent protein (GFP) fusion proteins were examined. Truncation analyses identified the N-terminal 30 amino acid residues to be required for OsLACS9 plastid localization. Overall, the data in this study provide an advanced understanding of the function of OsLACS9 and its role in starch degradation and plant growth. Full article

(This article belongs to the Special Issue The Molecular Basis of Carbon and Nitrogen Metabolism in Plants)

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23 pages, 4425 KiB

Open AccessArticle

Transcriptome Analysis Reveals Differences in Key Genes and Pathways Regulating Carbon and Nitrogen Metabolism in Cotton Genotypes under N Starvation and Resupply

by Asif Iqbal, Qiang Dong, Xiangru Wang, Huiping Gui, Hengheng Zhang, Xiling Zhang and Meizhen Song

Int. J. Mol. Sci. 2020, 21(4), 1500; https://doi.org/10.3390/ijms21041500 - 22 Feb 2020

Cited by 36 | Viewed by 4371

Abstract

Nitrogen (N) is the most important limiting factor for cotton production worldwide. Genotype-dependent ability to cope with N shortage has been only partially explored in cotton, and in this context, the comparison of molecular responses of cotton genotypes with different nitrogen use efficiency (NUE) is of particular interest to dissect the key molecular mechanisms underlying NUE. In this study, we employed Illumina RNA-Sequencing to determine the genotypic difference in transcriptome profile using two cotton genotypes differing in NUE (CCRI-69, N-efficient, and XLZ-30, N-inefficient) under N starvation and resupply treatments. The results showed that a large genetic variation existed in differentially expressed genes (DEGs) related to amino acid, carbon, and nitrogen metabolism between CCRI-69 and XLZ-30. Further analysis of metabolic changes in cotton genotypes under N resupply showed that nitrogen metabolism and aromatic amino acid metabolism pathways were mainly enriched in CCRI-69 by regulating carbon metabolism pathways such as starch and sucrose metabolism, glycolysis/gluconeogenesis, and pentose phosphate pathway. Additionally, we performed an expression network analysis of genes related to amino acid, carbon, and nitrogen metabolism. In total, 75 and 33 genes were identified as hub genes in shoots and roots of cotton genotypes, respectively. In summary, the identified hub genes may provide new insights into coordinating carbon and nitrogen metabolism and improving NUE in cotton. Full article

(This article belongs to the Special Issue The Molecular Basis of Carbon and Nitrogen Metabolism in Plants)

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19 pages, 1852 KiB

Open AccessArticle

Physiological, Hormonal and Metabolic Responses of two Alfalfa Cultivars with Contrasting Responses to Drought

by David Soba, Bangwei Zhou, Cesar Arrese-Igor, Sergi Munné-Bosch and Iker Aranjuelo

Int. J. Mol. Sci. 2019, 20(20), 5099; https://doi.org/10.3390/ijms20205099 - 15 Oct 2019

Cited by 24 | Viewed by 4131

Abstract

Alfalfa (Medicago sativa L.) is frequently constrained by environmental conditions such as drought. Within this context, it is crucial to identify the physiological and metabolic traits conferring a better performance under stressful conditions. In the current study, two alfalfa cultivars (San Isidro and Zhong Mu) with different physiological strategies were selected and subjected to water limitation conditions. Together with the physiological analyses, we proceeded to characterize the isotopic, hormone, and metabolic profiles of the different plants. According to physiological and isotopic data, Zhong Mu has a water-saver strategy, reducing water lost by closing its stomata but fixing less carbon by photosynthesis, and therefore limiting its growth under water-stressed conditions. In contrast, San Isidro has enhanced root growth to replace the water lost through transpiration due to its more open stomata, thus maintaining its biomass. Zhong Mu nodules were less able to maintain nodule N₂ fixing activity (matching plant nitrogen (N) demand). Our data suggest that this cultivar-specific performance is linked to Asn accumulation and its consequent N-feedback nitrogenase inhibition. Additionally, we observed a hormonal reorchestration in both cultivars under drought. Therefore, our results showed an intra-specific response to drought at physiological and metabolic levels in the two alfalfa cultivars studied. Full article

(This article belongs to the Special Issue The Molecular Basis of Carbon and Nitrogen Metabolism in Plants)

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17 pages, 2560 KiB

Open AccessArticle

An Integrated Analysis of the Rice Transcriptome and Metabolome Reveals Differential Regulation of Carbon and Nitrogen Metabolism in Response to Nitrogen Availability

by Wei Xin, Lina Zhang, Wenzhong Zhang, Jiping Gao, Jun Yi, Xiaoxi Zhen, Ziang Li, Ying Zhao, Chengcheng Peng and Chen Zhao

Int. J. Mol. Sci. 2019, 20(9), 2349; https://doi.org/10.3390/ijms20092349 - 11 May 2019

Cited by 86 | Viewed by 8347

Abstract

Nitrogen (N) is an extremely important macronutrient for plant growth and development. It is the main limiting factor in most agricultural production. However, it is well known that the nitrogen use efficiency (NUE) of rice gradually decreases with the increase of the nitrogen application rate. In order to clarify the underlying metabolic and molecular mechanisms of this phenomenon, we performed an integrated analysis of the rice transcriptome and metabolome. Both differentially expressed genes (DEGs) and metabolite Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis indicated that carbon and nitrogen metabolism is significantly affected by nitrogen availability. Further analysis of carbon and nitrogen metabolism changes in rice under different nitrogen availability showed that high N inhibits nitrogen assimilation and aromatic metabolism pathways by regulating carbon metabolism pathways such as the tricarboxylic acid (TCA) cycle and the pentose phosphate pathway (PPP). Under low nitrogen, the TCA cycle is promoted to produce more energy and α-ketoglutarate, thereby enhancing nitrogen transport and assimilation. PPP is also inhibited by low N, which may be consistent with the lower NADPH demand under low nitrogen. Additionally, we performed a co-expression network analysis of genes and metabolites related to carbon and nitrogen metabolism. In total, 15 genes were identified as hub genes. In summary, this study reveals the influence of nitrogen levels on the regulation mechanisms for carbon and nitrogen metabolism in rice and provides new insights into coordinating carbon and nitrogen metabolism and improving nitrogen use efficiency in rice. Full article

(This article belongs to the Special Issue The Molecular Basis of Carbon and Nitrogen Metabolism in Plants)

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Review

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39 pages, 2885 KiB

Open AccessReview

Recent Advances in Carbon and Nitrogen Metabolism in C3 Plants

by Marouane Baslam, Toshiaki Mitsui, Kuni Sueyoshi and Takuji Ohyama

Int. J. Mol. Sci. 2021, 22(1), 318; https://doi.org/10.3390/ijms22010318 - 30 Dec 2020

Cited by 119 | Viewed by 16198

Abstract

C and N are the most important essential elements constituting organic compounds in plants. The shoots and roots depend on each other by exchanging C and N through the xylem and phloem transport systems. Complex mechanisms regulate C and N metabolism to optimize plant growth, agricultural crop production, and maintenance of the agroecosystem. In this paper, we cover the recent advances in understanding C and N metabolism, regulation, and transport in plants, as well as their underlying molecular mechanisms. Special emphasis is given to the mechanisms of starch metabolism in plastids and the changes in responses to environmental stress that were previously overlooked, since these changes provide an essential store of C that fuels plant metabolism and growth. We present general insights into the system biology approaches that have expanded our understanding of core biological questions related to C and N metabolism. Finally, this review synthesizes recent advances in our understanding of the trade-off concept that links C and N status to the plant’s response to microorganisms. Full article

(This article belongs to the Special Issue The Molecular Basis of Carbon and Nitrogen Metabolism in Plants)

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15 pages, 1232 KiB

Open AccessReview

Roles of Non-Coding RNAs in Response to Nitrogen Availability in Plants

by Makiha Fukuda, Toru Fujiwara and Sho Nishida

Int. J. Mol. Sci. 2020, 21(22), 8508; https://doi.org/10.3390/ijms21228508 - 12 Nov 2020

Cited by 15 | Viewed by 3277

Abstract

Nitrogen (N) is an essential nutrient for plant growth and development; therefore, N deficiency is a major limiting factor in crop production. Plants have evolved mechanisms to cope with N deficiency, and the role of protein-coding genes in these mechanisms has been well studied. In the last decades, regulatory non-coding RNAs (ncRNAs), such as microRNAs (miRNAs), small interfering RNAs (siRNAs), and long ncRNAs (lncRNAs), have emerged as important regulators of gene expression in diverse biological processes. Recent advances in technologies for transcriptome analysis have enabled identification of N-responsive ncRNAs on a genome-wide scale. Characterization of these ncRNAs is expected to improve our understanding of the gene regulatory mechanisms of N response. In this review, we highlight recent progress in identification and characterization of N-responsive ncRNAs in Arabidopsis thaliana and several other plant species including maize, rice, and Populus. Full article

(This article belongs to the Special Issue The Molecular Basis of Carbon and Nitrogen Metabolism in Plants)

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