Respiratory burst oxidases and apoplastic peroxidases facilitate ammonium syndrome development in Arabidopsis

Podgórska, Anna; Burian, Maria; Dobrzyńska, Katarzyna; Rasmusson, Allan G.; Szal, Bożena

doi:10.1016/j.envexpbot.2020.104279

Cited by 11 publications

(6 citation statements)

References 105 publications

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“…Similar results have been observed previously on M. aeruginosa grown under NO 3 − -N. 18,25,35 + -N supplies are high 36,37 and is also known as the "NH 4 + syndrome" in higher plants. 38 Previous studies in Synechocystis sp. PCC 6803 have reported increased photoinhibitory damage of PSII under NH 4 + -N-rich conditions.…”

Section: ■ Results and Discussionmentioning

confidence: 98%

“…However, in the NH 4 + -N-only group, the abundant NH 4 + -N supply significantly inhibited cell growth and N assimilation in the later stage, and 28.45% of NH 4 + -N was ultimately left in the medium. The phenomenon has been interpreted as NH 4 + -N toxicity in the organism when external NH 4 + -N supplies are high , and is also known as the “NH 4 + syndrome” in higher plants . Previous studies in Synechocystis sp.…”

Section: Resultsmentioning

confidence: 99%

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Uncovering the Differential Growth of Microcystis aeruginosa Cultivated under Nitrate and Ammonium from a Photophysiological Perspective

Yang

Dong

Liu³

et al. 2023

ACS EST Water

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Cyanobacteria have a relatively high affinity for NH4 +, yet a NO3 –-rich environment is comparatively conducive to their proliferation. To date, little information is available on why NO3 –-N favors cyanobacterial biomass accumulation. This study investigated the dependence of biomass, nitrogen assimilation characteristics, and photophysiological performance of Microcystis aeruginosa on the forms of nitrogen supply, including NO3 –-N-only, NH4 +-N-only, and NO3 –-N + NH4 +-N. The results indicated that despite the retarded growth of M. aeruginosa, cells supplied with NO3 –-N-only maintained a simultaneous promotion in the growth rate, nitrogen assimilation efficiency, and photosynthetic capacity, resulting in high biomass production. Cells supplied with NH4 +-N-only and NO3 –-N + NH4 +-N were able to rapidly assimilate nitrogen during initial cell proliferation, showing a preferential use of NH4 +-N and the inhibition of NO3 – uptake by NH4 +. However, growth repression occurred as cultivation time was prolonged when NH4 +-N was excessively supplied, mainly due to PSII photodamage, intracellular redox imbalance, and increased electron energy accumulation. Thus, cells supplied with NH4 +-N-only had to reduce light energy capture, increase photoprotection, and consume excess electrons to mitigate the damage. These findings are critical for improving our understanding of the role of different nitrogen forms in the regulation of cyanobacterial photophysiological performance and growth.

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Section: ■ Results and Discussionmentioning

confidence: 98%

Section: Resultsmentioning

confidence: 99%

Uncovering the Differential Growth of Microcystis aeruginosa Cultivated under Nitrate and Ammonium from a Photophysiological Perspective

Yang

Dong

Liu³

et al. 2023

ACS EST Water

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“…Multiple approaches have shown that high ammonium concentrations are strongly phytotoxic and promote ROS formation, leading to oxidative stress ( Bittsánszky et al, 2015 ; Podgórska and Szal, 2015 ). Increasing NH 4 + supply may play a role in the oxidative stress by enhancing transcripts level and the NADPH oxidase activity, which is known as respiratory-burst oxidase homologs (RBOHs), which can oxidize cytosolic NADPH and transfer an electron across the cell membrane to generate O 2 – in the cytosol and cell wall ( Swanson and Gilroy, 2010 ; Podgórska et al, 2021 ). In our study, we found that two upregulated DEGs were involved in the respiratory-burst oxidase expression ( Supplementary Table 3 ).…”

Section: Discussionmentioning

confidence: 99%

“…In this study, we found that a high NH 4 + /NO 3 – ratio significantly increased root lignin content ( Figure 10 ), likely because ROS directly modify the structure of the root cell wall by their involvement in lignin formation ( Tsukagoshi, 2016 ). Indeed, ROS facilitates POD activity in the presence of NH 4 + ( Podgórska et al, 2021 ). Furthermore, we found that increasing the NH 4 + /NO 3 – ratios significantly increased the activities of PAL, 4CL, CCR, CAD, COMT, and POD ( Figure 11 ), which are key enzymes involved in lignin biosynthesis.…”

Section: Discussionmentioning

confidence: 99%

Transcriptome and Proteomics Analysis of Wheat Seedling Roots Reveals That Increasing NH4+/NO3– Ratio Induced Root Lignification and Reduced Nitrogen Utilization

Yang

Zhao

et al. 2022

Front. Plant Sci.

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Wheat growth and nitrogen (N) uptake gradually decrease in response to high NH4+/NO3– ratio. However, the mechanisms underlying the response of wheat seedling roots to changes in NH4+/NO3– ratio remain unclear. In this study, we investigated wheat growth, transcriptome, and proteome profiles of roots in response to increasing NH4+/NO3– ratios (Na: 100/0; Nr1: 75/25, Nr2: 50/50, Nr3: 25/75, and Nn: 0/100). High NH4+/NO3– ratio significantly reduced leaf relative chlorophyll content, Fv/Fm, and ΦII values. Both total root length and specific root length decreased with increasing NH4+/NO3– ratios. Moreover, the rise in NH4+/NO3– ratio significantly promoted O2– production. Furthermore, transcriptome sequencing and tandem mass tag-based quantitative proteome analyses identified 14,376 differentially expressed genes (DEGs) and 1,819 differentially expressed proteins (DEPs). The Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment analysis indicated that glutathione metabolism and phenylpropanoid biosynthesis were the main two shared enriched pathways across ratio comparisons. Upregulated DEGs and DEPs involving glutathione S-transferases may contribute to the prevention of oxidative stress. An increment in the NH4+/NO3– ratio induced the expression of genes and proteins involved in lignin biosynthesis, which increased root lignin content. Additionally, phylogenetic tree analysis showed that both A0A3B6NPP6 and A0A3B6LM09 belong to the cinnamyl-alcohol dehydrogenase subfamily. Fifteen downregulated DEGs were identified as high-affinity nitrate transporters or nitrate transporters. Upregulated TraesCS3D02G344800 and TraesCS3A02G350800 were involved in ammonium transport. Downregulated A0A3B6Q9B3 is involved in nitrate transport, whereas A0A3B6PQS3 is a ferredoxin-nitrite reductase. This may explain why an increase in the NH4+/NO3– ratio significantly reduced root NO3–-N content but increased NH4+-N content. Overall, these results demonstrated that increasing the NH4+/NO3– ratio at the seedling stage induced the accumulation of reactive oxygen species, which in turn enhanced root glutathione metabolism and lignification, thereby resulting in increased root oxidative tolerance at the cost of reducing nitrate transport and utilization, which reduced leaf photosynthetic capacity and, ultimately, plant biomass accumulation.

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“…Moreover, excess N fertilizer application often suppresses crop growth, decreases kernel yield, and causes environmental pollution [10]. In particular, when using NH 4 + as the sole N source, most plants exhibit severe growth retardation, leaf chlorosis, a lower net photosynthetic rate, and other toxic symptoms, commonly referred to as NH 4 + syndrome [11,12]. Therefore, optimizing N fertilization can improve nitrogen use efficiency (NUE), reduce the cost of N inputs, and decrease environmental pollution [13].…”

Section: Introductionmentioning

confidence: 99%

Bicarbonate-Dependent Detoxification by Mitigating Ammonium-Induced Hypoxic Stress in Triticum aestivum Root

Liu,

Zhang,

Tang

et al. 2024

Biology

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Ammonium (NH4+) toxicity is ubiquitous in plants. To investigate the underlying mechanisms of this toxicity and bicarbonate (HCO3−)-dependent alleviation, wheat plants were hydroponically cultivated in half-strength Hoagland nutrient solution containing 7.5 mM NO3− (CK), 7.5 mM NH4+ (SA), or 7.5 mM NH4+ + 3 mM HCO3− (AC). Transcriptomic analysis revealed that compared to CK, SA treatment at 48 h significantly upregulated the expression of genes encoding fermentation enzymes (pyruvate decarboxylase (PDC), alcohol dehydrogenase (ADH), and lactate dehydrogenase (LDH)) and oxygen consumption enzymes (respiratory burst oxidase homologs, dioxygenases, and alternative oxidases), downregulated the expression of genes encoding oxygen transporters (PIP-type aquaporins, non-symbiotic hemoglobins), and those involved in energy metabolism, including tricarboxylic acid (TCA) cycle enzymes and ATP synthases, but upregulated the glycolytic enzymes in the roots and downregulated the expression of genes involved in the cell cycle and elongation. The physiological assay showed that SA treatment significantly increased PDC, ADH, and LDH activity by 36.69%, 43.66%, and 61.60%, respectively; root ethanol concentration by 62.95%; and lactate efflux by 23.20%, and significantly decreased the concentrations of pyruvate and most TCA cycle intermediates, the complex V activity, ATP content, and ATP/ADP ratio. As a consequence, SA significantly inhibited root growth. AC treatment reversed the changes caused by SA and alleviated the inhibition of root growth. In conclusion, NH4+ treatment alone may cause hypoxic stress in the roots, inhibit energy generation, suppress cell division and elongation, and ultimately inhibit root growth, and adding HCO3− remarkably alleviates the NH4+-induced inhibitory effects on root growth largely by attenuating the hypoxic stress.

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Respiratory burst oxidases and apoplastic peroxidases facilitate ammonium syndrome development in Arabidopsis

Cited by 11 publications

References 105 publications

Uncovering the Differential Growth of Microcystis aeruginosa Cultivated under Nitrate and Ammonium from a Photophysiological Perspective

Uncovering the Differential Growth of Microcystis aeruginosa Cultivated under Nitrate and Ammonium from a Photophysiological Perspective

Transcriptome and Proteomics Analysis of Wheat Seedling Roots Reveals That Increasing NH4+/NO3– Ratio Induced Root Lignification and Reduced Nitrogen Utilization

Bicarbonate-Dependent Detoxification by Mitigating Ammonium-Induced Hypoxic Stress in Triticum aestivum Root

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