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Nitrate and ammonium lead to distinct global dynamic phosphorylation patterns when resupplied to nitrogen-starved Arabidopsis seedlings.

ABSTRACT: Nitrogen is an essential macronutrient for plant growth and development. Inorganic nitrogen and its assimilation products control various metabolic, physiological and developmental processes. Although the transcriptional responses induced by nitrogen have been extensively studied in the past, our work here focused on the discovery of candidate proteins for regulatory events that are complementary to transcriptional changes. Most signaling pathways involve modulation of protein abundance and/or activity by protein phosphorylation. Therefore, we analyzed the dynamic changes in protein phosphorylation in membrane and soluble proteins from plants exposed to rapid changes in nutrient availability over a time course of 30 min. Plants were starved of nitrogen and subsequently resupplied with nitrogen in the form of nitrate or ammonium. Proteins with maximum change in their phosphorylation level at up to 5 min after nitrogen resupply (fast responses) included GPI-anchored proteins, receptor kinases and transcription factors, while proteins with maximum change in their phosphorylation level after 10 min of nitrogen resupply (late responses) included proteins involved in protein synthesis and degradation, as well as proteins with functions in central metabolism and hormone metabolism. Resupply of nitrogen in the form of nitrate or ammonium resulted in distinct phosphorylation patterns, mainly of proteins with signaling functions, transcription factors and transporters.

SUBMITTER: Engelsberger WR

PROVIDER: S-EPMC3380553 | biostudies-literature | 2012 Mar

REPOSITORIES: biostudies-literature

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Nitrate and ammonium lead to distinct global dynamic phosphorylation patterns when resupplied to nitrogen-starved Arabidopsis seedlings.

Engelsberger Wolfgang R WR Schulze Waltraud X WX

The Plant journal : for cell and molecular biology 20120120 6

Nitrogen is an essential macronutrient for plant growth and development. Inorganic nitrogen and its assimilation products control various metabolic, physiological and developmental processes. Although the transcriptional responses induced by nitrogen have been extensively studied in the past, our work here focused on the discovery of candidate proteins for regulatory events that are complementary to transcriptional changes. Most signaling pathways involve modulation of protein abundance and/or a ...[more]

PMID: 22060019

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Project description:Dissimilatory nitrate reduction to ammonium (DNRA), denitrification, anaerobic ammonium oxidation (anammox), and biological N2 fixation (BNF) can influence the nitrogen (N) use efficiency of rice production. While the effect of N application on BNF is known, little is known about its effect on NO3- partitioning between DNRA, denitrification, and anammox. Here, we investigated the effect of N application on DNRA, denitrification, anammox, and BNF and on the abundance of relevant genes in three paddy soils in Australia. Rice was grown in a glasshouse with N fertilizer (150 kg N ha-1) and without N fertilizer for 75 days, and the rhizosphere and bulk soils were collected separately for laboratory incubation and quantitative PCR analysis. Nitrogen application reduced DNRA rates by >16% in all the soils regardless of the rhizospheric zone, but it did not affect the nrfA gene abundance. Without N, the amount and proportion of NO3- reduced by DNRA (0.42 to 0.52 μg g-1 soil day-1 and 45 to 55%, respectively) were similar to or higher than the amount and proportion reduced by denitrification. However, with N the amount of NO3- reduced by DNRA (0.32 to 0.40 μg g-1 soil day-1) was 40 to 50% lower than the amount of NO3- reduced by denitrification. Denitrification loss increased by >20% with N addition and was affected by the rhizospheric zones. Nitrogen loss was minimal through anammox, while BNF added 0.02 to 0.25 μg N g-1 soil day-1 We found that DNRA plays a significant positive role in paddy soil N retention, as it accounts for up to 55% of the total NO3- reduction, but this is reduced by N application.IMPORTANCE This study provides evidence that nitrogen addition reduces nitrogen retention through DNRA and increases nitrogen loss via denitrification in a paddy soil ecosystem. DNRA is one of the major NO3- reduction processes, and it can outcompete denitrification in NO3- consumption when rice paddies are low in nitrogen. A significant level of DNRA activity in paddy soils indicates that DNRA plays an important role in retaining nitrogen by reducing NO3- availability for denitrification and leaching. Our study shows that by reducing N addition to rice paddies, there is a positive effect from reduced nitrogen loss but, more importantly, from the conversion of NO3- to NH4+, which is the favored form of mineral nitrogen for plant uptake.

Project description:BackgroundIn order to grow, plants rely on soil nutrients which can vary both spatially and temporally depending on the environment, the soil type or the microbial activity. An essential nutrient is nitrogen, which is mainly accessible as nitrate and ammonium. Many studies have investigated transport genes for these ions in Arabidopsis thaliana and recently in crop species, including Maize, Rice and Barley. However, in most crop species, an understanding of the participants in nitrate and ammonium transport across the soil plant continuum remains undefined.ResultsWe have mapped a non-exhaustive set of putative nitrate and ammonium transporters in maize. The selected transporters were defined based on previous studies comparing nitrate transport pathways conserved between Arabidopsis and Zea mays (Plett D et. al, PLOS ONE 5:e15289, 2010). We also selected genes from published studies (Gu R et. al, Plant and Cell Physiology, 54:1515-1524, 2013, Garnett T et. al, New Phytol 198:82-94, 2013, Garnett T et. al, Frontiers in Plant Sci 6, 2015, Dechorgnat J et. al, Front Plant Sci 9:531, 2018). To analyse these genes, the plants were grown in a semi-hydroponic system to carefully control nitrogen delivery and then harvested at both vegetative and reproductive stages. The expression patterns of 26 putative nitrogen transporters were then tested. Six putative genes were found not expressed in our conditions. Transcripts of 20 other genes were detected at both the vegetative and reproductive stages of maize development. We observed the expression of nitrogen transporters in all organs tested: roots, young leaves, old leaves, silks, cobs, tassels and husk leaves. We also followed the gene expression response to nitrogen starvation and resupply and uncovered mainly three expression patterns: (i) genes unresponsiveness to nitrogen supply; (ii) genes showing an increase of expression after nitrogen starvation; (iii) genes showing a decrease of expression after nitrogen starvation.ConclusionsThese data allowed the mapping of putative nitrogen transporters in maize at both the vegetative and reproductive stages of development. No growth-dependent expression was seen in our conditions. We found that nitrogen transporter genes were expressed in all the organs tested and in many cases were regulated by the availability of nitrogen supplied to the plant. The gene expression patterns in relation to organ specificity and nitrogen availability denote a speciality of nitrate and ammonium transporter genes and their probable function depending on the plant organ and the environment.

Dataset Information

Nitrate and ammonium lead to distinct global dynamic phosphorylation patterns when resupplied to nitrogen-starved Arabidopsis seedlings.

Publications

Nitrate and ammonium lead to distinct global dynamic phosphorylation patterns when resupplied to nitrogen-starved Arabidopsis seedlings.

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