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Multi‐omics analysis of xylem sap uncovers dynamic modulation of poplar defenses by ammonium and nitrate

ABSTRACT: Xylem sap is the major transport route for nutrients from roots to shoots. In the present study, we investigated how variations in nitrogen (N) nutrition affected the metabolome and proteome of xylem sap and the growth of the xylem endophyte Brennaria salicis, and we also report transcriptional re-wiring of leaf defenses in poplar (Populus × canescens). We supplied poplars with high, intermediate or low concentrations of ammonium or nitrate. We identified 288 unique proteins in xylem sap. Approximately 85% of the xylem sap proteins were shared among ammonium- and nitrate-supplied plants. The number of proteins increased with increasing N supply but the major functional categories (catabolic processes, cell wall-related enzymes, defense) were unaffected. Ammonium nutrition caused higher abundances of amino acids and carbohydrates, whereas nitrate caused higher malate levels in xylem sap. Pipecolic acid and N-hydroxy-pipecolic acid increased, whereas salicylic acid and jasmonoyl-isoleucine decreased, with increasing N nutrition. Untargeted metabolome analyses revealed 2179 features in xylem sap, of which 863 were differentially affected by N treatments. We identified 124 metabolites, mainly from specialized metabolism of the groups of salicinoids, phenylpropanoids, phenolics, flavonoids, and benzoates. Their abundances increased with decreasing N, except coumarins. Brennaria salicis growth was reduced in nutrient-supplemented xylem sap of low- and high- NO₃ ^- -fed plants compared to that of NH₄ ⁺ -fed plants. The drastic changes in xylem sap composition caused massive changes in the transcriptional landscape of leaves and recruited defenses related to systemic acquired and induced systemic resistance. Our study uncovers unexpected complexity and variability of xylem composition with consequences for plant defenses.

INSTRUMENT(S): Liquid Chromatography MS - negative - reverse phase, Liquid Chromatography MS - positive - reverse phase

SUBMITTER: Kirstin / Ilka Feussner / Abreu

PROVIDER: MTBLS2305 | MetaboLights | 2022-07-04

REPOSITORIES: MetaboLights

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	MTBLS2305	Other
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	a_MTBLS2305_LC-MS_negative_reverse-phase_metabolite_profiling.txt	Txt
	a_MTBLS2305_LC-MS_positive_reverse-phase_metabolite_profiling.txt	Txt
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Multi-omics analysis of xylem sap uncovers dynamic modulation of poplar defenses by ammonium and nitrate.

Kasper Karl K Abreu Ilka N IN Feussner Kirstin K Zienkiewicz Krzysztof K Herrfurth Cornelia C Ischebeck Till T Janz Dennis D Majcherczyk Andrzej A Schmitt Kerstin K Valerius Oliver O Braus Gerhard H GH Feussner Ivo I Polle Andrea A

The Plant journal : for cell and molecular biology 20220527 1

Xylem sap is the major transport route for nutrients from roots to shoots. In the present study, we investigated how variations in nitrogen (N) nutrition affected the metabolome and proteome of xylem sap and the growth of the xylem endophyte Brennaria salicis, and we also report transcriptional re-wiring of leaf defenses in poplar (Populus × canescens). We supplied poplars with high, intermediate or low concentrations of ammonium or nitrate. We identified 288 unique proteins in xylem sap. Approx ...[more]

PMID: 35535561

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Project description:Plant nutrition takes advantage by the simultaneous presence of more N forms in the rhizosphere. In the last decades the interplay between ammonium and nitrate acquisition systems in roots has been deeply investigated. Although widely used as fertilizers, the occurrence of cross connection between urea and ammonium nutrition has been scarcely studied in plants, especially at molecular level. In a recent paper we provided evidence that maize plants fed with urea and ammonium mix showed a better N-uptake efficiency than plants fed with ammonium or urea alone. To elucidate the molecular mechanism underlying this response, transcriptomic and metabolomic changes occurring in maize plants were investigated. Transcriptomic analyses indicated that several transporters and enzymes involved in N-nutrition were found upregulated by all three N-treatments (AMT1.3, NRT1.1, NRT2.1, GS1, GOGAT, GDH), confirming that urea is a direct source of N for plants. Depending on N-form available in nutrient solution a peculiar response at transcriptomic and metabolomic level was observed, especially after 24 hours of treatment. In comparison to one single N-form, urea and ammonium mix induced a prompt assimilation of N, characterized by an overaccumulation of main amino acids in shoots, and an upregulation of ZmAMT1.1. Moreover even a peculiar modulation of aquaporins, carbonic anydrases, glutamine synthetase, amino aspartate, as well as the glycolysis-TCA cycle was induced in roots by urea and ammonium mix. Depending on N-form available in the external media, even changes in phytohormone’s composition were observed in maize (CKs, ABA, JA); in particular, already after 24 hours of treatment, urea induced the accumulation of trans-zeatin in shoots. Through a multiomics approach, we provide for the first time molecular characterization of maize response to urea and ammonium nutrition. This study paves the way to formulate guidelines for the optimization of N fertilization of crops to improve the N use efficiency in plants and therefore limit N losses in the environment.

Project description:In comparison with provision of either ammonium or nitrate alone, simultaneously supplying both forms of N results in superior growth and yield for the majority of plants including rice. Using a rice 22K oligo-array, we performed transcriptome analysis to identify genes of rice (Oryza sativa L. ssp. japonica) responsive to change of N-supply forms and N-starvation. Using the supply of ammonium nitrate (one to one molar ratio) as control, the total number of root genes that were equal or more than two fold up- or down- regulated was 445, 324, and 781 by upon supply of either ammonium or nitrate or continuous N starvation, respectively for 96 h. In the shoot the equivalent numbers were much smaller only 32, 58, and 165, respectively. Clustering of the rice genes associated with different environmental stresses revealed substantial organ specificity of the root and shoot to N starvation, and also to the N supply form. Genes encoding transporters for ammonium and nitrate, nitrate reductase, glutamate dehydrogenase, and aspartate amino transferase, showed great response to change of the N supply form, especially to N starvation. Some of the genes involved in chlorophyll metabolism, carbon fixation and assimilation, were enhanced by ammonium supply only, but significantly suppressed by N-starvation. In the shoot there was increased expression of more general stress genes under nitrate when compared to ammonium nutrition. In the root the reverse situation was true with more apparent stress under ammonium nutrition. The microarray approach has revealed new levels of complexity in the response of rice to the form of N supply. Experiment Overall Design: Rice seedlings were grown in a hydroponic system in a growth chamber with control of both temperature and light. After normal growth for two weeks and for one week with completely avoiding any N source, the plants at four and a half leaf stage were re-supplied with ammonium nitrate (equal amount of either form of N), or only ammonium (ammonium sulphate and ammonium chloride), or only nitrate (calcium nitrate and magnesium nitrate), and continuing at zero N (N starvation). All the other essential nutrients were the same for all four treatments, except for sulfate and chloride which ranged between 1.1 â 2.6 mM and 0.5 â 2.5 mM, respectively. In Arabidopsis, addition of 3 mM Cl to âcontrolsâ did not produce any changes in the expression of genes in an experiment investigating the re-supply of 3 mM nitrate (Scheible et al., 2004). In other microarray experiments, extra addition of 5 mM Cl for Arabidopsis (Wang et al., 2000; Wang et al., 2004) and 1.4 mM sulphate for tomato (Wang et al., 2001) were used to replace nitrate for identifying the N deprivation responsive genes. Therefore, we assume that the relative smaller difference in sulfate and chloride concentrations among the four treatments in the normal supply range for plants would not significantly affect the expression profile of genes responsible for changes in N supply form and starvation in our experiments. Experiment Overall Design: For identifying the genes responding to the various N conditions by micro-array analysis, we extracted total RNA respectively from the roots and shoots at the 96 h after initiation of the four respective treatments. We used amplified and labeled cRNA from ammonium nitrate treatment as control, we performed array-hybridization for the cRNA from the treatment of single ammonium form, single nitrate form, or continuous N depletion, respectively. Agilent 60-mer oligonucleotide arrays containing 21,938 unique transcription units (Agilent Technologies, Tokyo, Japan) were used. Two biological replicates of each treatment were performed for microarray analyses.