Improved sulfur nutrition provides the basis for enhanced production of sulfur-containing defense compounds in Arabidopsis thaliana upon inoculation with Alternaria brassicicola

Kruse, Cordula; Haas, Florian H.; Jost, Ricarda; Reiser, Bianca; Reichelt, Michael; Wirtz, Markus; Gershenzon, Jonathan; Schnug, Ewald; Hell, Rüdiger

doi:10.1016/j.jplph.2011.12.017

Cited by 19 publications

(17 citation statements)

References 17 publications

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“…This suggests a contribution of LeOASTLp1 to vascular S-enhanced protection by SDC generation and S 0 synthesis as proposed earlier by Cooper and Williams (2004) and Kruse et al (2007). The Cys synthesizing enzymes are known to be stimulated by a fungal infection and high S supply (Kruse et al 2012), which further supports the connection of pathogen and S-induced SED production and plant tolerance. In addition, a well-orchestrated cellular Cys homeostasis is thought to guide the establishment and signaling of a plant response toward fungal pathogens (Álvarez et al 2012).…”

supporting

confidence: 81%

Spatial gene expression analysis in tomato hypocotyls suggests cysteine as key precursor of vascular sulfur accumulation implicated in Verticillium dahliae defense

Klug

Hogekamp

Specht

et al. 2014

Physiologia Plantarum

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Verticillium dahliae is a prominent generator of plant vascular wilting disease and sulfur (S)-enhanced defense (SED) mechanisms contribute to its in-planta elimination. The accumulation of S-containing defense compounds (SDCs) including elemental S (S(0) ) has been described based on the comparison of two near-isogenic tomato (Solanum lycopersicum) lines differing in fungal susceptibility. To better understand the effect of S nutrition on V. dahliae resistance both lines were supplied with low, optimal or supraoptimal sulfate-S. An absolute quantification demonstrated a most effective fungal elimination due to luxury plant S nutrition. High-pressure liquid chromatography (HPLC) showed a strong regulation of Cys levels and an S-responsive GSH pool rise in the bulk hypocotyl. High-frequency S peak accumulations were detected in vascular bundles of resistant tomato plants after fungal colonization by laser ablation-inductively coupled plasma-mass spectrometry (LA-ICP-MS). Global transcriptomic analysis suggested that early steps of the primary S metabolism did not promote the SDCs synthesis in the whole hypocotyl as gene expression was downregulated after infection. Enhanced S fertilization mostly alleviated the repressive fungal effect but did not reverse it. Upregulation of glutathione (GSH)-associated genes in bulk hypocotyls but not in vascular bundles indicated a global antioxidative role of GSH. To finally assign the contribution of S metabolism-associated genes to high S(0) accumulations exclusively found in the resistant tomato line, a spatial gene expression approach was applied. Laser microdissection of infected vascular bundles revealed a switch toward transcription of genes connected with cysteine (Cys) synthesis. The upregulation of LeOASTLp1 suggests a role for Cys as key precursor for local S accumulations (possibly S(0) ) in the vascular bundles of the V. dahliae-resistant tomato line.

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supporting

confidence: 81%

Spatial gene expression analysis in tomato hypocotyls suggests cysteine as key precursor of vascular sulfur accumulation implicated in Verticillium dahliae defense

Klug

Hogekamp

Specht

et al. 2014

Physiologia Plantarum

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“…Most likely, within the plastids, the sulfate is reduced immediately and incorporated into cysteine, which serves as a building block of numerous sulfur‐containing stress‐defense compounds, e.g. glutathione GSH (Kruse et al ., ).…”

Section: Resultsmentioning

confidence: 97%

Sulfate availability affects ABA levels and germination response to ABA and salt stress in Arabidopsis thaliana

et al. 2014

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SUMMARYSulfur-containing compounds play a critical role in the response of plants to abiotic stress factors including drought. The phytohormone abscisic acid (ABA) is the key regulator of responses to drought and high-salt stress. However, our knowledge about interaction of S-metabolism and ABA biosynthesis is scarce. Here we report that sulfate supply affects synthesis and steady-state levels of ABA in Arabidopsis wild-type seedlings. By using different mutants of the sulfate uptake and reduction pathway, we confirmed the impact of sulfate supply on steady-state ABA content in Arabidopsis and demonstrated that this impact was due to cysteine availability. Loss of the chloroplast sulfate transporter3;1 function (sultr3;1) resulted in significantly decreased aldehyde oxidase (AO) activity and ABA levels in seedlings and seeds. These mutant phenotypes could be reverted by exogenous application of cysteine or ectopic expression of SULTR3;1. In addition the sultr3;1 mutant showed a decrease of xanthine dehydrogenase activity, but not of nitrate reductase, strongly indicating that in seedlings cysteine availability limits activity of the molybdenum co-factor sulfurase, ABA3, which requires cysteine as the S-donor for sulfuration. Transcription of ABA3 and NCED3, encoding another key enzyme of the ABA biosynthesis pathway, was regulated by S-supply in wild-type seedlings. In contrast, ABA up-regulated the transcript level of SULTR3;1 and other S-metabolism-related genes. Our results provide evidence for a significant co-regulation of S-metabolism and ABA biosynthesis that operates to ensure sufficient cysteine for AO maturation and highlights the importance of sulfur for stress tolerance of plants.

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“…Previous studies have reported that plant responses to pathogen attack (such as AMF infection) often involve the activation of sulphur metabolism (Kruse et al, ; Sieh et al, ). In this study, several proteins involved in sulfur metabolism were up‐regulated after AMF inoculation under AS (AS‐AM vs. AS analysis; Table S5 and Figure ).…”

Section: Discussionmentioning

confidence: 99%

Isobaric tags for relative and absolute quantification‐based proteomic analysis of Puccinellia tenuiflora inoculated with arbuscular mycorrhizal fungi reveal stress response mechanisms in alkali‐degraded soil

et al. 2019

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Alkali soil is a major abiotic constraint that limits plant distribution and yield in the northeast of China. Puccinellia tenuiflora is considered the most promising grass species for salt‐alkali grassland restoration. However, there is little information on the molecular mechanisms underlying how arbuscular mycorrhizal fungi (AMF) enhances P. tenuiflora stress responses in alkali‐degraded soil. In this study, AMF colonization, growth, photosynthetic pigments, and inorganic ion contents were measured. Isobaric tags for relative and absolute quantification‐based quantitative proteomic technology were employed to identify the differentially abundant proteins in P. tenuiflora seedlings with or without AMF under alkalinity stress. The results showed that AMF colonization increased seedling biomass, photosynthetic pigment contents, and K+/Na+ ratio under alkalinity stress. Moreover, a total of 598 proteins were significantly differentially regulated in P. tenuiflora seedlings after AMF inoculation under alkalinity stress compared with under alkalinity stress alone. The results showed that AMF inoculation significantly improved protein synthesis, reactive oxygen species scavenging, and nitrogen metabolism to promote the biosynthesis of osmotic substances in response to alkalinity stress. In addition, P. tenuiflora seedlings produced more energy to compensate for the energy loss caused by alkalinity stress after AMF inoculation. In conclusion, these findings provide new insights into the physiological mechanisms of the response to alkali‐degraded soil in P. tenuiflora seedlings with AMF and also clarify the role of AMF in the molecular regulation network of P. tenuiflora under alkalinity stress.

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Improved sulfur nutrition provides the basis for enhanced production of sulfur-containing defense compounds in Arabidopsis thaliana upon inoculation with Alternaria brassicicola

Cited by 19 publications

References 17 publications

Spatial gene expression analysis in tomato hypocotyls suggests cysteine as key precursor of vascular sulfur accumulation implicated in Verticillium dahliae defense

Spatial gene expression analysis in tomato hypocotyls suggests cysteine as key precursor of vascular sulfur accumulation implicated in Verticillium dahliae defense

Sulfate availability affects ABA levels and germination response to ABA and salt stress in Arabidopsis thaliana

Isobaric tags for relative and absolute quantification‐based proteomic analysis of Puccinellia tenuiflora inoculated with arbuscular mycorrhizal fungi reveal stress response mechanisms in alkali‐degraded soil

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