UGT76B1, a promiscuous hub of small molecule-based immune signaling, glucosylates N-hydroxypipecolic acid, and balances plant immunity

Bauer, Sibylle; Mekonnen, Dereje Worku; Hartmann, Michael; Yildiz, Ipek; Janowski, Robert; Lange, Birgit; Geist, Birgit; Zeier, Jürgen; Schäffner, Anton R.

doi:10.1093/plcell/koaa044

Cited by 69 publications

(72 citation statements)

References 59 publications

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“…Overexpression of AtUGT76D1 leads to high SA accumulation, upregulation of defense genes and the autoactive HR phenotype, while the immune responses were compromised when AtUGT76D1 is knocked out implying that AtUGT76D1 is a positive regulator in plant innate immunity (Huang et al, 2018). Interestingly, AtUGT76B1, a close homolog which had 38.8% similarity of amino acid with AtUGT76D1, was recently found to use N-hydroxy-pipecolic acid (NHP) as substrate and act in systemic-acquired resistance (Bauer et al, 2021;Holmes et al, 2021;Mohnike et al, 2021). Loss-of-function mts of AtUGT76B1 confer a dwarf phenotype and constitutive defense response, with high NHP and SA accumulation and enhanced disease resistance to PstDC3000 (Bauer et al, 2021;Mohnike et al, 2021).…”

Section: Sa and Glycosylation Of Sa Derivatives May Play A Role In Defense Responsementioning

confidence: 99%

“…Interestingly, AtUGT76B1, a close homolog which had 38.8% similarity of amino acid with AtUGT76D1, was recently found to use N-hydroxy-pipecolic acid (NHP) as substrate and act in systemic-acquired resistance (Bauer et al, 2021;Holmes et al, 2021;Mohnike et al, 2021). Loss-of-function mts of AtUGT76B1 confer a dwarf phenotype and constitutive defense response, with high NHP and SA accumulation and enhanced disease resistance to PstDC3000 (Bauer et al, 2021;Mohnike et al, 2021). The 2,5-DHBA glucosides were also accumulated in tomato and cucumber after infection with the pathogen, citrus exocortis viroid (CEVd) and prunus necrotic ringspot virus (PNRSV) (isolate NCM1), respectively (Fayos et al, 2006).…”

Section: Sa and Glycosylation Of Sa Derivatives May Play A Role In Defense Responsementioning

confidence: 99%

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Multi-Omics Analyses Reveal the Regulatory Network and the Function of ZmUGTs in Maize Defense Response

Wang

et al. 2021

Front. Plant Sci.

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Maize is one of the major crops in the world; however, diseases caused by various pathogens seriously affect its yield and quality. The maize Rp1-D21 mutant (mt) caused by the intragenic recombination between two nucleotide-binding, leucine-rich repeat (NLR) proteins, exhibits autoactive hypersensitive response (HR). In this study, we integrated transcriptomic and metabolomic analyses to identify differentially expressed genes (DEGs) and differentially accumulated metabolites (DAMs) in Rp1-D21 mt compared to the wild type (WT). Genes involved in pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI) and effector-triggered immunity (ETI) were enriched among the DEGs. The salicylic acid (SA) pathway and the phenylpropanoid biosynthesis pathway were induced at both the transcriptional and metabolic levels. The DAMs identified included lipids, flavones, and phenolic acids, including 2,5-DHBA O-hexoside, the production of which is catalyzed by uridinediphosphate (UDP)-dependent glycosyltransferase (UGT). Four maize UGTs (ZmUGTs) homologous genes were among the DEGs. Functional analysis by transient co-expression in Nicotiana benthamiana showed that ZmUGT9250 and ZmUGT5174, but not ZmUGT9256 and ZmUGT8707, partially suppressed the HR triggered by Rp1-D21 or its N-terminal coiled-coil signaling domain (CCD21). None of the four ZmUGTs interacted physically with CCD21 in yeast two-hybrid or co-immunoprecipitation assays. We discuss the possibility that ZmUGTs might be involved in defense response by regulating SA homeostasis.

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Section: Sa and Glycosylation Of Sa Derivatives May Play A Role In Defense Responsementioning

confidence: 99%

Section: Sa and Glycosylation Of Sa Derivatives May Play A Role In Defense Responsementioning

confidence: 99%

Multi-Omics Analyses Reveal the Regulatory Network and the Function of ZmUGTs in Maize Defense Response

Wang

et al. 2021

Front. Plant Sci.

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“…The impact of SA on growth and development is well-documented (Carviel et al, 2009;Rivas-San Vicente and Plasencia, 2011; Frontiers in Plant Science | www.frontiersin.org 5 March 2022 | Volume 13 | Article 841688 Carella et al, 2014;van Butselaar and Van den Ackerveken, 2020;Pokotylo et al, 2021); however, the effect of NHP is only starting to be explored (Figure 2). For example, altering free NHP levels by inactivating UGT76B1-mediated glycosylation to NHPG can affect plant growth by decreasing rosette size and biomass (Bauer et al, 2021;Cai et al, 2021;Mohnike et al, 2021). Inhibited plant development and enhanced SAR was observed in the ugt76b1 mutant, while overexpression led to opposite phenotypes (Bauer et al, 2021;Cai et al, 2021;Mohnike et al, 2021).…”

Section: Mechanistic Impact Of Nhp On Plant Growth and Developmentmentioning

confidence: 99%

Salicylic Acid and N-Hydroxypipecolic Acid at the Fulcrum of the Plant Immunity-Growth Equilibrium

2022

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Salicylic acid (SA) and N-hydroxypipecolic acid (NHP) are two central plant immune signals involved in both resistance at local sites of pathogen infection (basal resistance) and at distal uninfected sites after primary infection (systemic acquired resistance). Major discoveries and advances have led to deeper understanding of their biosynthesis and signaling during plant defense responses. In addition to their well-defined roles in immunity, recent research is emerging on their direct mechanistic impacts on plant growth and development. In this review, we will first provide an overview of how SA and NHP regulate local and systemic immune responses in plants. We will emphasize how these two signals are mutually potentiated and are convergent on multiple aspects—from biosynthesis to homeostasis, and from signaling to gene expression and phenotypic responses. We will then highlight how SA and NHP are emerging to be crucial regulators of the growth-defense balance, showcasing recent multi-faceted studies on their metabolism, receptor signaling and direct growth/development-related host targets. Overall, this article reflects current advances and provides future outlooks on SA/NHP biology and their functional significance as central signals for plant immunity and growth. Because global climate change will increasingly influence plant health and resilience, it is paramount to fundamentally understand how these two tightly linked plant signals are at the nexus of the growth-defense balance.

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“…A series of studies have provided evidence that NHP plays a critical role in SAR induction in different plant species ( Holmes et al, 2019 ; Schnake et al, 2020 ). Recent research illustrates that UDP-dependent glycosyltransferase 76B1 (UGT76B1) inactivates NHP by forming the inactive NHP-N-O-glucoside (NHPG) to rationally control the growth-immunity trade-off in crop plants ( Bauer et al, 2021 ; Cai et al, 2021 ; Holmes et al, 2021 ; Mohnike et al, 2021 ; Zeier, 2021 ).…”

Section: Introductionmentioning

confidence: 99%

Protein Phosphorylation Changes During Systemic Acquired Resistance in Arabidopsis thaliana

Zhou

Tan

et al. 2021

Front. Plant Sci.

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Systemic acquired resistance (SAR) in plants is a defense response that provides resistance against a wide range of pathogens at the whole-plant level following primary infection. Although the molecular mechanisms of SAR have been extensively studied in recent years, the role of phosphorylation that occurs in systemic leaves of SAR-induced plants is poorly understood. We used a data-independent acquisition (DIA) phosphoproteomics platform based on high-resolution mass spectrometry in an Arabidopsis thaliana model to identify phosphoproteins related to SAR establishment. A total of 8011 phosphorylation sites from 3234 proteins were identified in systemic leaves of Pseudomonas syringae pv. maculicola ES4326 (Psm ES4326) and mock locally inoculated plants. A total of 859 significantly changed phosphoproteins from 1119 significantly changed phosphopeptides were detected in systemic leaves of Psm ES4326 locally inoculated plants, including numerous transcription factors and kinases. A variety of defense response-related proteins were found to be differentially phosphorylated in systemic leaves of Psm ES4326 locally inoculated leaves, suggesting that these proteins may be functionally involved in SAR through phosphorylation or dephosphorylation. Significantly changed phosphoproteins were enriched mainly in categories related to response to abscisic acid, regulation of stomatal movement, plant–pathogen interaction, MAPK signaling pathway, purine metabolism, photosynthesis-antenna proteins, and flavonoid biosynthesis. A total of 28 proteins were regulated at both protein and phosphorylation levels during SAR. RT-qPCR analysis revealed that changes in phosphorylation levels of proteins during SAR did not result from changes in transcript abundance. This study provides comprehensive details of key phosphoproteins associated with SAR, which will facilitate further research on the molecular mechanisms of SAR.

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UGT76B1, a promiscuous hub of small molecule-based immune signaling, glucosylates N-hydroxypipecolic acid, and balances plant immunity

Cited by 69 publications

References 59 publications

Multi-Omics Analyses Reveal the Regulatory Network and the Function of ZmUGTs in Maize Defense Response

Multi-Omics Analyses Reveal the Regulatory Network and the Function of ZmUGTs in Maize Defense Response

Salicylic Acid and N-Hydroxypipecolic Acid at the Fulcrum of the Plant Immunity-Growth Equilibrium

Protein Phosphorylation Changes During Systemic Acquired Resistance in Arabidopsis thaliana

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