Biochemical Principles and Functional Aspects of Pipecolic Acid Biosynthesis in Plant Immunity

Hartmann, Michael; Kim, Denis; Bernsdorff, Friederike; Ajami-Rashidi, Ziba; Scholten, Nicola; Schreiber, Stefan; Zeier, Tatyana; Schuck, Stefan; Reichel-Deland, Vanessa; Zeier, Jürgen

doi:10.1104/pp.17.00222

Cited by 118 publications

(141 citation statements)

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“…Pipecolic acid (Pip), an L-Lys-derived nonprotein amino acid (Hartmann et al, 2017), is another SAR regulatory metabolite that accumulates in response to pathogen inoculation (Návarová et al, 2012). Unlike in the case of SA, FL tended to promote Pip accumulation in both Young and Mature leaves but especially the latter (Supplemental Fig.…”

Section: Highly Up-regulated Genes Under Flmentioning

confidence: 99%

Fluctuating Light Interacts with Time of Day and Leaf Development Stage to Reprogram Gene Expression

et al. 2019

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Natural light environments are highly variable. Flexible adjustment between light energy utilization and photoprotection is therefore of vital importance for plant performance and fitness in the field. Short-term reactions to changing light intensity are triggered inside chloroplasts and leaves within seconds to minutes, whereas long-term adjustments proceed over hours and days, integrating multiple signals. While the mechanisms of long-term acclimation to light intensity have been studied by changing constant growth light intensity during the day, responses to fluctuating growth light intensity have rarely been inspected in detail. We performed transcriptome profiling in Arabidopsis (Arabidopsis thaliana) leaves to investigate long-term gene expression responses to fluctuating light (FL). In particular, we examined whether responses differ between young and mature leaves or between morning and the end of the day. Our results highlight global reprogramming of gene expression under FL, including that of genes related to photoprotection, photosynthesis, and photorespiration and to pigment, prenylquinone, and vitamin metabolism. The FL-induced changes in gene expression varied between young and mature leaves at the same time point and between the same leaves in the morning and at the end of the day, indicating interactions of FL acclimation with leaf development stage and time of day. Only 46 genes were up-or down-regulated in both young and mature leaves at both time points. Combined analyses of gene coexpression and cis-elements pointed to a role of the circadian clock and light in coordinating the acclimatory responses of functionally related genes. Our results also suggest a possible cross talk between FL acclimation and systemic acquired resistance-like gene expression in young leaves.Adjustments of photosynthetic light energy utilization and photoprotection to changing light intensity are triggered over different time scales. Rapid changes (seconds to minutes) are induced inside chloroplasts by reduction of electron transport chain or upon formation of a [H + ] gradient (DpH) across the thylakoid membrane. Short-term responses have been studied intensively to unveil various regulatory mechanisms involved therein. Reduction of the plastoquinone (PQ) pool by preferential excitation of PSII relative to PSI, for example, leads to activation of thylakoid protein kinase STN7, which phosphorylates PSII light-harvesting complex (LHC) to trigger its displacement from PSII to PSI in a process termed state transition (Bellafiore et al., 2005). Light-dependent acidification of thylakoid lumen protonates the PSBS protein to quickly induce thermal energy dissipation (or nonphotochemical quenching [NPQ]) and thus down-regulate PSII (Li et al., 2000). Lumen acidification also activates a xanthophyll-cycle enzyme, violaxanthin deepoxidase (VDE), to convert violaxanthin to antheraxanthin and zeaxanthin, which enhances NPQ (Niyogi et al., 1998). Furthermore, alternative electron (e 2 ) flows (e.g. waterwater cycle and cyclic e 2...

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Section: Highly Up-regulated Genes Under Flmentioning

confidence: 99%

Fluctuating Light Interacts with Time of Day and Leaf Development Stage to Reprogram Gene Expression

et al. 2019

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“…Pip is biosynthesized in dependence of AGD2‐LIKE DEFENSE RESPONSE PROTEIN 1 ( ALD1 ), a defense gene upregulated systemically in the foliage upon localized leaf inoculation (Song et al ., ; Návarová et al ., ). ALD1 functions as an l ‐Lys α‐aminotransferase and converts l ‐Lys to the cyclic, unsaturated intermediate 2,3‐dehydropipecolic acid, which is in turn reduced to Pip by SAR‐DEFICIENT 4 ( SARD4 ) and a further reductase activity (Ding et al ., ; Hartmann et al ., ). Pip exerts its SAR‐activating capacity in dependence of the essential SAR player FLAVIN‐DEPENDENT‐MONOOXYGENASE 1 ( FMO1 ), which is systemically expressed in SAR‐induced plants (Mishina and Zeier, ; Návarová et al ., ).…”

Section: Introductionmentioning

confidence: 97%

A critical role for Arabidopsis MILDEW RESISTANCE LOCUS O2 in systemic acquired resistance

et al. 2018

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Members of the MILDEW RESISTANCE LOCUS O (MLO) gene family confer susceptibility to powdery mildews in different plant species, and their existence therefore seems to be disadvantageous for the plant. We recognized that expression of the Arabidopsis MLO2 gene is induced after inoculation with the bacterial pathogen Pseudomonas syringae, promoted by salicylic acid (SA) signaling, and systemically enhanced in the foliage of plants exhibiting systemic acquired resistance (SAR). Importantly, distinct mlo2 mutant lines were unable to systemically increase resistance to bacterial infection after inoculation with P. syringae, indicating that the function of MLO2 is necessary for biologically induced SAR in Arabidopsis. Our data also suggest that the close homolog MLO6 has a supportive but less critical role in SAR. In contrast to SAR, basal resistance to bacterial infection was not affected in mlo2. Remarkably, SAR-defective mlo2 mutants were still competent in systemically increasing the levels of the SAR-activating metabolites pipecolic acid (Pip) and SA after inoculation, and to enhance SAR-related gene expression in distal plant parts. Furthermore, although MLO2 was not required for SA- or Pip-inducible defense gene expression, it was essential for the proper induction of disease resistance by both SAR signals. We conclude that MLO2 acts as a critical downstream component in the execution of SAR to bacterial infection, being required for the translation of elevated defense responses into disease resistance. Moreover, our data suggest a function for MLO2 in the activation of plant defense priming during challenge by P. syringae.

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“…SAR confers broad-spectrum immunity and is triggered by a pathogen-inducible L-Lys catabolic pathway that produces the nonprotein amino acid pipecolic acid (Pip) and its oxidized derivative N-hydroxypipecolic acid (NHP). NHP accumulation is necessary for SAR and the associated defense-priming phenomenon, and a positive interplay between NHP and SA ensures the strong resistance elevation of SAR-induced plants (Návarová et al, 2012;Bernsdorff et al, 2016;Hartmann et al, 2017. The defensive proteins ENHANCED DISEASE SUSCEPTIBILITY1 (EDS1) and PHYTOALEXIN-DE-FICIENT4 (PAD4) are important components of PTI, ETI, and SAR, and they positively regulate the induction of both SA and NHP biosynthesis (Jirage et al, 1999;Feys et al, 2001;Wiermer et al, 2005;Hartmann and Zeier, 2019).…”

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A Role for Tocopherol Biosynthesis in Arabidopsis Basal Immunity to Bacterial Infection

et al. 2019

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ORCID IDs: 0000-0003-4828-958X (M.H.); 0000-0002-9532-8687 (N.S.); 0000-0002-8703-5403 (J.Z.).Tocopherols are lipid-soluble antioxidants synthesized in plastids of plants and other photosynthetic organisms. The four known tocopherols, a-, b-, g-, and d-tocopherol, differ in number and position of methyl groups on their chromanol head group. In unstressed Arabidopsis (Arabidopsis thaliana) leaves, a-tocopherol constitutes the main tocopherol form, whereas seeds predominantly contain g-tocopherol. Here, we show that inoculation of Arabidopsis leaves with the bacterial pathogen Pseudomonas syringae induces the expression of genes involved in early steps of tocopherol biosynthesis and triggers strong accumulation of g-tocopherol, moderate production of d-tocopherol, and generation of the benzoquinol precursors of tocopherols. The pathogen-inducible biosynthesis of tocopherols is promoted by the immune regulators ENHANCED DISEASE SUSCEPTIBILITY1 and PHYTOALEXIN-DEFICIENT4. In addition, tocopherols accumulate in response to bacterial flagellin and reactive oxygen species. By quantifying tocopherol forms in inoculated wild-type plants and biosynthetic pathway mutants, we provide biochemical insights into the pathogen-inducible tocopherol pathway. Notably, vitamin E deficient2 (vte2) mutant plants, which are compromised in both tocopherol and benzoquinol precursor accumulation, exhibit increased susceptibility toward compatible P. syringae and possess heightened levels of markers of lipid peroxidation after bacterial infection. The deficiency of triunsaturated fatty acids in vte2-1 fatty acid desaturase3-2 (fad3-2) fad7-2 fad8 quadruple mutants prevents increased lipid peroxidation in the vte2 background and restores pathogen resistance to wild-type levels. Therefore, the tocopherol biosynthetic pathway positively influences salicylic acid accumulation and guarantees effective basal resistance of Arabidopsis against compatible P. syringae, possibly by protecting leaves from the pathogen-induced oxidation of trienoic fatty acid-containing lipids.

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Biochemical Principles and Functional Aspects of Pipecolic Acid Biosynthesis in Plant Immunity

Cited by 118 publications

References 84 publications

Fluctuating Light Interacts with Time of Day and Leaf Development Stage to Reprogram Gene Expression

Fluctuating Light Interacts with Time of Day and Leaf Development Stage to Reprogram Gene Expression

A critical role for Arabidopsis MILDEW RESISTANCE LOCUS O2 in systemic acquired resistance

A Role for Tocopherol Biosynthesis in Arabidopsis Basal Immunity to Bacterial Infection

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