N-hydroxypipecolic acid induces systemic acquired resistance and transcriptional reprogramming via TGA transcription factors.


Journal

Plant, cell & environment
ISSN: 1365-3040
Titre abrégé: Plant Cell Environ
Pays: United States
ID NLM: 9309004

Informations de publication

Date de publication:
06 2023
Historique:
received: 18 02 2022
accepted: 12 02 2023
medline: 1 5 2023
pubmed: 16 2 2023
entrez: 15 2 2023
Statut: ppublish

Résumé

N-hydroxypipecolic acid (NHP) accumulates in pathogen-inoculated and distant leaves of the Arabidopsis shoot and induces systemic acquired resistance (SAR) in dependence of the salicylic acid (SA) receptor NPR1. We report here that SAR triggered by exogenous NHP treatment requires the function of the transcription factors TGA2/5/6 in addition to NPR1, and is further positively affected by TGA1/4. Consistently, a tga2/5/6 triple knockout mutant is fully impaired in NHP-induced SAR gene expression, while a tga1/4 double mutant shows an attenuated, partial transcriptional response to NHP. Moreover, tga2/5/6 and tga1/4 exhibited fully and strongly impaired pathogen-triggered SAR, respectively, while SA-induced resistance was more moderately compromised in both lines. At the same time, tga2/5/6 was not and tga1/4 only partially impaired in the accumulation of NHP and SA at sites of bacterial attack. Strikingly, SAR gene expression in the systemic tissue induced by local bacterial inoculation or locally applied NHP fully required functional TGA2/5/6 and largely depended on TGA1/4 factors. The systemic accumulation of NHP and SA was attenuated but not abolished in the SAR-compromised and transcriptionally blocked tga mutants, suggesting their transport from inoculated to systemic tissue. Our results indicate the existence of a critical TGA- and NPR1-dependent transcriptional module that mediates the induction of SAR and systemic defence gene expression by NHP.

Identifiants

pubmed: 36790086
doi: 10.1111/pce.14572
doi:

Substances chimiques

Arabidopsis Proteins 0
N-hydroxypipecolic acid 0
Transcription Factors 0
Pipecolic Acids 0
Salicylic Acid O414PZ4LPZ

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1900-1920

Informations de copyright

© 2023 The Authors. Plant, Cell & Environment published by John Wiley & Sons Ltd.

Références

Bauer, S., Mekonnen, D.W., Hartmann, M., Yildiz, I., Janowski, R., Lange, B. et al. (2021) UGT76B1, a promiscuous hub of small molecule-based immune signaling, glucosylates N-hydroxypipecolic acid, and balances plant immunity. The Plant Cell, 33, 714-734.
Benjamini, Y. & Hochberg, Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society: Series B (Methodological), 57, 289-300.
Bernsdorff, F., Döring, A.-C., Gruner, K., Schuck, S., Bräutigam, A. & Zeier, J. (2016) Pipecolic acid orchestrates plant systemic acquired resistance and defense priming via salicylic acid-dependent and -independent pathways. The Plant Cell, 28, 102-129.
Blanco, F., Salinas, P., Cecchini, N.M., Jordana, X., Van Hummelen, P., Alvarez, M.E. et al. (2009) Early genomic responses to salicylic acid in Arabidopsis. Plant Molecular Biology, 70, 79-102.
Budimir, J., Treffon, K., Nair, A., Thurow, C. & Gatz, C. (2021) Redox-active cysteines in TGACG-BINDING FACTOR 1 (TGA1) do not play a role in salicylic acid or pathogen-induced expression of TGA1-regulated target genes in Arabidopsis thaliana. New Phytologist, 230, 2420-2432.
Cai, J., Jozwiak, A., Holoidovsky, L., Meijler, M.M., Meir, S., Rogachev, I. et al. (2021) Glycosylation of N-hydroxy-pipecolic acid equilibrates between systemic acquired resistance response and plant growth. Molecular Plant, 14, 440-455.
Cao, H., Glazebrook, J., Clarke, J.D., Volko, S. & Dong, X. (1997) The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell, 88, 57-63.
Chen, Y.-C., Holmes, E.C., Rajniak, J., Kim, J.-G., Tang, S., Fischer, C.R. et al. (2018) N-hydroxy-pipecolic acid is a mobile metabolite that induces systemic disease resistance in Arabidopsis. Proceedings of the National Academy of Sciences, 115, E4920-E4929.
Czechowski, T., Stitt, M., Altmann, T., Udvardi, M.K. & Scheible, W. (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiology, 139, 5-17.
Davletova, S., Schlauch, K., Coutu, J. & Mittler, R. (2005) The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiology, 139, 847-856.
Després, C., Chubak, C., Rochon, A., Clark, R., Bethune, T., Desveaux, D. et al. (2003) The Arabidopsis NPR1 disease resistance protein is a novel cofactor that confers redox regulation of DNA binding activity to the basic domain/leucine zipper transcription factor TGA1. The Plant Cell, 15, 2181-2191.
Ding, P. & Ding, Y. (2020) Stories of salicylic acid: a plant defense hormone. Trends in Plant Science, 25, 549-565.
Ding, P., Rekhter, D., Ding, Y., Feussner, K., Busta, L., Haroth, S. et al. (2016) Characterization of a pipecolic acid biosynthesis pathway required for systemic acquired resistance. The Plant Cell, 28, 2603-2615.
Ding, Y., Dommel, M.R., Wang, C., Li, Q., Zhao, Q., Zhang, X. et al. (2020) Differential quantitative requirements for NPR1 between basal immunity and systemic acquired resistance in Arabidopsis thaliana. Frontiers in Plant Science, 11, 570422.
Ding, Y., Sun, T., Ao, K., Peng, Y., Zhang, Y., Li, X. et al. (2018) Opposite roles of salicylic acid receptors NPR1 and NPR3/NPR4 in transcriptional regulation of plant immunity. Cell, 173, 1454-1467.
Fode, B., Siemsen, T., Thurow, C., Weigel, R. & Gatz, C. (2008) The Arabidopsis GRAS protein SCL14 interacts with class II TGA transcription factors and is essential for the activation of stress-inducible promoters. The Plant Cell, 20, 3122-3135.
Fu, Z.Q. & Dong, X. (2013) Systemic acquired resistance: turning local infection into global defense. Annual Review of Plant Biology, 64, 839-863.
Gatz, C. (2013) From pioneers to team players: TGA transcription factors provide a molecular link between different stress pathways. Molecular Plant-Microbe Interactions, 26, 151-159.
Glazebrook, J. (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annual Review of Phytopathology, 43, 205-227.
Goda, H., Sasaki, E., Akiyama, K., Maruyama-Nakashita, A., Nakabayashi, K., Li, W. et al. (2008) The AtGenExpress hormone and chemical treatment data set: experimental design, data evaluation, model data analysis and data access. The Plant Journal, 55, 526-542.
Gruner, K., Griebel, T., Návarová, H., Attaran, E. & Zeier, J. (2013) Reprogramming of plants during systemic acquired resistance. Frontiers in Plant Science, 4, 252.
Gruner, K., Zeier, T., Aretz, C. & Zeier, J. (2018) A critical role for Arabidopsis MILDEW RESISTANCE LOCUS O2 in systemic acquired resistance. The Plant Journal, 94, 1064-1082.
Hartmann, M., Kim, D., Bernsdorff, F., Ajami-Rashidi, Z., Scholten, N., Schreiber, S. et al. (2017) Biochemical principles and functional aspects of pipecolic acid biosynthesis in plant immunity. Plant Physiology, 174, 124-153.
Hartmann, M. & Zeier, J. (2018) l-lysine metabolism to N-hydroxypipecolic acid: an integral immune-activating pathway in plants. The Plant Journal, 96, 5-21.
Hartmann, M. & Zeier, J. (2019) N-hydroxypipecolic acid and salicylic acid: a metabolic duo for systemic acquired resistance. Current Opinion in Plant Biology, 50, 44-57.
Hartmann, M., Zeier, T., Bernsdorff, F., Reichel-Deland, V., Kim, D., Hohmann, M. et al. (2018) Flavin monooxygenase-generated N-hydroxypipecolic acid is a critical element of plant systemic immunity. Cell, 173, 456-469.
Herrera-Vásquez, A., Carvallo, L., Blanco, F., Tobar, M., Villarroel-Candia, E., Vicente-Carbajosa, J. et al. (2015) Transcriptional control of glutaredoxin GRXC9 expression by a salicylic acid-dependent and NPR1-independent pathway in Arabidopsis. Plant Molecular Biology Reporter, 33, 624-637.
Herrera-Vásquez, A., Fonseca, A., Ugalde, J.M., Lamig, L., Seguel, A., Moyano, T.C. et al. (2021) TGA class II transcription factors are essential to restrict oxidative stress in response to UV-B stress in Arabidopsis. Journal of Experimental Botany, 72, 1891-1905.
Holmes, E.C., Chen, Y.-C., Mudgett, M.B. & Sattely, E.S. (2021) Arabidopsis UGT76B1 glycosylates N-hydroxy-pipecolic acid and inactivates systemic acquired resistance in tomato. The Plant Cell, 33, 750-765.
Holmes, E.C., Chen, Y.-C., Sattely, E.S. & Mudgett, M.B. (2019) An engineered pathway for N-hydroxy-pipecolic acid synthesis enhances systemic acquired resistance in tomato. Science Signaling, 12, eaay306. https://doi.org/10.1126/scisignal.aay3066
Huang, W., Wang, Y., Li, X. & Zhang, Y. (2020) Biosynthesis and regulation of salicylic acid and N-hydroxypipecolic acid in plant immunity. Molecular Plant, 13, 31-41.
Johnson, C., Boden, E. & Arias, J. (2003) Salicylic acid and NPR1 induce the recruitment of trans-activating TGA factors to a defense gene promoter in Arabidopsis. The Plant Cell, 15, 1846-1858.
Jung, H.W., Tschaplinski, T.J., Wang, L., Glazebrook, J. & Greenberg, J.T. (2009) Priming in systemic plant immunity. Science, 324, 89-91.
Kesarwani, M., Yoo, J. & Dong, X. (2007) Genetic interactions of TGA transcription factors in the regulation of pathogenesis-related genes and disease resistance in Arabidopsis. Plant Physiology, 144, 336-346.
Lim, G.H., Liu, H., Yu, K., Liu, R., Shine, M.B., Fernandez, J. et al. (2020) The plant cuticle regulates apoplastic transport of salicylic acid during systemic acquired resistance. Sci Adv, 6, eaaz0478.
Liu, Y., Sun, T., Sun, Y., Zhang, Y., Radojičić, A., Ding, Y. et al. (2020) Diverse roles of the salicylic acid receptors NPR1 and NPR3/NPR4 in plant immunity. The Plant Cell, 32, 4002-4016.
Mishina, T.E., Griebel, T., Geuecke, M., Attaran, E. & Zeier, J. (2008) New insights into the molecular events underlying systemic acquired resistance. In: Lorito, M., Woo, S.L. & Scala, F. (Eds.) Biology of plant-microbe interactions, 6. St. Paul: International Society for Molecular Plant-Microbe Interactions.
Mishina, T.E. & Zeier, J. (2006) The Arabidopsis flavin-dependent monooxygenase FMO1 is an essential component of biologically induced systemic acquired resistance. Plant Physiology, 141, 1666-1675.
Mohnike, L., Rekhter, D., Huang, W., Feussner, K., Tian, H., Herrfurth, C. et al. (2021) The glycosyltransferase UGT76B1 modulates N-hydroxy-pipecolic acid homeostasis and plant immunity, Plant Cell, 33, 735-749.
Mou, Z., Fan, W. & Dong, X. (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell, 113, 935-944.
Murahashi, S.-I. & Shiota, T. (1987) Short-step synthesis of amino acids and N-hydroxyamino acids from amines. Tetrahedron Letters, 28, 6469-6472.
Nair, A., Goyal, I., Voß, E., Mrozek, P., Prajapati, S., Thurow, C. et al. (2021) N-hydroxypipecolic acid-induced transcription requires the salicylic acid signaling pathway at basal SA levels. Plant Physiology, 187, 2803-2819.
Návarová, H., Bernsdorff, F., Döring, A.-C. & Zeier, J. (2012) Pipecolic acid, an endogenous mediator of defense amplification and priming, is a critical regulator of inducible plant immunity. The Plant Cell, 24, 5123-5141.
Nawrath, C., Métraux, J.P., Nawrath, C. & Metraux, J.P. (1999) Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. The Plant Cell, 11, 1393-1404.
Ndamukong, I., Abdallat, A.A., Thurow, C., Fode, B., Zander, M., Weigel, R. et al. (2007) SA-inducible Arabidopsis glutaredoxin interacts with TGA factors and suppresses JA-responsive PDF1.2 transcription. The Plant Journal, 50, 128-139.
Rasmussen, J.B., Hammerschmidt, R. & Zook, M.N. (1991) Systemic induction of salicylic acid accumulation in cucumber after inoculation with Pseudomonas syringae pv syringae. Plant Physiology, 97, 1342-1347.
Rekhter, D., Lüdke, D., Ding, Y., Feussner, K., Zienkiewicz, K., Lipka, V. et al. (2019) Isochorismate-derived biosynthesis of the plant stress hormone salicylic acid. Science, 365, 498-502.
Schnake, A., Hartmann, M., Schreiber, S., Malik, J., Brahmann, L., Yildiz, I. et al. (2020) Inducible biosynthesis and immune function of the systemic acquired resistance inducer N-hydroxypipecolic acid in monocotyledonous and dicotyledonous plants. Journal of Experimental Botany, 71, 6444-6459.
Shah, J., Tsui, F. & Klessig, D.F. (1997) Characterization of a salicylic acid-insensitive mutant (sai1) of Arabidopsis thaliana, identified in a selective screen utilizing the SA-inducible expression of the tms2 gene. Molecular Plant-Microbe Interactions, 10, 69-78.
Shah, J. & Zeier, J. (2013) Long-distance communication and signal amplification in systemic acquired resistance. Frontiers in Plant Science, 4, 30.
Shearer, H.L., Cheng, Y.T., Wang, L., Liu, J., Boyle, P., Després, C. et al. (2012) Arabidopsis clade I TGA transcription factors regulate plant defenses in an NPR1-independent fashion. Molecular Plant-Microbe Interactions®, 25, 1459-1468.
Song, J.T., Lu, H., McDowell, J.M. & Greenberg, J.T. (2004) A key role for ALD1 in activation of local and systemic defenses in Arabidopsis. The Plant Journal, 40, 200-212.
Spoel, S.H., Koornneef, A., Claessens, S.M.C., Korzelius, J.P., Van Pelt, J.A., Mueller, M.J. et al. (2003) NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. The Plant Cell, 15, 760-770.
Sticher, L., Mauch-Mani, B. & Métraux, J. (1997) Systemic acquired resistance. Annual Review of Phytopathology, 35, 235-270.
Stotz, H.U., Mueller, S., Zoeller, M., Mueller, M.J. & Berger, S. (2013) TGA transcription factors and jasmonate-independent COI1 signalling regulate specific plant responses to reactive oxylipins. Journal of Experimental Botany, 64, 963-975.
Sun, T., Busta, L., Zhang, Q., Ding, P., Jetter, R. & Zhang, Y. (2018) TGACG-BINDING FACTOR 1 (TGA1) and TGA4 regulate salicylic acid and pipecolic acid biosynthesis by modulating the expression of SYSTEMIC ACQUIRED RESISTANCE DEFICIENT 1 (SARD1) and CALMODULIN-BINDING PROTEIN 60g (CBP60g). New Phytologist, 217, 344-354.
Sun, T., Zhang, Y., Li, Y., Zhang, Q., Ding, Y. & Zhang, Y. (2015) ChIP-seq reveals broad roles of SARD1 and CBP60g in regulating plant immunity. Nature Communications, 6, 10159.
Thibaud-Nissen, F., Wu, H., Richmond, T., Redman, J.C., Johnson, C., Green, R. et al. (2006) Development of Arabidopsis whole-genome microarrays and their application to the discovery of binding sites for the TGA2 transcription factor in salicylic acid-treated plants. The Plant Journal, 47, 152-162.
Torrens-Spence, M.P., Bobokalonova, A., Carballo, V., Glinkerman, C.M., Pluskal, T., Shen, A. et al. (2019) PBS3 and EPS1 complete salicylic acid biosynthesis from isochorismate in Arabidopsis. Molecular Plant, 12, 1577-1586.
Uknes, S., Mauch-Mani, B., Moyer, M., Potter, S., Williams, S., Dincher, S. et al. (1992) Acquired resistance in Arabidopsis. Plant Cell, 4, 645-656.
Vernooij, B., Friedrich, L., Morse, A., Reist, R., Kolditz-Jawhar, R., Ward, E. et al. (1994) Salicylic acid is not the translocated signal responsible for inducing systemic acquired resistance but is required in signal transduction. The Plant Cell, 6, 959-965.
Vlot, A.C., Sales, J.H., Lenk, M., Bauer, K., Brambilla, A., Sommer, A. et al. (2021) Systemic propagation of immunity in plants. New Phytologist, 229, 1234-1250.
Wang, L., Mitra, R.M., Hasselmann, K.D., Sato, M., Lenarz-Wyatt, L., Cohen, J.D. et al. (2008) The genetic network controlling the Arabidopsis transcriptional response to Pseudomonas syringae pv. maculicola: roles of major regulators and the phytotoxin coronatine. Molecular Plant-Microbe Interactions®, 21, 1408-1420.
Wildermuth, M.C., Dewdney, J., Wu, G. & Ausubel, F.M. (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature, 414, 562-565.
Wu, Y., Zhang, D., Chu, J.Y., Boyle, P., Wang, Y., Brindle, I.D. et al. (2012) The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid. Cell Reports, 1, 639-647.
Xu, B., Fan, Z., Lei, Y., Ping, Y., Jaisi, A. & Xiao, Y. (2018) Insights into pipecolic acid biosynthesis in Huperzia serrata. Organic Letters, 20, 2195-2198.
Yildiz, I., Mantz, M., Hartmann, M., Zeier, T., Kessel, J., Thurow, C. et al. (2021) The mobile SAR signal N-hydroxypipecolic acid induces NPR1-dependent transcriptional reprogramming and immune priming. Plant Physiology, 186, 1679-1705.
Zander, M., La Camera, S., Lamotte, O., Métraux, J.P. & Gatz, C. (2010) Arabidopsis thaliana class-II TGA transcription factors are essential activators of jasmonic acid/ethylene-induced defense responses. The Plant Journal, 61, 200-210.
Zeier, J. (2021) Metabolic regulation of systemic acquired resistance. Current Opinion in Plant Biology, 62, 102050.
Zhang, K., Halitschke, R., Yin, C., Liu, C.-J. & Gan, S.-S. (2013) Salicylic acid 3-hydroxylase regulates Arabidopsis leaf longevity by mediating salicylic acid catabolism. Proceedings of the National Academy of Sciences, 110, 14807-14812.
Zhang, Y., Tessaro, M.J., Lassner, M. & Li, X. (2003) Knockout analysis of Arabidopsis transcription factors TGA2, TGA5, and TGA6 reveals their redundant and essential roles in systemic acquired resistance. The Plant Cell, 15, 2647-2653.
Zhang, Y., Zhao, L., Zhao, J., Li, Y., Wang, J., Guo, R. et al. (2017) S5H/DMR6 encodes a salicylic acid 5-hydroxylase that fine-tunes salicylic acid homeostasis. Plant Physiology, 175, 1082-1093.
Zhou, J.-M., Trifa, Y., Silva, H., Pontier, D., Lam, E., Shah, J. et al. (2000) NPR1 differentially interacts with members of the TGA/OBF family of transcription factors that bind an element of the PR-1 gene required for induction by salicylic acid. Molecular Plant-Microbe Interactions®, 13, 191-202.

Auteurs

Ipek Yildiz (I)

Department of Biology, Institute for Molecular Ecophysiology of Plants, Heinrich Heine University, Düsseldorf, Germany.

Marlene Gross (M)

Department of Biology, Institute for Molecular Ecophysiology of Plants, Heinrich Heine University, Düsseldorf, Germany.

Denise Moser (D)

Department of Biology, Institute for Molecular Ecophysiology of Plants, Heinrich Heine University, Düsseldorf, Germany.

Patrick Petzsch (P)

Biological and Medical Research Center (BMFZ), Medical Faculty, Heinrich Heine University, Düsseldorf, Germany.

Karl Köhrer (K)

Biological and Medical Research Center (BMFZ), Medical Faculty, Heinrich Heine University, Düsseldorf, Germany.

Jürgen Zeier (J)

Department of Biology, Institute for Molecular Ecophysiology of Plants, Heinrich Heine University, Düsseldorf, Germany.
Cluster of Excellence on Plant Sciences (CEPLAS), Heinrich Heine University, Düsseldorf, Germany.

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