A root-based N-hydroxypipecolic acid standby circuit to direct immunity and growth of Arabidopsis shoots

Pieterse, C. M. J. et al. Induced systemic resistance by beneficial microbes. Annu. Rev. Phytopathol. 52, 347–375 (2014).

Article 
PubMed 
CAS 

Google Scholar
 

De Kesel, J. et al. The induced resistance lexicon: do’s and don’ts. Trends Plant Sci. 26, 685–691 (2021).

Article 
PubMed 

Google Scholar
 

Fu, Z. Q. & Dong, X. Systemic acquired resistance: turning local infection into global defense. Annu. Rev. Plant Biol. 64, 839–863 (2013).

Article 
PubMed 
CAS 

Google Scholar
 

Durrant, W. E. & Dong, X. Systemic acquired resistance. Annu. Rev. Phytopathol. 42, 185–209 (2004).

Article 
PubMed 
CAS 

Google Scholar
 

Conrath, U., Beckers, G. J. M., Langenbach, C. J. G. & Jaskiewicz, M. R. Priming for enhanced defense. Annu. Rev. Phytopathol. 53, 97–119 (2015).

Article 
PubMed 
CAS 

Google Scholar
 

Vlot, A. C., Klessig, D. F. & Park, S.-W. Systemic acquired resistance: the elusive signal(s). Curr. Opin. Plant Biol. 11, 436–442 (2008).

Article 
PubMed 
CAS 

Google Scholar
 

Vlot, A. C. et al. Systemic propagation of immunity in plants. N. Phytol. 229, 1234–1250 (2021).

Article 
CAS 

Google Scholar
 

Spoel, S. H. & Dong, X. Salicylic acid in plant immunity and beyond. Plant Cell 36, 1451–1464 (2024).

Article 
PubMed 
PubMed Central 

Google Scholar
 

Conrath, U., Pieterse, C. M. J. & Mauch-Mani, B. Priming in plant–pathogen interactions. Trends Plant Sci. 7, 210–216 (2002).

Article 
PubMed 
CAS 

Google Scholar
 

Zeier, J. Metabolic regulation of systemic acquired resistance. Curr. Opin. Plant Biol. 62, 102050 (2021).

Article 
PubMed 
CAS 

Google Scholar
 

Pieterse, C. M. J. et al. Pseudomonas simiae WCS417: star track of a model beneficial rhizobacterium. Plant Soil 461, 245–263 (2021).

Article 
CAS 

Google Scholar
 

Contreras-Cornejo, H. A., Macías-Rodríguez, L., Beltrán-Peña, E., Herrera-Estrella, A. & López-Bucio, J. Trichoderma-induced plant immunity likely involves both hormonal- and camalexin-dependent mechanisms in Arabidopsis thaliana and confers resistance against necrotrophic fungi Botrytis cinerea. Plant Signal. Behav. 6, 1554–1563 (2011).

Article 
PubMed 
PubMed Central 
CAS 

Google Scholar
 

Salas-Marina, M. A. et al. Colonization of Arabidopsis roots by Trichoderma atroviride promotes growth and enhances systemic disease resistance through jasmonic acid/ethylene and salicylic acid pathways. Eur. J. Plant Pathol. 131, 15–26 (2011).

Article 
CAS 

Google Scholar
 

van de Mortel, J. E. et al. Metabolic and transcriptomic changes induced in Arabidopsis by the rhizobacterium Pseudomonas fluorescens SS101. Plant Physiol. 160, 2173–2188 (2012).

Article 
PubMed 
PubMed Central 

Google Scholar
 

Tjamos, S. E., Flemetakis, E., Paplomatas, E. J. & Katinakis, P. Induction of resistance to Verticillium dahliae in Arabidopsis thaliana by the biocontrol agent K-165 and pathogenesis-related proteins gene expression. Mol. Plant Microbe Interact. 18, 555–561 (2005).

Article 
PubMed 
CAS 

Google Scholar
 

Martínez-Medina, A. et al. Deciphering the hormonal signalling network behind the systemic resistance induced by Trichoderma harzianum in tomato. Front. Plant Sci. 4, 206 (2013).

Article 
PubMed 
PubMed Central 

Google Scholar
 

Mathys, J. et al. Genome-wide characterization of ISR induced in Arabidopsis thaliana by Trichoderma hamatum T382 against Botrytis cinerea infection. Front. Plant Sci. 3, 108 (2012).

Article 
PubMed 
PubMed Central 

Google Scholar
 

Sommer, A. et al. A salicylic acid‐associated plant–microbe interaction attracts beneficial Flavobacterium sp. to the Arabidopsis thaliana phyllosphere. Physiol. Plant. 176, e14483 (2024).

Article 
PubMed 
CAS 

Google Scholar
 

Weston, D. J. et al. Pseudomonas fluorescens induces strain-dependent and strain-independent host plant responses in defense networks, primary metabolism, photosynthesis, and fitness. Mol. Plant Microbe Interact. 25, 765–778 (2012).

Article 
PubMed 
CAS 

Google Scholar
 

Hacquard, S. et al. Survival trade-offs in plant roots during colonization by closely related beneficial and pathogenic fungi. Nat. Commun. 7, 11362 (2016).

Article 
PubMed 
PubMed Central 
CAS 

Google Scholar
 

Pérez‐Alonso, M. et al. The calcium sensor CBL7 is required for Serendipita indica‐induced growth stimulation in Arabidopsis thaliana, controlling defense against the endophyte and K+ homoeostasis in the symbiosis. Plant Cell Environ. 45, 3367–3382 (2022).

Article 
PubMed 
PubMed Central 

Google Scholar
 

Martínez-Soto, D., Yu, H., Allen, K. S. & Ma, L.-J. Differential colonization of the plant vasculature between endophytic versus pathogenic Fusarium oxysporum strains. Mol. Plant Microbe Interact. 36, 4–13 (2023).

Article 
PubMed 
PubMed Central 

Google Scholar
 

Brotman, Y. et al. Trichoderma-plant root colonization: escaping early plant defense responses and activation of the antioxidant machinery for saline stress tolerance. PLoS Path. 9, e1003221 (2013).

Article 
CAS 

Google Scholar
 

Bernsdorff, F. et al. Pipecolic acid orchestrates plant systemic acquired resistance and defense priming via salicylic acid-dependent and -independent pathways. Plant Cell 28, 102–129 (2016).

Article 
PubMed 
CAS 

Google Scholar
 

Mishina, T. E. & Zeier, J. Pathogen‐associated molecular pattern recognition rather than development of tissue necrosis contributes to bacterial induction of systemic acquired resistance in Arabidopsis. Plant J. 50, 500–513 (2007).

Article 
PubMed 
CAS 

Google Scholar
 

Hartmann, M. et al. Flavin monooxygenase-generated N-hydroxypipecolic acid is a critical element of plant systemic immunity. Cell 173, 456–469 (2018).

Article 
PubMed 
CAS 

Google Scholar
 

Maldonado, A. M., Doerner, P., Dixon, R. A., Lamb, C. J. & Cameron, R. K. A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature 419, 399–403 (2002).

Article 
PubMed 
CAS 

Google Scholar
 

Jung, H. W., Tschaplinski, T. J., Wang, L., Glazebrook, J. & Greenberg, J. T. Priming in systemic plant immunity. Science 324, 89–91 (2009).

Article 
PubMed 

Google Scholar
 

Chanda, B. et al. Glycerol-3-phosphate is a critical mobile inducer of systemic immunity in plants. Nat. Genet. 43, 421–427 (2011).

Article 
PubMed 
CAS 

Google Scholar
 

Wenig, M. et al. Systemic acquired resistance networks amplify airborne defense cues. Nat. Commun. 10, 3813 (2019).

Article 
PubMed 
PubMed Central 

Google Scholar
 

Park, S.-W., Kaimoyo, E., Kumar, D., Mosher, S. & Klessig, D. F. Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318, 113–116 (2007).

Article 
PubMed 
CAS 

Google Scholar
 

Cai, J. et al. Glycosylation of N-hydroxy-pipecolic acid equilibrates between systemic acquired resistance response and plant growth. Mol. Plant 14, 440–455 (2021).

Article 
PubMed 
CAS 

Google Scholar
 

Bauer, S. et al. UGT76B1, a promiscuous hub of small molecule-based immune signaling, glucosylates N-hydroxypipecolic acid, and balances plant immunity. Plant Cell 33, 714–734 (2021).

Article 
PubMed 
PubMed Central 

Google Scholar
 

Mohnike, L. et al. The glycosyltransferase UGT76B1 modulates N-hydroxy-pipecolic acid homeostasis and plant immunity. Plant Cell 33, 735–749 (2021).

Article 
PubMed 
PubMed Central 

Google Scholar
 

Holmes, E. C., Chen, Y.-C., Mudgett, M. B. & Sattely, E. S. Arabidopsis UGT76B1 glycosylates N-hydroxy-pipecolic acid and inactivates systemic acquired resistance in tomato. Plant Cell 33, 750–765 (2021).

Article 
PubMed 
PubMed Central 

Google Scholar
 

von Saint Paul, V. et al. The Arabidopsis glucosyltransferase UGT76B1 conjugates isoleucic acid and modulates plant defense and senescence. Plant Cell 23, 4124–4145 (2011).

Article 

Google Scholar
 

Yildiz, I. et al. The mobile SAR signal N-hydroxypipecolic acid induces NPR1-dependent transcriptional reprogramming and immune priming. Plant Physiol. 186, 1679–1705 (2021).

Article 
PubMed 
PubMed Central 
CAS 

Google Scholar
 

Löwe, M. et al. N-hydroxypipecolic acid primes plants for enhanced microbial pattern-induced responses. Front. Plant Sci. 14, 1217771 (2023).

Article 
PubMed 
PubMed Central 

Google Scholar
 

Schnake, A. et al. Inducible biosynthesis and immune function of the systemic acquired resistance inducer N-hydroxypipecolic acid in monocotyledonous and dicotyledonous plants. J. Exp. Bot. 71, 6444–6459 (2020).

Article 
PubMed 
PubMed Central 
CAS 

Google Scholar
 

Noutoshi, Y. et al. Novel plant immune-priming compounds identified via high-throughput chemical screening target salicylic acid glucosyltransferases in Arabidopsis. Plant Cell 24, 3795–3804 (2012).

Article 
PubMed 
PubMed Central 
CAS 

Google Scholar
 

Olszak, B. et al. A putative flavin-containing mono-oxygenase as a marker for certain defense and cell death pathways. Plant Sci. 170, 614–623 (2006).

Article 
CAS 

Google Scholar
 

Joglekar, S. et al. Chemical activation of EDS1/PAD4 signaling leading to pathogen resistance in Arabidopsis. Plant Cell Physiol. 59, 1592–1607 (2018).

Article 
PubMed 
CAS 

Google Scholar
 

Ryu, K. H., Huang, L., Kang, H. M. & Schiefelbein, J. Single-cell RNA sequencing resolves molecular relationships among individual plant cells. Plant Physiol. 179, 1444–1456 (2019).

Article 
PubMed 
PubMed Central 
CAS 

Google Scholar
 

Fucile, G. et al. ePlant and the 3D data display initiative: integrative systems biology on the world wide web. PLoS ONE 6, e15237 (2011).

Article 
PubMed 
PubMed Central 
CAS 

Google Scholar
 

Shields, A., Shivnauth, V. & Castroverde, C. D. M. Salicylic acid and N-hydroxypipecolic acid at the fulcrum of the plant immunity–growth equilibrium. Front. Plant Sci. 13, 841688 (2022).

Article 
PubMed 
PubMed Central 

Google Scholar
 

Pieterse, C. M., Van Wees, S. C., Hoffland, E., Van Pelt, J. A. & Van Loon, L. C. Systemic resistance in Arabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogenesis-related gene expression. Plant Cell 8, 1225–1237 (1996).

PubMed 
PubMed Central 
CAS 

Google Scholar
 

Pieterse, C. M. J. et al. A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10, 1571–1580 (1998).

Article 
PubMed 
PubMed Central 
CAS 

Google Scholar
 

Hiruma, K. et al. Root endophyte Colletotrichum tofieldiae confers plant fitness benefits that are phosphate status dependent. Cell 165, 464–474 (2016).

Article 
PubMed 
PubMed Central 
CAS 

Google Scholar
 

Lyons, R. et al. Fusarium oxysporum triggers tissue-specific transcriptional reprogramming in Arabidopsis thaliana. PLoS ONE 10, e0121902 (2015).

Article 
PubMed 
PubMed Central 

Google Scholar
 

Edgar, C. I. et al. Salicylic acid mediates resistance to the vascular wilt pathogen Fusarium oxysporum in the model host Arabidopsis thaliana. Australas. Plant Pathol. 35, 581–591 (2006).

Article 
CAS 

Google Scholar
 

Alonso‐Ramírez, A. et al. Salicylic acid prevents Trichoderma harzianum from entering the vascular system of roots. Mol. Plant Pathol. 15, 823–831 (2014).

Article 
PubMed 
PubMed Central 

Google Scholar
 

Pedrotti, L., Mueller, M. J. & Waller, F. Piriformospora indica root colonization triggers local and systemic root responses and inhibits secondary colonization of distal roots. PLoS ONE 8, e69352 (2013).

Article 
PubMed 
PubMed Central 
CAS 

Google Scholar
 

Wang, L., Calabria, J., Chen, H.-W. & Somssich, M. The Arabidopsis thaliana–Fusarium oxysporum strain 5176 pathosystem: an overview. J. Exp. Bot. 73, 6052–6067 (2022).

Article 
PubMed 
PubMed Central 
CAS 

Google Scholar
 

Pieterse, C. M. J., Van der Does, D., Zamioudis, C., Leon-Reyes, A. & Van Wees, S. C. M. Hormonal modulation of plant immunity. Annu. Rev. Cell Dev. Biol. 28, 489–521 (2012).

Article 
PubMed 
CAS 

Google Scholar
 

Eichmann, R., Richards, L. & Schäfer, P. Hormones as go‐betweens in plant microbiome assembly. Plant J. 105, 518–541 (2021).

Article 
PubMed 
PubMed Central 
CAS 

Google Scholar
 

Trivedi, P., Leach, J. E., Tringe, S. G., Sa, T. & Singh, B. K. Plant–microbiome interactions: from community assembly to plant health. Nat. Rev. Microbiol. 18, 607–621 (2020).

Article 
PubMed 
CAS 

Google Scholar
 

Schimel, J., Balser, T. C. & Wallenstein, M. Microbial stress‐response physiology and its implications for ecosystem function. Ecology 88, 1386–1394 (2007).

Article 
PubMed 

Google Scholar
 

Chaudhry, V. et al. Shaping the leaf microbiota: plant–microbe–microbe interactions. J. Exp. Bot. 72, 36–56 (2021).

Article 
PubMed 
CAS 

Google Scholar
 

Chuberre, C. et al. Plant immunity is compartmentalized and specialized in roots. Front. Plant Sci. 9, 1692 (2018).

Article 
PubMed 
PubMed Central 

Google Scholar
 

Mishina, T. E. & Zeier, J. The Arabidopsis flavin-dependent monooxygenase FMO1 is an essential component of biologically induced systemic acquired resistance. Plant Physiol. 141, 1666–1675 (2006).

Article 
PubMed 
PubMed Central 
CAS 

Google Scholar
 

Zhang, W., Maksym, R., Georgii, E., Geist, B. & Schäffner, A. R. SA and NHP glucosyltransferase UGT76B1 affects plant defense in both SID2- and NPR1-dependent and independent manner. Plant Cell Rep. 43, 149 (2024).

Article 
PubMed 
PubMed Central 
CAS 

Google Scholar
 

Bensmihen, S. et al. Analysis of an activated ABI5 allele using a new selection method for transgenic Arabidopsis seeds. FEBS Lett. 561, 127–131 (2004).

Article 
PubMed 
CAS 

Google Scholar
 

Clough, S. J. & Bent, A. F. Floral dip: a simplified method for Agrobacterium‐mediated transformation of Arabidopsis thaliana. Plant J. 16, 735–743 (1998).

Article 
PubMed 
CAS 

Google Scholar
 

Stuttmann, J. et al. Highly efficient multiplex editing: one‐shot generation of 8× Nicotiana benthamiana and 12× Arabidopsis mutants. Plant J. 106, 8–22 (2021).

Article 
PubMed 
CAS 

Google Scholar
 

Engler, C. et al. A Golden Gate modular cloning toolbox for plants. ACS Synth. Biol. 3, 839–843 (2014).

Article 
PubMed 
CAS 

Google Scholar
 

Ordon, J. et al. Generation of chromosomal deletions in dicotyledonous plants employing a user‐friendly genome editing toolkit. Plant J. 89, 155–168 (2017).

Article 
PubMed 
CAS 

Google Scholar
 

Shimada, T. L., Shimada, T. & Hara‐Nishimura, I. A rapid and non‐destructive screenable marker, FAST, for identifying transformed seeds of Arabidopsis thaliana. Plant J. 61, 519–528 (2010).

Article 
PubMed 
CAS 

Google Scholar
 

Lagarde, D. et al. Tissue‐specific expression of Arabidopsis AKT1 gene is consistent with a role in K+ nutrition. Plant J. 9, 195–203 (1996).

Article 
PubMed 
CAS 

Google Scholar
 

Christmann, A., Weiler, E. W., Steudle, E. & Grill, E. A hydraulic signal in root‐to‐shoot signalling of water shortage. Plant J. 52, 167–174 (2007).

Article 
PubMed 
CAS 

Google Scholar
 

Osman, M., Stigloher, C., Mueller, M. J. & Waller, F. An improved growth medium for enhanced inoculum production of the plant growth-promoting fungus Serendipita indica. Plant Meth. 16, 39 (2020).

Article 
CAS 

Google Scholar
 

Katagiri, F., Thilmony, R. & He, S. Y. The Arabidopsis thaliana–Pseudomonas syringae interaction. Arabidopsis Book 1, e0039 (2002).

Article 
PubMed 
PubMed Central 

Google Scholar
 

Schäffner, A. R. & Xu, P. Original LC–MS and confocal data of the study ‘A root-based N-hydroxypipecolic acid standby circuit to direct immunity and growth of Arabidopsis shoots’ part 1. OSF https://doi.org/10.17605/OSF.IO/HKX75 (2025).

Schäffner, A. R. & Xu, P. Original LC–MS and confocal data of the study ‘A root-based N-hydroxypipecolic acid standby circuit to direct immunity and growth of Arabidopsis shoots’ part 2. OSF https://doi.org/10.17605/OSF.IO/EV796 (2025).