Pipecolic Acid Is Induced in Barley upon Infection and Triggers Immune Responses Associated with Elevated Nitric Oxide Accumulation

Abstract

Pipecolic acid (Pip) is an essential component of systemic acquired resistance, priming resistance in Arabidopsis thaliana against (hemi)biotrophic pathogens. Here, we studied the potential role of Pip in bacteria-induced systemic immunity in barley. Exudates of barley leaves infected with the systemic immunity–inducing pathogen Pseudomonas syringae pv. japonica induced immune responses in A. thaliana. The same leaf exudates contained elevated Pip levels compared with those of mock-treated barley leaves. Exogenous application of Pip induced resistance in barley against the hemibiotrophic bacterial pathogen Xanthomonas translucens pv. cerealis. Furthermore, both a systemic immunity–inducing infection and exogenous application of Pip enhanced the resistance of barley against the biotrophic powdery mildew pathogen Blumeria graminis f. sp. hordei. In contrast to a systemic immunity-inducing infection, Pip application did not influence lesion formation by a systemically applied inoculum of the necrotrophic fungus Pyrenophora teres. Nitric oxide (NO) levels in barley leaves increased after Pip application. Furthermore, X. translucens pv. cerealis induced the accumulation of superoxide anion radicals and this response was stronger in Pip-pretreated compared with mock-pretreated plants. Thus, the data suggest that Pip induces barley innate immune responses by triggering NO and priming reactive oxygen species accumulation.

Inducible biosynthesis and immune function of the systemic acquired resistance inducer N-hydroxypipecolic acid in monocotyledonous and dicotyledonous plants

“…Our metabolite analyses suggest that an endogenous activation of SAR in barley might proceed via NHP signaling. This assumption is compatible with the finding that H. vulgare plants fed with exogenous Pip acquired resistance to X. translucens infection ( Lenk et al , 2019 ).…”

“…Pip functions as the direct metabolic precursor of NHP ( Hartmann et al , 2018 ). Previous studies have reported that inoculation with a pathogen markedly induces the accumulation of Pip in different angiosperm species, including Arabidopsis, tobacco, potato, soybean, rice, and barley (Pálfi and Dézsi, 1968; Návarová et al , 2012 ; Vogel-Adghough et al , 2013 ; Aliferis et al , 2014 ; Abeysekara et al , 2016 ; Ádám et al , 2018 ; Lenk et al , 2019 ). Consistently, the results of the present study show that the levels of Pip increase strongly in leaves of tobacco, soybean, and barley inoculated with compatible Pseudomonas bacteria ( Figs 4 , 5 ).…”

“…Pip is also synthesized by an ALD1-/SARD4-mediated l -Lys catabolic pathway in the fir clubmoss Huperzia serrata ( Xu et al , 2018 ). Moreover, Pip has been shown to accumulate in several angiosperms other than Arabidopsis upon contact with a pathogen—for example, in soybean inoculated with the fungi Rhizoctonia solani and Fusarium virguliforme ( Aliferis et al , 2014 ; Abeysekara et al , 2016 ), in tobacco mosaic virus- or P. syringae -inoculated tobacco ( Nicotiana tabacum ) (Pálfi and Dézsi, 1968; Vogel-Adghough et al , 2013 ; Ádám et al , 2018 ), in rice infected with the blast fungus Magnaporthe oryzae (Pálfi and Dézsi, 1968), and in P. syringae -infected barley ( Lenk et al , 2019 ).…”

Systemic propagation of immunity in plants

“…In contrast, systemic immunity against Blumeria graminis f.sp. hordei might depend on SA, while Pip triggers systemic resistance in barley against both pathogens (Lenk et al ., 2018, 2019). Pip accumulates in barley petiole exudates after a resistance‐inducing infection, and exogenous Pip application induces NO accumulation and primes ROS production (Lenk et al ., 2019), providing evidence for a possible conservation of the Pip pathway of SAR between monocotyledonous and dicotyledonous plants (Fig.…”

UGT76B1, a promiscuous hub of small molecule-based immune signaling, glucosylates N-hydroxypipecolic acid and controls basal pathogen defense

“…For determination of SA-and Pip-related metabolites, frozen-materials were crushed to powder and lyophilized. The extraction and measurement of the compounds was carried out as described before with minor modifications (Wenig et al, 2019). Briefly, 20 mg of freeze-dried material was resuspended in 1.5 ml 70% methanol, vigorously shaken at 4 °C for 1 h and subsequently centrifuged at 18.000 x g for 10 min.…”