Signals of Systemic Immunity in Plants: Progress and Open Questions

Abstract

Systemic acquired resistance (SAR) is a defence mechanism that induces protection against a wide range of pathogens in distant, pathogen-free parts of plants after a primary inoculation. Multiple mobile compounds were identified as putative SAR signals or important factors for influencing movement of SAR signalling elements in Arabidopsis and tobacco. These include compounds with very different chemical structures like lipid transfer protein DIR1 (DEFECTIVE IN INDUCED RESISTANCE1), methyl salicylate (MeSA), dehydroabietinal (DA), azelaic acid (AzA), glycerol-3-phosphate dependent factor (G3P) and the lysine catabolite pipecolic acid (Pip). Genetic studies with different SAR-deficient mutants and silenced lines support the idea that some of these compounds (MeSA, DIR1 and G3P) are activated only when SAR is induced in darkness. In addition, although AzA doubled in phloem exudate of tobacco mosaic virus (TMV) infected tobacco leaves, external AzA treatment could not induce resistance neither to viral nor bacterial pathogens, independent of light conditions. Besides light intensity and timing of light exposition after primary inoculation, spectral distribution of light could also influence the SAR induction capacity. Recent data indicated that TMV and CMV (cucumber mosaic virus) infection in tobacco, like bacteria in Arabidopsis, caused massive accumulation of Pip. Treatment of tobacco leaves with Pip in the light, caused a drastic and significant local and systemic decrease in lesion size of TMV infection. Moreover, two very recent papers, added in proof, demonstrated the role of FMO1 (FLAVIN-DEPENDENT-MONOOXYGENASE1) in conversion of Pip to N-hydroxypipecolic acid (NHP). NHP systemically accumulates after microbial attack and acts as a potent inducer of plant immunity to bacterial and oomycete pathogens in Arabidopsis. These results argue for the pivotal role of Pip and NHP as an important signal compound of SAR response in different plants against different pathogens.

l‐lysine metabolism to N‐hydroxypipecolic acid: an integral immune‐activating pathway in plants

“…So far, SAR‐like effects of exogenous NHP and Pip in Arabidopsis have been observed against the hemibiotrophic bacterium P. syringae and the biotrophic oomycete Hpa (Návarová et al ., ; Hartmann et al ., ). Further, the application of Pip also induced resistance of tobacco plants to infection by P. syringae and tobacco mosaic virus (Vogel‐Adghough et al ., ; Ádám et al ., ). In addition, overexpression of a rice homolog of Arabidopsis ALD1 in transgenic rice plants increased immunity to the rice blast fungus M. oryzae (Jung et al ., ).…”

“…It is triggered by microbial inoculation of one or a few leaves and confers resistance within the whole foliage to subsequent attack by otherwise virulent pathogens (Shah and Zeier, ). Both plant basal immunity and SAR are regulated by signal‐active metabolites (Berens et al ., ; Ádám et al ., ; Shine et al ., ). Salicylic acid (SA) is a well‐documented defense metabolite required for the effective induction of plant immunity.…”

“…; Garcia‐Seco et al ., ). Significantly, many studies showed that Pip strongly accumulates in response to phytopathogens in the leaves of different plants, for example in rice infected with the blast fungus Magnaporthe oryzae , in virus‐infected tobacco ( Nicotiana tabacum ), potato and soybean (Pálfi and Dészi, ; Ádám et al ., ), in Arabidopsis and tobacco inoculated with the bacterium Pseudomonas syringae (Návarová et al ., ; Vogel‐Adghough et al ., ) and in soybean infected with the fungi Rhizoctonia solani and Fusarium virguliforme (Aliferis et al ., ; Abeysekara et al ., ).…”

Elicitor and Receptor Molecules: Orchestrators of Plant Defense and Immunity

“…Methyl-SA [61], a methylated form of SA, is produced once the cell has been infected by the pathogen. This volatile SAR-inducing molecule travels to other parts of the plant through the plasmodesmata [62][63][64]. Fu et al (2012) state that when SA is elevated at the area of infection, it will bind to the low-affinity binding receptor NPR3 (Nonexpressor of PR Genes 3) and cause the degeneration of cell-death suppressor NPR1, which subsequently results in HR [65].…”

Boosting photosynthetic machinery and defense priming with chitosan application on tomato plants infected withFusarium oxysporumf. sp.lycopersici

“…Resistance inducers can be synthetic substances, components derived from plants or microorganisms, as well as Microbial or Pathogen Associated Molecular Patterns (MAMPs or PAMPs) that induce a resistance response in the plant, triggering PTI (PAMP Triggered Immunity) (Ádám et al, 2018;Vidhyasekaran, 2016;Jones and Dangl, 2006). These resistance inducers trigger signaling through hormonal pathways (Salicylic Acid: SA, Jasmonic Acid: JA, and Ethylene: ET), changes in calcium concentrations, ubiquitin-dependent protein degradation, activation of G-proteins, and phosphorylation of Mitogen-Activated Protein Kinase (MAPKs), among others (REF).…”