Immune Programming in Plants Identified by EPR

It is widely known that plants can succumb to infection by pathogenic organisms such as viruses, bacteria, and fungi. However, it is less well known that plants can defend themselves against disease-causing organisms.

Plants do not have the complex adaptive immune system that protects many mammals, but plants do have a basal immune program that enables them to recognize conserved molecular patterns of potentially pathogenic micro-organisms1. This means that when a plant is invaded by one of these micro-organisms, it can limit the invasive spread of virulent pathogens within its tissues but may not be able to fully prevent disease development.

plant research

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Immune defense signaling

Defense signaling in response to pathogenic infection can be initiated by recognition of either conserved pathogen-derived molecules (pathogen-associated molecular pattern-triggered immunity [PTI]) or specialized pathogen effectors called avirulence factors (effector-triggered immunity [ETI]).

Both PTI and ETI result in local resistance, but ETI also induces an additional resistance mechanism known as systemic acquired resistance (SAR) 2. Through this mechanism, a localized leaf infection can activate a state of enhanced immunity throughout the plant’s entire foliage. SAR thus arms a plant with broad-spectrum resistance against future invasion by similar pathogens.

The activation of SAR results in massive transcriptional and metabolic reprogramming at the systemic level that primes the plant for a more rapid and effective defense response against future pathogen challenges. When the plant’s cell-surface receptors identify a pattern characteristic of pathogens, the production of chemical signals, such as methyl jasmonate, are triggered that elicit both local and systemic defense responses.

Plant metabolites are thus important regulatory components of plant basal resistance and SAR. Compounds known to be key players in the SAR pathway include salicylic acid, azelaic acid, nitric oxide, reactive oxygen species, glycerol-3-phosphate (G3P) and galactolipids3.

Pipecolic acid has been implicated as a regulator of plant SAR, but there is no direct evidence for such a role 4.

Pipecolic acid

Pipecolic acid is a lysine-derived non-protein amino acid that is associated with the regulation of plant systemic acquired resistance and basal immunity to bacterial pathogen infection3. It is derived from lysine catabolism by lysine aminotransferase (LAT).

Although pipecolic acid is known to accumulate on pathogen infection in both infected (local) and uninfected (distal) leaves, details of the underlying mechanisms of pipecolic acid -mediated SAR and its relation to other known chemical signals have not been uncovered.

The levels of pipecolic acid have been shown to differ considerably between local and distal leaves. Plants with defective LAT showed reduced accumulation of pipecolic acid in both local and distal leaves.

In contrast, plants unable to produce the enzyme that converts a metabolite of lysine catabolism, Δ1-piperideine-2-carboxylic acid, to pipecolic acid (SARD4) were only defective in the distal accumulation of pipecolic acid.

It is well-known that ALD1 regulates the biosynthesis of pipecolic acid, but the precise role of SARD4 is unclear. Since defective SARD4 only affects uninfected leaves, it is possible that SARD4-catalyzed pipecolic acid production may play a role in the SAR response.

Pipecolic acid involvement in SAR

A recent study evaluated whether pipecolic acid is required for SAR5. Pipecolic acid was applied locally to leaves of a plant with either localized infection with a weak strain of Pseudomonas syringae (Pst) or infiltrated magnesium chloride.

Methanol was applied to other leaves as a control. The distal untreated leaves of all plants were then challenged with a virulent strain of Pst, and the growth of Pst monitored 0 and 3 days after infiltration. Homogenized leaf samples were also analyzed by electron paramagnetic resonance (EPR) using a Bruker ESP 300 X-band spectrometer.

The results showed that the plants that had been infected with a weak Pst strain contained 10‑15 times less of the virulent Pst than the plants infiltrated with magnesium chloride. The plants that to which pipecolic acid had been applied also showed significantly less growth of virulent Pst compared with those infiltrated with methanol.

ESR spectra showed that the plants pre-treated with pipecolic acid had higher levels of the free radical, nitric oxide (NO), and other reactive oxygen species (ROS), which act upstream of G3P in the SAR signaling pathway. These data indicate that pipecolic acid is indeed a chemical inducer of SAR and functions primarily upstream of the G3P branch of the SAR pathway.

In addition, plants defective in NO, ROS, G3P, or salicylic acid biosynthesis showed reduced accumulate of pipecolic acid in their distal uninfected tissues although they had normal levels of pipecolic acid in their infected leaves. This reflects the effects seen in plants with defective SARD4.

The authors concluded that the transport of salicylic acid and G3P to the distal tissue is important for pipecolic acid biosynthesis, which in turn initiates the de novo synthesis of G3P. Together, these data establish the relationship between pipecolic acid and other structurally diverse chemical signals associated with SAR and highlight their coordinated function in the induction of SAR.

The latest findings describe a unique scenario whereby metabolites in a signaling cascade can stimulate each other’s biosynthesis depending on their relative levels and their site of action.

References

  1. Macho AP, Zipfel C. Mol Cell 2014;54: 63–272.
  2. Fu ZQ, Dong X. Annu Rev Plant Biol 2013;64:839–863.
  3. Lim G-H, et al. Cell Host Microbe 2016;19:541–549.
  4. Bernsdorff F, et al. Plant Cell 2016;28:102–129.
  5. Caixia Wang C, et al. Pipecolic acid confers systemic immunity by regulating free radicals. Science Advances 2018;4(5):eaar4509 https://advances.sciencemag.org/content/4/5/eaar4509

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Last updated: Jul 16, 2019 at 10:42 AM

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