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An engineered pathway for N-hydroxy-pipecolic acid synthesis enhances systemic acquired resistance in tomato.

ABSTRACT: Systemic acquired resistance (SAR) is a powerful immune response that triggers broad-spectrum disease resistance throughout a plant. In the model plant Arabidopsis thaliana, long-distance signaling and SAR activation in uninfected tissues occur without circulating immune cells and instead rely on the metabolite N-hydroxy-pipecolic acid (NHP). Engineering SAR in crop plants would enable external control of a plant's ability to mount a global defense response upon sudden changes in the environment. Such a metabolite-engineering approach would require the molecular machinery for producing and responding to NHP in the crop plant. Here, we used heterologous expression in Nicotiana benthamiana leaves to identify a minimal set of Arabidopsis genes necessary for the biosynthesis of NHP. Local expression of these genes in tomato leaves triggered SAR in distal tissues in the absence of a pathogen, suggesting that the SAR trait can be engineered to enhance a plant's endogenous ability to respond to pathogens. We also showed tomato produces endogenous NHP in response to a bacterial pathogen and that NHP is present across the plant kingdom, raising the possibility that an engineering strategy to enhance NHP-induced defenses could be possible in many crop plants.

SUBMITTER: Holmes EC

PROVIDER: S-EPMC7954083 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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An engineered pathway for N-hydroxy-pipecolic acid synthesis enhances systemic acquired resistance in tomato.

Holmes Eric C EC Chen Yun-Chu YC Sattely Elizabeth S ES Mudgett Mary Beth MB

Science signaling 20191022 604

Systemic acquired resistance (SAR) is a powerful immune response that triggers broad-spectrum disease resistance throughout a plant. In the model plant Arabidopsis thaliana, long-distance signaling and SAR activation in uninfected tissues occur without circulating immune cells and instead rely on the metabolite N-hydroxy-pipecolic acid (NHP). Engineering SAR in crop plants would enable external control of a plant's ability to mount a global defense response upon sudden changes in t ...[more]

PMID: 31641079

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Project description:We investigated the relationships of the two immune-regulatory plant metabolites salicylic acid (SA) and pipecolic acid (Pip) in the establishment of plant systemic acquired resistance (SAR) in Arabidopsis thaliana induced by the bacterial pathogen Pseudomonas syringae. To characterize the transcriptional SAR response, we used wild-type Col-0 plants, SA-deficient sid2 plants and Pip-deficient ald1 plants and performed RNA-sequencing analyses (Bernsdorff et al., Plant Cell, 2016). SAR establishment in the wild-type is characterized by a strong transcriptional response systemically induced in the foliage that prepares plants for future pathogen attack by pre-activating multiple stages of defense signaling. Whereas systemic Pip elevations are indispensable for SAR and necessary for virtually the whole transcriptional SAR response, a moderate but significant SA-independent component of SAR activation and SAR gene expression is revealed. Arabidopsis thaliana plants were grown individually in pots containing a mixture of soil, vermiculite and sand (8:1:1) in a controlled cultivation chamber with a 10-h day (9 AM to 7 PM; photon flux density 100 mol m-2 s-1) / 14-h night cycle and a relative humidity of 70 %. Day and night temperatures were set to 21C and 18C, respectively. Experiments were performed with 5- to 6-week-old, naive plants exhibiting a uniform appearance. To activate SAR, plants were infiltrated between 10 AM and 12 AM into three lower (1) leaves with suspensions of the bacterial pathogen Pseudomonas syringae pv. maculicola (OD600 = 0.005). Infiltration with 10 mM MgCl2 served as the mock-control treatment. Upper (2) leaves were harvested 48 h after the primary treatment for the determination of systemic gene expression by RNA-seq analyses. Three biologically independent, replicate SAR induction experiments were performed with Col-0 and sid2 plants (experimental set 1), and three other biologically independent experiments with Col-0 and ald1 plants (experimental set 2). In each SAR experiment, at least 6 upper (2) leaves from 6 different plants pre-treated in 1 leaves with Psm (MgCl2) were pooled for one biological Psm- (mock-control) replicate. In this way, 3 biologically independent, replicate samples per treatment and plant genotype were obtained within each SAR set.

Project description:Genome-wide microarray analyses revealed that during biological activation of systemic acquired resistance (SAR) in Arabidopsis, the transcript levels of several hundred plant genes were consistently up- (SAR(+) genes) or down-regulated (SAR(-) genes) in systemic, non-inoculated leaf tissue. This transcriptional reprogramming fully depended on the SAR regulator FLAVIN-DEPENDENT MONOOXYGENASE1 (FMO1). Functional gene categorization showed that genes associated with salicylic acid (SA)-associated defenses, signal transduction, transport, and the secretory machinery are overrepresented in the group of SAR(+) genes, and that the group of SAR(-) genes is enriched in genes activated via the jasmonate (JA)/ethylene (ET)-defense pathway, as well as in genes associated with cell wall remodeling and biosynthesis of constitutively produced secondary metabolites. This suggests that SAR-induced plants reallocate part of their physiological activity from vegetative growth towards SA-related defense activation. Alignment of the SAR expression data with other microarray information allowed us to define three clusters of SAR(+) genes. Cluster I consists of genes tightly regulated by SA. Cluster II genes can be expressed independently of SA, and this group is moderately enriched in H2O2- and abscisic acid (ABA)-responsive genes. The expression of the cluster III SAR(+) genes is partly SA-dependent. We propose that SA-independent signaling events in early stages of SAR activation enable the biosynthesis of SA and thus initiate SA-dependent SAR signaling. Both SA-independent and SA-dependent events tightly co-operate to realize SAR. SAR(+) genes function in the establishment of diverse resistance layers, in the direct execution of resistance against different (hemi-)biotrophic pathogen types, in suppression of the JA- and ABA-signaling pathways, in redox homeostasis, and in the containment of defense response activation. Our data further indicated that SAR-associated defense priming can be realized by partial pre-activation of particular defense pathways.

Project description:The intrinsic defense mechanisms of plants toward pathogenic bacteria have been widely investigated for years and are still at the center of interest in plant biosciences research. This study investigated the role of the AtbZIP62 gene encoding a transcription factor (TF) in the basal defense and systemic acquired resistance in Arabidopsis using the reverse genetics approach. To achieve that, the atbzip62 mutant line (lacking the AtbZIP62 gene) was challenged with Pseudomonas syringae pv. tomato (Pst DC3000) inoculated by infiltration into Arabidopsis leaves at the rosette stage. The results indicated that atbzip62 plants showed an enhanced resistance phenotype toward Pst DC3000 vir over time compared to Col-0 and the susceptible disease controls, atgsnor1-3 and atsid2. In addition, the transcript accumulation of pathogenesis-related genes, AtPR1 and AtPR2, increased significantly in atbzip62 over time (0-72 h post-inoculation, hpi) compared to that of atgsnor1-3 and atsid2 (susceptible lines), with AtPR1 prevailing over AtPR2. When coupled with the recorded pathogen growth (expressed as a colony-forming unit, CFU mL-1), the induction of PR genes, associated with the salicylic acid (SA) defense signaling, in part explained the observed enhanced resistance of atbzip62 mutant plants in response to Pst DC3000 vir. Furthermore, when Pst DC3000 avrB was inoculated, the expression of AtPR1 was upregulated in the systemic leaves of Col-0, while that of AtPR2 remained at a basal level in Col-0. Moreover, the expression of AtAZI (a systemic acquired resistance -related) gene was significantly upregulated at all time points (0-24 h post-inoculation, hpi) in atbzip62 compared to Col-0 and atgsnor1-3 and atsid2. Under the same conditions, AtG3DPH exhibited a high transcript accumulation level 48 hpi in the atbzip62 background. Therefore, all data put together suggest that AtPR1 and AtPR2 coupled with AtAZI and AtG3DPH, with AtAZI prevailing over AtG3DPH, would contribute to the recorded enhanced resistance phenotype of the atbzip62 mutant line against Pst DC3000. Thus, the AtbZIP62 TF is proposed as a negative regulator of basal defense and systemic acquired resistance in plants under Pst DC3000 infection.

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An engineered pathway for N-hydroxy-pipecolic acid synthesis enhances systemic acquired resistance in tomato.

Publications

An engineered pathway for <i>N</i>-hydroxy-pipecolic acid synthesis enhances systemic acquired resistance in tomato.

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