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Cultivar Variation in Hormonal Balance Is a Significant Determinant of Disease Susceptibility to Xanthomonas campestris pv. campestris in Brassica napus.

ABSTRACT: This study aimed to directly elucidate cultivar variation in disease susceptibility and disease responses in relation to hormonal status in the interaction of Brassica napus cultivars and Xanthomonas campestris pv. campestris (Xcc), the causal agent of black rot disease. Fully expanded leaves of six B. napus cultivars (cvs. Capitol, Youngsan, Saturnin, Colosse, Tamra, and Mosa) were inoculated with Xcc. At 14 days post-inoculation with Xcc, cultivar variation in susceptibility or resistance was interpreted with defense responses as estimated by redox status, defensive metabolites, and expression of phenylpropanoid synthesis-related genes in relation to endogenous hormonal status. Disease susceptibility of six cultivars was distinguished by necrotic lesions in the Xcc-inoculated leaves and characterized concurrently based on the higher increase in reactive oxygen species and lipid peroxidation. Among these cultivars, as the susceptibility was higher, the ratios of abscisic acid (ABA)/jasmonic acid (JA) and salicylic acid (SA)/JA tended to increase with enhanced expression of SA signaling regulatory gene NPR1 and transcriptional factor TGA1 and antagonistic suppression of JA-regulated gene PDF 1.2. In the resistant cultivar (cv. Capitol), accumulation of defensive metabolites with enhanced expression of genes involved in flavonoids (chalcone synthase), proanthocyanidins (anthocyanidin reductase), and hydroxycinnamic acids (ferulate-5-hydroxylase) biosynthesis and higher redox status were observed, whereas the opposite results were obtained for susceptible cultivars (cvs. Mosa and Tamra). These results clearly indicate that cultivar variation in susceptibility to infection by Xcc was determined by enhanced alteration of the SA/JA ratio, as a negative regulator of redox status and phenylpropanoid synthesis in the Brasica napus-Xcc pathosystem.

SUBMITTER: Islam MT

PROVIDER: S-EPMC5732936 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:To characterize cultivar variation in resistance gene (R-gene)-mediated calcium signaling and hormonal regulation in effector-triggered immunity (ETI) and disease susceptibility, Xanthomonas campestris pv. campestris (Xcc) was inoculated in two Brassica napus cultivars (cvs. Capitol and Mosa). At 14 days post inoculation (DPI) with Xcc, there was a necrotic lesion in cv. Mosa along with the significant accumulation of H2O2 and malondialdehyde (MDA), whereas no visual symptom was observed in cv. Capitol. The cultivar variations in the R-gene expressions were found in response to Xcc. ZAR1 is a coiled-coil-nucleotide binding site-leucine-rich repeat (CC-NB-LRR)-type R-gene that is significantly induced in cv. Capitol, whereas toll/interleukin-1 receptor-nucleotide binding site-leucine-rich repeat (TIR-NB-LRR)-type R-gene, TAO1, is significantly upregulated in cv. Mosa Xcc-inoculated plants. The defense-related gene's non-race-specific disease resistance 1 (NDR1) and mitogen-activated protein kinase 6 (MAPK6) were enhanced, whereas calcium-dependent protein kinase (CDPK5) and calcium-sensing protein 60g (CBP60g) were depressed in cv. Capitol Xcc inoculated plants, and opposite results were found in cv. Mosa. The calcium-sensing receptor (CAS), calmodulin (CaM), expression was induced in both the cultivars. However, the CAS induction rate was much higher in cv. Mosa than in cv. Capitol in response to Xcc. The phytohormone salicylic acid (SA) and jasmonic acid (JA) levels were significantly higher in cv. Capitol along with the enhanced SA receptors (NPR3 and NPR4) and JA synthesis and signaling-related gene expression (LOX2, PDF1.2), whereas the JA level was significantly lower in cv. Mosa Xcc inoculated plants. The SA synthesis and signaling-related genes (ICS1, NPR1) and SA were present at higher levels in cv. Mosa; additionally, the SA level present was much higher in the susceptible cultivar (cv. Mosa) than in the resistant cultivar (cv. Capitol) in response to Xcc. These results indicate that ZAR1 mediated the coordinated action of SA and JA synthesis and signaling to confirm ETI, whereas TAO1 enhanced the synthesis of SA through CAS and CBP60g to antagonize JA synthesis and signaling to cause disease susceptibility in the Brassica napus-Xcc pathosystem.

Project description:UnlabelledN-Acetylglucosamine (GlcNAc), the main component of chitin and a major constituent of bacterial peptidoglycan, is present only in trace amounts in plants, in contrast to the huge amount of various sugars that compose the polysaccharides of the plant cell wall. Thus, GlcNAc has not previously been considered a substrate exploited by phytopathogenic bacteria during plant infection. Xanthomonas campestris pv. campestris, the causal agent of black rot disease of Brassica plants, expresses a carbohydrate utilization system devoted to GlcNAc exploitation. In addition to genes involved in GlcNAc catabolism, this system codes for four TonB-dependent outer membrane transporters (TBDTs) and eight glycoside hydrolases. Expression of all these genes is under the control of GlcNAc. In vitro experiments showed that X. campestris pv. campestris exploits chitooligosaccharides, and there is indirect evidence that during the early stationary phase, X. campestris pv. campestris recycles bacterium-derived peptidoglycan/muropeptides. Results obtained also suggest that during plant infection and during growth in cabbage xylem sap, X. campestris pv. campestris encounters and metabolizes plant-derived GlcNAc-containing molecules. Specific TBDTs seem to be preferentially involved in the consumption of all these plant-, fungus- and bacterium-derived GlcNAc-containing molecules. This is the first evidence of GlcNAc consumption during infection by a phytopathogenic bacterium. Interestingly, N-glycans from plant N-glycosylated proteins are proposed to be substrates for glycoside hydrolases belonging to the X. campestris pv. campestris GlcNAc exploitation system. This observation extends the range of sources of GlcNAc metabolized by phytopathogenic bacteria during their life cycle.ImportanceDespite the central role of N-acetylglucosamine (GlcNAc) in nature, there is no evidence that phytopathogenic bacteria metabolize this compound during plant infection. Results obtained here suggest that Xanthomonas campestris pv. campestris, the causal agent of black rot disease on Brassica, encounters and metabolizes GlcNAc in planta and in vitro. Active and specific outer membrane transporters belonging to the TonB-dependent transporters family are proposed to import GlcNAc-containing complex molecules from the host, from the bacterium, and/or from the environment, and bacterial glycoside hydrolases induced by GlcNAc participate in their degradation. Our results extend the range of sources of GlcNAc metabolized by this phytopathogenic bacterium during its life cycle to include chitooligosaccharides that could originate from fungi or insects present in the plant environment, muropeptides leached during peptidoglycan recycling and bacterial lysis, and N-glycans from plant N-glycosylated proteins present in the plant cell wall as well as in xylem sap.

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Cultivar Variation in Hormonal Balance Is a Significant Determinant of Disease Susceptibility to Xanthomonas campestris pv. campestris in Brassica napus.

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