Direct antagonism overrides induced systemic resistance response by Bacillus subtilis UD1022 against dollar spot pathogen in creeping bentgrass

Systemic resistance is induced by pathogens and confers protection against a broad range of pathogens. Recent studies have indicated that salicylic acid (SA) derivative methyl salicylate (MeSA) serves as a long-distance phloem-mobile systemic resistance signal in tobacco, Arabidopsis, and potato. However, other experiments indicate that jasmonic acid (JA) is a critical mobile signal. Here, we present evidence suggesting both MeSA and methyl jasmonate (MeJA) are essential for systemic resistance against Tobacco mosaic virus (TMV), possibly acting as the initiating signals for systemic resistance. Foliar application of JA followed by SA triggered the strongest systemic resistance against TMV. Furthermore, we use a virus-induced gene-silencing-based genetics approach to investigate the function of JA and SA biosynthesis or signaling genes in systemic response against TMV infection. Silencing of SA or JA biosynthetic and signaling genes in Nicotiana benthamiana plants increased susceptibility to TMV. Genetic experiments also proved the irreplaceable roles of MeSA and MeJA in systemic resistance response. Systemic resistance was compromised when SA methyl transferase or JA carboxyl methyltransferase, which are required for MeSA and MeJA formation, respectively, were silenced. Moreover, high-performance liquid chromatography-mass spectrometry analysis indicated that JA and MeJA accumulated in phloem exudates of leaves at early stages and SA and MeSA accumulated at later stages, after TMV infection. Our data also indicated that JA and MeJA could regulate MeSA and SA production. Taken together, our results demonstrate that (Me)JA and (Me)SA are required for systemic resistance response against TMV.

The ability of nonpathogenic isolates of Fusarium oxysporum (npFo) to induce systemic resistance and defence responses against subsequent challenge with a pathogenic strain of F. oxysporum f. sp. asparagi (Foa) was examined in Asparagus officinalis. In a split‐root experiment, roots inoculated with npFo exhibited a hypersensitive response and those subsequently inoculated with Foa displayed resistance. Induction of systemic resistance in npFo‐treated plants led to significantly fewer necrotic lesions (P = 0·05) and reduced Foa disease severity compared with plants not treated with npFo. In hyphal‐sandwich root inoculation experiments, activities of peroxidase and phenylalanine ammonia‐lyase and lignin content were higher in npFo‐treated plants and increased more rapidly than in npFo‐untreated plants after Foa inoculation. Antifungal activity (inhibition of fungal spore germination and germ‐tube growth) from exudates of roots inoculated with Foa were observed for npFo‐treated plants but not for npFo‐untreated plants. Thus, isolates of npFo may function as inducers of systemic acquired resistance (SAR) and defence responses against Foa invasion in A. officinalis.

Beneficial root endophytic fungi induce systemic responses, growth promotion, and induced systemic resistance (ISR) in colonized host plants. The soil application of chitin, a main component of fungal cell walls, also systemically induces disease resistance. Therefore, chitin recognition and its downstream signaling pathway mediate ISR triggered by beneficial fungi colonizing the root. The present study compared systemic disease resistance and transcriptional responses induced by Trichoderma, a representative beneficial root endophytic fungus, and chitin in Arabidopsis. Significant plant growth promotion was observed under root colonization by the three beneficial fungi tested: Trichoderma atroviride, Serendipita indica, and S. vermifera. Only T. atroviride and S. indica triggered ISR against the necrotrophic fungal pathogen Alternaria brassicicola. Induced systemic resistance triggered by T. atroviride was compromised in the chitin-receptor mutant, whereas systemic resistance caused by the soil application of chitin was not. A transcriptome ana-lysis demonstrated that chitin-regulated genes were mostly shared with those regulated by T. atroviride; however, many of the latter were specific. The commonly enriched gene ontologies for these genes indicated that the T. atroviride inoculation and chitin application systemically controlled similar transcriptional responses, mainly associated with cell wall functions. Therefore, Trichoderma may trigger ISR primarily independent of the chitin-mediated signaling pathway; however, chitin and Trichoderma may systemically induce similar cellular functions aboveground.

Decreased vascular resistance and vasoconstrictor response during pregnancy enables an increase in cardiac output and regional blood flow to the uterine circulation. We sought to determine whether inhibition of vascular smooth muscle ATP-sensitive potassium (K+ATP) channel activity during pregnancy increased systemic and/or regional vascular resistance and resistance response to ANG II. A total of 32 catheterized, awake, pregnant or nonpregnant guinea pigs were treated with either the K+ATP channel inhibitor glibenclamide (3.5 mg/kg) or vehicle (DMSO) (n = 8/group). In nonpregnant and pregnant animals, glibenclamide raised blood pressure and systemic, uterine, and coronary vascular resistance, diminishing cardiac output and organ blood flow. Glibenclamide produced a greater rise in coronary vascular resistance in the pregnant than nonpregnant groups and increased renal and cerebral vascular resistance in the pregnant animals only. ANG II infusion raised blood pressure and systemic and renal vascular resistance and lowered cardiac output and renal blood flow in vehicle-treated animals. Glibenclamide augmented ANG II-induced systemic vasoconstriction in the nonpregnant and pregnant groups and the rise in uteroplacental vascular resistance in the pregnant animals. We concluded that K+ATP channel activity likely modulates systemic, uterine, and coronary vascular resistance and opposes ANG II-induced systemic vasoconstriction in nonpregnant and pregnant guinea pigs. Pregnancy augments K+ATP channel activity in the uterine, coronary, renal, and cerebral vascular beds and the uteroplacental circulation during ANG II infusion. Thus increased K+ATP channel activity appears to influence regional control of vascular resistance during guinea pig pregnancy but cannot account for the characteristic decrease in systemic vascular resistance and ANG II-induced systemic vasoconstrictor response.

We used DNA microarrays to examine local and systemic transcriptional responses to herbivory by gypsy moth larvae (GM) and exogenous jasmonic acid (JAtrt) in leaves of Populus nigra L. to identify candidate signaling and defense genes and also to examine primary metabolism, as might relate to tolerance of damage. GM and JAtrt altered expression of over 800 genes, most of which have putative roles in defense signaling, secondary metabolism, and primary metabolism. Additionally, numerous uncharacterized genes responded to herbivory, providing a rich resource for future studies. There was limited overlap (14%) between the responses to GM and JAtrt. GM did, however, result in strong upregulation of genes involved not only in JA biosynthesis but also abscisic acid biosynthesis and other signaling pathways. GM induced known resistance transcripts, including polyphenolic biosynthetic genes, proteinase inhibitors, and amino acid deaminases. According to GOStats pathway level analysis, GM altered primary metabolism, including aromatic amino acid biosynthesis, fatty acid β-oxidation, and carbohydrate and organic acid metabolism. These alterations may be related to increased demands for substrate for secondary metabolites or may serve a tolerance-related role. Responses were more intense locally in treated leaves than in untreated (systemic) leaves and systemic responses were mostly a subset of the genes induced locally. A stronger local response might be needed to cope with localized stresses and wound healing. Since Populus in general and this clone in particular are known for their systemic induced resistance, genes induced both locally and systemically may be the highest quality candidates for resistance.

A new family of synthetic, membrane-active, ultrashort lipopeptides composed of only four amino acids linked to fatty acids was tested for the ability to induce systemic resistance and defense responses in plants. We found that two peptides wherein the third residue is a d-enantiomer (italic), C16-KKKK and C16-KLLK, can induce medium alkalinization of tobacco suspension-cultured cells and expression of defense-related genes in cucumber and Arabidopsis seedlings. Moreover, these compounds can prime systemic induction of antimicrobial compounds in cucumber leaves similarly to the plant-beneficial fungus Trichoderma asperellum T203 and provide systemic protection against the phytopathogens Botrytis cinerea B05, Pseudomonas syringae pv. lachrimans, and P. syringae pv. tomato DC3000. Thus, short cationic lipopeptides are a new category of compounds with potentially high utility in the induction of systemic resistance in plants.

The aim of this study was to examine the effect of chronic hypoxia on systemic vascular reactivity and the role of prostaglandins in modulating the vascular response to chronic hypoxia. Meclofenamate, a prostaglandin synthesis inhibitor, increased the systemic vascular resistance response to the alpha-adrenergic agonist, phenylephrine, in awake, unrestrained guinea pigs exposed for 6 wk to high altitude (3,900 m), but it did not alter the response in animals kept at low altitude (1,600 m). The systemic vascular resistance response to phenylephrine before treatment with meclofenamate was the same in high- and low-altitude animals. Meclofenamate also increased the contractile response to phenylephrine in aortic rings isolated from high- but not low-altitude animals. The systemic vascular resistance response to angiotensin II was the same in high- and low-altitude animals, and meclofenamate increased this response to the same extent in both groups. Thus chronic hypoxia appeared to enhance vascular production of dilator prostaglandins during beta-adrenergic stimulation.

Systemic resistance (SR) occurs when systemic signals derived from sites of previous pathogen attacks result in increased resistance levels to subsequent pathogenesis at distal sites. Although much research on this phenomenon has been conducted in dicotyledonous species, little is known about SR in monocotyledonous models. In this study we investigate SR in maize caused by foliar infection with Cochliobolus heterostrophus- the causal agent of southern leaf blight (SLB) disease - and by leaf damage. In juvenile maize, we observed that both prior infection with C. heterostrophus and cutting of the third and fourth leaves led to enhanced resistance to SLB in the fifth leaf. Levels of SR induction were variable between genotypes and between growth conditions. C. heterostrophus infection induced local and systemic expression of the defense-associated transcript ZmPR1. We discuss the implications of these findings that provide insights into the systemic disease resistance response in maize.

Systemic DNA damage responses: organismal adaptations to genome instability

Adiposity is commonly associated with adipose tissue dysfunction and many overnutrition-related metabolic diseases including type 2 diabetes. Much attention has been paid to reducing adiposity as a way to improve adipose tissue function and systemic insulin sensitivity. PFKFB3/iPFK2 is a master regulator of adipocyte nutrient metabolism. Using PFKFB3(+/-) mice, the present study investigated the role of PFKFB3/iPFK2 in regulating diet-induced adiposity and systemic insulin resistance. On a high-fat diet (HFD), PFKFB3(+/-) mice gained much less body weight than did wild-type littermates. This was attributed to a smaller increase in adiposity in PFKFB3(+/-) mice than in wild-type controls. However, HFD-induced systemic insulin resistance was more severe in PFKFB3(+/-) mice than in wild-type littermates. Compared with wild-type littermates, PFKFB3(+/-) mice exhibited increased severity of HFD-induced adipose tissue dysfunction, as evidenced by increased adipose tissue lipolysis, inappropriate adipokine expression, and decreased insulin signaling, as well as increased levels of proinflammatory cytokines in both isolated adipose tissue macrophages and adipocytes. In an in vitro system, knockdown of PFKFB3/iPFK2 in 3T3-L1 adipocytes caused a decrease in the rate of glucose incorporation into lipid but an increase in the production of reactive oxygen species. Furthermore, knockdown of PFKFB3/iPFK2 in 3T3-L1 adipocytes inappropriately altered the expression of adipokines, decreased insulin signaling, increased the phosphorylation states of JNK and NFkappaB p65, and enhanced the production of proinflammatory cytokines. Together, these data suggest that PFKFB3/iPFK2, although contributing to adiposity, protects against diet-induced insulin resistance and adipose tissue inflammatory response.

The effects of transfer of the endothelial nitric oxide synthase (eNOS) gene to the lung were studied in mice. After intratracheal administration of AdCMVbetagal, expression of the beta-galactosidase reporter gene was detected in pulmonary airway cells, in alveolar cells, and in small pulmonary arteries. Gene expression with AdCMVbetagal peaked 1 day after administration and decayed over a 7- to 14-day period, whereas gene expression after AdRSVbetagal transfection peaked on day 5 and was sustained over a 21- to 28-day period. One day after administration of AdCMVeNOS, eNOS protein levels were increased, and there was a small reduction in mean pulmonary arterial pressure and pulmonary vascular resistance. The pressure-flow relationship in the pulmonary vascular bed was shifted to the right in animals transfected with eNOS, and pulmonary vasodepressor responses to bradykinin and the type V cGMP-selective phosphodiesterase inhibitor zaprinast were enhanced, whereas systemic responses were not altered. Pulmonary vasopressor responses to endothelin-1 (ET-1), angiotensin II, and ventilatory hypoxia were reduced significantly in animals transfected with the eNOS gene, whereas pressor responses to norepinephrine and U46619 were not changed. Systemic pressor responses to ET-1 and angiotensin II were similar in eNOS-transfected mice and in control mice. Intratracheal administration of AdRSVeNOS attenuated the increase in pulmonary arterial pressure in mice exposed to the fibrogenic anticancer agent bleomycin. These data suggest that transfer of the eNOS gene in vivo can selectively reduce pulmonary vascular resistance and pulmonary pressor responses to ET-1, angiotensin II, and hypoxia; enhance pulmonary depressor responses; and attenuate pulmonary hypertension induced by bleomycin. Moreover, these data suggest that in vivo gene transfer may be a useful therapeutic intervention for the treatment of pulmonary hypertensive disorders.

Plants are exposed to varied biotic stresses, including sequential or simultaneous attack by insects and pathogens. To overcome these complex stresses, plants must perceive each of the stresses, then integrate and relay the information throughout the plant body and eventually activate local and systemic resistance responses. Previous molecular genetic studies identified jasmonic acid and salicylic acid as key plant hormones of wound and immune responses. These hormones, combined with their antagonistic interaction, play critical roles in the initiation and regulation of defense responses against insects and pathogens. Aside from molecular and genetic information, the latest in vivo imaging technology has revealed that plant defense responses are regulated spatially and temporally. In this review, we summarize the current knowledge of local and systemic defense responses against wounding and diseases with a focus on past and recent advances in imaging technologies. We discuss how imaging-based multiparametric analysis has improved our understanding of the spatiotemporal regulation of dynamic plant stress responses. We also emphasize the importance of compiling the knowledge generated from individual studies on plant wounding and immune responses for a more seamless understanding of plant defense responses in the natural environment.

HASTY-dependent miRNA cell-to-cell movement is required for systemic pathogen resistance in Arabidopsis.

Laminarin, a beta-1,3 glucan with single beta-glucose branches at position 6, was chemically sulfated to produce PS3 with a degree of sulfation of 2.4. PS3 has previously been shown to activate the salicylic acid (SA) signaling pathway in infiltrated tobacco and Arabidopsis thaliana leaf tissues. Here, we investigated whether PS3 induces systemic defense and resistance responses in tobacco. Using a radiolabeled compound, it was first demonstrated that PS3 remains strictly localized to the infiltrated tissues. PS3 is also resistant to beta-glucanase degradation. In transgenic PR1-beta-glucuronidase (GUS) tobacco plants, PS3 causes a strong increase in GUS activity in treated tissues but none in untreated leaves. PS3-infiltrated tissues challenged with tobacco mosaic virus (TMV) 8 d after elicitor application show a decrease in both the lesion number and the lesion size, whereas treatment with laminarin, the unsulfated native glucan, affected only the lesion number. PS3 does not induce systemic acquired resistance to TMV. PS3 and laminarin show synergistic effects in promoting the oxidative burst in tobacco cell suspensions and in increasing the expression of genes encoding O-methyltransferases of the phenylpropanoid pathway in tobacco plants. No synergistic effect was observed on the expression of either the SA-dependent acidic PR1 gene or the ethylene-dependent basic PR5 gene in tobacco plants.

Systemic acquired resistance (SAR) is usually described as a phenomenon whereby localized inoculation with a necrotizing pathogen renders a plant more resistant to subsequent pathogen infection. Here we show that Pseudomonas syringae strains for which Arabidopsis thaliana represents a non-host plant systemically elevate resistance although the underlying interactions neither trigger a hypersensitive response nor cause necrotic disease symptoms. A similar enhancement of systemic resistance was observed when elicitor-active preparations of two typical bacterial pathogen-associated molecular patterns (PAMPs), flagellin and lipopolysaccharides (LPS), were applied in a localized manner. Several lines of evidence indicate that the observed systemic resistance responses are identical to SAR. Localized applications of non-adapted bacteria, flagellin or LPS elevate levels of the SAR regulatory metabolite salicylic acid (SA) and pathogenesis-related (PR) gene expression not only in treated but also in distant leaves. All treatments also systemically increase expression of the SAR marker gene FLAVIN-DEPENDENT MONOOXYGENASE 1. Further, a whole set of SAR-deficient Arabidopsis lines, including mutants in SA biosynthesis and signalling, are impaired in establishing the systemic resistance response triggered by non-host bacteria or PAMPs. We also show that the magnitude of defence reactions such as SA accumulation, PR gene expression or camalexin accumulation induced at sites of virulent or avirulent P. syringae inoculation but not the extent of tissue necrosis during these interactions determines the extent of SAR in distant leaves. Our data indicate that PAMPs significantly contribute to SAR initiation in Arabidopsis and that tissue necroses at inoculation sites are dispensable for SAR activation.