Genes up-regulated by PPA1, OPDA, B. cinerea inoculation and abiotic stresses and dependent on TGA2/5/6.
Arjun ShamAl-Azzawi AhmedSalma Al-AmeriAl-Mahmoud BassamAwwad FalahAl-Rawashdeh AhmedRabah IratniAbuQamar Synan
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Salicylic acid (SA), Jasmonic acid (JA) and ethylene (ET) have the significant roles in the plants physiologically and in defense against pathogens. To elucidate the role of these three phytohormones in the development of Induced systemic resistance (ISR), it is a systemic immune response that occurs when the roots are colonized by beneficial microbes. The study model of SRI is the combination of specific beneficial strains of Pseudomonas fluorescens PTA-CT2 with Arabidopsis thaliana, the course of camalexin levels was monitored before and after infection with the fungus Botrytis cinerea. To conduct this, we use different mutants and transgenic plants that fail in the pathway of JA (jar1), ethylene (ein2) or NahG (transgenic line degrading salicylic acid [SA]). We are therefore monitoring the evolution of camalexin, a highly lipophilic phytoalexin, before and after bacterization and/or infection. As a consequence of the study, the bacterization induces potentiation of the defenses, which depends on the three signaling pathways. In addition, the recognition of the beneficial bacteria is reduced by JA and ET.
Jasmonic acid
Phytoalexin
Systemic Acquired Resistance
Pseudomonas fluorescens
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Ttranscription factors WRKY play vital roles in response to biotic and abiotic stresses, and previous studies have predominantly focused on model plants and fairly limited research has been performed with tomato. In the present study, a novel pathogen-induced WRKY gene named SpWRKY6 was isolated from the late blight resistant tomato (Solanum pimpinellifolium) cultivar L3708 using in silico cloning and reverse transcription polymerase chain reaction (RT-PCR) methods. Multiple sequence alignment with other plant WRKYs indicates that SpWRKY6 contains two WRKY domains and belongs to group I WRKY transcription factors. Furthermore, some cis-acting elements associated with responses to environmental stresses were observed in the promoter region of this gene. Gene expression patterns were determined by analyzing microarray data of SpWRKY6 in tomato and of an orthologous gene from Arabidopsis thaliana using the Genevestigator tool. The results reveal a very strong biotic and abiotic stress responsive behaviour of this gene. Moreover, bioinformatics results were confirmed by real time quantitative polymerase chain reaction and show that SpWRKY6 expression was rapidly induced after infection with Phytophthora infestans and Botrytis cinerea, respectively. Expression of SpWRKY6 was up-regulated by application of various phytohormones including salicylic acid, methyl jasmonate, and abscisic acid. Likewise, the SpWRKY6 expression was induced by NaCl, drought, heat, cold, and HgCl2 treatments.
WRKY protein domain
Methyl jasmonate
Phytophthora infestans
Biotic stress
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Wounding of Arabidopsis leaves causes a powerful but transient protection against Botrytis infection
Physical injury inflicted on living tissue makes it vulnerable to invasion by pathogens. Wounding of Arabidopsis thaliana leaves, however, does not conform to this concept and leads to immunity to Botrytis cinerea, the causal agent of grey mould. In wounded leaves, hyphal growth was strongly inhibited compared to unwounded controls. Wound-induced resistance was not associated with salicylic acid-, jasmonic acid- or ethylene-dependent defence responses. The phytoalexin camalexin was found to be involved in this defence response as camalexin-deficient mutants were not protected after wounding and the B. cinerea strains used here were sensitive to this compound. Wounding alone did not lead to camalexin production but primed its accumulation after inoculation with B. cinerea, further supporting the role of camalexin in wound-induced resistance. In parallel with increased camalexin production, genes involved in the biosynthesis of camalexin were induced faster in wounded and infected plants in comparison with unwounded and infected plants. Glutathione was also found to be required for resistance, as mutants deficient in gamma-glutamylcysteine synthetase showed susceptibility to B. cinerea after wounding, indicating that wild-type basal levels of glutathione are required for the wound-induced resistance. Furthermore, expression of the gene encoding glutathione-S-transferase 1 was primed by wounding in leaves inoculated with B. cinerea. In addition, the priming of MAP kinase activity was observed after inoculation of wounded leaves with B. cinerea compared to unwounded inoculated controls. Our results demonstrate how abiotic stress can induce immunity to virulent strains of B. cinerea, a process that involves camalexin and glutathione.
Phytoalexin
Jasmonic acid
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The Ethylene-Responsive Factors (ERFs) comprise a large family of transcriptional factors that play critical roles in plant immunity. Gray mold disease caused by Botrytis cinerea, a typical necrotrophic fungal pathogen, is the serious disease that threatens tomato production worldwide. However, littler is known about the molecular mechanism regulating the immunity to B. cinerea in tomato. In the present study, virus-induced gene silencing (VIGS)-based functional analyses of 18 members of B3 group (also called Group IX) in tomato ERF family were performed to identify putative ERFs that are involved in disease resistance against B. cinerea. VIGS-based silencing of either SlERF.B1 or SlERF.C2 had lethal effect while silencing of SlERF.A3 (Pit4) significantly suppressed vegetative growth of tomato plants. Importantly, silencing of SlERF.A1, SlERF.A3, SlERF.B4, or SlERF.C3 resulted in increased susceptibility to B. cinerea, attenuated the B. cinerea-induced expression of jasmonic acid/ethylene-mediated signaling responsive defense genes and promoted the B. cinerea-induced H2O2 accumulation. However, silencing of SlERF.A3 also decreased the resistance against Pseudomonas syringae pv. tomato (Pst) DC3000 but silencing of SlERF.A1, SlERF.B4 or SlERF.C3 did not affect the resistance to this bacterial pathogen. Expression of SlERF.A1, SlERF.A3, SlERF.B4, or SlERF.C3 was induced by B. cinerea and by defense signaling hormones such as salicylic acid, methyl jasmonate, and 1-aminocyclopropane-1-carboxylic acid (an ethylene precursor). SlERF.A1, SlERF.B4, SlERF.C3, and SlERF.A3 proteins were found to localize in nucleus of cells and possess transactivation activity in yeasts. These data suggest that SlERF.A1, SlERF.B4, and SlERF.C3, three previously uncharacterized ERFs in B3 group, and SlERF.A3, a previously identified ERF with function in immunity to Pst DC3000, play important roles in resistance against B. cinerea in tomato.
Botrytis
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Pseudomonas syringae
Jasmonic acid
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T1N6_22, a short-chain dehydrogenase/reductase family protein, was identified as a positive regulator in Arabidopsis thaliana resistance against Botrytis cinerea and Alternaria brassicae in our preliminary study. In this study, we found that the expression levels of the T1N6_22 gene were induced and up-regulated in A. thaliana ecotype Columbia (Col-0) after B. cinerea and Pseudomonas syringae pv. tomato DC3000 inoculation. Compared with the Col-0 and t1n6_22/T1N6_22 plants, the expression of PAL, PR4, PPO, SOD and CAT genes were down-regulated in the t1n6_22 plants. In Col-0 plants treated with salicylic acid (SA) and the SA analogue benzo(1,2,3)thiadiazole-7-carbothioic acid S-methyl ester (BTH), the expression levels of T1N6_22 were significantly enhanced, whereas the expression levels of T1N6_22 were reduced by jasmonic acid treatment. Meanwhile, the t1n6_22 mutant exhibited enhanced resistance, whereas the wild-type Col-0 and complemented plants (t1n6_22/T1N6_22) showed susceptibility to Pst DC3000. After inoculation with B. cinerea and Pst DC3000, the expression levels of defence-related genes PR1, PR3, PR5, NPR1 and PDF1.2 in t1n6_22 were significantly different from those in Col-0 and t1n6_22/T1N6_22 plants. Taken together, the T1N6_22 gene played a negative role in Arabidopsis resistance to Pst DC3000. The T1N6_22 gene may be involved in the regulation of salicylic acid and jasmonic-acid–signalling pathways to affect the resistance of Arabidopsis to B. cinerea and Pst DC3000.
Pseudomonas syringae
Jasmonic acid
NPR1
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Abstract Transgenic tomato (Solanum lycopersicum) lines overexpressing yeast spermidine synthase (ySpdSyn), an enzyme involved in polyamine (PA) biosynthesis, were developed. These transgenic lines accumulate higher levels of spermidine (Spd) than the wild-type plants and were examined for responses to the fungal necrotrophs Botrytis cinerea and Alternaria solani, bacterial pathogen Pseudomonas syringae pv tomato DC3000, and larvae of the chewing insect tobacco hornworm (Manduca sexta). The Spd-accumulating transgenic tomato lines were more susceptible to B. cinerea than the wild-type plants; however, responses to A. solani, P. syringae, or M. sexta were similar to the wild-type plants. Exogenous application of ethylene precursors, S-adenosyl-Met and 1-aminocyclopropane-1-carboxylic acid, or PA biosynthesis inhibitors reversed the response of the transgenic plants to B. cinerea. The increased susceptibility of the ySpdSyn transgenic tomato to B. cinerea was associated with down-regulation of gene transcripts involved in ethylene biosynthesis and signaling. These data suggest that PA-mediated susceptibility to B. cinerea is linked to interference with the functions of ethylene in plant defense.
Pseudomonas syringae
Alternaria solani
Polyamine
Genetically modified tomato
Wild type
NPR1
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Although heat shock proteins (HSPs), a family of ubiquitous molecular chaperones, are well characterized in heat stress-related responses, their function in plant defense remains largely unclear. Here, we report the role of VvHSP24, a class B HSP from Vitis vinifera, in β-aminobutyric acid (BABA)-induced priming defense against the necrotrophic fungus Botrytis cinerea in grapes. Grapes treated with 10 mmol L-1 BABA exhibited transiently increased transcript levels of VvNPR1 and several SA-inducible genes, including PR1, PR2, and PR5. Additionally, phytoalexins accumulated upon inoculation with the gray mold fungus B. cinerea, which coincided with the action of a priming mode implicated in pathogen-driven resistance. Intriguingly, electrophoretic mobility shift (EMSA), yeast two-hybrid (Y2H) and His pull-down assays demonstrated that the nuclear chaperone VvHSP24 cannot modulate the transcript of PR genes but does directly interact with VvNPR1 in vivo or in vitro. Furthermore, we found that VvHSP24 overexpression enhanced the transcript levels of NPR1 and SA-responsive genes (PR1, PR2, and PR5) and increased the resistance of transgenic Arabidopsis thaliana to B. cinerea compared with wildtype Col-0. An opposite trend between CRISPR mutants of AtHSFB1 (the orthologous gene of VvHSP24 in Arabidopsis) and wildtype plants was observed. Hence, our results suggest that VvHSP24 has a potential role in NPR1-dependent plant resistance to fungal pathogen. BABA-induced priming defense in grapes may require posttranslational modification of the chaperone VvHSP24 to activate VvNPR1 transcript, leading to PR gene expressions and resistance phenotypes.
NPR1
Wild type
Chaperone (clinical)
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Summary C is ‐(+)‐12‐oxo‐phytodienoic acid ( OPDA ) is likely to play signaling roles in plant defense that do not depend on its further conversion to the phytohormone jasmonic acid. To elucidate the role of OPDA in S olanum lycopersicum (tomato) plant defense, we have silenced the 12‐oxophytodienoate reductase 3 ( OPR 3 ) gene. Two independent transgenic tomato lines ( Si OPR 3‐1 and Si OPR 3‐2 ) showed significantly reduced OPR 3 expression upon infection with the necrotrophic pathogen B otrytis cinerea . Moreover, Si OPR 3 plants are more susceptible to this pathogen, and this susceptibility is accompanied by a significant decrease in OPDA levels and by the production of JA ‐Ile being almost abolished. OPR 3 silencing also leads to a major reduction in the expression of other genes of the jasmonic acid ( JA ) synthesis and signaling pathways after infection. These results confirm that in tomato plants, as in A rabidopsis, OPR 3 determines OPDA availability for JA biosynthesis. In addition, we show that an intact JA biosynthetic pathway is required for proper callose deposition, as its pathogen‐induced accumulation is reduced in Si OPR 3 plants. Interestingly, OPDA , but not JA , treatment restored basal resistance to B . cinerea and induced callose deposition in Si OPR 3‐1 and Si OPR 3‐2 transgenic plants. These results provide clear evidence that OPDA by itself plays a major role in the basal defense of tomato plants against this necrotrophic pathogen.
Callose
Jasmonic acid
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Pseudomonas syringae
Methyl jasmonate
Callose
Systemic Acquired Resistance
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