scholarly journals Necrotrophic Pathogens Use the Salicylic Acid Signaling Pathway to Promote Disease Development in Tomato

2012 ◽  
Vol 25 (12) ◽  
pp. 1584-1593 ◽  
Author(s):  
Taha Abd El Rahman ◽  
Mohamed El Oirdi ◽  
Rocio Gonzalez-Lamothe ◽  
Kamal Bouarab

Plants use different immune pathways to combat pathogens. The activation of the jasmonic acid (JA)-signaling pathway is required for resistance against necrotrophic pathogens; however, to combat biotrophic pathogens, the plants activate mainly the salicylic acid (SA)-signaling pathway. SA can antagonize JA signaling and vice versa. NPR1 (noninducible pathogenesis-related 1) is considered a master regulator of SA signaling. NPR1 interacts with TGA transcription factors, ultimately leading to the activation of SA-dependent responses. SA has been shown to promote disease development caused by the necrotrophic pathogen Botrytis cinerea through NPR1, by suppressing the expression of two JA-dependent defense genes, proteinase inhibitors I and II. We show here that the transcription factor TGA1.a contributes to disease development caused by B. cinerea in tomato by suppressing the expression of proteinase inhibitors I and II. Finally, we present evidence that the SA-signaling pathway contributes to disease development caused by another necrotrophic pathogen, Alternaria solani, in tomato. Disease development promoted by SA through NPR1 requires the TGA1.a transcription factor. These data highlight how necrotrophs manipulate the SA-signaling pathway to promote their disease in tomato.

2018 ◽  
Vol 116 (2) ◽  
pp. 490-495 ◽  
Author(s):  
Hong-Xing Xu ◽  
Li-Xin Qian ◽  
Xing-Wei Wang ◽  
Ruo-Xuan Shao ◽  
Yue Hong ◽  
...  

Phloem-feeding insects feed on plant phloem using their stylets. While ingesting phloem sap, these insects secrete saliva to circumvent plant defenses. Previous studies have shown that, to facilitate their feeding, many phloem-feeding insects can elicit the salicylic acid- (SA-) signaling pathway and thus suppress effective jasmonic acid defenses. However, the molecular basis for the regulation of the plant's defense by phloem-feeding insects remains largely unknown. Here, we show that Bt56, a whitefly-secreted low molecular weight salivary protein, is highly expressed in the whitefly primary salivary gland and is delivered into host plants during feeding. Overexpression of the Bt56 gene in planta promotes susceptibility of tobacco to the whitefly and elicits the SA-signaling pathway. In contrast, silencing the whitefly Bt56 gene significantly decreases whitefly performance on host plants and interrupts whitefly phloem feeding with whiteflies losing the ability to activate the SA pathway. Protein-protein interaction assays show that the Bt56 protein directly interacts with a tobacco KNOTTED 1-like homeobox transcription factor that decreases whitefly performance and suppresses whitefly-induced SA accumulation. The Bt56 orthologous genes are highly conserved but differentially expressed in different species of whiteflies. In conclusion, Bt56 is a key salivary effector that promotes whitefly performance by eliciting salicylic acid-signaling pathway.


2018 ◽  
Vol 46 (2) ◽  
pp. 356-364
Author(s):  
Ufkun SARISOY ◽  
Burcu SECKIN DINLER ◽  
Eda TASCI

Non-expressor of Pathogen Related 1 (NPR1) is a regulatory gene of the salicylic acid (SA) signaling pathway, the detailed mechanism of which is still not well understood. This study investigated the effects of NPR1-dependent SA level change on increasing salt tolerance of soybean leaves with acclimation. Salt-sensitive (‘SA88’) and salt-tolerant (‘Erensoy’) soybean (Glycine max L.) plants were treated with increasing NaCl concentrations (25, 50, 75, and 100 mM; acclimation) and with 100 mM NaCl directly (non-acclimation) in two groups. The results showed that acclimation treatment alleviated salt-induced damage in the sensitive cultivar with increasing superoxide anion radical scavenging activity, and decreasing hydrogen peroxide (H2O2) and malondialdehyde (MDA) content. However, the APX, CAT, and GST enzyme activities were increased by acclimation treatment, with the highest increase observed in GST enzymes. Interestingly, the Gmnpr1 gene expression was upregulated in all treatments but was more pronounced in non-acclimation. Furthermore, the highest increase in endogenous SA level was under acclimation treatment in ‘SA88’. In conclusion, the results firstly showed that an acclimation process is useful for increasing salt tolerance in sensitive soybean plants with only ROS-inducted NPR1-independent SA accumulation but not through the NPR1-dependent SA signaling pathway.


2006 ◽  
Vol 19 (6) ◽  
pp. 655-664 ◽  
Author(s):  
Qi Li ◽  
Qi-Guang Xie ◽  
Jennifer Smith-Becker ◽  
Duroy A. Navarre ◽  
Isgouhi Kaloshian

The tomato Mi-1 gene confers resistance to root-knot nematodes (Meloidogyne spp.), potato aphids (Macrosiphum euphorbiae), and whiteflies (Bemisia tabaci and B. tabaci biotype B). Resistance to potato aphid is developmentally regulated and is not associated with induction of a hypersensitive response. The NahG transgene that eliminates endogenous salicylic acid (SA) was used to test the role of the SA signaling pathway in the resistance mediated by Mi-1 to potato aphids. Aphids survived longer on NahG tomato plants than on wild type. However, aphid reproduction was not affected on NahG tomato. Aphid resistance in Mi-1 NahG plants was completely abolished and the phenotype was successfully rescued by application of BTH (benzo(1,2,3)-thiaiazole-7-carbothioic acid S-methyl ester), indicating that the SA signaling pathway is an important component of Mi-1-mediated aphid resistance. Using virus-induced gene silencing, one or more mitogen-activated protein kinase (MAPK) cascades required for Mi-1-mediated aphid resistance were identified. Silencing plants for MAPK kinase (LeMKK2) and MAPKs (LeMPK2 and LeMPK1, or LeMPK3) resulted in attenuation of Mi-1-mediated aphid resistance. These results further demonstrate that resistance gene-mediated signaling events against piercing-sucking insects are similar to those against other plant pathogens.


2009 ◽  
Vol 22 (2) ◽  
pp. 166-175 ◽  
Author(s):  
Go Atsumi ◽  
Uiko Kagaya ◽  
Hiroaki Kitazawa ◽  
Kenji Suto Nakahara ◽  
Ichiro Uyeda

The wild-type strain (Cl-WT) of Clover yellow vein virus (ClYVV) systemically induces cell death in pea cv. Plant introduction (PI) 118501 but not in PI 226564. A single incompletely dominant gene, Cyn1, controls systemic cell death in PI 118501. Here, we show that activation of the salicylic acid (SA) signaling pathway enhances ClYVV virulence in susceptible pea cultivars. The kinetics of virus accumulation was not significantly different between PI 118501 (Cyn1) and PI 226564 (cyn1); however, the SA-responsive chitinase gene (SA-CHI) and the hypersensitive response (HR)-related gene homologous to tobacco HSR203J were induced only in PI 118501 (Cyn1). Two mutant viruses with mutations in P1/HCPro, which is an RNA-silencing suppressor, reduced the ability to induce cell death and SA-CHI expression. The application of SA and of its analog benzo (1,2,3) thiadiazole-7-carbothioic acid S-methyl ester (BTH) partially complemented the reduced virulence of mutant viruses. These results suggest that high activation of the SA signaling pathway is required for ClYVV virulence. Interestingly, BTH could enhance Cl-WT symptoms in PI 226564 (cyn1). However, it could not enhance symptoms induced by White clover mosaic virus and Bean yellow mosaic virus. Our report suggests that the SA signaling pathway has opposing functions in compatible interactions, depending on the virus–host combination.


2021 ◽  
Vol 22 (22) ◽  
pp. 12197
Author(s):  
Nengxu Sun ◽  
Xiangjiu Kong ◽  
Yueyan Liu ◽  
Tingting Gong ◽  
Xiaoyong Gu ◽  
...  

Salicylic acid (SA) and jasmonic acid (JA) are essential plant immune hormones, which could induce plant resistance to multiple pathogens. However, whether common components are employed by both SA and JA to induce defense is largely unknown. In this study, we found that the enhanced disease susceptibility 8 (EDS8) mutant was compromised in plant defenses to hemibiotrophic pathogen Pseudomonas syringae pv. maculicola ES4326 and necrotrophic pathogen Botrytis cinerea, and was deficient in plant responses to both SA and JA. The EDS8 was identified to be THO1, which encodes a subunit of the THO/TREX complex, by using mapping-by-sequencing. To check whether the EDS8 itself or the THO/TREX complex mediates SA and JA signaling, the mutant of another subunit of the THO/TREX complex, THO3, was tested. THO3 mutation reduced both SA and JA induced defenses, indicating that the THO/TREX complex is critical for plant responses to these two hormones. We further proved that the THO/TREX interacting protein SERRATE, a factor regulating alternative splicing (AS), was involved in plant responses to SA and JA. Thus, the AS events in the eds8 mutant after SA or JA treatment were determined, and we found that the SA and JA induced different alternative splicing events were majorly modulated by EDS8. In summary, our study proves that the THO/TREX complex active in AS is involved in both SA and JA induced plant defenses.


2021 ◽  
Vol 12 ◽  
Author(s):  
Zhiyuan Lv ◽  
Lijuan Hao ◽  
Bi Ma ◽  
Ziwen He ◽  
Yiwei Luo ◽  
...  

Ciboria carunculoides is the dominant causal agent of mulberry sclerotial disease, and it is a necrotrophic fungal pathogen with a narrow host range that causes devastating diseases in mulberry fruit. However, little is known about the interaction between C. carunculoides and mulberry. Here, our transcriptome sequencing results showed that the transcription of genes in the secondary metabolism and defense-related hormone pathways were significantly altered in infected mulberry fruit. Due to the antimicrobial properties of proanthocyanidins (PAs), the activation of PA biosynthetic pathways contributes to defense against pathogens. Salicylic acid (SA) and jasmonic acid (JA) are major plant defense hormones. However, SA signaling and JA signaling are antagonistic to each other. Our results showed that SA signaling was activated, while JA signaling was inhibited, in mulberry fruit infected with C. carunculoides. Yet SA mediated responses are double-edged sword against necrotrophic pathogens, as SA not only activates systemic acquired resistance (SAR) but also suppresses JA signaling. We also show here that the small secreted protein CcSSP1 of C. carunculoides activates SA signaling by targeting pathogenesis-related protein 1 (PR1). These findings reveal that the infection strategy of C. carunculoides functions by regulating SA signaling to inhibit host defense responses.


2010 ◽  
Vol 23 (6) ◽  
pp. 791-798 ◽  
Author(s):  
Chang-Jie Jiang ◽  
Masaki Shimono ◽  
Shoji Sugano ◽  
Mikiko Kojima ◽  
Katsumi Yazawa ◽  
...  

Plant hormones play pivotal signaling roles in plant–pathogen interactions. Here, we report characterization of an antagonistic interaction of abscisic acid (ABA) with salicylic acid (SA) signaling pathways in the rice–Magnaporthe grisea interaction. Exogenous application of ABA drastically compromised the rice resistance to both compatible and incompatible M. grisea strains, indicating that ABA negatively regulates both basal and resistance gene–mediated blast resistance. ABA markedly suppressed the transcriptional upregulation of WRKY45 and OsNPR1, the two key components of the SA signaling pathway in rice, induced by SA or benzothiadiazole or by blast infection. Overexpression of OsNPR1 or WRKY45 largely negated the enhancement of blast susceptibility by ABA, suggesting that ABA acts upstream of WRKY45 and OsNPR1 in the rice SA pathway. ABA-responsive genes were induced during blast infection in a pattern reciprocal to those of WRKY45 and OsPR1b in the compatible rice–blast interaction but only marginally in the incompatible one. These results suggest that the balance of SA and ABA signaling is an important determinant for the outcome of the rice–M. grisea interaction. ABA was detected in hyphae and conidia of M. grisea as well as in culture media, implying that blast-fungus-derived ABA could play a role in triggering ABA signaling at host infection sites.


2020 ◽  
Vol 11 ◽  
Author(s):  
Zenglin Zhang ◽  
Mengmeng Xu ◽  
Yongfeng Guo

Leaf senescence is regulated by a large number of internal and environmental factors. Here, we report that AtUSR1 (U-box Senescence Related 1) which encodes a plant Ring/U-box protein, is involved in age-dependent and dark-induced leaf senescence in Arabidopsis. Expression of AtUSR1 gene in leaves was up-regulated in darkness and during aging. Plants of usr1, an AtUSR1 gene knock-down mutant, showed a significant delay in age-dependent and dark-induced leaf senescence and the delayed senescence phenotype was rescued when the AtUSR1 gene was transferred back to the mutant plants. Meanwhile, overexpression of AtUSR1 caused accelerated leaf senescence. Furthermore, the role of AtUSR1 in regulating leaf senescence is related to MYC2-mediuated jasmonic acid (JA) signaling pathway. MeJA treatments promoted the accumulation of AtUSR1 transcripts and this expression activation was dependent on the function of MYC2, a key transcription factor in JA signaling. Dual-luciferase assay results indicated that MYC2 promoted the expression of AtUSR1. Overexpression of AtUSR1 in myc2 mutant plants showed precocious senescence, while myc2 mutation alone caused a delay in leaf senescence, suggesting that AtUSR1 functions downstream to MYC2 in the JA signaling pathway in promoting leaf senescence.


Rice ◽  
2020 ◽  
Vol 13 (1) ◽  
Author(s):  
An-Po Cheng ◽  
Szu-Yu Chen ◽  
Ming-Hsin Lai ◽  
Dong-Hong Wu ◽  
Shih-Shun Lin ◽  
...  

Abstract Background Bakanae is a seedborne disease caused by Fusarium fujikuroi. Rice seedlings emerging from infected seeds can show diverse symptoms such as elongated and slender stem and leaves, pale coloring, a large leaf angle, stunted growth and even death. Little is known about rice defense mechanisms at early stages of disease development. Results This study focused on investigating early defenses against F. fujikuroi in a susceptible cultivar, Zerawchanica karatals (ZK), and a resistant cultivar, Tainung 67 (TNG67). Quantitative PCR revealed that F. fujikuroi colonizes the root and stem but not leaf tissues. Illumina sequencing was conducted to analyze the stem transcriptomes of F. fujikuroi-inoculated and mock-inoculated ZK and TNG67 plants collected at 7 days post inoculation (dpi). More differentially expressed genes (DEGs) were identified in ZK (n = 169) than TNG67 (n = 118), and gene ontology terms related to transcription factor activity and phosphorylation were specifically enriched in ZK DEGs. Among the complex phytohormone biosynthesis and signaling pathways, only DEGs involved in the jasmonic acid (JA) signaling pathway were identified. Fourteen DEGs encoding pattern-recognition receptors, transcription factors, and JA signaling pathway components were validated by performing quantitative reverse transcription PCR analysis of individual plants. Significant repression of jasmonate ZIM-domain (JAZ) genes (OsJAZ9, OsJAZ10, and OsJAZ13) at 3 dpi and 7 dpi in both cultivars, indicated the activation of JA signaling during early interactions between rice and F. fujikuroi. Differential expression was not detected for salicylic acid marker genes encoding phenylalanine ammonia-lyase 1 and non-expressor of pathogenesis-related genes 1. Moreover, while MeJA did not affect the viability of F. fujikuroi, MeJA treatment of rice seeds (prior to or after inoculation) alleviated and delayed bakanae disease development in susceptible ZK. Conclusions Different from previous transcriptome studies, which analyzed the leaves of infected plants, this study provides insights into defense-related gene expression patterns in F. fujikuroi–colonized rice stem tissues. Twelve out of the 14 selected DEGs were for the first time shown to be associated with disease resistance, and JA-mediated resistance was identified as a crucial component of rice defense against F. fujikuroi. Detailed mechanisms underlying the JA-mediated bakanae resistance and the novel defense-related DEGs are worthy of further investigation.


2020 ◽  
Vol 21 (19) ◽  
pp. 7126
Author(s):  
Qiang Ma ◽  
Nuohan Wang ◽  
Liang Ma ◽  
Jianhua Lu ◽  
Hantao Wang ◽  
...  

Verticillium wilt will seriously affect cotton yield and fiber quality. BEL1-Like transcription factors are involved in the regulation of secondary cell wall (SCW) formation, especially the biosynthesis of lignin that also plays a key role in cotton disease resistance. However, there is no report on the role of BEL1-Like transcription factor in the regulation of plant biological stress. In this study, tissue expression pattern analysis showed that a BEL1-Like transcription factor GhBLH7-D06 was predominantly expressed in vascular tissues and the SCW thickening stage of fiber development, while its expression could also respond to Verticillium dahliae infection and the phytohormone MeJA treatment, which indicated that GhBLH7-D06 might be involved in the defense response of Verticillium wilt. Using virus-induced gene silencing (VIGS) technology, we found silencing the expression of GhBLH7-D06 could enhance the resistance of cotton plants to Verticillium wilt, and the acquisition of resistance might be mainly due to the significant overexpression of genes related to lignin biosynthesis and JA signaling pathway, which also proves that GhBLH7-D06 negatively regulates the resistance of cotton to Verticillium wilt. Based on the results of yeast two-hybrid (Y2H) library screening and confirmation by bimolecular fluorescence complementary (BiFC) experiment, we found an Ovate Family Protein (OFP) transcription factor GhOFP3-D13 which was also a negative regulator of cotton Verticillium wilt resistance could that interacts with GhBLH7-D06. Furthermore, the dual-luciferase reporter assay and yeast one-hybrid (Y1H) experiment indicated that GhBLH7-D06 could target binding to the promoter region of GhPAL-A06 to suppress its expression and eventually lead to the inhibition of lignin biosynthesis. In general, the GhBLH7-D06/GhOFP3-D13 complex can negatively regulate resistance to Verticillium wilt of cotton by inhibiting lignin biosynthesis and JA signaling pathway.


Sign in / Sign up

Export Citation Format

Share Document