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Development of disease-resistant rice using regulatory components of induced disease resistance.

Takatsuji H - Front Plant Sci (2014)

Bottom Line: This priming effect was similar to that of chemical defense inducers, although the fitness costs were amplified by some environmental factors.WRKY45 is degraded by the ubiquitin-proteasome system, and the dual role of this degradation partly explains the priming effect.The synergistic interaction between SA and cytokinin signaling that activates WRKY45 also likely contributes to the priming effect.

View Article: PubMed Central - PubMed

Affiliation: Disease Resistant Crops Research Unit, Genetically Modified Organism Research Center, National Institute of Agrobiological Sciences Tsukuba, Japan.

ABSTRACT
Infectious diseases cause huge crop losses annually. In response to pathogen attacks, plants activate defense systems that are mediated through various signaling pathways. The salicylic acid (SA) signaling pathway is the most powerful of these pathways. Several regulatory components of the SA signaling pathway have been identified, and are potential targets for genetic manipulation of plants' disease resistance. However, the resistance associated with these regulatory components is often accompanied by fitness costs; that is, negative effects on plant growth and crop yield. Chemical defense inducers, such as benzothiadiazole and probenazole, act on the SA pathway and induce strong resistance to various pathogens without major fitness costs, owing to their 'priming effect.' Studies on how benzothiadiazole induces disease resistance in rice have identified WRKY45, a key transcription factor in the branched SA pathway, and OsNPR1/NH1. Rice plants overexpressing WRKY45 were extremely resistant to rice blast disease caused by the fungus Magnaporthe oryzae and bacterial leaf blight disease caused by Xanthomonas oryzae pv. oryzae (Xoo), the two major rice diseases. Disease resistance is often accompanied by fitness costs; however, WRKY45 overexpression imposed relatively small fitness costs on rice because of its priming effect. This priming effect was similar to that of chemical defense inducers, although the fitness costs were amplified by some environmental factors. WRKY45 is degraded by the ubiquitin-proteasome system, and the dual role of this degradation partly explains the priming effect. The synergistic interaction between SA and cytokinin signaling that activates WRKY45 also likely contributes to the priming effect. With a main focus on these studies, I review the current knowledge of SA-pathway-dependent defense in rice by comparing it with that in Arabidopsis, and discuss potential strategies to develop disease-resistant rice using signaling components.

No MeSH data available.


Related in: MedlinePlus

Current status of knowledge about the SA signaling pathway in rice. The rice SA pathway branches into OsNPR1- and WRKY45-dependent sub-pathways. OsNPR1 positively regulates defense reactions and suppresses JA signaling, and also down-regulates cellular activities such as photosynthesis, thereby playing a role in resource allocation during defense responses. WRKY45 positively regulates disease resistance through downstream transcription factors; WRKY62, OsNAC4, and HSF1. The role of WRKY62 in defense needs further investigation because there are conflicting data. The degradation of WRKY45 by the UPS has two effects: defense suppression in the absence of pathogens; and defense enhancement upon SA-pathway activation and/or pathogen infection. ABA signaling, which mediates abiotic stresses, negatively regulates the SA-pathway-dependent defense by acting upstream of WRKY45 and OsNPR1 (red lines). Cytokinin signaling, which is activated by M. oryzae infection, acts synergistically with the SA pathway to trigger defense responses, thereby possibly underpinning the priming effect (purple lines). WRKY13, a transcriptional repressor, positively regulates OsNPR1 and disease resistance by acting upstream of OsNPR1. WRKY13 also plays a role in down-regulating drought tolerance of rice through repressing SNAC1. By contrast, WRKY76 suppresses disease resistance while enhancing cold tolerance.
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Figure 2: Current status of knowledge about the SA signaling pathway in rice. The rice SA pathway branches into OsNPR1- and WRKY45-dependent sub-pathways. OsNPR1 positively regulates defense reactions and suppresses JA signaling, and also down-regulates cellular activities such as photosynthesis, thereby playing a role in resource allocation during defense responses. WRKY45 positively regulates disease resistance through downstream transcription factors; WRKY62, OsNAC4, and HSF1. The role of WRKY62 in defense needs further investigation because there are conflicting data. The degradation of WRKY45 by the UPS has two effects: defense suppression in the absence of pathogens; and defense enhancement upon SA-pathway activation and/or pathogen infection. ABA signaling, which mediates abiotic stresses, negatively regulates the SA-pathway-dependent defense by acting upstream of WRKY45 and OsNPR1 (red lines). Cytokinin signaling, which is activated by M. oryzae infection, acts synergistically with the SA pathway to trigger defense responses, thereby possibly underpinning the priming effect (purple lines). WRKY13, a transcriptional repressor, positively regulates OsNPR1 and disease resistance by acting upstream of OsNPR1. WRKY13 also plays a role in down-regulating drought tolerance of rice through repressing SNAC1. By contrast, WRKY76 suppresses disease resistance while enhancing cold tolerance.

Mentions: NPR1 regulates nearly all of the BTH-responsive genes in Arabidopsis (Wang et al., 2006), except during early phases of pathogen infection (Li et al., 2004; Uquillas et al., 2004; Blanco et al., 2005). By contrast, the SA pathway in rice appears to branch into OsNPR1/NH1- and WRKY45-mediated sub-pathways (Figure 2), as revealed by an epistasis analysis and global gene expression analyses of BTH-responsive genes in OsNPR1/NH1-kd and WRKY45-kd rice transformants (Shimono et al., 2007; Sugano et al., 2010; Takatsuji et al., 2010; Nakayama et al., 2013). Overexpression of OsNPR1/NH1 down-regulated some genes, but up-regulated many other genes including numerous defense-related genes. The genes down-regulated by OsNPR1/NH1 included several involved in photosynthesis and protein synthesis. These results suggest that one of the functions of OsNPR1/NH1 is to divert resources from housekeeping cellular activities such as photosynthesis to defense responses (Figure 2; Sugano et al., 2010). A similar function was also inferred for Arabidopsis NPR1, based on the genome-wide transcriptome analysis of BTH-responsive genes in the Arabidopsis npr1 mutant (Wang et al., 2006; Sugano et al., 2010).


Development of disease-resistant rice using regulatory components of induced disease resistance.

Takatsuji H - Front Plant Sci (2014)

Current status of knowledge about the SA signaling pathway in rice. The rice SA pathway branches into OsNPR1- and WRKY45-dependent sub-pathways. OsNPR1 positively regulates defense reactions and suppresses JA signaling, and also down-regulates cellular activities such as photosynthesis, thereby playing a role in resource allocation during defense responses. WRKY45 positively regulates disease resistance through downstream transcription factors; WRKY62, OsNAC4, and HSF1. The role of WRKY62 in defense needs further investigation because there are conflicting data. The degradation of WRKY45 by the UPS has two effects: defense suppression in the absence of pathogens; and defense enhancement upon SA-pathway activation and/or pathogen infection. ABA signaling, which mediates abiotic stresses, negatively regulates the SA-pathway-dependent defense by acting upstream of WRKY45 and OsNPR1 (red lines). Cytokinin signaling, which is activated by M. oryzae infection, acts synergistically with the SA pathway to trigger defense responses, thereby possibly underpinning the priming effect (purple lines). WRKY13, a transcriptional repressor, positively regulates OsNPR1 and disease resistance by acting upstream of OsNPR1. WRKY13 also plays a role in down-regulating drought tolerance of rice through repressing SNAC1. By contrast, WRKY76 suppresses disease resistance while enhancing cold tolerance.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4230042&req=5

Figure 2: Current status of knowledge about the SA signaling pathway in rice. The rice SA pathway branches into OsNPR1- and WRKY45-dependent sub-pathways. OsNPR1 positively regulates defense reactions and suppresses JA signaling, and also down-regulates cellular activities such as photosynthesis, thereby playing a role in resource allocation during defense responses. WRKY45 positively regulates disease resistance through downstream transcription factors; WRKY62, OsNAC4, and HSF1. The role of WRKY62 in defense needs further investigation because there are conflicting data. The degradation of WRKY45 by the UPS has two effects: defense suppression in the absence of pathogens; and defense enhancement upon SA-pathway activation and/or pathogen infection. ABA signaling, which mediates abiotic stresses, negatively regulates the SA-pathway-dependent defense by acting upstream of WRKY45 and OsNPR1 (red lines). Cytokinin signaling, which is activated by M. oryzae infection, acts synergistically with the SA pathway to trigger defense responses, thereby possibly underpinning the priming effect (purple lines). WRKY13, a transcriptional repressor, positively regulates OsNPR1 and disease resistance by acting upstream of OsNPR1. WRKY13 also plays a role in down-regulating drought tolerance of rice through repressing SNAC1. By contrast, WRKY76 suppresses disease resistance while enhancing cold tolerance.
Mentions: NPR1 regulates nearly all of the BTH-responsive genes in Arabidopsis (Wang et al., 2006), except during early phases of pathogen infection (Li et al., 2004; Uquillas et al., 2004; Blanco et al., 2005). By contrast, the SA pathway in rice appears to branch into OsNPR1/NH1- and WRKY45-mediated sub-pathways (Figure 2), as revealed by an epistasis analysis and global gene expression analyses of BTH-responsive genes in OsNPR1/NH1-kd and WRKY45-kd rice transformants (Shimono et al., 2007; Sugano et al., 2010; Takatsuji et al., 2010; Nakayama et al., 2013). Overexpression of OsNPR1/NH1 down-regulated some genes, but up-regulated many other genes including numerous defense-related genes. The genes down-regulated by OsNPR1/NH1 included several involved in photosynthesis and protein synthesis. These results suggest that one of the functions of OsNPR1/NH1 is to divert resources from housekeeping cellular activities such as photosynthesis to defense responses (Figure 2; Sugano et al., 2010). A similar function was also inferred for Arabidopsis NPR1, based on the genome-wide transcriptome analysis of BTH-responsive genes in the Arabidopsis npr1 mutant (Wang et al., 2006; Sugano et al., 2010).

Bottom Line: This priming effect was similar to that of chemical defense inducers, although the fitness costs were amplified by some environmental factors.WRKY45 is degraded by the ubiquitin-proteasome system, and the dual role of this degradation partly explains the priming effect.The synergistic interaction between SA and cytokinin signaling that activates WRKY45 also likely contributes to the priming effect.

View Article: PubMed Central - PubMed

Affiliation: Disease Resistant Crops Research Unit, Genetically Modified Organism Research Center, National Institute of Agrobiological Sciences Tsukuba, Japan.

ABSTRACT
Infectious diseases cause huge crop losses annually. In response to pathogen attacks, plants activate defense systems that are mediated through various signaling pathways. The salicylic acid (SA) signaling pathway is the most powerful of these pathways. Several regulatory components of the SA signaling pathway have been identified, and are potential targets for genetic manipulation of plants' disease resistance. However, the resistance associated with these regulatory components is often accompanied by fitness costs; that is, negative effects on plant growth and crop yield. Chemical defense inducers, such as benzothiadiazole and probenazole, act on the SA pathway and induce strong resistance to various pathogens without major fitness costs, owing to their 'priming effect.' Studies on how benzothiadiazole induces disease resistance in rice have identified WRKY45, a key transcription factor in the branched SA pathway, and OsNPR1/NH1. Rice plants overexpressing WRKY45 were extremely resistant to rice blast disease caused by the fungus Magnaporthe oryzae and bacterial leaf blight disease caused by Xanthomonas oryzae pv. oryzae (Xoo), the two major rice diseases. Disease resistance is often accompanied by fitness costs; however, WRKY45 overexpression imposed relatively small fitness costs on rice because of its priming effect. This priming effect was similar to that of chemical defense inducers, although the fitness costs were amplified by some environmental factors. WRKY45 is degraded by the ubiquitin-proteasome system, and the dual role of this degradation partly explains the priming effect. The synergistic interaction between SA and cytokinin signaling that activates WRKY45 also likely contributes to the priming effect. With a main focus on these studies, I review the current knowledge of SA-pathway-dependent defense in rice by comparing it with that in Arabidopsis, and discuss potential strategies to develop disease-resistant rice using signaling components.

No MeSH data available.


Related in: MedlinePlus