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Redox proteomics of tomato in response to Pseudomonas syringae infection.

Balmant KM, Parker J, Yoo MJ, Zhu N, Dufresne C, Chen S - Hortic Res (2015)

Bottom Line: In addition, the results of the redox changes were compared and corrected with the protein level changes.A total of 90 potential redox-regulated proteins were identified with functions in carbohydrate and energy metabolism, biosynthesis of cysteine, sucrose and brassinosteroid, cell wall biogenesis, polysaccharide/starch biosynthesis, cuticle development, lipid metabolism, proteolysis, tricarboxylic acid cycle, protein targeting to vacuole, and oxidation-reduction.This inventory of previously unknown protein redox switches in tomato pathogen defense lays a foundation for future research toward understanding the biological significance of protein redox modifications in plant defense responses.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Genetics Institute, University of Florida , Gainesville, FL, USA ; Plant Molecular and Cellular Biology Program, University of Florida , Gainesville, FL, USA.

ABSTRACT
Unlike mammals with adaptive immunity, plants rely on their innate immunity based on pattern-triggered immunity (PTI) and effector-triggered immunity (ETI) for pathogen defense. Reactive oxygen species, known to play crucial roles in PTI and ETI, can perturb cellular redox homeostasis and lead to changes of redox-sensitive proteins through modification of cysteine sulfhydryl groups. Although redox regulation of protein functions has emerged as an important mechanism in several biological processes, little is known about redox proteins and how they function in PTI and ETI. In this study, cysTMT proteomics technology was used to identify similarities and differences of protein redox modifications in tomato resistant (PtoR) and susceptible (prf3) genotypes in response to Pseudomonas syringae pv tomato (Pst) infection. In addition, the results of the redox changes were compared and corrected with the protein level changes. A total of 90 potential redox-regulated proteins were identified with functions in carbohydrate and energy metabolism, biosynthesis of cysteine, sucrose and brassinosteroid, cell wall biogenesis, polysaccharide/starch biosynthesis, cuticle development, lipid metabolism, proteolysis, tricarboxylic acid cycle, protein targeting to vacuole, and oxidation-reduction. This inventory of previously unknown protein redox switches in tomato pathogen defense lays a foundation for future research toward understanding the biological significance of protein redox modifications in plant defense responses.

No MeSH data available.


Related in: MedlinePlus

The role of redox regulation in plant defense response. (a) Role of redox regulation of primary metabolic enzymes in plant defense response at early stage of infection. Redox regulation may serve as an activity switch to turn on or off the different connections between primary metabolism and defense response, playing a role in energy as well as signaling to directly or indirectly trigger defense responses. (b) Role of cysteine synthase oxidation and GS in plant defense response. Cysteine is the sulfur amino acid precursor of GSH, which plays a crucial role in maintaining cellular redox homeostasis. Oxidation of cysteine synthase may cause an increase in enzyme activity, leading to synthesis of more cysteines and further increase in the amount of GSH. Glutamate is a precursor of GSH and glutamine. Oxidation of GS decreases its activity, leading to less glutamine. This may cause an increase in the availability of glutamate for GSH production. (c) Role of redox regulation of enzymes belonging to carbohydrate metabolism, protein synthesis, and chaperone activity in plant defense response. It is likely that a synchronized interaction between sugar and hormonal signaling pathways leads to effective immune responses. Redox regulation of proteins of carbohydrate metabolism might affect apoplastic sugar levels, through which SAR is regulated. Redox regulation of proteins involved in protein synthesis may regulate enzyme activity in protein synthesis, which is an energy-consuming process, and therefore it is considered an important regulation step in stress responses. Oxidative stress is known to enhance misfolded proteins in the endoplasmic reticulum (ER), causing ER stress or unfolded protein response where proteins with chaperone activity play a crucial role. (d) Role of oxidation of KAT2 in the antagonistic interaction between SA and JA. Oxidation of KAT2, which is one of the three core enzymes that catalyze β-oxidation of JA synthesis, may lead to inactivation of KAT2.
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fig5: The role of redox regulation in plant defense response. (a) Role of redox regulation of primary metabolic enzymes in plant defense response at early stage of infection. Redox regulation may serve as an activity switch to turn on or off the different connections between primary metabolism and defense response, playing a role in energy as well as signaling to directly or indirectly trigger defense responses. (b) Role of cysteine synthase oxidation and GS in plant defense response. Cysteine is the sulfur amino acid precursor of GSH, which plays a crucial role in maintaining cellular redox homeostasis. Oxidation of cysteine synthase may cause an increase in enzyme activity, leading to synthesis of more cysteines and further increase in the amount of GSH. Glutamate is a precursor of GSH and glutamine. Oxidation of GS decreases its activity, leading to less glutamine. This may cause an increase in the availability of glutamate for GSH production. (c) Role of redox regulation of enzymes belonging to carbohydrate metabolism, protein synthesis, and chaperone activity in plant defense response. It is likely that a synchronized interaction between sugar and hormonal signaling pathways leads to effective immune responses. Redox regulation of proteins of carbohydrate metabolism might affect apoplastic sugar levels, through which SAR is regulated. Redox regulation of proteins involved in protein synthesis may regulate enzyme activity in protein synthesis, which is an energy-consuming process, and therefore it is considered an important regulation step in stress responses. Oxidative stress is known to enhance misfolded proteins in the endoplasmic reticulum (ER), causing ER stress or unfolded protein response where proteins with chaperone activity play a crucial role. (d) Role of oxidation of KAT2 in the antagonistic interaction between SA and JA. Oxidation of KAT2, which is one of the three core enzymes that catalyze β-oxidation of JA synthesis, may lead to inactivation of KAT2.

Mentions: Some studies have shown the association between defense responses and primary metabolism in processes involved in energy production, such as glycolysis and the pentose phosphate pathway, TCA cycle, mitochondrial electron transport, ATP biosynthesis, and biosynthesis of some amino acids.49,50 In PtoR plants, Pst infection caused redox regulation of serine hydromethyltranferase, ATP synthase, aminomethyltransferase, phosphoglycerate kinase, and fructose 1,6-biphosphatase that were identified as being more reduced upon Pst infection (Table 2). Among the proteins, ATP synthase and phosphoglycerate kinase were found to be redox-regulated in previous studies.19,42 With the exception of aminomethyltransferase, all the other proteins are known to be thioredoxin targets.51 In the prf3 plants, only three proteins related to primary metabolism were found to be redox-regulated after Pst infection. Triosephosphate isomerase was reduced, while ATP synthase CF1 beta subunit (chloroplastic) and ATP synthase subunit beta (mitochondrial) were oxidized in response to pathogen infection (Table 1). Triosephosphate isomerase protein was already previously reported to be S-nitrosylated during HR.52 All the three proteins are known to be thioredoxin targets.51 It is accepted that the complexity of plant defense responses requires abundant amount of energy.49 In addition, the primary metabolic pathways play a role as a source of signaling molecules to directly or indirectly trigger defense responses.53 Based on the above results, it is plausible that redox regulation of these proteins serves as an activity switch to turn on or off the different connections between carbohydrate metabolism and defense responses (Figure 5a).


Redox proteomics of tomato in response to Pseudomonas syringae infection.

Balmant KM, Parker J, Yoo MJ, Zhu N, Dufresne C, Chen S - Hortic Res (2015)

The role of redox regulation in plant defense response. (a) Role of redox regulation of primary metabolic enzymes in plant defense response at early stage of infection. Redox regulation may serve as an activity switch to turn on or off the different connections between primary metabolism and defense response, playing a role in energy as well as signaling to directly or indirectly trigger defense responses. (b) Role of cysteine synthase oxidation and GS in plant defense response. Cysteine is the sulfur amino acid precursor of GSH, which plays a crucial role in maintaining cellular redox homeostasis. Oxidation of cysteine synthase may cause an increase in enzyme activity, leading to synthesis of more cysteines and further increase in the amount of GSH. Glutamate is a precursor of GSH and glutamine. Oxidation of GS decreases its activity, leading to less glutamine. This may cause an increase in the availability of glutamate for GSH production. (c) Role of redox regulation of enzymes belonging to carbohydrate metabolism, protein synthesis, and chaperone activity in plant defense response. It is likely that a synchronized interaction between sugar and hormonal signaling pathways leads to effective immune responses. Redox regulation of proteins of carbohydrate metabolism might affect apoplastic sugar levels, through which SAR is regulated. Redox regulation of proteins involved in protein synthesis may regulate enzyme activity in protein synthesis, which is an energy-consuming process, and therefore it is considered an important regulation step in stress responses. Oxidative stress is known to enhance misfolded proteins in the endoplasmic reticulum (ER), causing ER stress or unfolded protein response where proteins with chaperone activity play a crucial role. (d) Role of oxidation of KAT2 in the antagonistic interaction between SA and JA. Oxidation of KAT2, which is one of the three core enzymes that catalyze β-oxidation of JA synthesis, may lead to inactivation of KAT2.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4591677&req=5

fig5: The role of redox regulation in plant defense response. (a) Role of redox regulation of primary metabolic enzymes in plant defense response at early stage of infection. Redox regulation may serve as an activity switch to turn on or off the different connections between primary metabolism and defense response, playing a role in energy as well as signaling to directly or indirectly trigger defense responses. (b) Role of cysteine synthase oxidation and GS in plant defense response. Cysteine is the sulfur amino acid precursor of GSH, which plays a crucial role in maintaining cellular redox homeostasis. Oxidation of cysteine synthase may cause an increase in enzyme activity, leading to synthesis of more cysteines and further increase in the amount of GSH. Glutamate is a precursor of GSH and glutamine. Oxidation of GS decreases its activity, leading to less glutamine. This may cause an increase in the availability of glutamate for GSH production. (c) Role of redox regulation of enzymes belonging to carbohydrate metabolism, protein synthesis, and chaperone activity in plant defense response. It is likely that a synchronized interaction between sugar and hormonal signaling pathways leads to effective immune responses. Redox regulation of proteins of carbohydrate metabolism might affect apoplastic sugar levels, through which SAR is regulated. Redox regulation of proteins involved in protein synthesis may regulate enzyme activity in protein synthesis, which is an energy-consuming process, and therefore it is considered an important regulation step in stress responses. Oxidative stress is known to enhance misfolded proteins in the endoplasmic reticulum (ER), causing ER stress or unfolded protein response where proteins with chaperone activity play a crucial role. (d) Role of oxidation of KAT2 in the antagonistic interaction between SA and JA. Oxidation of KAT2, which is one of the three core enzymes that catalyze β-oxidation of JA synthesis, may lead to inactivation of KAT2.
Mentions: Some studies have shown the association between defense responses and primary metabolism in processes involved in energy production, such as glycolysis and the pentose phosphate pathway, TCA cycle, mitochondrial electron transport, ATP biosynthesis, and biosynthesis of some amino acids.49,50 In PtoR plants, Pst infection caused redox regulation of serine hydromethyltranferase, ATP synthase, aminomethyltransferase, phosphoglycerate kinase, and fructose 1,6-biphosphatase that were identified as being more reduced upon Pst infection (Table 2). Among the proteins, ATP synthase and phosphoglycerate kinase were found to be redox-regulated in previous studies.19,42 With the exception of aminomethyltransferase, all the other proteins are known to be thioredoxin targets.51 In the prf3 plants, only three proteins related to primary metabolism were found to be redox-regulated after Pst infection. Triosephosphate isomerase was reduced, while ATP synthase CF1 beta subunit (chloroplastic) and ATP synthase subunit beta (mitochondrial) were oxidized in response to pathogen infection (Table 1). Triosephosphate isomerase protein was already previously reported to be S-nitrosylated during HR.52 All the three proteins are known to be thioredoxin targets.51 It is accepted that the complexity of plant defense responses requires abundant amount of energy.49 In addition, the primary metabolic pathways play a role as a source of signaling molecules to directly or indirectly trigger defense responses.53 Based on the above results, it is plausible that redox regulation of these proteins serves as an activity switch to turn on or off the different connections between carbohydrate metabolism and defense responses (Figure 5a).

Bottom Line: In addition, the results of the redox changes were compared and corrected with the protein level changes.A total of 90 potential redox-regulated proteins were identified with functions in carbohydrate and energy metabolism, biosynthesis of cysteine, sucrose and brassinosteroid, cell wall biogenesis, polysaccharide/starch biosynthesis, cuticle development, lipid metabolism, proteolysis, tricarboxylic acid cycle, protein targeting to vacuole, and oxidation-reduction.This inventory of previously unknown protein redox switches in tomato pathogen defense lays a foundation for future research toward understanding the biological significance of protein redox modifications in plant defense responses.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Genetics Institute, University of Florida , Gainesville, FL, USA ; Plant Molecular and Cellular Biology Program, University of Florida , Gainesville, FL, USA.

ABSTRACT
Unlike mammals with adaptive immunity, plants rely on their innate immunity based on pattern-triggered immunity (PTI) and effector-triggered immunity (ETI) for pathogen defense. Reactive oxygen species, known to play crucial roles in PTI and ETI, can perturb cellular redox homeostasis and lead to changes of redox-sensitive proteins through modification of cysteine sulfhydryl groups. Although redox regulation of protein functions has emerged as an important mechanism in several biological processes, little is known about redox proteins and how they function in PTI and ETI. In this study, cysTMT proteomics technology was used to identify similarities and differences of protein redox modifications in tomato resistant (PtoR) and susceptible (prf3) genotypes in response to Pseudomonas syringae pv tomato (Pst) infection. In addition, the results of the redox changes were compared and corrected with the protein level changes. A total of 90 potential redox-regulated proteins were identified with functions in carbohydrate and energy metabolism, biosynthesis of cysteine, sucrose and brassinosteroid, cell wall biogenesis, polysaccharide/starch biosynthesis, cuticle development, lipid metabolism, proteolysis, tricarboxylic acid cycle, protein targeting to vacuole, and oxidation-reduction. This inventory of previously unknown protein redox switches in tomato pathogen defense lays a foundation for future research toward understanding the biological significance of protein redox modifications in plant defense responses.

No MeSH data available.


Related in: MedlinePlus