The Resistance of Narrow-Leafed Lupin to Diaporthe toxica Is Based on the Rapid Activation of Defense Response Genes
Abstract
:1. Introduction
2. Results
2.1. Isolates of Diaporthe toxica Represented a Diverse Gene Pool That Is Related to the Host Plant
2.2. PhtjR and Phr1 Alleles Conferred a High Level of Resistance to Diaporthe toxica
2.3. Resistance to D. toxica Was Associated with Rapid Transcriptome Reprogramming
2.4. Early Reaction of Resistant Lines Was Based on the Activation of the Defense Response and Oxylipin Biosynthesis Genes
2.5. Genes from Defense Response Pathways Experienced up to a Thousandfold Upregulation in Inoculated Plants
3. Discussion
3.1. Genotype Profiling of Diaporthe toxica Isolates
3.2. Mechanisms Involved in Lupinus angustifolius’ Defense Response to Diaporthe toxica
3.2.1. Peroxidases and Reaction Oxygen Species
3.2.2. Glutathione S-Transferase-Like Genes
3.2.3. WRKY Transcription Factors
3.2.4. Isoflavonoid Biosynthesis Pathway
3.2.5. Lipoxygenase Pathway
3.2.6. Xyloglucan Endotransglucosylases/Hydrolases
3.2.7. Systemic Acquired Resistance Signaling
3.2.8. Pathogenesis-Related Protein Class PR10
3.2.9. Concluding Remarks
4. Materials and Methods
4.1. DNA Polymorphisms of D. toxica Isolates
4.2. Plant Material
4.3. Genotyping for the Phr1 and PhtjR Alleles
4.4. D. toxica Experiment in Controlled Conditions
4.5. RNA Isolation
4.6. RNA Sequencing and Data Analysis
4.7. Selection of Genes for Quantitative Expression Profiling
4.8. Quantitative Gene Expression Analysis
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Abbreviations
cv. | cultivar |
DIR1 | defective in induced resistance 1 |
dpi | day post inoculation |
GST | glutathione S-transferase |
ITS | internal transcribed spacer |
Phr1 | allele conferring D. toxica resistance in the 75A:258 L. angustifolius line |
Phr2 | allele conferring D. toxica resistance in the L. angustifolius cultivar Merrit |
PhtjR | allele conferring D. toxica resistance in the L. angustifolius cultivar Wonga |
RAPD | random amplification of polymorphic DNA |
SAM22 | starvation-associated message 22 |
SAR | systemic acquired resistance |
WGCNA | weighted gene co-expression network analysis |
XTH | xyloglucan endotransglucosylase/hydrolase |
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Accession | Line | Ph25M1 Phr1 | Ph258M2 Phr1 | PhtjM7 PhtjR | InDel2 PhtjR | InDel10 PhtjR | Disease Index 2017 1 | Disease Index 2018 2 | Resistance Genes |
---|---|---|---|---|---|---|---|---|---|
96191 | Wonga | S 3 | S | R | R | R | 1.8 ± 1.3 | 1.3 ± 0.4 | PhtjR |
96214 | Tanjil | S | S | R | R | R | 2.2 ± 1.4 | 2.2 ± 1.4 | PhtjR |
26979 | 75A:258 | R 4 | R | S | S | S | 1.7 ± 1.3 | 1.7 ± 1.3 | Phr1 |
96102 | Unicrop | S | S | S | S | S | 3.4 ± 1.7 | 3.4 ± 1.5 | - |
96121 | Emir | S | S | S | S | S | 5.2 ± 1.8 | 4.1 ± 1.1 | - |
96210 | Baron | S | S | S | S | S | 4.3 ± 1.3 | 5.2 ± 1.4 | - |
Line | Response | 1 dpi 1 | 5 dpi | 9 dpi | 16 dpi | 23 dpi |
---|---|---|---|---|---|---|
75A:258 (Phr1, phtjR) | Repression | 83 | 24 | 36 | 86 | 153 |
Induction | 259 | 672 | 156 | 418 | 691 | |
Wonga (phr1, PhtjR) | Repression | 65 | 132 | 418 | - 2 | - |
Induction | 364 | 534 | 1166 | |||
Emir (phr1, phtjR) | Repression | 53 | 26 | 208 | - | - |
Induction | 101 | 230 | 1496 |
Line. | 75A:258 | Wonga | Emir | ||||||
---|---|---|---|---|---|---|---|---|---|
Days Post Inoculation | 1 1 | 5 | 9 | 1 | 5 | 9 | 1 | 5 | 9 |
Defense response | 2.4 2 | >3 | >3 | 2.7 | >3 | >3 | >3 | >3 | |
Response to stress | >3 | >3 | >3 | >3 | >3 | 1.8 | |||
Oxidation-reduction process | >3 | >3 | 2.7 | >3 | >3 | ||||
Antibiotic catabolic process | >3 | >3 | >3 | >3 | |||||
Cofactor catabolic process | 2.7 | >3 | 3.0 | >3 | |||||
Drug catabolic process | 2.7 | >3 | 3.0 | >3 | |||||
Hydrogen peroxide catabolic process | >3 | >3 | >3 | >3 | |||||
Hydrogen peroxide metabolic process | >3 | >3 | >3 | >3 | |||||
Nucleic acid-templated transcription | 2.2 | 1.9 | 2.5 | 2.0 | |||||
Reactive oxygen species metabolic process | >3 | >3 | >3 | >3 | |||||
Regulation of biosynthetic process | 2.7 | 2.5 | >3 | >3 | |||||
Regulation of cellular biosynthetic process | 2.7 | 2.5 | >3 | >3 | |||||
Regulation of cellular macromolecule biosynthetic process | 3.0 | 3.0 | >3 | >3 | |||||
Regulation of cellular metabolic process | 1.8 | 1.7 | 2.5 | 2.0 | |||||
Regulation of gene expression | 2.2 | 2.5 | 2.5 | 2.1 | |||||
Regulation of macromolecule biosynthetic process | 2.7 | 2.7 | >3 | >3 | |||||
Regulation of macromolecule metabolic process | 1.4 | 1.7 | 1.9 | 1.5 | |||||
Regulation of nitrogen compound metabolic process | 2.2 | 1.9 | 3.0 | 2.5 | |||||
Regulation of nucleic acid-templated transcription | 3.0 | >3 | >3 | >3 | |||||
Regulation of nucleobase-containing compound metabolic process | 2.7 | 2.7 | >3 | >3 | |||||
Regulation of primary metabolic process | 2.0 | 1.8 | 3.0 | 2.0 | |||||
Regulation of RNA biosynthetic process | 3.0 | >3 | >3 | >3 | |||||
Regulation of RNA metabolic process | 2.7 | 3.0 | >3 | >3 | |||||
Regulation of transcription, DNA-templated | 3.0 | >3 | >3 | >3 | |||||
Response to oxidative stress | 1.7 | 3.0 | 3.0 | 1.7 | |||||
RNA biosynthetic process | 2.2 | 1.9 | 2.5 | 1.9 | |||||
Transcription, DNA-templated | 2.2 | 2.0 | 2.5 | 1.9 | |||||
Antibiotic metabolic process | 2.7 | 1.8 | 2.0 | ||||||
Oxylipin biosynthetic process | >3 | >3 | |||||||
Oxylipin metabolic process | >3 | >3 | |||||||
Regulation of metabolic process | 1.4 | 1.5 | |||||||
Response to drug | 2.2 | 2.7 | |||||||
Response to stimulus | 1.8 | 1.5 |
Line | 75A:258 | Wonga | Emir | ||||||
---|---|---|---|---|---|---|---|---|---|
Days Post Inoculation | 1 1 | 5 | 9 | 1 | 5 | 9 | 1 | 5 | 9 |
Chitin binding | >3 2 | 2.7 | >3 | 1.5 | >3 | 1.4 | |||
Heme binding | 2.3 | >3 | >3 | 2.1 | >3 | >3 | |||
Oxidoreductase activity | >3 | >3 | >3 | 2.2 | >3 | >3 | |||
Sequence-specific DNA binding | 1.4 | >3 | >3 | >3 | 2.5 | >3 | |||
Tetrapyrrole binding | 2.2 | >3 | >3 | 1.6 | >3 | >3 | |||
DNA-binding transcription factor activity | >3 | >3 | >3 | >3 | >3 | ||||
Transcription regulator activity | >3 | >3 | >3 | >3 | >3 | ||||
Antioxidant activity | >3 | 2.7 | >3 | >3 | |||||
Cofactor binding | 1.4 | 1.6 | >3 | 3.0 | |||||
DNA binding | 2.5 | 2.7 | >3 | >3 | |||||
Endopeptidase inhibitor activity | 3.0 | 2.7 | 3.0 | 2.3 | |||||
Endopeptidase regulator activity | 3.0 | 2.7 | 3.0 | 2.3 | |||||
Oxidoreductase activity, acting on peroxide as acceptor | >3 | 3.0 | >3 | >3 | |||||
Peptidase inhibitor activity | 3.0 | 2.7 | 3.0 | 2.3 | |||||
Peptidase regulator activity | 3.0 | 2.4 | 2.4 | 1.9 | |||||
Peroxidase activity | >3 | 3.0 | >3 | >3 | |||||
Serine-type endopeptidase inhibitor activity | 3.0 | 3.0 | 1.4 | 1.3 | |||||
Catalytic activity | >3 | 1.7 | >3 | ||||||
Dioxygenase activity | >3 | 1.7 | 2.7 | ||||||
Electron transfer activity | 1.6 | 3.0 | 3.0 |
Gene | 75A:258 | Wonga | Emir | ||||||||
---|---|---|---|---|---|---|---|---|---|---|---|
1 1 | 5 | 9 | 16 | 23 | 1 | 5 | 9 | 1 | 5 | 9 | |
TanjilG_24849 | 5.8 2 | 9.3 | 7.7 | 11.9 | 8.9 | 5.2 | 6.4 | 10.3 | 5.9 | 6.9 | 10.2 |
TanjilG_24253 | 5.2 3 | 7.4 | 4.0 | 18.9 | 23.5 | 6.2 | 5.9 | 9.5 | 8.1 | 20.0 | 9.5 |
TanjilG_05213 | 2.9 | 6.5 | 3.7 | 4.1 | 5.0 | 4.1 | 4.7 | 5.0 | 1.5 | 3.0 | 7.8 |
TanjilG_08982 | −2.0 | 20.7 | 18.4 | - 4 | 17.3 | 21.0 | 21.1 | 7.2 | 17.6 | - | 23.1 |
TanjilG_19904 | 2.6 | 4.5 | 3.9 | 3.5 | 4.4 | 3.0 | 3.3 | 9.0 | 2.3 | 3.3 | 7.7 |
TanjilG_10317 | 2.0 | 4.5 | 3.2 | 3.2 | 3.8 | 2.5 | 2.4 | 6.3 | 3.2 | 2.9 | 6.3 |
TanjilG_13015 | 2.4 | 4.2 | 2.8 | 3.5 | 3.7 | 2.6 | 3.5 | 5.5 | 2.9 | 3.9 | 8.1 |
TanjilG_27897 | 4.7 | 24.8 | 24.0 | 19.4 | 23.5 | 4.9 | 25.0 | 27.5 | 22.1 | 21.3 | 11.1 |
TanjilG_02482 | 18.0 | 23.8 | 23.8 | - | 25.9 | - | 22.7 | 27.7 | 21.4 | 22.8 | 28.4 |
TanjilG_23505 | 3.5 | 4.7 | 3.9 | 6.4 | 6.8 | 3.7 | 3.2 | 8.1 | 1.7 | 4.7 | 6.8 |
TanjilG_15237 | 3.9 | 6.8 | 24.7 | 22.5 | 7.0 | 7.6 | 8.0 | 28.1 | 2.6 | 3.5 | 25.8 |
TanjilG_10302 | 15.4 | 42.7 | 3.1 | 38.3 | 40.8 | 36.8 | 5.4 | 8.0 | 2.7 | 38.4 | 9.4 |
Gene | 75A:258 | Wonga | Emir | ||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
1 1 | 5 | 9 | 16 | 23 | 1 | 5 | 9 | 16 | 23 | 1 | 5 | 9 | 16 | 23 | |
TanjilG_24849 | 10.1 2 | 11.3 | 8.4 | 8.6 | 8.4 | 4.2 | 9.9 | 10.9 | 9.2 | 8.2 | 4.6 | 9.1 | 10.2 | 12.5 | 11.4 |
TanjilG_24253 | 8.1 | 9.3 | 5.2 | 5.7 | 5.6 | −0.7 | 6.0 | 11.1 | 8.8 | 7.7 | 1.9 | 5.4 | 11.8 | 12.6 | 11.6 |
TanjilG_05213 | 3.7 | 8.4 | 5.2 | 5.8 | 4.9 | 4.4 | 5.2 | 8.2 | 3.5 | 3.7 | 2.4 | 4.3 | 8.7 | 8.7 | 8.2 |
TanjilG_08982 | 0.7 | 0.6 3 | 0.2 | −0.4 | 0.0 | 0.3 | 2.2 | 3.0 | 1.4 | 1.4 | 0.4 | 2.1 | 3.6 | 3.9 | 2.1 |
TanjilG_19904 | 2.3 | 2.8 | 2.2 | 3.4 | 3.0 | 5.3 | 4.6 | 7.6 | 5.8 | 6.4 | 1.1 | 2.6 | 5.7 | 7.5 | 6.5 |
TanjilG_10317 | 2.1 | 4.3 | 2.8 | 1.4 | 2.4 | 1.1 | 1.7 | 6.2 | 5.6 | 5.8 | 1.7 | 1.5 | 4.1 | 5.7 | 6.4 |
TanjilG_13015 | 3.5 | 5.1 | 3.5 | 1.7 | 3.1 | 3.1 | 4.8 | 7.6 | 3.6 | 4.6 | 1.1 | 3.4 | 6.7 | 6.7 | 6.9 |
TanjilG_27897 | 7.1 | 7.8 | 7.8 | 4.0 | 6.1 | 6.8 | 10.0 | 10.5 | 10.2 | 10.6 | 2.0 | 3.4 | 10.6 | 11.7 | 12.4 |
TanjilG_02482 | 1.7 | 1.4 | 0.1 | 9.4 | 3.3 | −0.8 | 1.7 | 4.2 | 1.6 | 0.6 | −1.0 | 0.6 | 7.2 | 3.1 | 1.9 |
TanjilG_23505 | 6.5 | 4.3 | 4.6 | 3.8 | 5.1 | 4.2 | 4.1 | 8.2 | 6.1 | 5.4 | 2.9 | 4.6 | 6.9 | 6.6 | 8.4 |
TanjilG_15237 | 8.2 | 9.0 | 8.9 | 3.6 | 5.3 | 7.8 | 9.7 | 14.4 | 11.8 | 8.3 | 4.8 | 4.3 | 9.5 | 15.5 | 11.9 |
TanjilG_10302 | 6.3 | 7.9 | 6.1 | 8.7 | 4.7 | 3.8 | 7.8 | 8.5 | 5.2 | 6.1 | 2.9 | 5.6 | 10.2 | 10.7 | 8.9 |
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Książkiewicz, M.; Rychel-Bielska, S.; Plewiński, P.; Nuc, M.; Irzykowski, W.; Jędryczka, M.; Krajewski, P. The Resistance of Narrow-Leafed Lupin to Diaporthe toxica Is Based on the Rapid Activation of Defense Response Genes. Int. J. Mol. Sci. 2021, 22, 574. https://doi.org/10.3390/ijms22020574
Książkiewicz M, Rychel-Bielska S, Plewiński P, Nuc M, Irzykowski W, Jędryczka M, Krajewski P. The Resistance of Narrow-Leafed Lupin to Diaporthe toxica Is Based on the Rapid Activation of Defense Response Genes. International Journal of Molecular Sciences. 2021; 22(2):574. https://doi.org/10.3390/ijms22020574
Chicago/Turabian StyleKsiążkiewicz, Michał, Sandra Rychel-Bielska, Piotr Plewiński, Maria Nuc, Witold Irzykowski, Małgorzata Jędryczka, and Paweł Krajewski. 2021. "The Resistance of Narrow-Leafed Lupin to Diaporthe toxica Is Based on the Rapid Activation of Defense Response Genes" International Journal of Molecular Sciences 22, no. 2: 574. https://doi.org/10.3390/ijms22020574
APA StyleKsiążkiewicz, M., Rychel-Bielska, S., Plewiński, P., Nuc, M., Irzykowski, W., Jędryczka, M., & Krajewski, P. (2021). The Resistance of Narrow-Leafed Lupin to Diaporthe toxica Is Based on the Rapid Activation of Defense Response Genes. International Journal of Molecular Sciences, 22(2), 574. https://doi.org/10.3390/ijms22020574