Potential Role of Photosynthesis in the Regulation of Reactive Oxygen Species and Defence Responses to Blumeria graminis f. sp. tritici in Wheat
Abstract
:1. Introduction
2. Results
2.1. Transcriptome Analysis of L658 and L958 during Bgt Infection
2.2. Difference in H2O2 Accumulation and Related DEG Expression between L658 and L958
2.3. Changes in Photosynthesis and Photosynthesis-Related Genes in Response to Bgt
2.4. Identification of DEGs Related to Phytohormones and PR Proteins
3. Discussion
3.1. Initial Stronger H2O2 Burst and Secondary Lasting H2O2 Burst Were Regulated by Antioxidant Enzyme Activities and H2O2-Related Genes and Occurred in Incompatible Reactions
3.2. Global Downregulation of Photosynthesis-Related Genes Likely Disrupted Photosynthesis and Promoted the Generation of H2O2
3.3. Mutually Antagonistic Interactions between SA and JA/ET Are Involved in the Regulation of Defence Against Bgt by Regulating Different PR Genes Expression
4. Materials and Methods
4.1. Plant and Pathogen Materials
4.2. Cytological Observations of H2O2 and Cell Death
4.3. Determination of Antioxidant Enzyme Activity
4.4. Determination of Photosynthesis Indices
4.5. Measurements of Chlorophyll Fluorescence and Quantum Yields of PSII
4.6. RNA Extraction, cDNA Library Construction, and RNA-Seq
4.7. Alignment of RNA-Seq Reads and Differential Gene Expression Analysis
4.8. Reliable Analysis by qRT-PCR
4.9. Statistical Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
Abbreviations
ABA | Abscisic Acid |
ACO | 1-aminocyclopropane-1-carboxylate oxidase |
ACS | 1-aminocyclopropane-1-carboxylate synthase |
AOS | Allene Oxide Synthase |
AOX | Amine Oxidase |
APX | Peroxidase |
ATPase | ATP synthase |
Bgt | Blumeria graminis f. sp. tritici |
Cabs | Chlorophyll a/b-binding proteins |
CAT | Catalase |
EIN | Ethylene insensitive |
ERF | Ethylene-responsive transcription factor |
ET | Ethylene |
Fd-I | Ferredoxin-I |
FNR | Ferredoxin: NADP+ oxidoreductase |
ICS | Isochorismate Synthase |
JA | Jasmonic Acid |
LOX | Lipoxygenase |
NPR1 | Non-expressor of Pathogenesis Related genes 1 |
OXO | Oxalate Oxidase |
PGT | Primary Germ Tube |
POD | Peroxidase |
POX | Polyamine Oxidase |
PP | Penetration Peg |
PR1 | Pathogenesis-related 1 |
PR5 | Pathogenesis-related 5 |
PR10 | Pathogenesis-related 10 |
PR14 | Pathogenesis-related 14 |
RbcS/L | Ribulose bisphosphate carboxylase small chain/large chain |
RBOH | Respiratory Burst Oxidase Homologue protein |
RCA | Rubisco Activase |
ROS | Reactive Oxygen Species |
SA | Salicylic Acid |
SABP | Salicylic Acid-binding protein |
SOD | Superoxide dismutase |
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Gene ID | R0-S0 a | R6-S6 b | R12-S12 c | R24-S24 d | R48-S48 e | R72-S72 f | Functional Annotation G |
---|---|---|---|---|---|---|---|
H2O2-Producing-Related DEGs | |||||||
TraesCS6A01G180600 | −6.446 | −7.180 | −6.906 | −10.076 | −7.352 | −9.351 | Respiratory burst oxidase homologue protein E |
TraesCS5B01G299000 | / | / | / | / | / | −2.425 | Respiratory burst oxidase homologue protein C |
TraesCS5A01G527600 | / | / | / | / | / | −2.885 | Respiratory burst oxidase homologue protein B |
TraesCS4B01G282700 | / | / | −3.409 | / | / | / | Primary amine oxidase |
TraesCS7D01G375700 | −3.550 | −3.876 | −2.744 | −3.351 | −5.309 | −6.213 | Polyamine oxidase |
TraesCS7A01G378800 | −4.452 | −4.832 | / | / | −5.345 | −6.612 | Polyamine oxidase |
TraesCS7B01G280700 | 2.374 | / | / | / | 2.694 | 3.339 | Polyamine oxidase |
TraesCS4A01G279300 | / | / | / | / | / | −6.283 | Oxalate oxidase GF-2.8 |
TraesCS4D01G032000 | 3.726 | / | 3.098 | / | / | / | Oxalate oxidase GF-2.8 |
TraesCS4B01G033300 | / | / | 2.727 | / | / | / | Oxalate oxidase GF-2.8 |
TraesCS4A01G279200 | / | / | 2.310 | / | / | / | Oxalate oxidase GF-2.8 |
TraesCS4A01G279100 | / | / | 3.483 | / | / | / | Oxalate oxidase GF-2.8 |
TraesCS4A01G181800 | / | / | 3.865 | / | / | / | Oxalate oxidase GF-2.8 |
TraesCS4B01G033100 | / | / | / | / | / | −3.112 | Oxalate oxidase 2 |
TraesCS4D01G032200 | / | / | 2.298 | / | / | / | Oxalate oxidase 2 |
TraesCS4D01G032100 | −6.459 | / | 3.202 | / | / | / | Oxalate oxidase 2 |
H2O2-Scavenging-Related DEGs | |||||||
TraesCS6B01G278100 | / | / | / | −2.137 | / | / | glutathione peroxidase 6, |
TraesCS1B01G115800 | 3.734 | 3.949 | 4.754 | 3.230 | 4.803 | 3.701 | Peroxidase N |
TraesCS1A01G104300 | −3.329 | / | / | / | −2.280 | −3.797 | Peroxidase A2 |
TraesCS6B01G063900 | / | / | / | / | / | −2.037 | Peroxidase 70 |
TraesCS6B01G063400 | / | / | / | / | / | −3.498 | Peroxidase 70 |
TraesCS6A01G047200 | / | / | / | / | / | −3.376 | Peroxidase 70 |
TraesCS6D01G303900 | / | / | −4.580 | / | −4.299 | / | Peroxidase 56 |
TraesCS6A01G324200 | / | / | −3.592 | / | / | / | Peroxidase 56 |
TraesCS1B01G115900 | −4.877 | −3.536 | −2.526 | −2.277 | −2.918 | −4.076 | Peroxidase 54 |
TraesCS1D01G096400 | −2.815 | / | / | / | −2.264 | −3.499 | Peroxidase 54 |
TraesCS7B01G132400 | / | 4.140 | / | / | / | 2.170 | Peroxidase 5 |
TraesCS1B01G096900 | / | / | −2.658 | / | / | −3.204 | Peroxidase 5 |
TraesCS1A01G079400 | / | / | −2.630 | / | / | / | Peroxidase 5 |
TraesCS4A01G196000 | / | / | −2.166 | / | / | / | Peroxidase 4 |
TraesCS5D01G144300 | / | / | / | / | / | −2.114 | Peroxidase 4 |
TraesCS5B01G147200 | / | / | / | / | / | −2.496 | Peroxidase 4 |
TraesCS2B01G098100 | / | / | / | 2.053 | / | / | Peroxidase 21 |
TraesCS3A01G297200 | 3.631 | / | / | / | / | / | Peroxidase 2 |
TraesCS2B01G124600 | / | −7.661 | / | / | / | / | Peroxidase 2 |
TraesCS3A01G297100 | / | / | / | / | / | −4.351 | Peroxidase 2 |
TraesCS2D01G584600 | −2.622 | / | / | / | / | / | Peroxidase 12 |
TraesCS2D01G583200 | / | / | 2.692 | / | / | / | Peroxidase 12 |
TraesCS2A01G573900 | / | / | / | / | 3.487 | / | Peroxidase 12 |
TraesCS2B01G125200 | / | / | 7.952 | / | / | / | Peroxidase 1 |
TraesCS2B01G125100 | / | / | / | / | 10.195 | / | Peroxidase 1 |
TraesCS2D01G107900 | / | −7.959 | / | / | / | / | Peroxidase |
TraesCS2B01G125300 | / | / | / | / | / | −7.743 | Peroxidase |
TraesCS4A01G106300 | −2.428 | −2.317 | / | / | / | −2.335 | L-ascorbate peroxidase 1 |
TraesCS6A01G118300 | −2.666 | / | / | −2.721 | −3.727 | −2.990 | Cationic peroxidase 1 |
TraesCS6A01G041700 | −4.483 | −4.691 | −3.521 | −5.265 | −4.937 | −5.815 | Catalase isozyme 2 |
Gene ID | R0-S0 a | R6-S6 b | R12-S12 c | R24-S24 d | R48-S48 e | R72-S72 f | Functional Annotation G |
---|---|---|---|---|---|---|---|
SA Pathway-Related DEGs | |||||||
TraesCS3B01G354100 | / | / | −3.145 | / | / | / | Salicylic acid-binding protein 2 |
TraesCS3A01G325300 | / | / | −2.796 | / | / | / | Salicylic acid-binding protein 2 |
TraesCS3A01G325200 | / | / | −3.361 | / | / | / | Salicylic acid-binding protein 2 |
TraesCS5D01G196200 | / | / | −2.201 | / | / | / | Isochorismate synthase 2, chloroplastic |
TraesCS7A01G021800 | 11.409 | 7.903 | 12.994 | 8.314 | 12.449 | 12.138 | Regulatory protein NPR1 |
JA Pathway-Related DEGs | |||||||
TraesCS2A01G525500 | / | / | / | / | / | −3.867 | Seed linoleate 9S-lipoxygenase-3 |
TraesCS6A01G132500 | −7.376 | −7.356 | −5.173 | −7.744 | −8.013 | −12.116 | Putative linoleate 9S-lipoxygenase 3 |
TraesCS6A01G132200 | −13.320 | −9.317 | −10.259 | −8.741 | −14.0 | −15.902 | Putative linoleate 9S-lipoxygenase 3 |
TraesCS2D01G528500 | / | / | / | / | / | −3.547 | Probable linoleate 9S-lipoxygenase 5 |
TraesCS2B01G555400 | / | −2.347 | −2.003 | / | −2.112 | −4.107 | Probable linoleate 9S-lipoxygenase 5 |
TraesCS6A01G181200 | −9.490 | −10.091 | −10.025 | −9.787 | −9.954 | −9.287 | Probable linoleate 9S-lipoxygenase 4 |
TraesCS6B01G193400 | / | / | / | −2.024 | / | −2.136 | Lipoxygenase 2.3, chloroplastic |
TraesCS6A01G166000 | −2.911 | −3.863 | −2.692 | −2.986 | −3.050 | −3.241 | Lipoxygenase 2.3, chloroplastic |
TraesCS5D01G013400 | / | −3.160 | / | / | / | −4.632 | Lipoxygenase 2.1, chloroplastic |
TraesCS5B01G006500 | / | / | / | / | / | −4.578 | Lipoxygenase 2.1, chloroplastic |
TraesCS5A01G007900 | / | −3.314 | / | / | / | −4.997 | Lipoxygenase 2.1, chloroplastic |
TraesCS4D01G035200 | / | / | / | / | / | −2.177 | Linoleate 9S-lipoxygenase 1 |
TraesCS4B01G037900 | / | / | / | / | / | −2.780 | Linoleate 9S-lipoxygenase 1 |
TraesCS4B01G037700 | / | / | / | / | / | −2.609 | Linoleate 9S-lipoxygenase 1 |
TraesCS4D01G238800 | / | / | / | / | / | −2.213 | Allene oxide synthase 2 |
TraesCS4D01G238700 | / | −5.215 | / | / | / | −6.243 | Allene oxide synthase 2 |
TraesCS4A01G061800 | / | −4.649 | / | / | / | −5.560 | Allene oxide synthase 2 |
TraesCS5D01G413200 | / | / | / | / | / | −2.171 | Allene oxide synthase 1, chloroplastic |
ET Pathway-Related DEGs | |||||||
TraesCS4D01G267500 | / | / | / | / | / | −2.162 | Ethylene-responsive transcription factor RAP2-4 |
TraesCS7D01G469200 | 2.464 | 3.022 | / | 2.404 | 3.519 | 3.703 | Ethylene-responsive transcription factor RAP2-13 |
TraesCS6D01G217800 | / | / | / | / | / | −2.935 | Ethylene-responsive transcription factor ERF053 |
TraesCS6B01G263800 | / | / | / | / | / | −2.383 | Ethylene-responsive transcription factor ERF053 |
TraesCS6A01G235100 | / | / | / | / | / | −2.041 | Ethylene-responsive transcription factor ERF053 |
TraesCS2A01G427700 | / | / | / | / | / | −2.389 | Ethylene-responsive transcription factor 7 |
TraesCS6A01G171900 | / | / | −2.474 | −2.076 | / | / | Ethylene-responsive transcription factor 3 |
TraesCS6B01G281000 | / | / | / | / | / | −4.540 | Ethylene-responsive transcription factor 2 |
TraesCS5D01G549200 | 2.379 | / | / | / | / | / | Ethylene-responsive transcription factor 1B |
TraesCS2D01G391400 | / | / | / | / | 3.664 | / | Ethylene-responsive transcription factor 1B |
TraesCS6D01G225500 | / | / | / | / | / | −4.057 | Ethylene-responsive transcription factor 1 |
TraesCS6A01G243300 | / | / | / | / | / | −2.602 | Ethylene-responsive transcription factor 1 |
TraesCS6A01G125700 | −10.243 | −10.428 | −11.097 | −9.384 | −8.635 | −8.945 | AP2-like ethylene-responsive transcription factor |
TraesCS5A01G547500 | −2.579 | −9.546 | −2.814 | −3.525 | / | −3.283 | Ethylene-insensitive protein 2 |
TraesCS6A01G181900 | −2.973 | −2.685 | −3.204 | −3.132 | −3.230 | −2.830 | EIN3-binding F-box protein 1 |
TraesCS2D01G394200 | / | / | / | / | / | −3.141 | 1-aminocyclopropane-1-carboxylate synthase |
TraesCS2B01G414800 | / | / | / | / | 2.471 | −2.460 | 1-aminocyclopropane-1-carboxylate synthase |
TraesCS4B01G005800 | −3.100 | −2.836 | −3.930 | −3.304 | −4.105 | −3.435 | 1-aminocyclopropane-1-carboxylate oxidase homologue 1 |
TraesCS4A01G499800 | 5.816 | 9.167 | 5.375 | / | / | / | 1-aminocyclopropane-1-carboxylate oxidase homologue 1 |
TraesCS6B01G356200 | / | / | / | / | 2.046 | / | 1-aminocyclopropane-1-carboxylate oxidase 3 |
TraesCS6B01G356000 | / | / | / | 2.029 | / | / | 1-aminocyclopropane-1-carboxylate oxidase 3 |
TraesCS5B01G232600 | / | / | −2.121 | / | / | / | 1-aminocyclopropane-1-carboxylate oxidase 1 |
TraesCS5B01G232700 | / | / | / | −2.167 | −2.657 | −2.075 | 1-aminocyclopropane-1-carboxylate oxidase 1 |
Gene ID | R0-S0 a | R6-S6 b | R12-S12 c | R24-S24 d | R48-S48 e | R72-S72 f | Functional Annotation G |
---|---|---|---|---|---|---|---|
TraesCS5A01G336600 | / | / | −3.422 | / | / | / | Thaumatin-like protein 1a |
TraesCS4D01G227400 | / | / | / | / | / | −2.092 | Thaumatin-like protein 1 |
TraesCS4A01G070700 | / | / | / | / | / | −2.481 | Thaumatin-like protein 1 |
TraesCSU01G146600 | 7.428 | / | 6.732 | / | / | / | Thaumatin-like protein |
TraesCS6B01G473800 | 8.349 | 5.325 | 10.464 | / | / | / | Thaumatin-like protein |
TraesCS6B01G157700 | / | / | −10.474 | / | / | / | Thaumatin-like protein |
TraesCS6A01G129400 | / | / | −9.800 | / | / | / | Thaumatin-like protein |
TraesCS5A01G018200 | 3.579 | / | / | / | / | −3.910 | Thaumatin-like protein |
TraesCS5A01G017900 | 6.417 | / | / | / | / | / | Thaumatin-like protein |
TraesCS4A01G498000 | 12.101 | 7.376 | 7.329 | 5.273 | / | / | Thaumatin-like protein |
TraesCS2A01G110300 | 6.281 | / | / | / | / | / | Thaumatin-like protein |
TraesCS7D01G252400 | / | 4.006 | / | 5.578 | 6.710 | 9.868 | Pathogenesis-related protein 5 |
TraesCS5D01G446900 | 7.736 | / | / | / | / | / | Pathogenesis-related protein 1 |
TraesCS5D01G446800 | 8.967 | / | / | / | / | / | Pathogenesis-related protein 1 |
TraesCS5B01G442700 | 7.025 | / | / | / | / | / | Pathogenesis-related protein 1 |
TraesCS5B01G442600 | 8.469 | / | / | / | / | / | Pathogenesis-related protein 1 |
TraesCS5A01G439800 | 9.128 | / | 7.573 | / | / | / | Pathogenesis-related protein 1 |
TraesCS5A01G189200 | / | / | / | 3.043 | 3.487 | / | Pathogenesis-related protein 1 |
TraesCS6A01G184600 | −3.957 | −3.644 | −3.377 | −4.044 | −4.598 | −4.097 | Nuclear ribonuclease |
TraesCS2D01G260000 | / | / | −2.898 | / | / | / | Ribonuclease 3 |
TraesCS6D01G320200 | / | / | / | −2.215 | / | −2.929 | Ribonuclease 1 |
TraesCS6A01G339600 | / | / | / | / | / | −2.331 | Ribonuclease 1 |
TraesCS2B01G182900 | / | / | / | −4.933 | / | −5.114 | Ribonuclease 1 |
TraesCS2A01G157400 | / | / | / | / | / | −2.490 | Ribonuclease 1 |
TraesCS1D01G149800 | / | −2.714 | −3.982 | / | / | −2.658 | Ribonuclease 1 |
TraesCS1D01G149700 | / | −4.139 | −5.318 | / | −4.500 | −5.191 | Ribonuclease 1 |
TraesCS1B01G170200 | / | −4.257 | −6.333 | / | / | / | Ribonuclease 1 |
TraesCS1B01G170100 | −2.735 | −5.066 | −4.986 | −3.003 | −5.493 | −6.239 | Ribonuclease 1 |
TraesCS1A01G152800 | −3.828 | −4.337 | −6.606 | −2.809 | −3.895 | −4.556 | Ribonuclease 1 |
TraesCS1A01G152600 | −2.595 | −5.057 | −4.745 | −2.907 | −5.539 | −6.020 | Ribonuclease 1 |
TraesCS4B01G267300 | / | / | −2.348 | / | / | / | Non-specific lipid-transfer protein-like protein |
TraesCS4A01G038400 | / | / | / | / | / | −2.042 | Non-specific lipid-transfer protein-like protein |
TraesCSU01G251500 | −2.325 | −2.823 | −4.662 | −3.183 | −4.485 | −3.858 | Non-specific lipid-transfer protein 4.3 |
TraesCSU01G147100 | −2.496 | −2.880 | −4.956 | −3.222 | −4.536 | −3.531 | Non-specific lipid-transfer protein 4.3 |
TraesCSU01G057300 | / | / | −2.685 | / | / | / | Non-specific lipid-transfer protein 4.3 |
TraesCSU01G057200 | / | / | −2.781 | / | / | / | Non-specific lipid-transfer protein 4.3 |
TraesCS3B01G064100 | −2.204 | −2.562 | −4.634 | −2.799 | −3.872 | −2.701 | Non-specific lipid-transfer protein 4.3 |
TraesCS3B01G063700 | −2.223 | −2.301 | −4.238 | −2.537 | −3.851 | −2.788 | Non-specific lipid-transfer protein 4.3 |
TraesCS3B01G063100 | / | / | −3.290 | −2.240 | −3.665 | −2.777 | Non-specific lipid-transfer protein 4.3 |
TraesCS3B01G063000 | / | / | −2.874 | / | −3.378 | −2.383 | Non-specific lipid-transfer protein 4.3 |
TraesCSU01G253500 | −2.544 | −3.492 | −4.653 | −3.085 | −3.277 | −3.503 | Non-specific lipid-transfer protein 4.1 |
TraesCSU01G237900 | −2.469 | −3.284 | −4.612 | −3.033 | −3.186 | −3.472 | Non-specific lipid-transfer protein 4.1 |
TraesCSU01G154200 | −2.469 | −3.291 | −4.524 | −2.990 | −3.226 | −3.472 | Non-specific lipid-transfer protein 4.1 |
TraesCSU01G147200 | −3.126 | −4.274 | −5.409 | −3.635 | −3.963 | −3.991 | Non-specific lipid-transfer protein 4.1 |
TraesCSU01G056900 | / | / | / | / | / | −3.454 | Non-specific lipid-transfer protein 4.1 |
TraesCSU01G056700 | / | / | −2.123 | / | / | / | Non-specific lipid-transfer protein 4.1 |
TraesCS3B01G064000 | −2.457 | −3.605 | −3.873 | −2.220 | −2.893 | −2.491 | Non-specific lipid-transfer protein 4.1 |
TraesCS3B01G063600 | / | −2.791 | −3.285 | / | −2.356 | −2.436 | Non-specific lipid-transfer protein 4.1 |
TraesCS3B01G063200 | / | / | −4.401 | −2.399 | −2.962 | −2.729 | Non-specific lipid-transfer protein 4.1 |
TraesCS2A01G477700 | / | / | −5.115 | / | / | / | Non-specific lipid-transfer protein |
TraesCS5A01G433100 | / | 9.147 | 5.006 | 4.132 | / | 4.231 | Non-specific lipid transfer protein GPI-anchored 2 |
TraesCS3D01G331400 | / | / | −2.567 | / | / | / | Non-specific lipid transfer protein GPI-anchored 2 |
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Hu, Y.; Zhong, S.; Zhang, M.; Liang, Y.; Gong, G.; Chang, X.; Tan, F.; Yang, H.; Qiu, X.; Luo, L.; et al. Potential Role of Photosynthesis in the Regulation of Reactive Oxygen Species and Defence Responses to Blumeria graminis f. sp. tritici in Wheat. Int. J. Mol. Sci. 2020, 21, 5767. https://doi.org/10.3390/ijms21165767
Hu Y, Zhong S, Zhang M, Liang Y, Gong G, Chang X, Tan F, Yang H, Qiu X, Luo L, et al. Potential Role of Photosynthesis in the Regulation of Reactive Oxygen Species and Defence Responses to Blumeria graminis f. sp. tritici in Wheat. International Journal of Molecular Sciences. 2020; 21(16):5767. https://doi.org/10.3390/ijms21165767
Chicago/Turabian StyleHu, Yuting, Shengfu Zhong, Min Zhang, Yinping Liang, Guoshu Gong, Xiaoli Chang, Feiquan Tan, Huai Yang, Xiaoyan Qiu, Liya Luo, and et al. 2020. "Potential Role of Photosynthesis in the Regulation of Reactive Oxygen Species and Defence Responses to Blumeria graminis f. sp. tritici in Wheat" International Journal of Molecular Sciences 21, no. 16: 5767. https://doi.org/10.3390/ijms21165767