Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE (Open Access)

New insights into defense responses against Verticillium dahliae infection revealed by a quantitative proteomic analysis in Arabidopsis thaliana

Min Wu A B C # , Qiulin Li D # , Guixian Xia B , Yongshan Zhang D and Fuxin Wang https://orcid.org/0000-0003-4497-3667 A B E *
+ Author Affiliations
- Author Affiliations

A College of Life Sciences, Hebei University, Baoding 071002, China.

B Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China.

C University of Chinese Academy of Sciences, Beijing 100049, China.

D State Key Laboratory of Cotton Biology, Institute of Cotton Research, Chinese Academy of Agriculture Sciences, Anyang, Henan 455000, China.

E Key Laboratory of Microbial Diversity Research and Application of Hebei Province, Baoding 071002, China.

* Correspondence to: wangfuxin@hbu.edu.cn
# These authors contributed equally to this paper

Handling Editor: Calum Wilson

Functional Plant Biology 49(11) 980-994 https://doi.org/10.1071/FP22006
Submitted: 9 January 2022  Accepted: 8 July 2022   Published: 1 August 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution 4.0 International License (CC BY)

Abstract

Verticillium wilt is a highly destructive fungal disease that attacks a broad range of plants, including many major crops. However, the mechanism underlying plant immunity toward Verticillium dahliae is very complex and requires further study. By combining bioinformatics analysis and experimental validation, we investigated plant defence responses against V. dahliae infection in the model plant Arabidopsis thaliana L. A total of 301 increased and 214 decreased differentially abundant proteins (DAPs) between mock and infected wild type (WT) plants were acquired and bioinformatics analyses were then conducted and compared (increased vs decreased) in detail. In addition to the currently known mechanisms, several new clues about plant immunity against V. dahliae infection were found in this study: (1) exosome formation was dramatically induced by V. dahliae attack; (2) tryptophan-derived camalexin and cyanogenic biosynthesis were durably promoted in response to infection; and (3) various newly identified components were activated for hub immunity responses. These new clues provide valuable information that extends the current knowledge about the molecular basis of plant immunity against V. dahliae infection.

Keywords: Arabidopsis, camalexin, cyanogenic biosynthesis, exosome, iTRAQ, plant immunity, proteome, Verticillium dahliae.


References

An Q, Ehlers K, Kogel K-H, Van Bel AJE, Hückelhoven R (2006a) Multivesicular compartments proliferate in susceptible and resistant MLA12-barley leaves in response to infection by the biotrophic powdery mildew fungus. New Phytologist 172, 563–576.
Multivesicular compartments proliferate in susceptible and resistant MLA12-barley leaves in response to infection by the biotrophic powdery mildew fungus.Crossref | GoogleScholarGoogle Scholar |

An Q, Hückelhoven R, Kogel K-H, Van Bel AJE (2006b) Multivesicular bodies participate in a cell wall-associated defence response in barley leaves attacked by the pathogenic powdery mildew fungus. Cellular Microbiology 8, 1009–1019.
Multivesicular bodies participate in a cell wall-associated defence response in barley leaves attacked by the pathogenic powdery mildew fungus.Crossref | GoogleScholarGoogle Scholar |

Antanaviciute L, Šurbanovski N, Harrison N, McLeary KJ, Simpson DW, Wilson F, Sargent DJ, Harrison RJ (2015) Mapping QTL associated with Verticillium dahliae resistance in the cultivated strawberry (Fragaria × ananassa). Horticulture Research 2, 15009
Mapping QTL associated with Verticillium dahliae resistance in the cultivated strawberry (Fragaria × ananassa).Crossref | GoogleScholarGoogle Scholar |

Barth C, Jander G (2006) Arabidopsis myrosinases TGG1 and TGG2 have redundant function in glucosinolate breakdown and insect defense. The Plant Journal 46, 549–562.
Arabidopsis myrosinases TGG1 and TGG2 have redundant function in glucosinolate breakdown and insect defense.Crossref | GoogleScholarGoogle Scholar |

Bednarek P, Piślewska-Bednarek M, Svatoš A, Schneider B, Doubský J, Mansurova M, Humphry M, Consonni C, Panstruga R, Sanchez-Vallet A, Molina A, Schulze-Lefert P (2009) A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science 323, 101–106.
A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense.Crossref | GoogleScholarGoogle Scholar |

Bednarek P, Piślewska-Bednarek M, Ver Loren van Themaat E, Maddula RK, Svatoš A, Schulze-Lefert P (2011) Conservation and clade-specific diversification of pathogen-inducible tryptophan and indole glucosinolate metabolism in Arabidopsis thaliana relatives. New Phytologist 192, 713–726.
Conservation and clade-specific diversification of pathogen-inducible tryptophan and indole glucosinolate metabolism in Arabidopsis thaliana relatives.Crossref | GoogleScholarGoogle Scholar |

Cai Q, Qiao L, Wang M, He B, Lin F-M, Palmquist J, Huang S-D, Jin H (2018) Plants send small RNAs in extracellular vesicles to fungal pathogen to silence virulence genes. Science 360, 1126–1129.
Plants send small RNAs in extracellular vesicles to fungal pathogen to silence virulence genes.Crossref | GoogleScholarGoogle Scholar |

Cheng H-Q, Han L-B, Yang C-L, Wu X-M, Zhong N-Q, Wu J-H, Wang F-X, Wang H-Y, Xia G-X (2016) The cotton MYB108 forms a positive feedback regulation loop with CML11 and participates in the defense response against Verticillium dahliae infection. Journal of Experimental Botany 67, 1935–1950.
The cotton MYB108 forms a positive feedback regulation loop with CML11 and participates in the defense response against Verticillium dahliae infection.Crossref | GoogleScholarGoogle Scholar |

Cui Y, Gao J, He Y, Jiang L (2020) Plant extracellular vesicles. Protoplasma 257, 3–12.
Plant extracellular vesicles.Crossref | GoogleScholarGoogle Scholar |

Deketelaere S, Tyvaert L, França SC, Höfte M (2017) Desirable traits of a good biocontrol agent against Verticillium Wilt. Frontiers in Microbiology 8, 1186
Desirable traits of a good biocontrol agent against Verticillium Wilt.Crossref | GoogleScholarGoogle Scholar |

Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Research 38, W64–W70.
agriGO: a GO analysis toolkit for the agricultural community.Crossref | GoogleScholarGoogle Scholar |

Ellendorff U, Fradin EF, de Jonge R, Thomma BPHJ (2009) RNA silencing is required for Arabidopsis defence against Verticillium wilt disease. Journal of Experimental Botany 60, 591–602.
RNA silencing is required for Arabidopsis defence against Verticillium wilt disease.Crossref | GoogleScholarGoogle Scholar |

Fang X, Chen J, Dai L, Ma H, Zhang H, Yang J, Wang F, Yan C (2015) Proteomic dissection of plant responses to various pathogens. Proteomics 15, 1525–1543.
Proteomic dissection of plant responses to various pathogens.Crossref | GoogleScholarGoogle Scholar |

Fradin EF, Zhang Z, Juarez Ayala JC, Castroverde CDM, Nazar RN, Robb J, Liu C-M, Thomma BPHJ (2009) Genetic dissection of Verticillium wilt resistance mediated by tomato Ve1. Plant Physiology 150, 320–332.
Genetic dissection of Verticillium wilt resistance mediated by tomato Ve1.Crossref | GoogleScholarGoogle Scholar |

Fradin EF, Abd-El-Haliem A, Masini L, van den Berg GCM, Joosten MHAJ, Thomma BPHJ (2011) Interfamily transfer of tomato Ve1 mediates Verticillium resistance in Arabidopsis. Plant Physiology 156, 2255–2265.
Interfamily transfer of tomato Ve1 mediates Verticillium resistance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Gao X, Wheeler T, Li Z, Kenerley CM, He P, Shan L (2011) Silencing GhNDR1 and GhMKK2 compromises cotton resistance to Verticillium wilt. The Plant Journal 66, 293–305.
Silencing GhNDR1 and GhMKK2 compromises cotton resistance to Verticillium wilt.Crossref | GoogleScholarGoogle Scholar |

Gao W, Long L, Zhu L-F, Xu L, Gao W-H, Sun L-Q, Liu L-L, Zhang X-L (2013) Proteomic and virus-induced gene silencing (VIGS) analyses reveal that gossypol, brassinosteroids, and jasmonic acid contribute to the resistance of cotton to Verticillium dahliae. Molecular & Cellular Proteomics 12, 3690–3703.
Proteomic and virus-induced gene silencing (VIGS) analyses reveal that gossypol, brassinosteroids, and jasmonic acid contribute to the resistance of cotton to Verticillium dahliae.Crossref | GoogleScholarGoogle Scholar |

Gao M, He Y, Yin X, Zhong X, Yan B, Wu Y, Chen J, Li X, Zhai K, Huang Y, Gong X, Chang H, Xie S, Liu J, Yue J, Xu J, Zhang G, Deng Y, Wang E, Tharreau D, Wang G-L, Yang W, He Z (2021) Ca2+ sensor-mediated ROS scavenging suppresses rice immunity and is exploited by a fungal effector. Cell 184, 5391–5404.e17.
Ca2+ sensor-mediated ROS scavenging suppresses rice immunity and is exploited by a fungal effector.Crossref | GoogleScholarGoogle Scholar |

Hammerschmidt R (1999) PHYTOALEXINS: what have we learned after 60 years? Annual Review of Phytopathology 37, 285–306.
PHYTOALEXINS: what have we learned after 60 years?Crossref | GoogleScholarGoogle Scholar |

Han L-B, Li Y-B, Wang F-X, Wang W-Y, Liu J, Wu J-H, Zhong N-Q, Wu S-J, Jiao G-L, Wang H-Y, Xia G-X (2019) The cotton apoplastic protein CRR1 stabilizes chitinase 28 to facilitate defense against the fungal pathogen Verticillium dahliae. The Plant Cell 31, 520–536.
The cotton apoplastic protein CRR1 stabilizes chitinase 28 to facilitate defense against the fungal pathogen Verticillium dahliae.Crossref | GoogleScholarGoogle Scholar |

Harding C, Heuser J, Stahl P (1983) Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes. Journal of Cell Biology 97, 329–339.
Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes.Crossref | GoogleScholarGoogle Scholar |

He Y, Xu J, Wang X, He X, Wang Y, Zhou J, Zhang S, Meng X (2019) The Arabidopsis pleiotropic drug resistance transporters PEN3 and PDR12 mediate camalexin secretion for resistance to Botrytis cinerea. The Plant Cell 31, 2206–2222.
The Arabidopsis pleiotropic drug resistance transporters PEN3 and PDR12 mediate camalexin secretion for resistance to Botrytis cinerea.Crossref | GoogleScholarGoogle Scholar |

Hu X, Puri KD, Gurung S, Klosterman SJ, Wallis CM, Britton M, Durbin-Johnson B, Phinney B, Salemi M, Short DPG, Subbarao KV (2019) Proteome and metabolome analyses reveal differential responses in tomato–Verticillium dahliae-interactions. Journal of Proteomics 207, 103449
Proteome and metabolome analyses reveal differential responses in tomato–Verticillium dahliae-interactions.Crossref | GoogleScholarGoogle Scholar |

Huot B, Yao J, Montgomery BL, He SY (2014) Growth–defense tradeoffs in plants: a balancing act to optimize fitness. Molecular Plant 7, 1267–1287.
Growth–defense tradeoffs in plants: a balancing act to optimize fitness.Crossref | GoogleScholarGoogle Scholar |

Iven T, König S, Singh S, Braus-Stromeyer SA, Bischoff M, Tietze LF, Braus GH, Lipka V, Feussner I, Dröge-Laser W (2012) Transcriptional activation and production of tryptophan-derived secondary metabolites in Arabidopsis roots contributes to the defense against the fungal vascular pathogen Verticillium longisporum. Molecular Plant 5, 1389–1402.
Transcriptional activation and production of tryptophan-derived secondary metabolites in Arabidopsis roots contributes to the defense against the fungal vascular pathogen Verticillium longisporum.Crossref | GoogleScholarGoogle Scholar |

Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M (2012) KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Research 40, D109–D114.
KEGG for integration and interpretation of large-scale molecular data sets.Crossref | GoogleScholarGoogle Scholar |

Karasov TL, Chae E, Herman JJ, Bergelson J (2017) Mechanisms to mitigate the trade-off between growth and defense. The Plant Cell 29, 666–680.
Mechanisms to mitigate the trade-off between growth and defense.Crossref | GoogleScholarGoogle Scholar |

Kawchuk LM, Hachey J, Lynch DR, Kulcsar F, van Rooijen G, Waterer DR, Robertson A, Kokko E, Byers R, Howard RJ, Fischer R, Prüfer D (2001) Tomato Ve disease resistance genes encode cell surface-like receptors. Proceedings of the National Academy of Sciences of the United States of America 98, 6511–6515.

Li Y-B, Han L-B, Wang H-Y, Zhang J, Sun S-T, Feng D-Q, Yang C-L, Sun Y-D, Zhong N-Q, Xia G-X (2016) The thioredoxin GbNRX1 plays a crucial role in homeostasis of apoplastic reactive oxygen species in response to Verticillium dahliae infection in cotton. Plant Physiology 170, 2392–2406.
The thioredoxin GbNRX1 plays a crucial role in homeostasis of apoplastic reactive oxygen species in response to Verticillium dahliae infection in cotton.Crossref | GoogleScholarGoogle Scholar |

Li Z-K, Chen B, Li X-X, Wang J-P, Zhang Y, Wang X-F, Yan Y-Y, Ke H-F, Yang J, Wu J-H, Wang G-N, Zhang G-Y, Wu L-Q, Wang X-Y, Ma Z-Y (2019) A newly identified cluster of glutathione S-transferase genes provides Verticillium wilt resistance in cotton. The Plant Journal 98, 213–227.
A newly identified cluster of glutathione S-transferase genes provides Verticillium wilt resistance in cotton.Crossref | GoogleScholarGoogle Scholar |

Liu Y, Schiff M, Czymmek K, Tallóczy Z, Levine B, Dinesh-Kumar SP (2005) Autophagy regulates programmed cell death during the plant innate immune response. Cell 121, 567–577.
Autophagy regulates programmed cell death during the plant innate immune response.Crossref | GoogleScholarGoogle Scholar |

Mandelc S, Timperman I, Radišek S, Devreese B, Samyn B, Javornik B (2013) Comparative proteomic profiling in compatible and incompatible interactions between hop roots and Verticillium albo-atrum. Plant Physiology and Biochemistry 68, 23–31.
Comparative proteomic profiling in compatible and incompatible interactions between hop roots and Verticillium albo-atrum.Crossref | GoogleScholarGoogle Scholar |

Miao Y, Xu L, He X, Zhang L, Shaban M, Zhang X, Zhu L (2019) Suppression of tryptophan synthase activates cotton immunity by triggering cell death via promoting SA synthesis. The Plant Journal 98, 329–345.
Suppression of tryptophan synthase activates cotton immunity by triggering cell death via promoting SA synthesis.Crossref | GoogleScholarGoogle Scholar |

Mo H, Wang X, Zhang Y, Zhang G, Zhang J, Ma Z (2015) Cotton polyamine oxidase is required for spermine and camalexin signalling in the defence response to Verticillium dahliae. The Plant Journal 83, 962–975.
Cotton polyamine oxidase is required for spermine and camalexin signalling in the defence response to Verticillium dahliae.Crossref | GoogleScholarGoogle Scholar |

Pegg GF, Brady BL (2002) ‘Verticillium wilts.’ (CABI: Wallingford, UK)

Qin J, Wang K, Sun L, Xing H, Wang S, Li L, Chen S, Guo H-S, Zhang J (2018) The plant-specific transcription factors CBP60g and SARD1 are targeted by a Verticillium secretory protein VdSCP41 to modulate immunity. elife 7, e34902
The plant-specific transcription factors CBP60g and SARD1 are targeted by a Verticillium secretory protein VdSCP41 to modulate immunity.Crossref | GoogleScholarGoogle Scholar |

Rajniak J, Barco B, Clay NK, Sattely ES (2015) A new cyanogenic metabolite in Arabidopsis required for inducible pathogen defence. Nature 525, 376–379.
A new cyanogenic metabolite in Arabidopsis required for inducible pathogen defence.Crossref | GoogleScholarGoogle Scholar |

Rutter BD, Innes RW (2017) Extracellular vesicles isolated from the leaf apoplast carry stress-response proteins. Plant Physiology 173, 728–741.
Extracellular vesicles isolated from the leaf apoplast carry stress-response proteins.Crossref | GoogleScholarGoogle Scholar |

Rutter BD, Innes RW (2018) Extracellular vesicles as key mediators of plant–microbe interactions. Current Opinion in Plant Biology 44, 16–22.
Extracellular vesicles as key mediators of plant–microbe interactions.Crossref | GoogleScholarGoogle Scholar |

Schenke D, Cai D (2020) Phytohormone crosstalk in the host-Verticillium interaction. Plant Signaling & Behavior 15, 1803567
Phytohormone crosstalk in the host-Verticillium interaction.Crossref | GoogleScholarGoogle Scholar |

Scholz SS, Schmidt-Heck W, Guthke R, Furch ACU, Reichelt M, Gershenzon J, Oelmüller R (2018) Verticillium dahliae-Arabidopsis interaction causes changes in gene expression profiles and jasmonate levels on different time scales. Frontiers in Microbiology 9, 217
Verticillium dahliae-Arabidopsis interaction causes changes in gene expression profiles and jasmonate levels on different time scales.Crossref | GoogleScholarGoogle Scholar |

Schorey JS, Cheng Y, Singh PP, Smith VL (2015) Exosomes and other extracellular vesicles in host–pathogen interactions. EMBO reports 16, 24–43.
Exosomes and other extracellular vesicles in host–pathogen interactions.Crossref | GoogleScholarGoogle Scholar |

Shaban M, Miao Y, Ullah A, Khan AQ, Menghwar H, Khan AH, Ahmed MM, Tabassum MA, Zhu L (2018) Physiological and molecular mechanism of defense in cotton against Verticillium dahliae. Plant Physiology and Biochemistry 125, 193–204.
Physiological and molecular mechanism of defense in cotton against Verticillium dahliae.Crossref | GoogleScholarGoogle Scholar |

Song R, Li J, Xie C, Jian W, Yang X (2020) An overview of the molecular genetics of plant resistance to the Verticillium wilt pathogen Verticillium dahliae. International Journal of Molecular Sciences 21, 1120
An overview of the molecular genetics of plant resistance to the Verticillium wilt pathogen Verticillium dahliae.Crossref | GoogleScholarGoogle Scholar |

Su X, Qi X, Cheng H (2014) Molecular cloning and characterization of enhanced disease susceptibility 1 (EDS1) from Gossypium barbadense. Molecular Biology Reports 41, 3821–3828.
Molecular cloning and characterization of enhanced disease susceptibility 1 (EDS1) from Gossypium barbadense.Crossref | GoogleScholarGoogle Scholar |

Su T, Xu J, Li Y, Lei L, Zhao L, Yang H, Feng J, Liu G, Ren D (2011) Glutathione-indole-3-acetonitrile is required for camalexin biosynthesis in Arabidopsis thaliana. The Plant Cell 23, 364–380.
Glutathione-indole-3-acetonitrile is required for camalexin biosynthesis in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Su X, Lu G, Guo H, Zhang K, Li X, Cheng H (2018) The dynamic transcriptome and metabolomics profiling in Verticillium dahliae inoculated Arabidopsis thaliana. Scientific Reports 8, 15401

Szklarczyk D, Gable AL, Lyon D, Junge A, Wyder S, Huerta-Cepas J, Simonovic M, Doncheva NT, Morris JH, Bork P, Jensen LJ, Mering C (2019) STRING v11: protein–protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Research 47, D607–D613.
STRING v11: protein–protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets.Crossref | GoogleScholarGoogle Scholar |

Tsuji J, Jackson EP, Gage DA, Hammerschmidt R, Somerville SC (1992) Phytoalexin accumulation in Arabidopsis thaliana during the hypersensitive reaction to Pseudomonas syringae pv syringae. Plant Physiology 98, 1304–1309.
Phytoalexin accumulation in Arabidopsis thaliana during the hypersensitive reaction to Pseudomonas syringae pv syringae.Crossref | GoogleScholarGoogle Scholar |

Wang F-X, Ma Y-P, Yang C-L, Zhao P-M, Yao Y, Jian G-L, Luo Y-M, Xia G-X (2011) Proteomic analysis of the sea-island cotton roots infected by wilt pathogen Verticillium dahliae. Proteomics 11, 4296–4309.
Proteomic analysis of the sea-island cotton roots infected by wilt pathogen Verticillium dahliae.Crossref | GoogleScholarGoogle Scholar |

Wang Y, Liang C, Wu S, Zhang X, Tang J, Jian G, Jiao G, Li F, Chu C (2016) Significant improvement of cotton Verticillium wilt resistance by manipulating the expression of Gastrodia antifungal proteins. Molecular Plant 9, 1436–1439.
Significant improvement of cotton Verticillium wilt resistance by manipulating the expression of Gastrodia antifungal proteins.Crossref | GoogleScholarGoogle Scholar |

Wang F-X, Luo Y-M, Ye Z-Q, Cao X, Liang J-N, Wang Q, Wu Y, Wu J-H, Wang H-Y, Zhang M, Cheng H-Q, Xia G-X (2018) iTRAQ-based proteomics analysis of autophagy-mediated immune responses against the vascular fungal pathogen Verticillium dahliae in Arabidopsis. Autophagy 14, 598–618.
iTRAQ-based proteomics analysis of autophagy-mediated immune responses against the vascular fungal pathogen Verticillium dahliae in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Witzel K, Buhtz A, Grosch R (2017) Temporal impact of the vascular wilt pathogen Verticillium dahliae on tomato root proteome. Journal of Proteomics 169, 215–224.
Temporal impact of the vascular wilt pathogen Verticillium dahliae on tomato root proteome.Crossref | GoogleScholarGoogle Scholar |

Xiong X-P, Sun S-C, Zhu Q-H, Zhang X-Y, Liu F, Li Y-J, Xue F, Sun J (2021) Transcriptome analysis and RNA interference reveal GhGDH2 regulating cotton resistance to Verticillium wilt by JA and SA signaling pathways. Frontiers in Plant Science 12, 654676
Transcriptome analysis and RNA interference reveal GhGDH2 regulating cotton resistance to Verticillium wilt by JA and SA signaling pathways.Crossref | GoogleScholarGoogle Scholar |

Yang J, Wang X, Xie M, Wang G, Li Z, Zhang Y, Wu L, Zhang G, Ma Z (2020) Proteomic analyses on xylem sap provides insights into the defense response of Gossypium hirsutum against Verticillium dahliae. Journal of Proteomics 213, 103599
Proteomic analyses on xylem sap provides insights into the defense response of Gossypium hirsutum against Verticillium dahliae.Crossref | GoogleScholarGoogle Scholar |

Zhang T, Jin Y, Zhao J-H, Gao F, Zhou B-J, Fang Y-Y, Guo H-S (2016) Host-induced gene silencing of the target gene in fungal cells confers effective resistance to the cotton wilt disease pathogen Verticillium dahliae. Molecular Plant 9, 939–942.
Host-induced gene silencing of the target gene in fungal cells confers effective resistance to the cotton wilt disease pathogen Verticillium dahliae.Crossref | GoogleScholarGoogle Scholar |

Zhou N, Tootle TL, Glazebrook J (1999) Arabidopsis PAD3, a gene required for camalexin biosynthesis, encodes a putative cytochrome P450 monooxygenase. The Plant Cell 11, 2419–2428.
Arabidopsis PAD3, a gene required for camalexin biosynthesis, encodes a putative cytochrome P450 monooxygenase.Crossref | GoogleScholarGoogle Scholar |

Zhou J, Wang X, He Y, Sang T, Wang P, Dai S, Zhang S, Meng X (2020) Differential phosphorylation of the transcription factor WRKY33 by the protein kinases CPK5/CPK6 and MPK3/MPK6 cooperatively regulates camalexin biosynthesis in Arabidopsis. The Plant Cell 32, 2621–2638.
Differential phosphorylation of the transcription factor WRKY33 by the protein kinases CPK5/CPK6 and MPK3/MPK6 cooperatively regulates camalexin biosynthesis in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |