Fungal resistance mediated by maize wall-associated kinase ZmWAK-RLK1 correlates with reduced benzoxazinoid content

Ping Yang; Coraline Praz; Beibei Li; Jyoti Singla; Christelle A. M. Robert; Bettina Kessel; Daniela Scheuermann; Linda Lüthi; Milena Ouzunova; Matthias Erb; Simon G. Krattinger; Beat Keller

doi:10.1111/nph.15419

Fungal resistance mediated by maize wall-associated kinase ZmWAK-RLK1 correlates with reduced benzoxazinoid content

Ping Yang, Coraline Praz, Beibei Li, Jyoti Singla, Christelle A. M. Robert, Bettina Kessel, Daniela Scheuermann, Linda Lüthi, Milena Ouzunova, Matthias Erb, Simon G. Krattinger, Beat Keller

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Abstract

Wall-associated kinases (WAKs) have recently been identified as major components of fungal and bacterial disease resistance in several cereal crop species. However, the molecular mechanisms of WAK-mediated resistance remain largely unknown. \nHere, we investigated the function of the maize gene ZmWAK-RLK1 (Htn1) that confers quantitative resistance to northern corn leaf blight (NCLB) caused by the hemibiotrophic fungal pathogen Exserohilum turcicum. \nZmWAK-RLK1 was found to localize to the plasma membrane and its presence resulted in a modification of the infection process by reducing pathogen penetration into host tissues. A large-scale transcriptome analysis of near-isogenic lines (NILs) differing for ZmWAK-RLK1 revealed that several differentially expressed genes are involved in the biosynthesis of the secondary metabolites benzoxazinoids (BXs). The contents of several BXs including DIM2BOA-Glc were significantly lower when ZmWAK-RLK1 is present. DIM2BOA-Glc concentration was significantly elevated in ZmWAK-RLK1 mutants with compromised NCLB resistance. Maize mutants that were affected in overall BXs biosynthesis or content of DIM2BOA-Glc showed increased NCLB resistance. \nWe conclude that Htn1-mediated NCLB resistance is associated with a reduction of BX secondary metabolites. These findings suggest a link between WAK-mediated quantitative disease resistance and changes in biochemical fluxes starting with indole-3-glycerol phosphate.

Original language	English (US)
Pages (from-to)	976-987
Number of pages	12
Journal	New Phytologist
Volume	221
Issue number	2
DOIs	https://doi.org/10.1111/nph.15419
State	Published - Sep 4 2018

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https://repository.kaust.edu.sa/bitstream/10754/628523/2/20180608_py.pdf

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@article{5c091b29f23343ed8f4ad69ef860dbf2,

title = "Fungal resistance mediated by maize wall-associated kinase ZmWAK-RLK1 correlates with reduced benzoxazinoid content",

abstract = "Wall-associated kinases (WAKs) have recently been identified as major components of fungal and bacterial disease resistance in several cereal crop species. However, the molecular mechanisms of WAK-mediated resistance remain largely unknown. \nHere, we investigated the function of the maize gene ZmWAK-RLK1 (Htn1) that confers quantitative resistance to northern corn leaf blight (NCLB) caused by the hemibiotrophic fungal pathogen Exserohilum turcicum. \nZmWAK-RLK1 was found to localize to the plasma membrane and its presence resulted in a modification of the infection process by reducing pathogen penetration into host tissues. A large-scale transcriptome analysis of near-isogenic lines (NILs) differing for ZmWAK-RLK1 revealed that several differentially expressed genes are involved in the biosynthesis of the secondary metabolites benzoxazinoids (BXs). The contents of several BXs including DIM2BOA-Glc were significantly lower when ZmWAK-RLK1 is present. DIM2BOA-Glc concentration was significantly elevated in ZmWAK-RLK1 mutants with compromised NCLB resistance. Maize mutants that were affected in overall BXs biosynthesis or content of DIM2BOA-Glc showed increased NCLB resistance. \nWe conclude that Htn1-mediated NCLB resistance is associated with a reduction of BX secondary metabolites. These findings suggest a link between WAK-mediated quantitative disease resistance and changes in biochemical fluxes starting with indole-3-glycerol phosphate.",

author = "Ping Yang and Coraline Praz and Beibei Li and Jyoti Singla and Robert, {Christelle A. M.} and Bettina Kessel and Daniela Scheuermann and Linda L{\"u}thi and Milena Ouzunova and Matthias Erb and Krattinger, {Simon G.} and Beat Keller",

note = "KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: The authors would like to thank Dr Severine Hurni (UZH) for helpful discussions, Professor Jiaqiang Sun (Institute of Crop Sciences, CAAS) for assistance in performance of Western blot, Professor Jianfeng Wen for assistance in performance of experiments with maize protoplasts, Professor Georg Jander (Cornell University) for kindly providing bx mutants, and Mr Alessandro Artemisio, Mr Gerhard Herren, Mr Karl Huwiler, Mr Thibault Vassor and Ms Matisse Petit-Prost for technical support. This work was supported by Swiss National Science Foundation Grant 310030_163260 to B Keller. SGK is supported by an Ambizione grant of the Swiss National Science Foundation. PY is supported by Agricultural Science and Technology Innovation Program of CAAS and Fundamental Research Funds for Central Non-Profit of Institute of Crop Sciences of CAAS, China.",

year = "2018",

month = sep,

day = "4",

doi = "10.1111/nph.15419",

language = "English (US)",

volume = "221",

pages = "976--987",

journal = "New Phytologist",

issn = "0028-646X",

publisher = "Wiley-Blackwell Publishing Ltd",

number = "2",

}

TY - JOUR

T1 - Fungal resistance mediated by maize wall-associated kinase ZmWAK-RLK1 correlates with reduced benzoxazinoid content

AU - Yang, Ping

AU - Praz, Coraline

AU - Li, Beibei

AU - Singla, Jyoti

AU - Robert, Christelle A. M.

AU - Kessel, Bettina

AU - Scheuermann, Daniela

AU - Lüthi, Linda

AU - Ouzunova, Milena

AU - Erb, Matthias

AU - Krattinger, Simon G.

AU - Keller, Beat

N1 - KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: The authors would like to thank Dr Severine Hurni (UZH) for helpful discussions, Professor Jiaqiang Sun (Institute of Crop Sciences, CAAS) for assistance in performance of Western blot, Professor Jianfeng Wen for assistance in performance of experiments with maize protoplasts, Professor Georg Jander (Cornell University) for kindly providing bx mutants, and Mr Alessandro Artemisio, Mr Gerhard Herren, Mr Karl Huwiler, Mr Thibault Vassor and Ms Matisse Petit-Prost for technical support. This work was supported by Swiss National Science Foundation Grant 310030_163260 to B Keller. SGK is supported by an Ambizione grant of the Swiss National Science Foundation. PY is supported by Agricultural Science and Technology Innovation Program of CAAS and Fundamental Research Funds for Central Non-Profit of Institute of Crop Sciences of CAAS, China.

PY - 2018/9/4

Y1 - 2018/9/4

N2 - Wall-associated kinases (WAKs) have recently been identified as major components of fungal and bacterial disease resistance in several cereal crop species. However, the molecular mechanisms of WAK-mediated resistance remain largely unknown. \nHere, we investigated the function of the maize gene ZmWAK-RLK1 (Htn1) that confers quantitative resistance to northern corn leaf blight (NCLB) caused by the hemibiotrophic fungal pathogen Exserohilum turcicum. \nZmWAK-RLK1 was found to localize to the plasma membrane and its presence resulted in a modification of the infection process by reducing pathogen penetration into host tissues. A large-scale transcriptome analysis of near-isogenic lines (NILs) differing for ZmWAK-RLK1 revealed that several differentially expressed genes are involved in the biosynthesis of the secondary metabolites benzoxazinoids (BXs). The contents of several BXs including DIM2BOA-Glc were significantly lower when ZmWAK-RLK1 is present. DIM2BOA-Glc concentration was significantly elevated in ZmWAK-RLK1 mutants with compromised NCLB resistance. Maize mutants that were affected in overall BXs biosynthesis or content of DIM2BOA-Glc showed increased NCLB resistance. \nWe conclude that Htn1-mediated NCLB resistance is associated with a reduction of BX secondary metabolites. These findings suggest a link between WAK-mediated quantitative disease resistance and changes in biochemical fluxes starting with indole-3-glycerol phosphate.

AB - Wall-associated kinases (WAKs) have recently been identified as major components of fungal and bacterial disease resistance in several cereal crop species. However, the molecular mechanisms of WAK-mediated resistance remain largely unknown. \nHere, we investigated the function of the maize gene ZmWAK-RLK1 (Htn1) that confers quantitative resistance to northern corn leaf blight (NCLB) caused by the hemibiotrophic fungal pathogen Exserohilum turcicum. \nZmWAK-RLK1 was found to localize to the plasma membrane and its presence resulted in a modification of the infection process by reducing pathogen penetration into host tissues. A large-scale transcriptome analysis of near-isogenic lines (NILs) differing for ZmWAK-RLK1 revealed that several differentially expressed genes are involved in the biosynthesis of the secondary metabolites benzoxazinoids (BXs). The contents of several BXs including DIM2BOA-Glc were significantly lower when ZmWAK-RLK1 is present. DIM2BOA-Glc concentration was significantly elevated in ZmWAK-RLK1 mutants with compromised NCLB resistance. Maize mutants that were affected in overall BXs biosynthesis or content of DIM2BOA-Glc showed increased NCLB resistance. \nWe conclude that Htn1-mediated NCLB resistance is associated with a reduction of BX secondary metabolites. These findings suggest a link between WAK-mediated quantitative disease resistance and changes in biochemical fluxes starting with indole-3-glycerol phosphate.

UR - http://hdl.handle.net/10754/628523

UR - https://nph.onlinelibrary.wiley.com/doi/full/10.1111/nph.15419

UR - http://www.scopus.com/inward/record.url?scp=85052874500&partnerID=8YFLogxK

U2 - 10.1111/nph.15419

DO - 10.1111/nph.15419

M3 - Article

SN - 0028-646X

VL - 221

SP - 976

EP - 987

JO - New Phytologist

JF - New Phytologist

IS - 2

ER -

Fungal resistance mediated by maize wall-associated kinase ZmWAK-RLK1 correlates with reduced benzoxazinoid content

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