OXI1 induces immunity by coordinating N-hydroxypipecolic acid, salicylic acid and camalexin synthesis

Anamika Rawat; Michael Hartmann; Anne Harzen; Raphael Lugan; Sara Christina Stolze; Celine Forzani; Laura Abts; Sophie Reißenweber; Naganand Rayapuram; Hirofumi Nakagami; Jürgen Zeier; Heribert Hirt

doi:10.1111/nph.18592

OXI1 induces immunity by coordinating N-hydroxypipecolic acid, salicylic acid and camalexin synthesis

Anamika Rawat, Michael Hartmann, Anne Harzen, Raphael Lugan, Sara Christina Stolze, Celine Forzani, Laura Abts, Sophie Reißenweber, Naganand Rayapuram, Hirofumi Nakagami, Jürgen Zeier, Heribert Hirt

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5 Scopus citations

Abstract

Expression of OXI1 is induced by a number of stress conditions and regulates the interaction of plants with pathogenic and beneficial microbes. In this work, we generated Arabidopsis OXI1 knock out and genomic OXI1 overexpression lines and show by transcriptome, proteome and metabolome analysis that OXI1 triggers ALD1, SARD4 and FMO1 expression to promote the biosynthesis of pipecolic acid (Pip) and N-hydroxy pipecolic acid (NHP). OXI1 contributes to enhanced immunity by induced SA biosynthesis via CBP60g-induced expression of SID2 and camalexin accumulation via WRKY33-targeted transcription of PAD3. OXI1 regulates genes involved in ROS generation such as RbohD and RbohF. OXI1 knock out plants show enhanced expression of nuclear and chloroplast genes of photosynthesis and enhanced growth under ambient conditions, while OXI1 overexpressing plants accumulate NHP, SA, camalexin and ROS and show a gain-of-function cell death phenotype and enhanced pathogen resistance. The OXI1 gain-of-function phenotypes are completely suppressed when compromising NHP synthesis in the fmo1 or ald1 background, showing that OXI1 regulation of immunity is mediated via the NHP pathway. Overall, these results show that OXI1 plays a key role in basal and effector-triggered plant immunity by regulating defense and programmed cell death via biosynthesis of SA, NHP and camalexin.

Original language	English (US)
Journal	New Phytologist
DOIs	https://doi.org/10.1111/nph.18592
State	Published - Nov 1 2022

Bibliographical note

KAUST Repository Item: Exported on 2022-11-04
Acknowledged KAUST grant number(s): BAS/1/1062–01-0, URF/1/2965-01-01
Acknowledgements: We would like to thank all members of the Hirt and Zeier labs. The work was supported by grants to HH by the Laboratory of Excellence Saclay Plant Sciences IPS2 and the King Abdullah University of Science and Technology (KAUST) (BAS/1/1062–01-0 and URF/1/2965-01-01), and by a grant to JZ by the German Research Foundation (DFG grant ZE467/6-2). The IPS2 benefits from the support of the LabEx Saclay Plant Sciences-SPS (ANR-10-LABX-0040-SPS). HN was supported by the Max Planck Society.

ASJC Scopus subject areas

General Medicine

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10.1111/nph.18592

https://repository.kaust.edu.sa/bitstream/10754/685390/1/New%20Phytologist%20-%202022%20-%20Rawat%20-%20OXI1%20induces%20immunity%20by%20coordinating%20N%e2%80%90hydroxypipecolic%20acid%20%20salicylic%20acid%20and.pdf

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@article{91c6800f511341b982c37f285b49f2a5,

title = "OXI1 induces immunity by coordinating N-hydroxypipecolic acid, salicylic acid and camalexin synthesis",

abstract = "Expression of OXI1 is induced by a number of stress conditions and regulates the interaction of plants with pathogenic and beneficial microbes. In this work, we generated Arabidopsis OXI1 knock out and genomic OXI1 overexpression lines and show by transcriptome, proteome and metabolome analysis that OXI1 triggers ALD1, SARD4 and FMO1 expression to promote the biosynthesis of pipecolic acid (Pip) and N-hydroxy pipecolic acid (NHP). OXI1 contributes to enhanced immunity by induced SA biosynthesis via CBP60g-induced expression of SID2 and camalexin accumulation via WRKY33-targeted transcription of PAD3. OXI1 regulates genes involved in ROS generation such as RbohD and RbohF. OXI1 knock out plants show enhanced expression of nuclear and chloroplast genes of photosynthesis and enhanced growth under ambient conditions, while OXI1 overexpressing plants accumulate NHP, SA, camalexin and ROS and show a gain-of-function cell death phenotype and enhanced pathogen resistance. The OXI1 gain-of-function phenotypes are completely suppressed when compromising NHP synthesis in the fmo1 or ald1 background, showing that OXI1 regulation of immunity is mediated via the NHP pathway. Overall, these results show that OXI1 plays a key role in basal and effector-triggered plant immunity by regulating defense and programmed cell death via biosynthesis of SA, NHP and camalexin.",

author = "Anamika Rawat and Michael Hartmann and Anne Harzen and Raphael Lugan and Stolze, {Sara Christina} and Celine Forzani and Laura Abts and Sophie Rei{\ss}enweber and Naganand Rayapuram and Hirofumi Nakagami and J{\"u}rgen Zeier and Heribert Hirt",

note = "KAUST Repository Item: Exported on 2022-11-04 Acknowledged KAUST grant number(s): BAS/1/1062–01-0, URF/1/2965-01-01 Acknowledgements: We would like to thank all members of the Hirt and Zeier labs. The work was supported by grants to HH by the Laboratory of Excellence Saclay Plant Sciences IPS2 and the King Abdullah University of Science and Technology (KAUST) (BAS/1/1062–01-0 and URF/1/2965-01-01), and by a grant to JZ by the German Research Foundation (DFG grant ZE467/6-2). The IPS2 benefits from the support of the LabEx Saclay Plant Sciences-SPS (ANR-10-LABX-0040-SPS). HN was supported by the Max Planck Society.",

year = "2022",

month = nov,

day = "1",

doi = "10.1111/nph.18592",

language = "English (US)",

journal = "New Phytologist",

issn = "0028-646X",

publisher = "Wiley",

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T1 - OXI1 induces immunity by coordinating N-hydroxypipecolic acid, salicylic acid and camalexin synthesis

AU - Rawat, Anamika

AU - Hartmann, Michael

AU - Harzen, Anne

AU - Lugan, Raphael

AU - Stolze, Sara Christina

AU - Forzani, Celine

AU - Abts, Laura

AU - Reißenweber, Sophie

AU - Rayapuram, Naganand

AU - Nakagami, Hirofumi

AU - Zeier, Jürgen

AU - Hirt, Heribert

N1 - KAUST Repository Item: Exported on 2022-11-04 Acknowledged KAUST grant number(s): BAS/1/1062–01-0, URF/1/2965-01-01 Acknowledgements: We would like to thank all members of the Hirt and Zeier labs. The work was supported by grants to HH by the Laboratory of Excellence Saclay Plant Sciences IPS2 and the King Abdullah University of Science and Technology (KAUST) (BAS/1/1062–01-0 and URF/1/2965-01-01), and by a grant to JZ by the German Research Foundation (DFG grant ZE467/6-2). The IPS2 benefits from the support of the LabEx Saclay Plant Sciences-SPS (ANR-10-LABX-0040-SPS). HN was supported by the Max Planck Society.

PY - 2022/11/1

Y1 - 2022/11/1

N2 - Expression of OXI1 is induced by a number of stress conditions and regulates the interaction of plants with pathogenic and beneficial microbes. In this work, we generated Arabidopsis OXI1 knock out and genomic OXI1 overexpression lines and show by transcriptome, proteome and metabolome analysis that OXI1 triggers ALD1, SARD4 and FMO1 expression to promote the biosynthesis of pipecolic acid (Pip) and N-hydroxy pipecolic acid (NHP). OXI1 contributes to enhanced immunity by induced SA biosynthesis via CBP60g-induced expression of SID2 and camalexin accumulation via WRKY33-targeted transcription of PAD3. OXI1 regulates genes involved in ROS generation such as RbohD and RbohF. OXI1 knock out plants show enhanced expression of nuclear and chloroplast genes of photosynthesis and enhanced growth under ambient conditions, while OXI1 overexpressing plants accumulate NHP, SA, camalexin and ROS and show a gain-of-function cell death phenotype and enhanced pathogen resistance. The OXI1 gain-of-function phenotypes are completely suppressed when compromising NHP synthesis in the fmo1 or ald1 background, showing that OXI1 regulation of immunity is mediated via the NHP pathway. Overall, these results show that OXI1 plays a key role in basal and effector-triggered plant immunity by regulating defense and programmed cell death via biosynthesis of SA, NHP and camalexin.

AB - Expression of OXI1 is induced by a number of stress conditions and regulates the interaction of plants with pathogenic and beneficial microbes. In this work, we generated Arabidopsis OXI1 knock out and genomic OXI1 overexpression lines and show by transcriptome, proteome and metabolome analysis that OXI1 triggers ALD1, SARD4 and FMO1 expression to promote the biosynthesis of pipecolic acid (Pip) and N-hydroxy pipecolic acid (NHP). OXI1 contributes to enhanced immunity by induced SA biosynthesis via CBP60g-induced expression of SID2 and camalexin accumulation via WRKY33-targeted transcription of PAD3. OXI1 regulates genes involved in ROS generation such as RbohD and RbohF. OXI1 knock out plants show enhanced expression of nuclear and chloroplast genes of photosynthesis and enhanced growth under ambient conditions, while OXI1 overexpressing plants accumulate NHP, SA, camalexin and ROS and show a gain-of-function cell death phenotype and enhanced pathogen resistance. The OXI1 gain-of-function phenotypes are completely suppressed when compromising NHP synthesis in the fmo1 or ald1 background, showing that OXI1 regulation of immunity is mediated via the NHP pathway. Overall, these results show that OXI1 plays a key role in basal and effector-triggered plant immunity by regulating defense and programmed cell death via biosynthesis of SA, NHP and camalexin.

UR - http://hdl.handle.net/10754/685390

UR - https://onlinelibrary.wiley.com/doi/10.1111/nph.18592

U2 - 10.1111/nph.18592

DO - 10.1111/nph.18592

M3 - Article

C2 - 36319610

SN - 0028-646X

JO - New Phytologist

JF - New Phytologist

ER -

OXI1 induces immunity by coordinating N-hydroxypipecolic acid, salicylic acid and camalexin synthesis

Abstract

Bibliographical note

ASJC Scopus subject areas

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