A NAC triad modulates plant immunity by negatively regulating N-hydroxy pipecolic acid biosynthesis

Jianghua Cai, Sayantan Panda, Yana Kazachkova, Eden Amzallag, Zhengguo Li, Sagit Meir, Ilana Rogachev and Asaph Aharoni ()
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Jianghua Cai: Weizmann Institute of Science
Sayantan Panda: Weizmann Institute of Science
Yana Kazachkova: Weizmann Institute of Science
Eden Amzallag: The Hebrew University of Jerusalem
Zhengguo Li: Chongqing University
Sagit Meir: Weizmann Institute of Science
Ilana Rogachev: Weizmann Institute of Science
Asaph Aharoni: Weizmann Institute of Science

Nature Communications, 2024, vol. 15, issue 1, 1-16

Abstract: Abstract N-hydroxy pipecolic acid (NHP) plays an important role in plant immunity. In contrast to its biosynthesis, our current knowledge with respect to the transcriptional regulation of the NHP pathway is limited. This study commences with the engineering of Arabidopsis plants that constitutively produce high NHP levels and display enhanced immunity. Label-free proteomics reveals a NAC-type transcription factor (NAC90) that is strongly induced in these plants. We find that NAC90 is a target gene of SAR DEFICIENT 1 (SARD1) and induced by pathogen, salicylic acid (SA), and NHP. NAC90 knockout mutants exhibit constitutive immune activation, earlier senescence, higher levels of NHP and SA, as well as increased expression of NHP and SA biosynthetic genes. In contrast, NAC90 overexpression lines are compromised in disease resistance and accumulated reduced levels of NHP and SA. NAC90 could interact with NAC61 and NAC36 which are also induced by pathogen, SA, and NHP. We next discover that this protein triad directly represses expression of the NHP and SA biosynthetic genes AGD2-LIKE DEFENSE RESPONSE PROTEIN 1 (ALD1), FLAVIN MONOOXYGENASE 1 (FMO1), and ISOCHORISMATE SYNTHASE 1 (ICS1). Constitutive immune response in nac90 is abolished once blocking NHP biosynthesis in the fmo1 background, signifying that NAC90 negative regulation of immunity is mediated via NHP biosynthesis. Our findings expand the currently documented NHP regulatory network suggesting a model that together with NHP glycosylation, NAC repressors take part in a ‘gas-and-brake’ transcriptional mechanism to control NHP production and the plant growth and defense trade-off.

Date: 2024
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DOI: 10.1038/s41467-024-51515-2

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