AbstractN-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.

羟基胡椒酸（NHP）在植物免疫中起着重要作用。与其生物合成相反，我们目前关于NHP途径转录调控的知识是有限的。这项研究从拟南芥植物的工程开始，这些植物组成性地产生高NHP水平并显示出增强的免疫力。

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.

无标记蛋白质组学揭示了在这些植物中强烈诱导的NAC型转录因子（NAC90）。我们发现NAC90是SAR缺陷1（SARD1）的靶基因，由病原体，水杨酸（SA）和NHP诱导。NAC90敲除突变体表现出组成型免疫激活，较早衰老，较高水平的NHP和SA，以及NHP和SA生物合成基因的表达增加。

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).

相反，NAC90过表达系的抗病性受损，NHP和SA水平降低。NAC90可能与病原体，SA和NHP诱导的NAC61和NAC36相互作用。。

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..

一旦在fmo1背景中阻断NHP生物合成，nac90中的组成型免疫应答就会被消除，这表明nac90对免疫的负调节是通过NHP生物合成介导的。。。

IntroductionPlant defense responses are initiated by the recognition of pathogen-associated molecular patterns (PAMPs) or effectors molecules, which as a consequence result in activation of PAMP-triggered immunity or effector-triggered immunity, respectively1. In recent years, outstanding strides have been made in dissecting the regulatory mechanisms and components necessary for plant defense.

引言植物防御反应是通过识别病原体相关分子模式（PAMP）或效应分子启动的，其结果分别导致PAMP触发的免疫或效应子触发的免疫的激活1。近年来，在剖析植物防御所必需的调控机制和组成部分方面取得了重大进展。

Following attack by pathogens, salicylic acid (SA) accumulates in plants2,3. External application of SA or its chemical analogs can enhance the plants resistance to various diseases, whereas plants lacking SA biosynthesis, perception, or signal transduction display severely compromised resistance and failure in systemic acquired resistance (SAR) establishment4,5,6.

在病原体攻击后，水杨酸（SA）在植物中积累2,3。SA或其化学类似物的外部应用可以增强植物对各种疾病的抗性，而缺乏SA生物合成，感知或信号转导的植物在系统获得性抗性（SAR）建立中表现出严重的抗性受损和失败4,5,6。

Apart from SA, several additional metabolites have been implicated in plant defense response, including methyl salicylate (MeSA)7, azelaic acid (AzA)8, glycerol-3-phosphate (G3P)9, dehydroabietinal (DA)10, N-hydroxy pipecolic acid (NHP)11,12, β-aminobutyric acid (BABA)13, L-glutamate14, and melatonin15.NHP is a non-protein amino acid derived from lysine that systemically accumulates in plants during pathogen infection and is essential for plant defense activation and SAR establishment11,12.

除SA外，植物防御反应还涉及其他几种代谢物，包括水杨酸甲酯（MeSA）7，壬二酸（AzA）8，甘油-3-磷酸（G3P）9，脱氢枞酸（DA）10，N-羟基哌啶酸（NHP）11,12，β-氨基丁酸（BABA）13，L-谷氨酸14和褪黑激素15.NHP是一种非蛋白质氨基酸，来源于赖氨酸，在病原体感染期间在植物中系统积累，对植物防御激活和SAR建立至关重要11,12。

Significant progress has been made in understanding the NHP biosynthetic pathway. It starts from L-lysine and involves three enzymes: AGD2-LIKE DEFENSE RESPONSE PROTEIN 1 (ALD1), SAR-DEFICIENT 4 (SARD4), and FLAVIN MONOOXYGENASE 1 (FMO1). Lysine is converted by ALD1 to form 2,3-dehydropipecolic acid, which is then reduced by SARD4 to generate pipecolic acid (Pip)16,17,18.

在理解NHP生物合成途径方面取得了重大进展。它从L-赖氨酸开始，涉及三种酶：AGD2样防御反应蛋白1（ALD1），SAR缺陷型4（SARD4）和黄素单加氧酶1（FMO1）。赖氨酸被ALD1转化为2,3-脱氢吡啶酸，然后被SARD4还原生成胡椒酸（Pip）16,17,18。

Next, FMO1 hydroxylates Pip to form NHP11,12. The expression of these three NHP biosynthetic genes was strongly induced in plants in response to pathogen infection,.

接下来，FMO1羟基化Pip形成NHP11,12。这三种NHP生物合成基因的表达在植物中强烈诱导以响应病原体感染，。

Data availability

数据可用性

The proteomics raw data generated in this study have been deposited in a ProteomeXchange Consortium member under the accession number PXD054472. The proteomics data generated in this study are provided in the Supplementary Information file. The RNA-seq data in this study are available in the NCBI Sequence Read Archive database under the accession number PRJNA996953 [https://www.ncbi.nlm.nih.gov/bioproject/?term=996953]. Source data are provided with this paper..

本研究中产生的蛋白质组学原始数据已保存在ProteomeXchange联盟成员中，登录号为PXD054472。本研究中产生的蛋白质组学数据在补充信息文件中提供。本研究中的RNA-seq数据可在NCBI序列读取存档数据库中获得，登录号为PRJNA996953[https://www.ncbi.nlm.nih.gov/bioproject/?term=996953]。本文提供了源数据。。

ReferencesJones, J. D. & Dangl, J. L. The plant immune system. Nature 444, 323–329 (2006).Article

参考Jones，J.D。和Dangl，J.L。植物免疫系统。《自然》444323-329（2006）。文章

ADS

广告

CAS

中科院

PubMed

PubMed

Google Scholar

谷歌学者

Malamy, J., Carr, J. P., Klessig, D. F. & Raskin, I. Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250, 1002–1004 (1990).Article

Malamy，J.，Carr，J.P.，Klessig，D.F。＆Raskin，I。水杨酸：烟草对病毒感染的抗性反应中可能的内源性信号。科学2501002-1004（1990）。文章

ADS

广告

CAS

中科院

PubMed

PubMed

Google Scholar

谷歌学者

Métraux, J. et al. Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science 250, 1004–1006 (1990).Article

Métraux，J。等人。黄瓜系统获得性抗性开始时水杨酸的增加。科学2501004-1006（1990）。文章

ADS

广告

PubMed

PubMed

Google Scholar

谷歌学者

Nawrath, C. & Métraux, J. Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell 11, 1393–1404 (1999).CAS

Nawrath，C。＆Métraux，J。拟南芥的水杨酸诱导缺陷型突变体表达PR-2和PR-5，并在病原体接种后积累高水平的camalexin。植物细胞111393-1404（1999）。中科院

PubMed

PubMed

PubMed Central

公共医学中心

Google Scholar

谷歌学者

Ward, E. R. et al. Coordinate gene activity in response to agents that induce systemic acquired resistance. Plant Cell 3, 1085–1094 (1991).Article

Ward，E.R.等人协调基因活性以响应诱导全身获得性耐药的药物。植物细胞31085-1094（1991）。文章

CAS

中科院

PubMed

PubMed

PubMed Central

公共医学中心

Google Scholar

谷歌学者

Wu, Y. et al. The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid. Cell Rep. 1, 639–647 (2012).Article

Wu，Y。等人。拟南芥NPR1蛋白是植物防御激素水杨酸的受体。Cell Rep.1639–647（2012）。文章

CAS

中科院

PubMed

PubMed

Google Scholar

谷歌学者

Park, S., Kaimoyo, E., Kumar, D., Mosher, S. & Klessig, D. F. Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318, 113–116 (2007).Article

。科学318113-116（2007）。文章

ADS

广告

CAS

中科院

PubMed

PubMed

Google Scholar

谷歌学者

Jung, H. W., Tschaplinski, T. J., Wang, L., Glazebrook, J. & Greenberg, J. T. Priming in systemic plant immunity. Science 324, 89–91 (2009).Article

Jung，H.W.，Tschaplinski，T.J.，Wang，L.，Glazebrook，J。＆Greenberg，J.T。引发系统性植物免疫。。文章

ADS

广告

PubMed

PubMed

Google Scholar

谷歌学者

Chanda, B. et al. Glycerol-3-phosphate is a critical mobile inducer of systemic immunity in plants. Nat. Genet. 43, 421–427 (2011).Article

Chanda，B。等人。甘油-3-磷酸是植物全身免疫的关键移动诱导剂。纳特·吉内特。43421-427（2011）。文章

ADS

广告

CAS

中科院

PubMed

PubMed

Google Scholar

谷歌学者

Chaturvedi, R. et al. An abietane diterpenoid is a potent activator of systemic acquired resistance. Plant J. 71, 161–172 (2012).Article

Chaturvedi，R。等人。abietane二萜类化合物是全身获得性耐药的有效激活剂。植物J.71161–172（2012）。文章

CAS

中科院

PubMed

PubMed

Google Scholar

谷歌学者

Chen, Y. et al. N-hydroxy-pipecolic acid is a mobile metabolite that induces systemic disease resistance in Arabidopsis. Proc. Natl Acad. Sci. USA 115, E4920–E4929 (2018).CAS

Chen，Y。等人。N-羟基哌啶酸是一种可移动的代谢物，可诱导拟南芥的全身抗病性。程序。国家科学院。科学。美国115，E4920–E4929（2018）。中科院

PubMed

PubMed

PubMed Central

公共医学中心

Google Scholar

谷歌学者

Hartmann, M. et al. Flavin monooxygenase-generated N-hydroxypipecolic acid is a critical element of plant systemic immunity. Cell 173, 456–469.e416 (2018).Article

Hartmann，M。等人。黄素单加氧酶产生的N-羟基哌啶酸是植物系统免疫的关键因素。细胞173456-469.e416（2018）。文章

CAS

中科院

PubMed

PubMed

Google Scholar

谷歌学者

Schwarzenbacher, R. E. et al. The IBI1 receptor of β-aminobutyric acid interacts with VOZ transcription factors to regulate abscisic acid signaling and callose-associated defense. Mol. Plant 13, 1455–1469 (2020).Article

Schwarzenbacher，R.E.等人。β-氨基丁酸的IBI1受体与VOZ转录因子相互作用，调节脱落酸信号传导和胼胝质相关防御。摩尔工厂131455-1469（2020）。文章

CAS

中科院

PubMed

PubMed

Google Scholar

谷歌学者

Goto, Y. et al. Exogenous treatment with glutamate induces immune responses in Arabidopsis. Mol. Plant-Microbe Interact. 33, 474–487 (2020).Article

Goto，Y。等人。谷氨酸的外源处理诱导拟南芥的免疫应答。分子植物微生物相互作用。33474-487（2020）。文章

CAS

中科院

PubMed

PubMed

Google Scholar

谷歌学者

Zeng, H., Bai, Y., Wei, Y., Reiter, R. J. & Shi, H. Phytomelatonin as a central molecule in plant disease resistance. J. Exp. Bot. 73, 5874–5885 (2022).Article

Zeng，H.，Bai，Y.，Wei，Y.，Reiter，R.J。＆Shi，H。植物褪黑激素作为植物抗病性的中心分子。J、 附件735874-5885（2022年）。文章

PubMed

PubMed

Google Scholar

谷歌学者

Návarová, H., Bernsdorff, F., Döring, A. & Zeier, J. Pipecolic acid, an endogenous mediator of defense amplification and priming, is a critical regulator of inducible plant immunity. Plant Cell 24, 5123–5141 (2012).Article

Návarová，H.，Bernsdorff，F.，Döring，A。＆Zeier，J。胡椒酸是防御扩增和引发的内源性介质，是诱导型植物免疫的关键调节剂。植物细胞245123-5141（2012）。文章

PubMed

PubMed

PubMed Central

公共医学中心

Google Scholar

谷歌学者

Hartmann, M. et al. Biochemical principles and functional aspects of pipecolic acid biosynthesis in plant immunity. Plant Physiol. 174, 124–153 (2017).Article

Hartmann，M.等人。植物免疫中胡椒酸生物合成的生化原理和功能方面。植物生理学。174124-153（2017）。文章

ADS

广告

CAS

中科院

PubMed

PubMed

PubMed Central

公共医学中心

Google Scholar

谷歌学者

Bernsdorff, F. et al. Pipecolic acid orchestrates plant systemic acquired resistance and defense priming via salicylic acid-dependent and-independent pathways. Plant Cell 28, 102–129 (2016).Article

Bernsdorff，F。等人。胡椒酸通过水杨酸依赖性和独立途径协调植物系统获得性抗性和防御启动。植物细胞28102-129（2016）。文章

CAS

中科院

PubMed

PubMed

Google Scholar

谷歌学者

Tian, H. & Zhang, Y. The emergence of a mobile signal for systemic acquired resistance. Plant Cell 31, 1414–1415 (2019).Article

Tian，H。＆Zhang，Y。系统性获得性抵抗的移动信号的出现。植物细胞311414-1415（2019）。文章

CAS

中科院

PubMed

PubMed

PubMed Central

公共医学中心

Google Scholar

谷歌学者

Holmes, E. C., Chen, Y., Sattely, E. S. & Mudgett, M. B. An engineered pathway for N-hydroxy-pipecolic acid synthesis enhances systemic acquired resistance in tomato. Sci. Signal. 12, eaay3066 (2019).Article

Holmes，E.C.，Chen，Y.，Sattly，E.S。和Mudgett，M.B。N-羟基哌啶酸合成的工程途径增强了番茄的系统获得性抗性。科学。信号。12，eaay3066（2019）。文章

CAS

中科院

PubMed

PubMed

PubMed Central

公共医学中心

Google Scholar

谷歌学者

Schnake, A. et al. Inducible biosynthesis and immune function of the systemic acquired resistance inducer N-hydroxypipecolic acid in monocotyledonous and dicotyledonous plants. J. Exp. Bot. 71, 6444–6459 (2020).Article

Schnake，A.等人。系统获得性抗性诱导剂N-羟基胡椒酸在单子叶植物和双子叶植物中的诱导生物合成和免疫功能。J、 附录716444-6459（2020年）。文章

CAS

中科院

PubMed

PubMed

PubMed Central

公共医学中心

Google Scholar

谷歌学者

Yildiz, I. et al. The mobile SAR signal N-hydroxypipecolic acid induces NPR1-dependent transcriptional reprogramming and immune priming. Plant Physiol. 186, 1679–1705 (2021).Article

Yildiz，I。等人。移动SAR信号N-羟基哌啶酸诱导NPR1依赖性转录重编程和免疫启动。植物生理学。1861679-1705（2021）。文章

CAS

中科院

PubMed

PubMed

PubMed Central

公共医学中心

Google Scholar

谷歌学者

Hartmann, M. & Zeier, J. l‐lysine metabolism to N‐hydroxypipecolic acid: an integral immune‐activating pathway in plants. Plant J. 96, 5–21 (2018).Article

Hartmann，M。＆Zeier，J。l-赖氨酸代谢为N-羟基哌啶酸：植物中不可或缺的免疫激活途径。植物J.96,5-21（2018）。文章

CAS

中科院

PubMed

PubMed

Google Scholar

谷歌学者

Cai, J. et al. Glycosylation of N-hydroxy-pipecolic acid equilibrates between systemic acquired resistance response and plant growth. Mol. Plant 14, 440–455 (2021).Article

Cai，J。等人。N-羟基哌啶酸的糖基化在系统获得性抗性反应和植物生长之间平衡。。文章

CAS

中科院

PubMed

PubMed

Google Scholar

谷歌学者

Bauer, S. et al. UGT76B1, a promiscuous hub of small molecule-based immune signaling, glucosylates N-hydroxypipecolic acid, and balances plant immunity. Plant Cell 33, 714–734 (2021).Article

Bauer，S。等人，UGT76B1是一种基于小分子的免疫信号传导的混杂中枢，可使N-羟基哌啶酸葡糖基化，并平衡植物免疫力。植物细胞33714-734（2021）。文章

PubMed

PubMed

PubMed Central

公共医学中心

Google Scholar

谷歌学者

Holmes, E. C., Chen, Y., Mudgett, M. B. & Sattely, E. S. Arabidopsis UGT76B1 glycosylates N-hydroxy-pipecolic acid and inactivates systemic acquired resistance in tomato. Plant Cell 33, 750–765 (2021).Article

Holmes，E.C.，Chen，Y.，Mudgett，M.B。＆Sattly，拟南芥UGT76B1糖基化N-羟基哌啶酸并使番茄的系统获得性抗性失活。植物细胞33750-765（2021）。文章

PubMed

PubMed

PubMed Central

公共医学中心

Google Scholar

谷歌学者

Mohnike, L. et al. The glycosyltransferase UGT76B1 modulates N-hydroxy-pipecolic acid homeostasis and plant immunity. Plant Cell 33, 735–749 (2021).Article

Mohnike，L。等人。糖基转移酶UGT76B1调节N-羟基哌啶酸稳态和植物免疫。植物细胞33735-749（2021）。文章

PubMed

PubMed

PubMed Central

公共医学中心

Google Scholar

谷歌学者

Zeier, J. Metabolic regulation of systemic acquired resistance. Curr. Opin. Plant Biol. 62, 102050 (2021).Article

。货币。奥平。植物生物学。62102050（2021）。文章

CAS

中科院

PubMed

PubMed

Google Scholar

谷歌学者

Wang, Y. et al. A MPK3/6-WRKY33-ALD1-pipecolic acid regulatory loop contributes to systemic acquired resistance. Plant Cell 30, 2480–2494 (2018).Article

Wang，Y。等人。MPK3/6-WRKY33-ALD1-哌啶酸调节环有助于全身获得性耐药。植物细胞302480-2494（2018）。文章

ADS

广告

CAS

中科院

PubMed

PubMed

PubMed Central

公共医学中心

Google Scholar

谷歌学者

Guerra, T. et al. Calcium‐dependent protein kinase 5 links calcium signaling with N‐hydroxy‐L‐pipecolic acid‐and SARD1‐dependent immune memory in systemic acquired resistance. N. Phytol. 225, 310–325 (2020).Article

Guerra，T。等人。钙依赖性蛋白激酶5将钙信号传导与N-羟基-L-哌啶酸和SARD1依赖性免疫记忆联系在一起，从而产生全身获得性耐药。N、 植物醇。225、310–325（2020）。文章

CAS

中科院

Google Scholar

谷歌学者

Sun, T. et al. ChIP-seq reveals broad roles of SARD1 and CBP60g in regulating plant immunity. Nat. Commun. 6, 1–12 (2015).Article

Sun，T。等人的ChIP-seq揭示了SARD1和CBP60g在调节植物免疫中的广泛作用。国家公社。6，1-12（2015）。文章

ADS

广告

Google Scholar

谷歌学者

Sun, T. et al. TGACG‐BINDING FACTOR 1 (TGA1) and TGA4 regulate salicylic acid and pipecolic acid biosynthesis by modulating the expression of SYSTEMIC ACQUIRED RESISTANCE DEFICIENT 1 (SARD1) and CALMODULIN‐BINDING PROTEIN 60g (CBP60g). N. Phytol. 217, 344–354 (2018).Article

。N、 植物醇。217344-354（2018）。文章

CAS

中科院

Google Scholar

谷歌学者

Zhou, M. et al. WRKY70 prevents axenic activation of plant immunity by direct repression of SARD1. N. Phytol. 217, 700–712 (2018).Article

Zhou，M。等人WRKY70通过直接抑制SARD1来防止植物免疫的无菌激活。N、 植物醇。217700-712（2018）。文章

CAS

中科院

Google Scholar

谷歌学者

Sun, T. et al. Redundant CAMTA transcription factors negatively regulate the biosynthesis of salicylic acid and N-hydroxypipecolic acid by modulating the expression of SARD1 and CBP60g. Mol. Plant 13, 144–156 (2020).Article

Sun，T。等人。冗余的CAMTA转录因子通过调节SARD1和CBP60g的表达负调节水杨酸和N-羟基胡椒酸的生物合成。摩尔植物13144-156（2020）。文章

CAS

中科院

PubMed

PubMed

Google Scholar

谷歌学者

Lan, J. et al. Epigenetic regulation of N‐hydroxypipecolic acid biosynthesis by the AIPP3‐PHD2‐CPL2 complex. J. Integr. Plant Biol. 65, 2660–2671 (2023).Article

Lan，J。等人。AIPP3-PHD2-CPL2复合物对N-羟基哌啶酸生物合成的表观遗传调控。J、 整数。植物生物学。652660-2671（2023）。文章

CAS

中科院

PubMed

PubMed

Google Scholar

谷歌学者

Yildiz, I. et al. N‐hydroxypipecolic acid induces systemic acquired resistance and transcriptional reprogramming via TGA transcription factors. Plant Cell Environ. 46, 1900–1920 (2023).Article

Yildiz，I。等人。N-羟基胡椒酸通过TGA转录因子诱导系统获得性抗性和转录重编程。植物细胞环境。461900-1920（2023）。文章

CAS

中科院

PubMed

PubMed

Google Scholar

谷歌学者

Kim, H. J. et al. Time-evolving genetic networks reveal a NAC troika that negatively regulates leaf senescence in Arabidopsis. Proc. Natl Acad. Sci. USA 115, E4930–E4939 (2018).ADS

Kim，H.J.等人，时间进化的遗传网络揭示了NAC三驾马车，它负调节拟南芥叶片衰老。程序。国家科学院。科学。美国115，E4930–E4939（2018）。广告

MathSciNet

MathSciNet

PubMed

PubMed

PubMed Central

公共医学中心

Google Scholar

谷歌学者

Huang, W., Wu, Z., Tian, H., Li, X. & Zhang, Y. Arabidopsis CALMODULIN-BINDING PROTEIN 60b plays dual roles in plant immunity. Plant Commun. 2, 100213 (2021).Article

Huang，W.，Wu，Z.，Tian，H.，Li，X。＆Zhang，Y。拟南芥钙调蛋白结合蛋白60b在植物免疫中起双重作用。植物群落。2100213（2021）。文章

CAS

中科院

PubMed

PubMed

PubMed Central

公共医学中心

Google Scholar

谷歌学者

Li, L. et al. Arabidopsis CBP60b is a central transcriptional activator of immunity. Plant Physiol. 186, 1645–1659 (2021).Article

Li，L。等人。拟南芥CBP60b是免疫的中枢转录激活因子。植物生理学。1861645-1659（2021）。文章

CAS

中科院

PubMed

PubMed

PubMed Central

公共医学中心

Google Scholar

谷歌学者

Hickman R. et al. Transcriptional dynamics of the salicylic acid response and its interplay with the jasmonic acid pathway. BioRxiv, 742742 (2019).Rekhter, D. et al. Isochorismate-derived biosynthesis of the plant stress hormone salicylic acid. Science 365, 498–502 (2019).Article

Hickman R.等人。水杨酸反应的转录动力学及其与茉莉酸途径的相互作用。BioRxiv，742742（2019）。Rekhter，D。等人。植物应激激素水杨酸的等位基因衍生生物合成。科学365498-502（2019）。文章

ADS

广告

CAS

中科院

PubMed

PubMed

Google Scholar

谷歌学者

Ernst, H. A., Nina Olsen, A., Skriver, K., Larsen, S. & Lo Leggio, L. Structure of the conserved domain of ANAC, a member of the NAC family of transcription factors. EMBO Rep. 5, 297–303 (2004).Article

Ernst，H.A.，Nina Olsen，A.，Skriver，K.，Larsen，S。＆Lo Leggio，L。ANAC保守结构域的结构，ANAC是NAC转录因子家族的成员。EMBO Rep.5297–303（2004）。文章

CAS

中科院

PubMed

PubMed

PubMed Central

公共医学中心

Google Scholar

谷歌学者

Olsen, A. N., Ernst, H. A., Leggio, L. L. & Skriver, K. DNA-binding specificity and molecular functions of NAC transcription factors. Plant Sci. 169, 785–797 (2005).Article

Olsen，A.N.，Ernst，H.A.，Leggio，L.L。＆Skriver，K。NAC转录因子的DNA结合特异性和分子功能。植物科学。169785-797（2005）。文章

CAS

中科院

Google Scholar

谷歌学者

Huang, W., Wang, Y., Li, X. & Zhang, Y. Biosynthesis and regulation of salicylic acid and N-hydroxypipecolic acid in plant immunity. Mol. Plant 13, 31–41 (2020).Article

Huang，W.，Wang，Y.，Li，X。＆Zhang，Y。水杨酸和N-羟基胡椒酸在植物免疫中的生物合成和调节。摩尔工厂13，31–41（2020）。文章

CAS

中科院

PubMed

PubMed

Google Scholar

谷歌学者

Cui, H. et al. A core function of EDS1 with PAD4 is to protect the salicylic acid defense sector in Arabidopsis immunity. N. Phytol. 213, 1802–1817 (2017).Article

Cui，H。等人。EDS1与PAD4的核心功能是保护拟南芥免疫中的水杨酸防御部门。N、 植物醇。2131802-1817（2017）。文章

CAS

中科院

Google Scholar

谷歌学者

Liu, Y. et al. Diverse roles of the salicylic acid receptors NPR1 and NPR3/NPR4 in plant immunity. Plant Cell 32, 4002–4016 (2020).Article

Liu，Y。等人。水杨酸受体NPR1和NPR3/NPR4在植物免疫中的不同作用。植物细胞324002-4016（2020）。文章

CAS

中科院

PubMed

PubMed

PubMed Central

公共医学中心

Google Scholar

谷歌学者

Bethke, G. et al. Activation of the Arabidopsis thaliana mitogen-activated protein kinase MPK11 by the flagellin-derived elicitor peptide, flg22. Mol. Plant-Microbe Interact. 25, 471–480 (2012).Article

Bethke，G。等人。鞭毛蛋白衍生的激发子肽flg22激活拟南芥丝裂原活化蛋白激酶MPK11。分子植物微生物相互作用。25471-480（2012）。文章

CAS

中科院

PubMed

PubMed

Google Scholar

谷歌学者

Feys, B. J., Moisan, L. J., Newman, M. & Parker, J. E. Direct interaction between the Arabidopsis disease resistance signaling proteins, EDS1 and PAD4. EMBO Rep. 20, 5400–5411 (2001).Article

Feys，B.J.，Moisan，L.J.，Newman，M。＆Parker，J.E。拟南芥抗病信号蛋白EDS1和PAD4之间的直接相互作用。EMBO Rep.205400–5411（2001）。文章

CAS

中科院

Google Scholar

谷歌学者

Lu, H., Rate, D. N., Song, J. T. & Greenberg, J. T. ACD6, a novel ankyrin protein, is a regulator and an effector of salicylic acid signaling in the Arabidopsis defense response. Plant Cell 15, 2408–2420 (2003).Article

Lu，H.，Rate，D.N.，Song，J.T。＆Greenberg，J.T。ACD6是一种新型锚蛋白，是拟南芥防御反应中水杨酸信号传导的调节剂和效应物。植物细胞152408-2420（2003）。文章

CAS

中科院

PubMed

PubMed

PubMed Central

公共医学中心

Google Scholar

谷歌学者

Mackey, D., Belkhadir, Y., Alonso, J. M., Ecker, J. R. & Dangl, J. L. Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112, 379–389 (2003).Article

Mackey，D.，Belkhadir，Y.，Alonso，J.M.，Ecker，J.R。＆Dangl，J.L。拟南芥RIN4是III型毒力效应子AvrRpt2的靶标并调节RPS2介导的抗性。细胞112379-389（2003）。文章

CAS

中科院

PubMed

PubMed

Google Scholar

谷歌学者

Zeilmaker, T. et al. DOWNY MILDEW RESISTANT 6 and DMR 6‐LIKE OXYGENASE 1 are partially redundant but distinct suppressors of immunity in Arabidopsis. Plant J. 81, 210–222 (2015).Article

Zeilmaker，T。等人。抗霜霉病6和DMR 6样加氧酶1在拟南芥中是部分冗余但独特的免疫抑制剂。植物J.81210–222（2015）。文章

CAS

中科院

PubMed

PubMed

Google Scholar

谷歌学者

Cai, J. & Aharoni, A. Amino acids and their derivatives mediating defense priming and growth tradeoff. Curr. Opin. Plant Biol. 69, 102288 (2022).Article

Cai，J。＆Aharoni，A。氨基酸及其衍生物介导防御启动和生长权衡。货币。奥平。植物生物学。69102288（2022）。文章

CAS

中科院

PubMed

PubMed

Google Scholar

谷歌学者

Zheng, X. et al. Coronatine promotes Pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation. Cell Host Microbe 11, 587–596 (2012).Article

Zheng，X。等人。冠菌素通过激活抑制水杨酸积累的信号级联来促进植物中丁香假单胞菌的毒力。细胞宿主微生物11587-596（2012）。文章

CAS

中科院

PubMed

PubMed

PubMed Central

公共医学中心

Google Scholar

谷歌学者

Poraty-Gavra, L. et al. The Arabidopsis Rho of plants GTPase AtROP6 functions in developmental and pathogen response pathways. Plant Physiol. 161, 1172–1188 (2013).Article

。植物生理学。1611172-1188（2013）。文章

CAS

中科院

PubMed

PubMed

PubMed Central

公共医学中心

Google Scholar

谷歌学者

Fan, J., Crooks, C. & Lamb, C. High‐throughput quantitative luminescence assay of the growth in planta of Pseudomonas syringae chromosomally tagged with Photorhabdus luminescens luxCDABE. Plant J. 53, 393–399 (2008).Article

Fan，J.，Crooks，C。＆Lamb，C。高通量定量发光测定丁香假单胞菌（Pseudomonas syringae）在植物中的生长，用发光杆菌luxCDABE进行染色体标记。植物J.53393–399（2008）。文章

CAS

中科院

PubMed

PubMed

Google Scholar

谷歌学者

Rufián, J. S., Rueda-Blanco, J., Beuzón, C. R. & Ruiz-Albert, J. Protocol: an improved method to quantify activation of systemic acquired resistance (SAR). Plant Methods 15, 1–8 (2019).Article

Rufián，J.S.，Rueda Blanco，J.，Beuzón，C.R。＆Ruiz-Albert，J。协议：量化系统获得性抗性（SAR）激活的改进方法。。文章

Google Scholar

谷歌学者

Lei, Y. et al. CRISPR-P: a web tool for synthetic single-guide RNA design of CRISPR-system in plants. Mol. Plant 7, 1494–1496 (2014).Article

Lei，Y。等人。CRISPR-P：用于植物中CRISPR系统合成单指导RNA设计的网络工具。摩尔植物71494-1496（2014）。文章

CAS

中科院

PubMed

PubMed

Google Scholar

谷歌学者

Ma, X. et al. A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Mol. Plant 8, 1274–1284 (2015).Article

Ma，X。等人。一种强大的CRISPR/Cas9系统，用于单子叶植物和双子叶植物中方便，高效的多重基因组编辑。摩尔植物81274-1284（2015）。文章

CAS

中科院

PubMed

PubMed

Google Scholar

谷歌学者

Grützner, R. et al. High-efficiency genome editing in plants mediated by a Cas9 gene containing multiple introns. Plant Commun. 2, 100135 (2021).Article

Grützner，R。等人。由含有多个内含子的Cas9基因介导的植物中的高效基因组编辑。植物群落。2100135（2021）。文章

PubMed

PubMed

Google Scholar

谷歌学者

Zhang, X., Henriques, R., Lin, S., Niu, Q. & Chua, N. Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nat. Protoc. 1, 641–646 (2006).Article

Zhang，X.，Henriques，R.，Lin，S.，Niu，Q。＆Chua，N。使用花浸法农杆菌介导的拟南芥转化。自然协议。1641-646（2006）。文章

CAS

中科院

PubMed

PubMed

Google Scholar

谷歌学者

Szymanski, J. et al. Label‐free deep shotgun proteomics reveals protein dynamics during tomato fruit tissues development. Plant J. 90, 396–417 (2017).Article

Szymanski，J。等人。无标记深鸟枪蛋白质组学揭示了番茄果实组织发育过程中的蛋白质动态。植物J.90396-417（2017）。文章

CAS

中科院

PubMed

PubMed

Google Scholar

谷歌学者

Wiśniewski, J. R., Zougman, A., Nagaraj, N. & Mann, M. Universal sample preparation method for proteome analysis. Nat. Methods 6, 359–362 (2009).Article

Wiśniewski，J.R.，Zougman，A.，Nagaraj，N。＆Mann，M。蛋白质组分析的通用样品制备方法。《自然方法》6359-362（2009）。文章

PubMed

PubMed

Google Scholar

谷歌学者

Cai, J., Chen, T., Wang, Y., Qin, G. & Tian, S. SlREM1 triggers cell death by activating an oxidative burst and other regulators. Plant Physiol. 183, 717–732 (2020).Article

。植物生理学。183717-732（2020）。文章

CAS

中科院

PubMed

PubMed

PubMed Central

公共医学中心

Google Scholar

谷歌学者

Hellens, R. P. et al. Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant Methods 1, 1–14 (2005).Article

Hellens，R.P.等人。用于功能基因组学的瞬时表达载体，植物中启动子活性的定量和RNA沉默。植物方法1,1-14（2005）。文章

Google Scholar

谷歌学者

Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25, 402–408 (2001).Article

Livak，K.J。＆Schmittgen，T.D。使用实时定量PCR和2-ΔΔCT方法分析相对基因表达数据。方法25402-408（2001）。文章

CAS

中科院

PubMed

PubMed

Google Scholar

谷歌学者

Wang, Y. et al. Tomato nuclear proteome reveals the involvement of specific E2 ubiquitin-conjugating enzymes in fruit ripening. Genome Biol. 15, 1–19 (2014).Article

Wang，Y。等人。番茄核蛋白质组揭示了特定E2泛素结合酶在果实成熟中的作用。基因组生物学。15，1-19（2014）。文章

Google Scholar

谷歌学者

Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547 (2018).Article

Kumar，S.，Stecher，G.，Li，M.，Knyaz，C。和Tamura，K。MEGA X：跨计算平台的分子进化遗传学分析。分子生物学。进化。351547（2018）。文章

CAS

中科院

PubMed

PubMed

PubMed Central

公共医学中心

Google Scholar

谷歌学者

Cai, J., Qin, G., Chen, T. & Tian, S. The mode of action of remorin1 in regulating fruit ripening at transcriptional and post‐transcriptional levels. N. Phytol. 219, 1406–1420 (2018).Article

Cai，J.，Qin，G.，Chen，T。＆Tian，S。remorin1在转录和转录后水平调节果实成熟的作用模式。N、 植物醇。2191406-1420（2018）。文章

CAS

中科院

Google Scholar

谷歌学者

Download referencesAcknowledgementsThe work is supported by the ERC-2019-ADG project SIREM (884316). We thank the Adelis Foundation, the Leona M. and Harry B. Helmsley Charitable Trust, the Jeanne and Joseph Nissim Foundation for Life Sciences, the Tom and Sondra Rykoff Family Foundation Research, and the Raymond Burton Plant Genome Research Fund for supporting the Aharoni lab.

下载参考文献致谢这项工作得到了ERC-2019-ADG项目SIREM（884316）的支持。我们感谢阿德利斯基金会，莱昂娜·M.和哈里·赫尔姆斯利慈善信托基金会，珍妮和约瑟夫·尼西姆生命科学基金会，汤姆和桑德拉·雷科夫家族基金会研究以及雷蒙德·伯顿植物基因组研究基金会对阿哈罗尼实验室的支持。

A.A. is the incumbent of the Peter J. Cohn Professorial Chair.Author informationAuthor notesSayantan PandaPresent address: Department of Cell and Metabolic Biology, Leibniz Institute of Plant Biochemistry, Halle (Saale), GermanyAuthors and AffiliationsDepartment of Plant and Environmental Sciences, Weizmann Institute of Science, Rehovot, IsraelJianghua Cai, Sayantan Panda, Yana Kazachkova, Sagit Meir, Ilana Rogachev & Asaph AharoniKey Laboratory of Plant Hormone Regulation and Molecular Breeding of Chongqing, School of Life Sciences, Chongqing University, Chongqing, ChinaJianghua Cai & Zhengguo LiCenter of Plant Functional Genomics and Synthetic Biology, Institute of Advanced Interdisciplinary Studies, Chongqing University, Chongqing, ChinaJianghua Cai & Zhengguo LiThe Robert H.

A、 是Peter J.Cohn教授主席的现任者。作者信息作者注：Sayantan PandaPresent address：德国哈勒（萨勒）莱布尼茨植物生物化学研究所细胞与代谢生物学系作者及附属机构雷霍沃特魏茨曼科学研究所植物与环境科学系蔡江华，Sayantan Panda，Yana Kazachkova，Sagit Meir，Ilana Rogachev＆Asaph AharoniKey重庆大学生命科学学院重庆植物激素调控与分子育种实验室蔡江华和郑国重庆大学高等跨学科研究所植物功能基因组学与合成生物学许可证郑国利特罗伯特·H。

Smith Institute of Plant Sciences and Genetics in Agriculture, The Hebrew University of Jerusalem, Rehovot, IsraelEden AmzallagAuthorsJianghua CaiView author publicationsYou can also search for this author in.

以色列耶路撒冷希伯来大学史密斯农业植物科学与遗传学研究所Rehovot AmzallagAuthorsJianghua CaiView作者出版物您也可以在中搜索这位作者。

PubMed Google ScholarSayantan PandaView author publicationsYou can also search for this author in

PubMed Google ScholarSayantan PandaView作者出版物您也可以在

PubMed Google ScholarYana KazachkovaView author publicationsYou can also search for this author in

PubMed Google ScholarYana KazachkovaView作者出版物您也可以在

PubMed Google ScholarEden AmzallagView author publicationsYou can also search for this author in

PubMed Google ScholarEden AmzallagView作者出版物您也可以在

PubMed Google ScholarZhengguo LiView author publicationsYou can also search for this author in

PubMed谷歌学者郑国LiView作者出版物您也可以在

PubMed Google ScholarSagit MeirView author publicationsYou can also search for this author in

PubMed Google ScholarSagit MeirView作者出版物您也可以在

PubMed Google ScholarIlana RogachevView author publicationsYou can also search for this author in

PubMed Google ScholarIlana RogachevView作者出版物您也可以在

PubMed Google ScholarAsaph AharoniView author publicationsYou can also search for this author in

PubMed Google ScholarAsaph AharoniView作者出版物您也可以在

PubMed Google ScholarContributionsJ.C. designed and performed the research and wrote the article. S.P. contributed to data analysis. Y.K. assisted with label-free proteomic analysis and operated the LC-MS. E.A. assisted with the generation of transgenic plants. S.M. and I.R. assisted with metabolomics data analysis and operated the LC-MS.

PubMed谷歌学术贡献。C、 设计并进行了研究并撰写了文章。S、 P.为数据分析做出了贡献。Y、 K.协助进行无标记蛋白质组学分析，并操作LC-MS。E.A.协助产生转基因植物。S、 M.和I.R.协助代谢组学数据分析并操作LC-MS。

Z.L. assisted with paper correction. A.A. designed the research and wrote the article.Corresponding authorCorrespondence to.

Z、 L.协助纸张更正。A、 A.设计研究并撰写文章。对应作者对应。

Asaph Aharoni.Ethics declarations

亚萨·阿哈罗尼。道德宣言

Competing interests

相互竞争的利益

The authors declare no competing interests.

作者声明没有利益冲突。

Peer review

同行评审

Peer review information

同行评审信息

Nature Communications thanks Yanmei Chen, Jürgen Zeier, and the other, anonymous, reviewers for their contribution to the peer review of this work. A peer review file is available.

Nature Communications感谢Yanmei Chen，Jürgen Zeier和其他匿名审稿人对这项工作的同行评审做出的贡献。可以获得同行评审文件。

Additional informationPublisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.Supplementary informationSupplementary InformationPeer Review FileDescription of additional supplementary filesSupplementary Data 1Supplementary Data 2Supplementary Data 3Supplementary Data 4Supplementary Data 5Supplementary Data 6Supplementary Data 7Reporting summarySource dataSource DataRights and permissions.

Additional informationPublisher的注释Springer Nature在已发布的地图和机构隶属关系中的管辖权主张方面保持中立。补充信息补充信息同行评审文件其他补充文件的描述补充数据1补充数据2补充数据3补充数据4补充数据5补充数据6补充数据7报告摘要源数据源数据权限。

Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material.

开放获取本文是根据知识共享署名非商业性NoDerivatives 4.0国际许可证授权的，该许可证允许以任何媒介或格式进行任何非商业性使用，共享，分发和复制，只要您对原始作者和来源给予适当的信任，提供知识共享许可证的链接，并指出您是否修改了许可材料。

You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder.

根据本许可证，您无权共享源自本文或其部分的改编材料。本文中的图像或其他第三方材料包含在文章的知识共享许可证中，除非该材料的信用额度中另有说明。如果材料未包含在文章的知识共享许可中，并且您的预期用途不受法律法规的许可或超出许可用途，则您需要直接获得版权所有者的许可。

To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/..

要查看此许可证的副本，请访问http://creativecommons.org/licenses/by-nc-nd/4.0/..

Reprints and permissionsAbout this articleCite this articleCai, J., Panda, S., Kazachkova, Y. et al. A NAC triad modulates plant immunity by negatively regulating N-hydroxy pipecolic acid biosynthesis.

。

Nat Commun 15, 7212 (2024). https://doi.org/10.1038/s41467-024-51515-2Download citationReceived: 02 July 2023Accepted: 08 August 2024Published: 22 August 2024DOI: https://doi.org/10.1038/s41467-024-51515-2Share this articleAnyone you share the following link with will be able to read this content:Get shareable linkSorry, a shareable link is not currently available for this article.Copy to clipboard.

《国家公社》157212（2024）。https://doi.org/10.1038/s41467-024-51515-2Download引文接收日期：2023年7月2日接收日期：2024年8月8日发布日期：2024年8月22日OI：https://doi.org/10.1038/s41467-024-51515-2Share本文与您共享以下链接的任何人都可以阅读此内容：获取可共享链接对不起，本文目前没有可共享的链接。复制到剪贴板。

Provided by the Springer Nature SharedIt content-sharing initiative

由Springer Nature SharedIt内容共享计划提供

CommentsBy submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

评论通过提交评论，您同意遵守我们的条款和社区指南。如果您发现有虐待行为或不符合我们的条款或准则，请将其标记为不合适。