Introduction

Bread wheat (Triticum aestivum L.) is one of the most important staple crops worldwide and provides 20% of the daily protein and food calories globally (Shewry & Hey, 2015; FAOSTAT, 2020). Powdery mildew caused by Blumeria graminis f. sp. tritici (Bgt) is a major devastating disease of wheat that leads to serious yield losses every year (Singh et al., 2016). In comparison to chemical control, the use of cultivars with disease resistance genes is a more comprehensive, economical and environmentally friendly approach (Randhawa et al., 2019). Understanding the molecular mechanisms and identifying genes involved in basal defense will be useful to exploit this new approach for disease resistance breeding.

Plants resist attacks by pathogens via innate immune responses, which are initiated by cell-surface immune receptors and intracellular immune receptors leading to pattern-triggered immunity (PTI) and effector-triggered immunity (ETI), respectively (Jones & Dangl, 2006; Zhou & Zhang, 2020). Both PTI and ETI are associated with the induction of defense responses, including accumulation of defense hormone SA and production of reactive oxygen species (ROS). Reactive oxygen species have been proposed to act as signaling molecules that further activate immune responses (Levine et al., 1994; Wang et al., 2011; Qi et al., 2017; Alhoraibi et al., 2019; Ding & Ding, 2020; Ngou et al., 2021; Yuan et al., 2021). Induction of PTI and ETI also involves large-scale transcriptional reprogramming and this process is synergistically linked with signal transducers (Wang et al., 2006; Dempsey & Klessig, 2012; Li et al., 2019). A battery of key players, such as Phytoalexin Deficient 4 (PAD4) and Enhanced Disease Susceptibility 1 (EDS1), have been identified as the major signal transducer during these processes (Feys et al., 2005; Zhang et al., 2010; Zhu et al., 2011). Both EDS1 and PAD4 encode lipase-like protein and function in R gene-mediated and basal disease resistance (Jirage et al., 1999). PAD4 physically interacts with EDS1 to transcriptionally mobilize antimicrobial defense pathways and the complex also is required for the accumulation of SA and hydrogen peroxide (H₂O₂) during systemic acquired acclimation and resistance (Mühlenbock et al., 2008; Rietz et al., 2011; Cui et al., 2017). Recent study further revealed that EDS1-PAD4 dimers act as convergence point for defence signalling cascades and play a broader role promoting basal immune responses that can be initiated by both PTI and ETI (Pruitt et al., 2021; Tian et al., 2021). Previous study revealed that EDS1 acts as a positive regulator against powdery mildew in wheat (G. Chen et al., 2018). However, little is known about the involvement of PAD4 homologs in wheat upon pathogen attacks, despite its key role in signal molecule-triggered immunity and integrated multiple signaling hub in stress response (Zhou et al., 1998; Wituszynska et al., 2013; Chen et al., 2015; Bernacki et al., 2019). Moreover, the underlying transcriptional mechanisms of PAD4 and EDS1 genes remain largely unknown.

As a major epigenetic regulatory mechanism, histone acetylation plays an important role in gene regulation involved in plant development and response to environmental changes (Servet et al., 2010; Shen et al., 2015; Kim et al., 2018; Y. Chen et al., 2018; Zhao et al., 2019). Histone acetylation homeostasis is regulated by two types of inverse enzymatic reactions mediated by histone acetyltransferase (HAT) and histone deacetylase (HDAC), respectively. An increasing body of work has suggested histone acetylation also as a new layer of regulation for transcriptional reprogramming during the activation of the pathogen defense systems (Zhou et al., 2005; Kim et al., 2008, 2020; Choi et al., 2012; Song & Walley, 2016; Wang et al., 2017; Liu et al., 2019). Intriguingly, the systemic acquired resistance can even be passed on to progeny through histone acetylation (Jaskiewicz et al., 2011; Luna et al., 2012; Fu & Dong, 2013). Although indicative of an involvement of histone acetylation in regulating pathogen defense responses, direct proof disclosing the function of HATs in establishing defense and whether acetylation modifiers induce specific regulatory pathways with other interaction factors to confer pathogen resistance has remained elusive.

In this study, we show that the histone acetyltransferase TaHAG1 plays a pivotal role in resistance to powdery mildew via promoting SA and ROS accumulation in wheat. We demonstrate that TaHAG1 interacts directly with a plant-specific zinc-dependent protein TaPLATZ5 to potentiate the expression of TaPAD4 by increasing the levels of histone acetylation. Our study reveals that a key transcription regulatory node in wheat confers powdery mildew resistance through activating pathogen-responsive genes, which could be effective for genetic improvement of disease resistance in wheat and other crops.

中文翻译：

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组蛋白乙酰转移酶 TaHAG1 与 TaPLATZ5 相互作用以激活 TaPAD4 表达并积极促进小麦的白粉病抗性

介绍

面包小麦 ( Triticum aestivum L.) 是全球最重要的主食作物之一，提供全球 20% 的日常蛋白质和食物热量（Shewry & Hey，2015 年；FAOSTAT，2020 年）。由Blumeria graminis f.引起的白粉病。sp。小麦( Bgt ) 是小麦的一种主要破坏性病害，每年都会导致严重的产量损失（Singh等人，2016 年）。与化学防治相比，使用具有抗病基因的品种是一种更全面、更经济、更环保的方法（Randhawa et al ., 2019). 了解分子机制和识别参与基础防御的基因将有助于利用这种新的抗病育种方法。

植物通过先天免疫反应抵抗病原体的攻击，先天免疫反应由细胞表面免疫受体和细胞内免疫受体启动，分别导致模式触发免疫 (PTI) 和效应触发免疫 (ETI) (Jones & Dangl, 2006 ; Zhou & 张, 2020 ). PTI 和 ETI 都与防御反应的诱导有关，包括防御激素 SA 的积累和活性氧 (ROS) 的产生。活性氧已被提议作为进一步激活免疫反应的信号分子（Levine等人，1994 年；Wang等人，2011 年；Qi等人，2017 年；Alhoraibi等人，2019 年；叮叮叮，2020；Ngou等人，2021 年；元等，2021）。PTI 和 ETI 的诱导还涉及大规模转录重编程，并且该过程与信号转导器协同相关（Wang等人，2006 年；Dempsey 和 Klessig，2012 年；Li等人，2019 年）。一系列关键参与者，例如植物抗毒素缺陷型 4 (PAD4) 和疾病易感性增强型 1 (EDS1)，已被确定为这些过程中的主要信号转导器（Feys等人，2005 年；Zhang等，2010 年；朱等，2011）。EDS1和PAD4均编码脂肪酶样蛋白，并在R基因介导的和基础抗病性中发挥作用（Jirage等，1999）。PAD4 与 EDS1 物理相互作用以转录调动抗菌防御途径，并且在系统获得性适应和抗性期间，该复合物也是 SA 和过氧化氢 (H ₂ O ₂ ) 积累所必需的（Mühlenbock等人，2008 年；Rietz等人，2011 ;崔等人., 2017 年）。最近的研究进一步表明，EDS1-PAD4 二聚体充当防御信号级联的汇聚点，并在促进可由 PTI 和 ETI 启动的基础免疫反应方面发挥更广泛的作用（Pruitt等人，2021 年；Tian等人，2021 年） . 先前的研究表明，EDS1可作为小麦白粉病的正调节因子（G. Chen等人，2018 年）。然而，尽管 PAD4 同系物在信号分子触发的免疫中起着关键作用，并且在应激反应中整合了多个信号中枢，但人们对PAD4同源物在病原体攻击中的参与知之甚少（Zhou等人，1998 年；Wituszynska等人，2013 年；陈等，2015；Bernacki等人，2019 年）。此外，PAD4和EDS1基因的潜在转录机制在很大程度上仍然未知。

作为一种主要的表观遗传调控机制，组蛋白乙酰化在植物发育和环境变化响应的基因调控中起着重要作用（Servet et al ., 2010 ; Shen et al ., 2015 ; Kim et al ., 2018 ; Y. Chen等，2018；赵等，2019). 组蛋白乙酰化稳态受组蛋白乙酰转移酶 (HAT) 和组蛋白脱乙酰酶 (HDAC) 分别介导的两种逆酶促反应的调节。越来越多的研究表明，组蛋白乙酰化也是病原体防御系统激活期间转录重编程的新调控层（Zhou等人，2005 年；Kim等人，2008 年，2020 年；Choi等人，2012 年） ; Song & Walley, 2016 ; Wang et al ., 2017 ; Liu et al ., 2019). 有趣的是，系统获得性抗性甚至可以通过组蛋白乙酰化传递给后代（Jaskiewicz等人，2011 年；Luna等人，2012 年；Fu & Dong，2013 年）。尽管表明组蛋白乙酰化参与调节病原体防御反应，但揭示 HAT 在建立防御中的功能以及乙酰化修饰剂是否诱导特定调节途径与其他相互作用因子赋予病原体抗性的直接证据仍然难以捉摸。

在这项研究中，我们表明组蛋白乙酰转移酶 TaHAG1 通过促进小麦中 SA 和 ROS 的积累在抗白粉病中发挥关键作用。我们证明 TaHAG1 直接与植物特异性锌依赖性蛋白 TaPLATZ5相互作用，通过增加组蛋白乙酰化水平来增强TaPAD4的表达。我们的研究表明，小麦的一个关键转录调控节点通过激活病原体反应基因赋予白粉病抗性，这可能对小麦和其他作物的抗病性遗传改良有效。