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MSD2-mediated ROS metabolism fine-tunes the timing of floral organ abscission in Arabidopsis
New Phytologist ( IF 8.3 ) Pub Date : 2022-06-11 , DOI: 10.1111/nph.18303
Jinsu Lee 1, 2 , Huize Chen 1, 3 , Gisuk Lee 4 , Aurélia Emonet 5 , Sang-Gyu Kim 4 , Donghwan Shim 6 , Yuree Lee 2, 7, 8
Affiliation  

Introduction

Abscission is the natural shedding of plant tissues such as leaves, flowers, seed pods, and fruits and plays an essential role in plant survival as a means of seed dispersal or removal of vulnerable or diseased tissues (Addicott, 1982). The specialized cell layers responsible for abscission are called abscission zones (AZs) and are usually formed together in early stages of organogenesis. When abscission is activated, cell wall-hydrolysing enzymes are secreted to disrupt the cell wall at the AZ in a highly coordinated process that integrates various developmental and environmental cues (Patharkar & Walker, 2019).

The molecular mechanism of abscission has been largely elucidated for the floral organs of Arabidopsis (Arabidopsis thaliana) (Cho et al., 2008; McKim et al., 2008; Liu et al., 2013; Lee et al., 2018). As constituents of reproductive organs, petals play an important role in attracting pollinators but are also easily exposed to predators and are vulnerable to environmental stress, making their timely removal after fertilization critical for plant survival. Various phytohormones, including ethylene, auxin, abscisic acid (ABA), and jasmonic acid (JA), are involved in activating abscission after fertilization has occurred (Patterson & Bleecker, 2004; Kim et al., 2013; Meir et al., 2019). The receptor-like kinases HAESA (HAE) and HAE-LIKE2 (HSL2) and their cognate peptide ligand INFLORESCENCE DEFICIENT IN ABSCISSION (IDA) initiate the signalling pathway controlling the expression of genes encoding cell wall enzymes (Cho et al., 2008; Stenvik et al., 2008; Aalen et al., 2013; Patharkar & Walker, 2015). HAE/HSL2 work with the other receptor-like proteins SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASEs (SERKs), including SERK1–4, to form complexes upon interaction with IDA to initiate floral abscission (Meng et al., 2016). The IDA-HAE pathway is conserved in various crop species such as tomato (Solanum lycopersicum), soybean (Glycine max), and tobacco (Nicotiana tabacum) and is involved in organ abscission (Tucker & Yang, 2012; Ventimilla et al., 2020, 2021). However, the IDA-HAE module is not limited to floral organ abscission, as it also participates in other cell separation processes such as lateral root emergence and root cap detachment (Kumpf et al., 2013; Shi et al., 2018). Additionally, the expression levels of IDA and IDA-LIKE (IDL) increase in response to abiotic and biotic stress conditions (Vie et al., 2015), suggesting that the IDA-HAE module plays a role in linking stress responses to development. However, how various environmental stimuli modulate IDA-HAE activity is not well understood.

Redox homeostasis plays critical roles in plant development and stress responses (Mhamdi & Van Breusegem, 2018; Huang et al., 2019). Reactive oxygen species (ROS) are by-products of various cellular processes, including photosynthesis and mitochondrial respiration, in different intracellular compartments. Plants have not only developed various systems for detoxifying ROS but also evolved mechanisms that can integrate ROS as signalling molecules, thus linking metabolism and responses to highly variable environments (Waszczak et al., 2018). Reactive oxygen species accumulation in the AZ has been reported in various species, including Arabidopsis, with roles in abscission signalling and cell wall remodelling (Sakamoto et al., 2008a,b; Bar-Dror et al., 2011; Yang et al., 2015; Liao et al., 2016; Lee et al., 2018). Various enzymes, such as NADPH oxidases, peroxidases, and polyamine oxidases, might be involved in ROS production in the AZ, but how their roles are interconnected and regulated is not clear.

NADPH oxidases located at the cell membrane generate superoxide that might be used as a signal in various developmental and stress conditions (Mittler et al., 2011; Huang et al., 2019). The Arabidopsis genome harbours 10 genes, RbohA–RbohJ (RESPIRATORY BURST OXIDASE HOMOLOG), encoding NADPH oxidases with functions in various developmental stages, including root and hypocotyl elongation, root hair development, fruit ripening, and cell wall remodelling during seed germination (Dunand et al., 2007; Muller et al., 2009; Yan et al., 2016). RbohD and RbohF are highly expressed in the AZ and provide the ROS substrates needed for peroxidase-dependent lignin formation, which forms a physical apoplastic barrier to precisely control the localization of cell wall enzymes (Lee et al., 2018). However, it remains unknown whether RBOHs are also involved in signalling to regulate the timing of abscission or cell wall loosening. How the generated ROS are metabolized is also unknown.

Extracellular superoxides (O2) produced by NADPH oxidases can be dismutated to hydrogen peroxide (H2O2) either spontaneously or enzymatically via apoplastic superoxide dismutases (SODs) and transported to the cytoplasm via aquaporins (Qi et al., 2017; Mhamdi & Van Breusegem, 2018). Superoxide dismutases can be divided into three classes as a function of the metal ions in their active centres: manganese (Mn), iron (Fe), and copper and zinc (Cu/Zn). Arabidopsis has eight known SODs: three Cu/Zn SODs (CSD1–3), three Fe SODs (FSD1–3), and two Mn SODs (MSD1–2) (Kliebenstein et al., 1998; Chen et al., 2022). Their subcellular localizations vary, with CSD2 and FSD1–3 in chloroplasts (Kliebenstein et al., 1998; Myouga et al., 2008; Dvorak et al., 2021), MSD1 in mitochondria (Morgan et al., 2008), CSD3 in peroxisomes (Kliebenstein et al., 1998; Huang et al., 2012), CSD1 and FSD1 in the cytoplasm (Kliebenstein et al., 1998; Dvorak et al., 2021), and FSD1 in the nucleus (Dvorak et al., 2021). MSD2 is an apoplastic SOD with Mn SOD activity that is secreted into vacuoles or the apoplast (Chen et al., 2022). SODs, which convert O2 into H2O2, not only detoxify O2 accumulated from various stress conditions and metabolic processes, but also affect the redox balance. Given the recent reports that different types of ROS perform distinct functions (Tsukagoshi et al., 2010; Lee et al., 2018), the role of SOD in influencing the balance between O2 and H2O2 may serve as an important signalling rheostat along with ROS-generating enzymes. Although several factors regulating the expression of SODs and the function of the encoded enzymes have recently been identified (Yamasaki et al., 2007; Xing et al., 2013; Dvorak et al., 2020; Hu et al., 2021), our understanding of their regulatory mechanisms and their relationship with other signalling pathways is still fragmentary.

In this study, we demonstrated that MSD2, a recently identified secretory SOD (Chen et al., 2022), is involved in the regulation of abscission signalling. MSD2 was preferentially expressed in the AZ of flowers, and the encoded MSD2 enzyme was secreted into the vacuole and extracellular spaces. In msd2 mutants, superoxide accumulated earlier than in the wild-type and was accompanied by an acceleration of floral organ shedding. Transcriptome analysis revealed that the expression of nitric oxide (NO)- and ABA-related genes is upregulated in msd2 mutants. NO and ABA abundance increased upon activation of abscission, and an exogenous supply of NO and ABA accelerated abscission, while treating plants with an NO scavenger blocked the accelerated abscission observed in msd2 mutants. We also established that the expression of IDA and HAE is affected by NO and ABA. These results suggest that the regulation of ROS metabolism by MSD2 affects the onset of abscission through the NO and ABA signalling pathways upstream of IDA-HAE.



中文翻译:

MSD2介导的ROS代谢微调拟南芥花器官脱落的时间

介绍

脱落是植物组织如叶子、花、种子荚和果实的自然脱落,并且作为种子散布或去除脆弱或患病组织的手段在植物生存中起着重要作用(Addicott,  1982)。负责脱落的特化细胞层称为脱落区 (AZ),通常在器官发生的早期阶段一起形成。当脱落被激活时,细胞壁水解酶会分泌出来,在一个高度协调的过程中破坏 AZ 的细胞壁,该过程整合了各种发育和环境线索(Patharkar & Walker,  2019)。

拟南芥 ( Arabidopsis thaliana )花器官脱落的分子机制已基本阐明(Cho et al .,  2008 ; McKim et al .,  2008 ; Liu et al .,  2013 ; Lee et al .,  2018 ))。作为生殖器官的组成部分,花瓣在吸引传粉者方面发挥着重要作用,但也很容易暴露于捕食者并容易受到环境压力,因此受精后及时去除对植物生存至关重要。多种植物激素,包括乙烯、生长素、脱落酸 (ABA) 和茉莉酸 (JA),在受精后参与激活脱落(Patterson & Bleecker,  2004 ; Kim et al .,  2013 ; Meir et al .,  2019)。受体样激酶 HAESA (HAE) 和 HAE-LIKE2 (HSL2) 及其同源肽配体 INFLORESCENCE DEFICIENT IN ABSCISSION (IDA) 启动了控制编码细胞壁酶基因表达的信号通路 (Cho et al .,  2008 ; Stenvik等人,  2008 年;Aalen等人,  2013 年;Patharkar & Walker,  2015 年)。HAE/HSL2 与其他受体样蛋白体细胞胚胎发生受体样激酶 (SERK),包括 SERK1-4,在与 IDA 相互作用时形成复合物以启动花脱落 (Meng et al .,  2016)。IDA-HAE 途径在番茄 ( Solanum lycopersicum )、大豆 ( Glycine max ) 和烟草 ( Nicotiana tabacum )等多种作物物种中是保守的,并参与器官脱落 (Tucker & Yang,  2012 ; Ventimilla et al .,  2020 , 2021 年)。然而,IDA-HAE 模块不仅限于花器官脱落,它还参与其他细胞分离过程,例如侧根出现和根冠脱离 (Kumpf et al .,  2013 ; Shi et al .,  2018 )。此外,IDA的表达水平和IDA-LIKE ( IDL ) 在响应非生物和生物胁迫条件时增加(Vie等人,  2015 年),表明 IDA-HAE 模块在将胁迫响应与发育联系起来方面发挥作用。然而,各种环境刺激如何调节 IDA-HAE 活性尚不清楚。

氧化还原稳态在植物发育和应激反应中起着关键作用(Mhamdi & Van Breusegem,  2018 年;Huang等人,  2019 年)。活性氧 (ROS) 是不同细胞内区室中各种细胞过程的副产品,包括光合作用和线粒体呼吸。植物不仅开发了各种用于解毒 ROS 的系统,而且还进化出了可以整合 ROS 作为信号分子的机制,从而将新陈代谢和对高度可变环境的反应联系起来(Waszczak et al .,  2018)。AZ 中的活性氧积累在包括拟南芥在内的各种物种中都有报道,在脱落信号传导和细胞壁重塑中发挥作用(Sakamoto等人,  2008ab;Bar-Dror等人,  2011;Yang等人,  2015;廖等人,  2016;李等人,  2018)。多种酶,如 NADPH 氧化酶、过氧化物酶和多胺氧化酶,可能参与 AZ 中 ROS 的产生,但它们的作用如何相互关联和调节尚不清楚。

位于细胞膜上的 NADPH 氧化酶产生超氧化物,可用作各种发育和应激条件下的信号(Mittler等人,  2011;Huang等人,  2019)。拟南芥基因组包含 10 个基因,RbohA-RbohJ ( RESSPIRATORY BURST OXIDASE HOMOLOG ),编码 NADPH 氧化酶,在不同发育阶段发挥作用,包括根和下胚轴伸长、根毛发育、果实成熟和种子萌发过程中的细胞壁重塑 (Dunand et等人,  2007 年;穆勒等人,  2009 年;严等人,  2016 年)。RbohDRbohF在 AZ 中高度表达,并提供过氧化物酶依赖性木质素形成所需的 ROS 底物,从而形成物理质外屏障,以精确控制细胞壁酶的定位 (Lee et al .,  2018 )。然而,RBOHs 是否也参与调节脱落或细胞壁松动时间的信号仍然未知。生成的 ROS 是如何代谢的也是未知的。

细胞外超氧化物 (2-) 由 NADPH 氧化酶产生的过氧化氢 (H 2 O 2 ) 可以通过质外体超氧化物歧化酶 (SOD) 自发地或酶促地歧化为过氧化氢 (H 2 O 2 ),并通过水通道蛋白转运到细胞质中 (Qi等人,  2017 年;Mhamdi & Van Breusegem,  2018 年) . 超氧化物歧化酶可根据其活性中心的金属离子分为三类:锰 (Mn)、铁 (Fe) 和铜和锌 (Cu/Zn)。拟南芥有八种已知的 SOD:三种铜/锌 SOD (CSD1-3)、三种铁 SOD (FSD1-3) 和两种锰 SOD (MSD1-2) (Kliebenstein et al .,  1998 ; Chen et al .,  2022)。它们的亚细胞定位各不相同,CSD2 和 FSD1-3 在叶绿体中(Kliebenstein等人,  1998;Myouga等人,  2008;Dvorak等人,  2021),MSD1 在线粒体中(Morgan等人,  2008),CSD3在线粒体中过氧化物酶体 (Kliebenstein et al .,  1998 ; Huang et al .,  2012 )、细胞质中的 CSD1 和 FSD1 (Kliebenstein et al .,  1998 ; Dvorak et al .,  2021 ) 和细胞核中的 FSD1 (Dvorak et al .,  2021)。MSD2 是一种具有 Mn SOD 活性的质外体 SOD,可分泌到液泡或质外体中(Chen等人,  2022)。SOD,可转化2-变成H 2 O 2,​​不仅解毒2-从各种应激条件和代谢过程中积累,也会影响氧化还原平衡。鉴于最近有报道称不同类型的 ROS 执行不同的功能(Tsukagoshi等人,  2010 年;Lee等人,  2018 年),SOD 在影响2-和 H 2 O 2可与产生 ROS 的酶一起作为重要的信号变阻器。尽管最近已经确定了一些调节SOD表达和编码酶功能的因素(Yamasaki等人,  2007;Xing等人,  2013;Dvorak等人,  2020;Hu等人,  2021),我们对它们的调控机制以及它们与其他信号通路的关系的理解仍然是零散的。

在这项研究中,我们证明了 MSD2,一种最近发现的分泌型 SOD (Chen et al .,  2022 ),参与了脱落信号的调节。MSD2优先在花的AZ表达,编码的MSD2酶分泌到液泡和细胞外空间中。在msd2突变体中,超氧化物比野生型更早积累,并伴随着花器官脱落的加速。转录组分析显示,一氧化氮 (NO) 和 ABA 相关基因的表达在msd2中上调突变体。NO 和 ABA 丰度在脱落激活后增加,并且 NO 和 ABA 的外源供应加速脱落,而用 NO 清除剂处理植物阻止了msd2突变体中观察到的加速脱落。我们还确定IDAHAE的表达受 NO 和 ABA 的影响。这些结果表明MSD2对ROS代谢的调节通过IDA-HAE上游的NO和ABA信号通路影响脱落的发生。

更新日期:2022-06-11
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