MicroRNAs (miRNAs) are widely involved in various biological processes of plants and contribute to plant resistance against various pathogens. In this study, upon sugarcane mosaic virus (SCMV) infection, the accumulation of maize (Zea mays) miR398b (ZmmiR398b) was significantly reduced in resistant inbred line Chang7‐2, while it was increased in susceptible inbred line Mo17. Degradome sequencing analysis coupled with transient co‐expression assays revealed that ZmmiR398b can target Cu/Zn‐superoxidase dismutase2 (ZmCSD2), ZmCSD4, and ZmCSD9 in vivo, of which the expression levels were all upregulated by SCMV infection in Chang7‐2 and Mo17. Moreover, overexpressing ZmmiR398b (OE398b) exhibited increased susceptibility to SCMV infection, probably by increasing reactive oxygen species (ROS) accumulation, which were consistent with ZmCSD2/4/9‐silenced maize plants. By contrast, silencing ZmmiR398b (STTM398b) through short tandem target mimic (STTM) technology enhanced maize resistance to SCMV infection and decreased ROS levels. Interestingly, copper (Cu)‐gradient hydroponic experiments demonstrated that Cu deficiency promoted SCMV infection while Cu sufficiency inhibited SCMV infection by regulating accumulations of ZmmiR398b and ZmCSD2/4/9 in maize. These results revealed that manipulating the ZmmiR398b‐ZmCSD2/4/9‐ROS module provides a prospective strategy for developing SCMV‐tolerant maize varieties.
{"title":"ZmmiR398b negatively regulates maize resistance to sugarcane mosaic virus infection by targeting ZmCSD2/4/9","authors":"Xinran Gao, Zhichao Du, Kaiqiang Hao, Sijia Zhang, Jian Li, Jinxiu Guo, Zhiping Wang, Shixue Zhao, Lijun Sang, Mengnan An, Zihao Xia, Yuanhua Wu","doi":"10.1111/mpp.13462","DOIUrl":"https://doi.org/10.1111/mpp.13462","url":null,"abstract":"MicroRNAs (miRNAs) are widely involved in various biological processes of plants and contribute to plant resistance against various pathogens. In this study, upon sugarcane mosaic virus (SCMV) infection, the accumulation of maize (<jats:italic>Zea mays</jats:italic>) miR398b (ZmmiR398b) was significantly reduced in resistant inbred line Chang7‐2, while it was increased in susceptible inbred line Mo17. Degradome sequencing analysis coupled with transient co‐expression assays revealed that ZmmiR398b can target <jats:italic>Cu/Zn‐superoxidase dismutase2</jats:italic> (<jats:italic>ZmCSD2</jats:italic>), <jats:italic>ZmCSD4</jats:italic>, and <jats:italic>ZmCSD9</jats:italic> in vivo, of which the expression levels were all upregulated by SCMV infection in Chang7‐2 and Mo17. Moreover, overexpressing <jats:italic>ZmmiR398b</jats:italic> (OE398b) exhibited increased susceptibility to SCMV infection, probably by increasing reactive oxygen species (ROS) accumulation, which were consistent with <jats:italic>ZmCSD2/4/9</jats:italic>‐silenced maize plants. By contrast, silencing <jats:italic>ZmmiR398b</jats:italic> (STTM398b) through short tandem target mimic (STTM) technology enhanced maize resistance to SCMV infection and decreased ROS levels. Interestingly, copper (Cu)‐gradient hydroponic experiments demonstrated that Cu deficiency promoted SCMV infection while Cu sufficiency inhibited SCMV infection by regulating accumulations of ZmmiR398b and <jats:italic>ZmCSD2/4/9</jats:italic> in maize. These results revealed that manipulating the ZmmiR398b<jats:italic>‐ZmCSD2/4/9‐</jats:italic>ROS module provides a prospective strategy for developing SCMV‐tolerant maize varieties.","PeriodicalId":18763,"journal":{"name":"Molecular plant pathology","volume":"69 1","pages":""},"PeriodicalIF":4.9,"publicationDate":"2024-05-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140842303","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Louisa Wirtz, Florencia Casanova, Ulrich Schaffrath, Alex Wegner
Reverse genetic approaches are common tools in genomics for elucidating gene functions, involving techniques such as gene deletion followed by screening for aberrant phenotypes. If the generation of gene deletion mutants fails, the question arises whether the failure stems from technical issues or because the gene of interest (GOI) is essential, meaning that the deletion causes lethality. In this report, we introduce a novel method for assessing gene essentiality using the phytopathogenic ascomycete Magnaporthe oryzae. The method is based on the observation that telomere vectors are lost in transformants during cultivation without selection pressure. We tested the hypothesis that essential genes can be identified in deletion mutants co‐transformed with a telomere vector. The M. oryzae gene MoPKC, described in literature as essential, was chosen as GOI. Using CRISPR/Cas9 technology transformants with deleted GOI were generated and backed up by a telomere vector carrying a copy of the GOI and conferring fenhexamid resistance. Transformants in which the GOI deletion in the genome was not successful lost the telomere vector on media without fenhexamid. In contrast, transformants with confirmed GOI deletion retained the telomere vector even in absence of fenhexamid selection. In the latter case, the maintenance of the telomere indicates that the GOI is essential for the surveillance of the fungi, as it would have been lost otherwise. The method presented here allows to test for essentiality of genes when no mutants can be obtained from gene deletion approaches, thereby expanding the toolbox for studying gene function in ascomycetes.
反向遗传方法是基因组学中阐明基因功能的常用工具，涉及基因缺失后筛选异常表型等技术。如果基因缺失突变体的生成失败，那么问题就来了，失败是源于技术问题，还是因为相关基因（GOI）是必需的，即基因缺失会导致致死。在本报告中，我们介绍了一种利用植物致病性子囊菌 Magnaporthe oryzae 评估基因本质的新方法。该方法基于对端粒载体在无选择压力的培养过程中在转化体中丢失的观察。我们对这一假设进行了测试，即可以在与端粒载体共同转化的缺失突变体中鉴定出重要基因。我们选择了文献中描述为必需基因的 M. oryzae 基因 MoPKC 作为 GOI。利用CRISPR/Cas9技术生成了删除了GOI的转化子，并由携带GOI拷贝的端粒载体提供支持，使其具有苯海拉明抗性。基因组中GOI缺失不成功的转化子在不含茚虫威的培养基上失去了端粒载体。与此相反，基因组中GOI缺失被确认的转化子即使在没有茚虫威选择的情况下也能保留端粒载体。在后一种情况下，端粒的保留表明 GOI 对真菌的监控是必不可少的，否则它就会丢失。本文介绍的方法可以在基因缺失方法无法获得突变体的情况下测试基因的必要性，从而扩大了研究子囊菌基因功能的工具箱。
{"title":"Development of a telomere vector‐based approach to overcome limitations caused by lethal phenotypes in the study of essential genes in Magnaporthe oryzae","authors":"Louisa Wirtz, Florencia Casanova, Ulrich Schaffrath, Alex Wegner","doi":"10.1111/mpp.13460","DOIUrl":"https://doi.org/10.1111/mpp.13460","url":null,"abstract":"Reverse genetic approaches are common tools in genomics for elucidating gene functions, involving techniques such as gene deletion followed by screening for aberrant phenotypes. If the generation of gene deletion mutants fails, the question arises whether the failure stems from technical issues or because the gene of interest (GOI) is essential, meaning that the deletion causes lethality. In this report, we introduce a novel method for assessing gene essentiality using the phytopathogenic ascomycete <jats:italic>Magnaporthe oryzae</jats:italic>. The method is based on the observation that telomere vectors are lost in transformants during cultivation without selection pressure. We tested the hypothesis that essential genes can be identified in deletion mutants co‐transformed with a telomere vector. The <jats:italic>M. oryzae</jats:italic> gene <jats:italic>MoPKC</jats:italic>, described in literature as essential, was chosen as GOI. Using CRISPR/Cas9 technology transformants with deleted GOI were generated and backed up by a telomere vector carrying a copy of the GOI and conferring fenhexamid resistance. Transformants in which the GOI deletion in the genome was not successful lost the telomere vector on media without fenhexamid. In contrast, transformants with confirmed GOI deletion retained the telomere vector even in absence of fenhexamid selection. In the latter case, the maintenance of the telomere indicates that the GOI is essential for the surveillance of the fungi, as it would have been lost otherwise. The method presented here allows to test for essentiality of genes when no mutants can be obtained from gene deletion approaches, thereby expanding the toolbox for studying gene function in ascomycetes.","PeriodicalId":18763,"journal":{"name":"Molecular plant pathology","volume":"91 1","pages":""},"PeriodicalIF":4.9,"publicationDate":"2024-05-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140842465","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Ming Ma, Liguang Tang, Rui Sun, Xueliang Lyu, Jiatao Xie, Yanping Fu, Bo Li, Tao Chen, Yang Lin, Xiao Yu, Weidong Chen, Daohong Jiang, Jiasen Cheng
Many plant pathogens secrete effector proteins into the host plant to suppress host immunity and facilitate pathogen colonization. The necrotrophic pathogen Sclerotinia sclerotiorum causes severe plant diseases and results in enormous economic losses, in which secreted proteins play a crucial role. SsCVNH was previously reported as a secreted protein, and its expression is significantly upregulated at 3 h after inoculation on the host plant. Here, we further demonstrated that deletion of SsCVNH leads to attenuated virulence. Heterologous expression of SsCVNH in Arabidopsis enhanced pathogen infection, inhibited the host PAMP‐triggered immunity (PTI) response and increased plant susceptibility to S. sclerotiorum. SsCVNH interacted with class III peroxidase AtPRX71, a positive regulator of innate immunity against plant pathogens. SsCVNH could also interact with other class III peroxidases, thus reducing peroxidase activity and suppressing plant immunity. Our results reveal a new infection strategy employed by S. sclerotiorum in which the fungus suppresses the function of class III peroxidases, the major component of PTI to promote its own infection.
许多植物病原体会向寄主植物分泌效应蛋白，以抑制寄主的免疫力并促进病原体的定殖。坏死性病原菌 Sclerotinia sclerotiorum 会导致严重的植物病害，造成巨大的经济损失，其中分泌蛋白起着至关重要的作用。之前有报道称 SsCVNH 是一种分泌蛋白，其表达在宿主植物接种后 3 小时显著上调。在这里，我们进一步证明了 SsCVNH 的缺失会导致毒力减弱。在拟南芥中异源表达 SsCVNH 会增强病原体感染，抑制宿主的 PAMP 触发免疫（PTI）反应，并增加植物对 S. sclerotiorum 的易感性。SsCVNH 与第三类过氧化物酶 AtPRX71 相互作用，后者是对抗植物病原体的先天性免疫的正调控因子。SsCVNH 还能与其他 III 类过氧化物酶相互作用，从而降低过氧化物酶的活性，抑制植物免疫。我们的研究结果揭示了 S. sclerotiorum 采用的一种新的感染策略，即真菌抑制 PTI 的主要成分 III 类过氧化物酶的功能，以促进自身感染。
{"title":"An effector SsCVNH promotes the virulence of Sclerotinia sclerotiorum through targeting class III peroxidase AtPRX71","authors":"Ming Ma, Liguang Tang, Rui Sun, Xueliang Lyu, Jiatao Xie, Yanping Fu, Bo Li, Tao Chen, Yang Lin, Xiao Yu, Weidong Chen, Daohong Jiang, Jiasen Cheng","doi":"10.1111/mpp.13464","DOIUrl":"https://doi.org/10.1111/mpp.13464","url":null,"abstract":"Many plant pathogens secrete effector proteins into the host plant to suppress host immunity and facilitate pathogen colonization. The necrotrophic pathogen <jats:italic>Sclerotinia sclerotiorum</jats:italic> causes severe plant diseases and results in enormous economic losses, in which secreted proteins play a crucial role. SsCVNH was previously reported as a secreted protein, and its expression is significantly upregulated at 3 h after inoculation on the host plant. Here, we further demonstrated that deletion of <jats:italic>SsCVNH</jats:italic> leads to attenuated virulence. Heterologous expression of <jats:italic>SsCVNH</jats:italic> in <jats:italic>Arabidopsis</jats:italic> enhanced pathogen infection, inhibited the host PAMP‐triggered immunity (PTI) response and increased plant susceptibility to <jats:italic>S. sclerotiorum</jats:italic>. SsCVNH interacted with class III peroxidase AtPRX71, a positive regulator of innate immunity against plant pathogens. SsCVNH could also interact with other class III peroxidases, thus reducing peroxidase activity and suppressing plant immunity. Our results reveal a new infection strategy employed by <jats:italic>S. sclerotiorum</jats:italic> in which the fungus suppresses the function of class III peroxidases, the major component of PTI to promote its own infection.","PeriodicalId":18763,"journal":{"name":"Molecular plant pathology","volume":"24 1","pages":""},"PeriodicalIF":4.9,"publicationDate":"2024-05-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140842128","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Tracy E. Hawk, Sarbottam Piya, Mst Shamira Sultana, Sobhan Bahrami Zadegan, Sarah Shipp, Nicole Coffey, Natalie B. McBride, John H. Rice, Tarek Hewezi
Mitogen‐activated protein kinase (MPK) cascades play central signalling roles in plant immunity and stress response. The soybean orthologue of MPK kinase2 (GmMKK2) was recently identified as a potential signalling node whose expression is upregulated in the feeding site induced by soybean cyst nematode (SCN, Heterodera glycines). To investigate the role of GmMKK2 in soybean–SCN interactions, we overexpressed a catabolically inactive variant referred to as kinase‐dead variant (KD‐GmMKK2) using transgenic hairy roots. KD‐GmMKK2 overexpression caused significant reduction in soybean susceptibility to SCN, while overexpression of the wild‐type variant (WT‐GmMKK2) exhibited no effect on susceptibility. Transcriptome analysis indicated that KD‐GmMKK2 overexpressing plants are primed for SCN resistance via constitutive activation of defence signalling, particularly those related to chitin, respiratory burst, hydrogen peroxide and salicylic acid. Phosphoproteomic profiling of the WT‐GmMKK2 and KD‐GmMKK2 root samples upon SCN infection resulted in the identification of 391 potential targets of GmMKK2. These targets are involved in a broad range of biological processes, including defence signalling, vesicle fusion, chromatin remodelling and nuclear organization among others. Furthermore, GmMKK2 mediates phosphorylation of numerous transcriptional and translational regulators, pointing to the presence of signalling shortcuts besides the canonical MAPK cascades to initiate downstream signalling that eventually regulates gene expression and translation initiation. Finally, the functional requirement of specific phosphorylation sites for soybean response to SCN infection was validated by overexpressing phospho‐mimic and phospho‐dead variants of two differentially phosphorylated proteins SUN1 and IDD4. Together, our analyses identify GmMKK2 impacts on signalling modules that regulate soybean response to SCN infection.
{"title":"Soybean MKK2 establishes intricate signalling pathways to regulate soybean response to cyst nematode infection","authors":"Tracy E. Hawk, Sarbottam Piya, Mst Shamira Sultana, Sobhan Bahrami Zadegan, Sarah Shipp, Nicole Coffey, Natalie B. McBride, John H. Rice, Tarek Hewezi","doi":"10.1111/mpp.13461","DOIUrl":"https://doi.org/10.1111/mpp.13461","url":null,"abstract":"Mitogen‐activated protein kinase (MPK) cascades play central signalling roles in plant immunity and stress response. The soybean orthologue of MPK kinase2 (GmMKK2) was recently identified as a potential signalling node whose expression is upregulated in the feeding site induced by soybean cyst nematode (SCN, <jats:italic>Heterodera glycines</jats:italic>). To investigate the role of GmMKK2 in soybean–SCN interactions, we overexpressed a catabolically inactive variant referred to as kinase‐dead variant (KD‐GmMKK2) using transgenic hairy roots. <jats:italic>KD‐GmMKK2</jats:italic> overexpression caused significant reduction in soybean susceptibility to SCN, while overexpression of the wild‐type variant (<jats:italic>WT‐GmMKK2</jats:italic>) exhibited no effect on susceptibility. Transcriptome analysis indicated that <jats:italic>KD‐GmMKK2</jats:italic> overexpressing plants are primed for SCN resistance via constitutive activation of defence signalling, particularly those related to chitin, respiratory burst, hydrogen peroxide and salicylic acid. Phosphoproteomic profiling of the <jats:italic>WT‐GmMKK2</jats:italic> and <jats:italic>KD‐GmMKK2</jats:italic> root samples upon SCN infection resulted in the identification of 391 potential targets of GmMKK2. These targets are involved in a broad range of biological processes, including defence signalling, vesicle fusion, chromatin remodelling and nuclear organization among others. Furthermore, GmMKK2 mediates phosphorylation of numerous transcriptional and translational regulators, pointing to the presence of signalling shortcuts besides the canonical MAPK cascades to initiate downstream signalling that eventually regulates gene expression and translation initiation. Finally, the functional requirement of specific phosphorylation sites for soybean response to SCN infection was validated by overexpressing phospho‐mimic and phospho‐dead variants of two differentially phosphorylated proteins SUN1 and IDD4. Together, our analyses identify GmMKK2 impacts on signalling modules that regulate soybean response to SCN infection.","PeriodicalId":18763,"journal":{"name":"Molecular plant pathology","volume":"36 1","pages":""},"PeriodicalIF":4.9,"publicationDate":"2024-05-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140833681","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Zizhang Li, Valeria Velásquez‐Zapata, J. Mitch Elmore, Xuan Li, Wenjun Xie, Sohini Deb, Xiao Tian, Sagnik Banerjee, Hans J. L. Jørgensen, Carsten Pedersen, Roger P. Wise, Hans Thordal‐Christensen
The barley powdery mildew fungus, Blumeria hordei (Bh), secretes hundreds of candidate secreted effector proteins (CSEPs) to facilitate pathogen infection and colonization. One of these, CSEP0008, is directly recognized by the barley nucleotide‐binding leucine‐rich‐repeat (NLR) receptor MLA1 and therefore is designated AVRA1. Here, we show that AVRA1 and the sequence‐unrelated Bh effector BEC1016 (CSEP0491) suppress immunity in barley. We used yeast two‐hybrid next‐generation interaction screens (Y2H‐NGIS), followed by binary Y2H and in planta protein–protein interactions studies, and identified a common barley target of AVRA1 and BEC1016, the endoplasmic reticulum (ER)‐localized J‐domain protein HvERdj3B. Silencing of this ER quality control (ERQC) protein increased Bh penetration. HvERdj3B is ER luminal, and we showed using split GFP that AVRA1 and BEC1016 translocate into the ER signal peptide‐independently. Overexpression of the two effectors impeded trafficking of a vacuolar marker through the ER; silencing of HvERdj3B also exhibited this same cellular phenotype, coinciding with the effectors targeting this ERQC component. Together, these results suggest that the barley innate immunity, preventing Bh entry into epidermal cells, requires ERQC. Here, the J‐domain protein HvERdj3B appears to be essential and can be regulated by AVRA1 and BEC1016. Plant disease resistance often occurs upon direct or indirect recognition of pathogen effectors by host NLR receptors. Previous work has shown that AVRA1 is directly recognized in the cytosol by the immune receptor MLA1. We speculate that the AVRA1 J‐domain target being inside the ER, where it is inapproachable by NLRs, has forced the plant to evolve this challenging direct recognition.
{"title":"Powdery mildew effectors AVRA1 and BEC1016 target the ER J‐domain protein HvERdj3B required for immunity in barley","authors":"Zizhang Li, Valeria Velásquez‐Zapata, J. Mitch Elmore, Xuan Li, Wenjun Xie, Sohini Deb, Xiao Tian, Sagnik Banerjee, Hans J. L. Jørgensen, Carsten Pedersen, Roger P. Wise, Hans Thordal‐Christensen","doi":"10.1111/mpp.13463","DOIUrl":"https://doi.org/10.1111/mpp.13463","url":null,"abstract":"The barley powdery mildew fungus, <jats:italic>Blumeria hordei</jats:italic> (Bh), secretes hundreds of candidate secreted effector proteins (CSEPs) to facilitate pathogen infection and colonization. One of these, CSEP0008, is directly recognized by the barley nucleotide‐binding leucine‐rich‐repeat (NLR) receptor MLA1 and therefore is designated AVR<jats:sub>A1</jats:sub>. Here, we show that AVR<jats:sub>A1</jats:sub> and the sequence‐unrelated Bh effector BEC1016 (CSEP0491) suppress immunity in barley. We used yeast two‐hybrid next‐generation interaction screens (Y2H‐NGIS), followed by binary Y2H and in planta protein–protein interactions studies, and identified a common barley target of AVR<jats:sub>A1</jats:sub> and BEC1016, the endoplasmic reticulum (ER)‐localized J‐domain protein <jats:italic>Hv</jats:italic>ERdj3B. Silencing of this ER quality control (ERQC) protein increased Bh penetration. <jats:italic>Hv</jats:italic>ERdj3B is ER luminal, and we showed using split GFP that AVR<jats:sub>A1</jats:sub> and BEC1016 translocate into the ER signal peptide‐independently. Overexpression of the two effectors impeded trafficking of a vacuolar marker through the ER; silencing of <jats:italic>Hv</jats:italic>ERdj3B also exhibited this same cellular phenotype, coinciding with the effectors targeting this ERQC component. Together, these results suggest that the barley innate immunity, preventing Bh entry into epidermal cells, requires ERQC. Here, the J‐domain protein <jats:italic>Hv</jats:italic>ERdj3B appears to be essential and can be regulated by AVR<jats:sub>A1</jats:sub> and BEC1016. Plant disease resistance often occurs upon direct or indirect recognition of pathogen effectors by host NLR receptors. Previous work has shown that AVR<jats:sub>A1</jats:sub> is directly recognized in the cytosol by the immune receptor MLA1. We speculate that the AVR<jats:sub>A1</jats:sub> J‐domain target being inside the ER, where it is inapproachable by NLRs, has forced the plant to evolve this challenging direct recognition.","PeriodicalId":18763,"journal":{"name":"Molecular plant pathology","volume":"10 1","pages":""},"PeriodicalIF":4.9,"publicationDate":"2024-05-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140833684","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
The movement of potyviruses, the largest genus of single-stranded, positive-sense RNA viruses responsible for serious diseases in crops, is very complex. As potyviruses developed strategies to hijack the host secretory pathway and plasmodesmata (PD) for their transport, the goal of this study was to identify membrane and/or PD-proteins that interact with the 6K2 protein, a potyviral protein involved in replication and cell-to-cell movement of turnip mosaic virus (TuMV). Using split-ubiquitin membrane yeast two-hybrid assays, we screened an Arabidopsis cDNA library for interactors of TuMV6K2. We isolated AtHVA22a (Hordeum vulgare abscisic acid responsive gene 22), which belongs to a multigenic family of transmembrane proteins, homologous to Receptor expression-enhancing protein (Reep)/Deleted in polyposis (DP1)/Yop1 family proteins in animal and yeast. HVA22/DP1/Yop1 family genes are widely distributed in eukaryotes, but the role of HVA22 proteins in plants is still not well known, although proteomics analysis of PD fractions purified from Arabidopsis suspension cells showed that AtHVA22a is highly enriched in a PD proteome. We confirmed the interaction between TuMV6K2 and AtHVA22a in yeast, as well as in planta by using bimolecular fluorescence complementation and showed that TuMV6K2/AtHVA22a interaction occurs at the level of the viral replication compartment during TuMV infection. Finally, we showed that the propagation of TuMV is increased when AtHVA22a is overexpressed in planta but slowed down upon mutagenesis of AtHVA22a by CRISPR-Cas9. Altogether, our results indicate that AtHVA22a plays an agonistic effect on TuMV propagation and that the C-terminal tail of the protein is important in this process.
{"title":"AtHVA22a, a plant-specific homologue of Reep/DP1/Yop1 family proteins is involved in turnip mosaic virus propagation.","authors":"Mingshuo Xue, Luc Sofer, Vincent Simon, Nathalie Arvy, Mamoudou Diop, Roxane Lion, Guillaume Beucher, Amandine Bordat, Jens Tilsner, Jean-Luc Gallois, Sylvie German-Retana","doi":"10.1111/mpp.13466","DOIUrl":"10.1111/mpp.13466","url":null,"abstract":"<p><p>The movement of potyviruses, the largest genus of single-stranded, positive-sense RNA viruses responsible for serious diseases in crops, is very complex. As potyviruses developed strategies to hijack the host secretory pathway and plasmodesmata (PD) for their transport, the goal of this study was to identify membrane and/or PD-proteins that interact with the 6K2 protein, a potyviral protein involved in replication and cell-to-cell movement of turnip mosaic virus (TuMV). Using split-ubiquitin membrane yeast two-hybrid assays, we screened an Arabidopsis cDNA library for interactors of <sup>TuMV</sup>6K2. We isolated AtHVA22a (Hordeum vulgare abscisic acid responsive gene 22), which belongs to a multigenic family of transmembrane proteins, homologous to Receptor expression-enhancing protein (Reep)/Deleted in polyposis (DP1)/Yop1 family proteins in animal and yeast. HVA22/DP1/Yop1 family genes are widely distributed in eukaryotes, but the role of HVA22 proteins in plants is still not well known, although proteomics analysis of PD fractions purified from Arabidopsis suspension cells showed that AtHVA22a is highly enriched in a PD proteome. We confirmed the interaction between <sup>TuMV</sup>6K2 and AtHVA22a in yeast, as well as in planta by using bimolecular fluorescence complementation and showed that <sup>TuMV</sup>6K2/AtHVA22a interaction occurs at the level of the viral replication compartment during TuMV infection. Finally, we showed that the propagation of TuMV is increased when AtHVA22a is overexpressed in planta but slowed down upon mutagenesis of AtHVA22a by CRISPR-Cas9. Altogether, our results indicate that AtHVA22a plays an agonistic effect on TuMV propagation and that the C-terminal tail of the protein is important in this process.</p>","PeriodicalId":18763,"journal":{"name":"Molecular plant pathology","volume":"25 5","pages":"e13466"},"PeriodicalIF":4.8,"publicationDate":"2024-05-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11104427/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141065455","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Xiaofei Liang, Wei Yu, Yanan Meng, Shengping Shang, Huanhuan Tian, Zhaohui Zhang, Jeffrey A. Rollins, Rong Zhang, Guangyu Sun
Apple Glomerella leaf spot (GLS) is an emerging fungal disease caused by Colletotrichum fructicola and other Colletotrichum species. These species are polyphyletic and it is currently unknown how these pathogens convergently evolved to infect apple. We generated chromosome‐level genome assemblies of a GLS‐adapted isolate and a non‐adapted isolate in C. fructicola using long‐read sequencing. Additionally, we resequenced 17 C. fructicola and C. aenigma isolates varying in GLS pathogenicity using short‐read sequencing. Genome comparisons revealed a conserved bipartite genome architecture involving minichromosomes (accessory chromosomes) shared by C. fructicola and other closely related species within the C. gloeosporioides species complex. Moreover, two repeat‐rich genomic regions (1.61 Mb in total) were specifically conserved among GLS‐pathogenic isolates in C. fructicola and C. aenigma. Single‐gene deletion of 10 accessory genes within the GLS‐specific regions of C. fructicola identified three that were essential for GLS pathogenicity. These genes encoded a putative non‐ribosomal peptide synthetase, a flavin‐binding monooxygenase and a small protein with unknown function. These results highlight the crucial role accessory genes play in the evolution of Colletotrichum pathogenicity and imply the significance of an unidentified secondary metabolite in GLS pathogenesis.
苹果球孢菌叶斑病（GLS）是一种新出现的真菌病害，由 Colletotrichum fructicola 和其他 Colletotrichum 菌种引起。这些物种是多态的，目前还不清楚这些病原体是如何进化到感染苹果的。我们利用长线程测序技术生成了果实疫霉菌中一个适应 GLS 的分离株和一个不适应 GLS 的分离株的染色体组。此外，我们还利用短线程测序技术对 17 个果蝇科 C. 和 C. aenigma 分离物进行了重新测序，这些分离物的 GLS 致病性各不相同。基因组比较显示，果孢子菌和球孢子菌种群中其他密切相关的菌种具有保守的两部分基因组结构，其中包括小染色体（附属染色体）。此外，在 C. fructicola 和 C. aenigma 的 GLS 致病分离株中，有两个重复丰富的基因组区域（共 1.61 Mb）是特别保守的。在 C. fructicola 的 GLS 特异性区域内对 10 个附属基因进行了单基因缺失，发现其中 3 个基因对 GLS 的致病性至关重要。这些基因编码一种假定的非核糖体肽合成酶、一种黄素结合单氧化酶和一种功能未知的小蛋白。这些结果凸显了附属基因在 Colletotrichum 致病性进化过程中发挥的关键作用，并暗示了一种未确定的次生代谢物在 GLS 致病过程中的重要性。
{"title":"Genome comparisons reveal accessory genes crucial for the evolution of apple Glomerella leaf spot pathogenicity in Colletotrichum fungi","authors":"Xiaofei Liang, Wei Yu, Yanan Meng, Shengping Shang, Huanhuan Tian, Zhaohui Zhang, Jeffrey A. Rollins, Rong Zhang, Guangyu Sun","doi":"10.1111/mpp.13454","DOIUrl":"https://doi.org/10.1111/mpp.13454","url":null,"abstract":"Apple Glomerella leaf spot (GLS) is an emerging fungal disease caused by <jats:italic>Colletotrichum fructicola</jats:italic> and other <jats:italic>Colletotrichum</jats:italic> species. These species are polyphyletic and it is currently unknown how these pathogens convergently evolved to infect apple. We generated chromosome‐level genome assemblies of a GLS‐adapted isolate and a non‐adapted isolate in <jats:italic>C. fructicola</jats:italic> using long‐read sequencing. Additionally, we resequenced 17 <jats:italic>C. fructicola</jats:italic> and <jats:italic>C. aenigma</jats:italic> isolates varying in GLS pathogenicity using short‐read sequencing. Genome comparisons revealed a conserved bipartite genome architecture involving minichromosomes (accessory chromosomes) shared by <jats:italic>C. fructicola</jats:italic> and other closely related species within the <jats:italic>C. gloeosporioides</jats:italic> species complex. Moreover, two repeat‐rich genomic regions (1.61 Mb in total) were specifically conserved among GLS‐pathogenic isolates in <jats:italic>C. fructicola</jats:italic> and <jats:italic>C. aenigma</jats:italic>. Single‐gene deletion of 10 accessory genes within the GLS‐specific regions of <jats:italic>C. fructicola</jats:italic> identified three that were essential for GLS pathogenicity. These genes encoded a putative non‐ribosomal peptide synthetase, a flavin‐binding monooxygenase and a small protein with unknown function. These results highlight the crucial role accessory genes play in the evolution of <jats:italic>Colletotrichum</jats:italic> pathogenicity and imply the significance of an unidentified secondary metabolite in GLS pathogenesis.","PeriodicalId":18763,"journal":{"name":"Molecular plant pathology","volume":"61 1","pages":""},"PeriodicalIF":4.9,"publicationDate":"2024-04-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140589337","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Qiushi Chen, Ya Li, Tianjiao Shen, Rong Wang, Meiling Su, Qiong Luo, Hua Shi, Guodong Lu, Zonghua Wang, Kevin G. Hardwick, Mo Wang
The spindle assembly checkpoint (SAC) proteins are conserved among eukaryotes safeguarding chromosome segregation fidelity during mitosis. However, their biological functions in plant‐pathogenic fungi remain largely unknown. In this study, we found that the SAC protein MoMad1 in rice blast fungus (Magnaporthe oryzae) localizes on the nuclear envelope and is dispensable for M. oryzae vegetative growth and tolerance to microtubule depolymerizing agent treatment. MoMad1 plays an important role in M. oryzae infection‐related development and pathogenicity. The monopolar spindle 1 homologue in M. oryzae (MoMps1) interacts with MoMad1 through its N‐terminal domain and phosphorylates MoMad1 at Ser‐18, which is conserved within the extended N termini of Mad1s from fungal plant pathogens. This phosphorylation is required for maintaining MoMad1 protein abundance and M. oryzae full virulence. Similar to the deletion of MoMad1, treatment with Mps1‐IN‐1 (an Mps1 inhibitor) caused compromised appressorium formation and decreased M. oryzae virulence, and these defects were dependent on its attenuating MoMad1 Ser‐18 phosphorylation. Therefore, our study indicates the function of Mad1 in rice blast fungal pathogenicity and sheds light on the potential of blocking Mad1 phosphorylation by Mps1 to control crop fungal diseases.
纺锤体装配检查点（SAC）蛋白是真核生物中的保守蛋白，在有丝分裂过程中保障染色体分离的保真度。然而，它们在植物病原真菌中的生物学功能在很大程度上仍然未知。本研究发现，稻瘟病真菌（Magnaporthe oryzae）中的 SAC 蛋白 MoMad1 定位于核膜上，对于稻瘟病真菌的无性生长和耐受微管解聚剂处理是不可或缺的。MoMad1 在与 M. oryzae 感染相关的发育和致病性中发挥着重要作用。M. oryzae 中的单极纺锤体 1 同源物（MoMps1）通过其 N 端结构域与 MoMad1 相互作用，并在 Ser-18 处磷酸化 MoMad1。这种磷酸化是维持 MoMad1 蛋白丰度和 M. oryzae 完全毒力所必需的。与缺失 MoMad1 相似，用 Mps1-IN-1（一种 Mps1 抑制剂）处理也会导致附着体形成受阻和 M. oryzae 毒力下降，而这些缺陷都依赖于它对 MoMad1 Ser-18 磷酸化的抑制作用。因此，我们的研究表明了Mad1在稻瘟病真菌致病性中的功能，并揭示了通过Mps1阻断Mad1磷酸化来控制作物真菌病害的潜力。
{"title":"Phosphorylation of Mad1 at serine 18 by Mps1 is required for the full virulence of rice blast fungus, Magnaporthe oryzae","authors":"Qiushi Chen, Ya Li, Tianjiao Shen, Rong Wang, Meiling Su, Qiong Luo, Hua Shi, Guodong Lu, Zonghua Wang, Kevin G. Hardwick, Mo Wang","doi":"10.1111/mpp.13456","DOIUrl":"https://doi.org/10.1111/mpp.13456","url":null,"abstract":"The spindle assembly checkpoint (SAC) proteins are conserved among eukaryotes safeguarding chromosome segregation fidelity during mitosis. However, their biological functions in plant‐pathogenic fungi remain largely unknown. In this study, we found that the SAC protein MoMad1 in rice blast fungus (<jats:italic>Magnaporthe oryzae</jats:italic>) localizes on the nuclear envelope and is dispensable for <jats:italic>M. oryzae</jats:italic> vegetative growth and tolerance to microtubule depolymerizing agent treatment. MoMad1 plays an important role in <jats:italic>M. oryzae</jats:italic> infection‐related development and pathogenicity. The monopolar spindle 1 homologue in <jats:italic>M. oryzae</jats:italic> (MoMps1) interacts with MoMad1 through its N‐terminal domain and phosphorylates MoMad1 at Ser‐18, which is conserved within the extended N termini of Mad1s from fungal plant pathogens. This phosphorylation is required for maintaining MoMad1 protein abundance and <jats:italic>M. oryzae</jats:italic> full virulence. Similar to the deletion of MoMad1, treatment with Mps1‐IN‐1 (an Mps1 inhibitor) caused compromised appressorium formation and decreased <jats:italic>M. oryzae</jats:italic> virulence, and these defects were dependent on its attenuating MoMad1 Ser‐18 phosphorylation. Therefore, our study indicates the function of Mad1 in rice blast fungal pathogenicity and sheds light on the potential of blocking Mad1 phosphorylation by Mps1 to control crop fungal diseases.","PeriodicalId":18763,"journal":{"name":"Molecular plant pathology","volume":"212 1","pages":""},"PeriodicalIF":4.9,"publicationDate":"2024-04-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140589336","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Tingting Pei, Dongshan Niu, Yongxin Ma, Minghui Zhan, Jie Deng, Pengmin Li, Fengwang Ma, Changhai Liu
Glomerella leaf spot (GLS), a fungal disease caused by Colletotrichum fructicola, severely affects apple (Malus domestica) quality and yield. In this study, we found that the transcription factor MdWRKY71 was significantly induced by C. fructicola infection in the GLS‐susceptible apple cultivar Royal Gala. The overexpression of MdWRKY71 in apple leaves resulted in increased susceptibility to C. fructicola, whereas RNA interference of MdWRKY71 in leaves showed the opposite phenotypes. These findings suggest that MdWRKY71 functions as a susceptibility factor for the apple—C. fructicola interaction. Furthermore, MdWRKY71 directly bound to the promoter of the salicylic acid (SA) degradation gene Downy Mildew Resistant 6 (DMR6)‐Like Oxygenase 1 (DLO1) and promoted its expression, resulting in a reduced SA level. The sensitivity of 35S:MdWRKY71 leaves to C. fructicola can be effectively alleviated by knocking down MdDLO1 expression, confirming the critical role of MdWRKY71‐mediated SA degradation via regulating MdDLO1 expression in GLS susceptibility. In summary, we identified a GLS susceptibility factor, MdWRKY71, that targets the apple SA degradation pathway to promote fungal infection.
由果孢子菌（Colletotrichum fructicola）引起的真菌病害--苹果叶斑病（GLS）严重影响苹果（Malus domestica）的品质和产量。在这项研究中，我们发现在易感 GLS 的苹果栽培品种 Royal Gala 中，果孢子菌感染会显著诱导转录因子 MdWRKY71。在苹果叶片中过表达 MdWRKY71 会增加对果孢子菌的易感性，而 RNA 干扰叶片中的 MdWRKY71 则显示出相反的表型。这些发现表明，MdWRKY71 是苹果与果蝇相互作用的易感因子。此外，MdWRKY71 直接与水杨酸（SA）降解基因抗霜霉病 6（DMR6）-Like 氧化酶 1（DLO1）的启动子结合并促进其表达，导致 SA 水平降低。通过敲低 MdDLO1 的表达，可以有效缓解 35S:MdWRKY71 叶片对 C. fructicola 的敏感性，证实了 MdWRKY71 通过调控 MdDLO1 的表达介导的 SA 降解在 GLS 易感性中的关键作用。总之，我们发现了一种 GLS 易感因子 MdWRKY71，它能靶向苹果 SA 降解途径促进真菌感染。
{"title":"MdWRKY71 promotes the susceptibility of apple to Glomerella leaf spot by controlling salicylic acid degradation","authors":"Tingting Pei, Dongshan Niu, Yongxin Ma, Minghui Zhan, Jie Deng, Pengmin Li, Fengwang Ma, Changhai Liu","doi":"10.1111/mpp.13457","DOIUrl":"https://doi.org/10.1111/mpp.13457","url":null,"abstract":"Glomerella leaf spot (GLS), a fungal disease caused by <jats:italic>Colletotrichum fructicola</jats:italic>, severely affects apple (<jats:italic>Malus domestica</jats:italic>) quality and yield. In this study, we found that the transcription factor MdWRKY71 was significantly induced by <jats:italic>C. fructicola</jats:italic> infection in the GLS‐susceptible apple cultivar Royal Gala. The overexpression of <jats:italic>MdWRKY71</jats:italic> in apple leaves resulted in increased susceptibility to <jats:italic>C. fructicola</jats:italic>, whereas RNA interference of <jats:italic>MdWRKY71</jats:italic> in leaves showed the opposite phenotypes. These findings suggest that MdWRKY71 functions as a susceptibility factor for the apple—<jats:italic>C. fructicola</jats:italic> interaction. Furthermore, MdWRKY71 directly bound to the promoter of the salicylic acid (SA) degradation gene <jats:italic>Downy Mildew Resistant 6</jats:italic> (<jats:italic>DMR6</jats:italic>)<jats:italic>‐Like Oxygenase 1</jats:italic> (<jats:italic>DLO1</jats:italic>) and promoted its expression, resulting in a reduced SA level. The sensitivity of 35S:<jats:italic>MdWRKY71</jats:italic> leaves to <jats:italic>C. fructicola</jats:italic> can be effectively alleviated by knocking down <jats:italic>MdDLO1</jats:italic> expression, confirming the critical role of MdWRKY71‐mediated SA degradation via regulating <jats:italic>MdDLO1</jats:italic> expression in GLS susceptibility. In summary, we identified a GLS susceptibility factor, MdWRKY71, that targets the apple SA degradation pathway to promote fungal infection.","PeriodicalId":18763,"journal":{"name":"Molecular plant pathology","volume":"25 1","pages":""},"PeriodicalIF":4.9,"publicationDate":"2024-04-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140589333","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Xi Chen, Yan Sun, Yu Yang, Yuxin Zhao, Chuanzhong Zhang, Xin Fang, Hong Gao, Ming Zhao, Shengfu He, Bo Song, Shanshan Liu, Junjiang Wu, Pengfei Xu, Shuzhen Zhang
Phytophthora root and stem rot of soybean (Glycine max), caused by the oomycete Phytophthora sojae, is an extremely destructive disease worldwide. In this study, we identified GmEIL1, which encodes an ethylene‐insensitive3 (EIN3) transcription factor. GmEIL1 was significantly induced following P. sojae infection of soybean plants. Compared to wild‐type soybean plants, transgenic soybean plants overexpressing GmEIL1 showed enhanced resistance to P. sojae and GmEIL1‐silenced RNA‐interference lines showed more severe symptoms when infected with P. sojae. We screened for target genes of GmEIL1 and confirmed that GmEIL1 bound directly to the GmERF113 promoter and regulated GmERF113 expression. Moreover, GmEIL1 positively regulated the expression of the pathogenesis‐related gene GmPR1. The GmEIL1‐regulated defence response to P. sojae involved both ethylene biosynthesis and the ethylene signalling pathway. These findings suggest that the GmEIL1‐GmERF113 module plays an important role in P. sojae resistance via the ethylene signalling pathway.
由卵菌 Phytophthora sojae 引起的大豆（Glycine max）茎腐病（Phytophthora root and stem rot）是一种在全球范围内破坏性极大的病害。在这项研究中，我们发现了编码乙烯不敏感3（EIN3）转录因子的GmEIL1。大豆植株感染 P. sojae 后，GmEIL1 被显著诱导。与野生型大豆植株相比，过表达 GmEIL1 的转基因大豆植株对 P. sojae 的抗性更强，而 GmEIL1 沉默的 RNA 干涉品系在感染 P. sojae 后症状更严重。我们筛选了 GmEIL1 的靶基因，证实 GmEIL1 可直接与 GmERF113 启动子结合并调控 GmERF113 的表达。此外，GmEIL1 还能正向调节致病相关基因 GmPR1 的表达。GmEIL1 调节的对 P. sojae 的防御反应涉及乙烯的生物合成和乙烯信号通路。这些研究结果表明，GmEIL1-GmERF113 模块通过乙烯信号途径在 P. sojae 的抗性中发挥了重要作用。
{"title":"The EIN3 transcription factor GmEIL1 improves soybean resistance to Phytophthora sojae","authors":"Xi Chen, Yan Sun, Yu Yang, Yuxin Zhao, Chuanzhong Zhang, Xin Fang, Hong Gao, Ming Zhao, Shengfu He, Bo Song, Shanshan Liu, Junjiang Wu, Pengfei Xu, Shuzhen Zhang","doi":"10.1111/mpp.13452","DOIUrl":"https://doi.org/10.1111/mpp.13452","url":null,"abstract":"Phytophthora root and stem rot of soybean (<jats:italic>Glycine max</jats:italic>), caused by the oomycete <jats:italic>Phytophthora sojae</jats:italic>, is an extremely destructive disease worldwide. In this study, we identified <jats:italic>GmEIL1</jats:italic>, which encodes an ethylene‐insensitive3 (EIN3) transcription factor. <jats:italic>GmEIL1</jats:italic> was significantly induced following <jats:italic>P. sojae</jats:italic> infection of soybean plants. Compared to wild‐type soybean plants, transgenic soybean plants overexpressing <jats:italic>GmEIL1</jats:italic> showed enhanced resistance to <jats:italic>P. sojae</jats:italic> and <jats:italic>GmEIL1</jats:italic>‐silenced RNA‐interference lines showed more severe symptoms when infected with <jats:italic>P. sojae</jats:italic>. We screened for target genes of GmEIL1 and confirmed that GmEIL1 bound directly to the <jats:italic>GmERF113</jats:italic> promoter and regulated <jats:italic>GmERF113</jats:italic> expression. Moreover, GmEIL1 positively regulated the expression of the pathogenesis‐related gene <jats:italic>GmPR1</jats:italic>. The GmEIL1‐regulated defence response to <jats:italic>P. sojae</jats:italic> involved both ethylene biosynthesis and the ethylene signalling pathway. These findings suggest that the GmEIL1‐<jats:italic>GmERF113</jats:italic> module plays an important role in <jats:italic>P. sojae</jats:italic> resistance via the ethylene signalling pathway.","PeriodicalId":18763,"journal":{"name":"Molecular plant pathology","volume":"164 1","pages":""},"PeriodicalIF":4.9,"publicationDate":"2024-04-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140589354","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
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