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":null,"pages":null},"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":null,"pages":null},"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":null,"pages":null},"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":null,"pages":null},"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":null,"pages":null},"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}
Maël Baudin, Marie Le Naour‐Vernet, Pierre Gladieux, Didier Tharreau, Marc‐Henri Lebrun, Karine Lambou, Marie Leys, Elisabeth Fournier, Stella Césari, Thomas Kroj
Pyricularia oryzae (syn. Magnaporthe oryzae), is a filamentous ascomycete that causes a major disease called blast on cereal crops, as well as on a wide variety of wild and cultivated grasses. Blast diseases have a tremendous impact worldwide particularly on rice and on wheat, where the disease emerged in South America in the 1980s, before spreading to Asia and Africa. Its economic importance, coupled with its amenability to molecular and genetic manipulation, have inspired extensive research efforts aiming at understanding its biology and evolution. In the past 40 years, this plant‐pathogenic fungus has emerged as a major model in molecular plant–microbe interactions. In this review, we focus on the clarification of the taxonomy and genetic structure of the species and its host range determinants. We also discuss recent molecular studies deciphering its lifecycle.TaxonomyKingdom: Fungi, phylum: Ascomycota, sub‐phylum: Pezizomycotina, class: Sordariomycetes, order: Magnaporthales, family: Pyriculariaceae, genus: Pyricularia.Host rangeP. oryzae has the ability to infect a wide range of Poaceae. It is structured into different host‐specialized lineages that are each associated with a few host plant genera. The fungus is best known to cause tremendous damage to rice crops, but it can also attack other economically important crops such as wheat, maize, barley, and finger millet.Disease symptomsP. oryzae can cause necrotic lesions or bleaching on all aerial parts of its host plants, including leaf blades, sheaths, and inflorescences (panicles, spikes, and seeds). Characteristic symptoms on leaves are diamond‐shaped silver lesions that often have a brown margin and whose appearance is influenced by numerous factors such as the plant genotype and environmental conditions.USEFUL WEBSITESResourcesURLGenomic data repositorieshttp://genome.jouy.inra.fr/gemo/Genomic data repositorieshttp://openriceblast.org/Genomic data repositories
{"title":"Pyricularia oryzae: Lab star and field scourge","authors":"Maël Baudin, Marie Le Naour‐Vernet, Pierre Gladieux, Didier Tharreau, Marc‐Henri Lebrun, Karine Lambou, Marie Leys, Elisabeth Fournier, Stella Césari, Thomas Kroj","doi":"10.1111/mpp.13449","DOIUrl":"https://doi.org/10.1111/mpp.13449","url":null,"abstract":"<jats:label /><jats:italic>Pyricularia oryzae</jats:italic> (syn. <jats:italic>Magnaporthe oryzae</jats:italic>), is a filamentous ascomycete that causes a major disease called blast on cereal crops, as well as on a wide variety of wild and cultivated grasses. Blast diseases have a tremendous impact worldwide particularly on rice and on wheat, where the disease emerged in South America in the 1980s, before spreading to Asia and Africa. Its economic importance, coupled with its amenability to molecular and genetic manipulation, have inspired extensive research efforts aiming at understanding its biology and evolution. In the past 40 years, this plant‐pathogenic fungus has emerged as a major model in molecular plant–microbe interactions. In this review, we focus on the clarification of the taxonomy and genetic structure of the species and its host range determinants. We also discuss recent molecular studies deciphering its lifecycle.TaxonomyKingdom: <jats:italic>Fungi</jats:italic>, phylum: <jats:italic>Ascomycota</jats:italic>, sub‐phylum: <jats:italic>Pezizomycotina</jats:italic>, class: <jats:italic>Sordariomycetes</jats:italic>, order: <jats:italic>Magnaporthales</jats:italic>, family: <jats:italic>Pyriculariaceae</jats:italic>, genus: <jats:italic>Pyricularia.</jats:italic>Host range<jats:italic>P. oryzae</jats:italic> has the ability to infect a wide range of <jats:italic>Poaceae</jats:italic>. It is structured into different host‐specialized lineages that are each associated with a few host plant genera. The fungus is best known to cause tremendous damage to rice crops, but it can also attack other economically important crops such as wheat, maize, barley, and finger millet.Disease symptoms<jats:italic>P. oryzae</jats:italic> can cause necrotic lesions or bleaching on all aerial parts of its host plants, including leaf blades, sheaths, and inflorescences (panicles, spikes, and seeds). Characteristic symptoms on leaves are diamond‐shaped silver lesions that often have a brown margin and whose appearance is influenced by numerous factors such as the plant genotype and environmental conditions.<jats:label /><jats:table-wrap position=\"anchor\"> <jats:caption>USEFUL WEBSITES</jats:caption> <jats:table frame=\"hsides\"> <jats:col /> <jats:col /> <jats:thead> <jats:tr> <jats:th>Resources</jats:th> <jats:th>URL</jats:th> </jats:tr> </jats:thead> <jats:tbody> <jats:tr> <jats:td>Genomic data repositories</jats:td> <jats:td> <jats:ext-link xmlns:xlink=\"http://www.w3.org/1999/xlink\" xlink:href=\"http://genome.jouy.inra.fr/gemo/\">http://genome.jouy.inra.fr/gemo/</jats:ext-link> </jats:td> </jats:tr> <jats:tr> <jats:td>Genomic data repositories</jats:td> <jats:td> <jats:ext-link xmlns:xlink=\"http://www.w3.org/1999/xlink\" xlink:href=\"http://openriceblast.org/\">http://openriceblast.org/</jats:ext-link> </jats:td> </jats:tr> <jats:tr> <jats:td>Genomic data repositories</jats:td> <jats:td> <jats:ext-link xmlns:xlink=\"http://www.w3.org/1999/xlink\" xlink:href=\"http","PeriodicalId":18763,"journal":{"name":"Molecular plant pathology","volume":null,"pages":null},"PeriodicalIF":4.9,"publicationDate":"2024-04-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140589437","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}
Hui Li, Raviraj Kalunke, Meenakshi Tetorya, Kirk J. Czymmek, Dilip M. Shah
Due to rapidly emerging resistance to single‐site fungicides in fungal pathogens of plants, there is a burgeoning need for safe and multisite fungicides. Plant antifungal peptides with multisite modes of action (MoA) have potential as bioinspired fungicides. Medicago truncatula defensin MtDef4 was previously reported to exhibit potent antifungal activity against fungal pathogens. Its MoA involves plasma membrane disruption and binding to intracellular targets. However, specific biochemical processes inhibited by this defensin and causing cell death have not been determined. Here, we show that MtDef4 exhibited potent antifungal activity against Botrytis cinerea. It induced severe plasma membrane and organelle irregularities in the germlings of this pathogen. It bound to fungal ribosomes and inhibited protein translation in vitro. A MtDef4 variant lacking antifungal activity exhibited greatly reduced protein translation inhibitory activity. A cation‐tolerant MtDef4 variant was generated that bound to β‐glucan of the fungal cell wall with higher affinity than MtDef4. It also conferred a greater reduction in the grey mould disease symptoms than MtDef4 when applied exogenously on Nicotiana benthamiana plants, tomato fruits and rose petals. Our findings revealed inhibition of protein synthesis as a likely target of MtDef4 and the potential of its cation‐tolerant variant as a peptide‐based fungicide.
{"title":"Modes of action and potential as a peptide‐based biofungicide of a plant defensin MtDef4","authors":"Hui Li, Raviraj Kalunke, Meenakshi Tetorya, Kirk J. Czymmek, Dilip M. Shah","doi":"10.1111/mpp.13458","DOIUrl":"https://doi.org/10.1111/mpp.13458","url":null,"abstract":"Due to rapidly emerging resistance to single‐site fungicides in fungal pathogens of plants, there is a burgeoning need for safe and multisite fungicides. Plant antifungal peptides with multisite modes of action (MoA) have potential as bioinspired fungicides. <jats:italic>Medicago truncatula</jats:italic> defensin MtDef4 was previously reported to exhibit potent antifungal activity against fungal pathogens. Its MoA involves plasma membrane disruption and binding to intracellular targets. However, specific biochemical processes inhibited by this defensin and causing cell death have not been determined. Here, we show that MtDef4 exhibited potent antifungal activity against <jats:italic>Botrytis cinerea</jats:italic>. It induced severe plasma membrane and organelle irregularities in the germlings of this pathogen. It bound to fungal ribosomes and inhibited protein translation in vitro. A MtDef4 variant lacking antifungal activity exhibited greatly reduced protein translation inhibitory activity. A cation‐tolerant MtDef4 variant was generated that bound to β‐glucan of the fungal cell wall with higher affinity than MtDef4. It also conferred a greater reduction in the grey mould disease symptoms than MtDef4 when applied exogenously on <jats:italic>Nicotiana benthamiana</jats:italic> plants, tomato fruits and rose petals. Our findings revealed inhibition of protein synthesis as a likely target of MtDef4 and the potential of its cation‐tolerant variant as a peptide‐based fungicide.","PeriodicalId":18763,"journal":{"name":"Molecular plant pathology","volume":null,"pages":null},"PeriodicalIF":4.9,"publicationDate":"2024-04-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140589666","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}
Alicia Fick, Velushka Swart, Aureliano Bombarely, Noëlani van den Berg
Plant cells undergo extensive transcriptional reprogramming following pathogen infection, with these reprogramming patterns becoming more complex when pathogens, such as hemibiotrophs, exhibit different lifestyles. These transcriptional changes are often orchestrated by MYB, WRKY and AP2/ERF transcription factors (TFs), which modulate both growth and defence‐related gene expression. Transcriptional analysis of defence‐related genes in avocado (Persea americana) infected with Phytophthora cinnamomi indicated differential immune response activation when comparing a partially resistant and susceptible rootstock. This study identified 226 MYB, 82 WRKY, and 174 AP2/ERF TF‐encoding genes in avocado, using a genome‐wide approach. Phylogenetic analysis revealed substantial sequence conservation within TF groups underscoring their functional significance. RNA‐sequencing analysis in a partially resistant and susceptible avocado rootstock infected with P. cinnamomi was indicative of an immune response switch occurring in either rootstock after 24 and 6 h post‐inoculation, respectively. Different clusters of co‐expressed TF genes were observed at these times, suggesting the activation of necrotroph‐related immune responses at varying intervals between the two rootstocks. This study aids our understanding of avocado immune response activation following P. cinnamomi infection, and the role of the TFs therein, elucidating the transcriptional reprogramming disparities between partially resistant and susceptible rootstocks.
{"title":"Comparative transcriptional analysis of Persea americana MYB, WRKY and AP2/ERF transcription factors following Phytophthora cinnamomi infection","authors":"Alicia Fick, Velushka Swart, Aureliano Bombarely, Noëlani van den Berg","doi":"10.1111/mpp.13453","DOIUrl":"https://doi.org/10.1111/mpp.13453","url":null,"abstract":"Plant cells undergo extensive transcriptional reprogramming following pathogen infection, with these reprogramming patterns becoming more complex when pathogens, such as hemibiotrophs, exhibit different lifestyles. These transcriptional changes are often orchestrated by MYB, WRKY and AP2/ERF transcription factors (TFs), which modulate both growth and defence‐related gene expression. Transcriptional analysis of defence‐related genes in avocado (<jats:italic>Persea americana</jats:italic>) infected with <jats:italic>Phytophthora cinnamomi</jats:italic> indicated differential immune response activation when comparing a partially resistant and susceptible rootstock. This study identified 226 <jats:italic>MYB</jats:italic>, 82 <jats:italic>WRKY</jats:italic>, and 174 AP2/ERF TF‐encoding genes in avocado, using a genome‐wide approach. Phylogenetic analysis revealed substantial sequence conservation within TF groups underscoring their functional significance. RNA‐sequencing analysis in a partially resistant and susceptible avocado rootstock infected with <jats:italic>P. cinnamomi</jats:italic> was indicative of an immune response switch occurring in either rootstock after 24 and 6 h post‐inoculation, respectively. Different clusters of co‐expressed <jats:italic>TF</jats:italic> genes were observed at these times, suggesting the activation of necrotroph‐related immune responses at varying intervals between the two rootstocks. This study aids our understanding of avocado immune response activation following <jats:italic>P. cinnamomi</jats:italic> infection, and the role of the TFs therein, elucidating the transcriptional reprogramming disparities between partially resistant and susceptible rootstocks.","PeriodicalId":18763,"journal":{"name":"Molecular plant pathology","volume":null,"pages":null},"PeriodicalIF":4.9,"publicationDate":"2024-04-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140589600","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}
Andrea Vadillo‐Dieguez, Ziyue Zeng, John W. Mansfield, Nastasiya F. Grinberg, Samantha C. Lynn, Adam Gregg, John Connell, Richard J. Harrison, Robert W. Jackson, Michelle T. Hulin
When compared with other phylogroups (PGs) of the Pseudomonas syringae species complex, P. syringae pv. syringae (Pss) strains within PG2 have a reduced repertoire of type III effectors (T3Es) but produce several phytotoxins. Effectors within the cherry pathogen Pss 9644 were grouped based on their frequency in strains from Prunus as the conserved effector locus (CEL) common to most P. syringae pathogens; a core of effectors common to PG2; a set of PRUNUS effectors common to cherry pathogens; and a FLEXIBLE set of T3Es. Pss 9644 also contains gene clusters for biosynthesis of toxins syringomycin, syringopeptin and syringolin A. After confirmation of virulence gene expression, mutants with a sequential series of T3E and toxin deletions were pathogenicity tested on wood, leaves and fruits of sweet cherry (Prunus avium) and leaves of ornamental cherry (Prunus incisa). The toxins had a key role in disease development in fruits but were less important in leaves and wood. An effectorless mutant retained some pathogenicity to fruit but not wood or leaves. Striking redundancy was observed amongst effector groups. The CEL effectors have important roles during the early stages of leaf infection and possibly acted synergistically with toxins in all tissues. Deletion of separate groups of T3Es had more effect in P. incisa than in P. avium. Mixed inocula were used to complement the toxin mutations in trans and indicated that strain mixtures may be important in the field. Our results highlight the niche‐specific role of toxins in P. avium tissues and the complexity of effector redundancy in the pathogen Pss 9644.
与丁香假单胞菌（Pseudomonas syringae）物种复合体的其他系统群（PGs）相比，PG2 中的 P. syringae pv. syringae（Pss）菌株的 III 型效应物（T3Es）种类较少，但能产生多种植物毒素。樱桃病原体 Pss 9644 中的效应物根据其在樱桃菌株中的出现频率进行了分组：大多数 P. syringae 病原菌共有的保守效应物基因座（CEL）；PG2 常见的核心效应物；樱桃病原体常见的 PRUNUS 效应物集合；以及 FLEXIBLE T3Es 集合。Pss 9644 还含有用于生物合成毒素西林霉素、西林肽和西林霉素 A 的基因簇。在确认了毒力基因的表达后，在甜樱桃（Prunus avium）的木材、叶片和果实以及观赏樱桃（Prunus incisa）的叶片上对一系列 T3E 和毒素缺失的突变体进行了致病性测试。毒素在果实的病害发展中起关键作用，但在叶片和木质部的作用较小。无效应突变体对果实保留了一定的致病性，但对木质部或叶片则没有。在效应器组之间观察到了惊人的冗余。CEL 效应子在叶片感染的早期阶段具有重要作用，并可能与毒素在所有组织中协同作用。删除单独的 T3Es 组对 P. incisa 的影响大于对 P. avium 的影响。混合接种体用于补充反式毒素突变，表明菌株混合物在田间可能很重要。我们的研究结果突显了毒素在P. avium组织中的生态位特异性作用，以及病原体Pss 9644中效应器冗余的复杂性。
{"title":"Genetic dissection of the tissue‐specific roles of type III effectors and phytotoxins in the pathogenicity of Pseudomonas syringae pv. syringae to cherry","authors":"Andrea Vadillo‐Dieguez, Ziyue Zeng, John W. Mansfield, Nastasiya F. Grinberg, Samantha C. Lynn, Adam Gregg, John Connell, Richard J. Harrison, Robert W. Jackson, Michelle T. Hulin","doi":"10.1111/mpp.13451","DOIUrl":"https://doi.org/10.1111/mpp.13451","url":null,"abstract":"When compared with other phylogroups (PGs) of the <jats:italic>Pseudomonas syringae</jats:italic> species complex, <jats:italic>P. syringae</jats:italic> pv. s<jats:italic>yringae</jats:italic> (Pss) strains within PG2 have a reduced repertoire of type III effectors (T3Es) but produce several phytotoxins. Effectors within the cherry pathogen Pss 9644 were grouped based on their frequency in strains from <jats:italic>Prunus</jats:italic> as the conserved effector locus (CEL) common to most <jats:italic>P. syringae</jats:italic> pathogens; a core of effectors common to PG2; a set of PRUNUS effectors common to cherry pathogens; and a FLEXIBLE set of T3Es. Pss 9644 also contains gene clusters for biosynthesis of toxins syringomycin, syringopeptin and syringolin A. After confirmation of virulence gene expression, mutants with a sequential series of T3E and toxin deletions were pathogenicity tested on wood, leaves and fruits of sweet cherry (<jats:italic>Prunus avium</jats:italic>) and leaves of ornamental cherry (<jats:italic>Prunus incisa</jats:italic>). The toxins had a key role in disease development in fruits but were less important in leaves and wood. An effectorless mutant retained some pathogenicity to fruit but not wood or leaves. Striking redundancy was observed amongst effector groups. The CEL effectors have important roles during the early stages of leaf infection and possibly acted synergistically with toxins in all tissues. Deletion of separate groups of T3Es had more effect in <jats:italic>P. incisa</jats:italic> than in <jats:italic>P. avium</jats:italic>. Mixed inocula were used to complement the toxin mutations in trans and indicated that strain mixtures may be important in the field. Our results highlight the niche‐specific role of toxins in <jats:italic>P. avium</jats:italic> tissues and the complexity of effector redundancy in the pathogen Pss 9644.","PeriodicalId":18763,"journal":{"name":"Molecular plant pathology","volume":null,"pages":null},"PeriodicalIF":4.9,"publicationDate":"2024-04-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140589550","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}
Martin S. Mullett, Anna R. Harris, Bruno Scanu, Kris Van Poucke, Jared LeBoldus, Elizabeth Stamm, Tyler B. Bourret, Petya K. Christova, Jonás Oliva, Miguel A. Redondo, Venche Talgø, Tamara Corcobado, Ivan Milenković, Marília Horta Jung, Joan Webber, Kurt Heungens, Thomas Jung
Phytophthora pseudosyringae is a self‐fertile pathogen of woody plants, particularly associated with tree species from the genera Fagus, Notholithocarpus, Nothofagus and Quercus, which is found across Europe and in parts of North America and Chile. It can behave as a soil pathogen infecting roots and the stem collar region, as well as an aerial pathogen infecting leaves, twigs and stem barks, causing particular damage in the United Kingdom and western North America. The population structure, migration and potential outcrossing of a worldwide collection of isolates were investigated using genotyping‐by‐sequencing. Coalescent‐based migration analysis revealed that the North American population originated from Europe. Historical gene flow has occurred between the continents in both directions to some extent, yet contemporary migration is overwhelmingly from Europe to North America. Two broad population clusters dominate the global population of the pathogen, with a subgroup derived from one of the main clusters found only in western North America. Index of association and network analyses indicate an influential level of outcrossing has occurred in this preferentially inbreeding, homothallic oomycete. Outcrossing between the two main population clusters has created distinct subgroups of admixed individuals that are, however, less common than the main population clusters. Differences in life history traits between the two main population clusters should be further investigated together with virulence and host range tests to evaluate the risk each population poses to natural environments worldwide.
{"title":"Phylogeography, origin and population structure of the self‐fertile emerging plant pathogen Phytophthora pseudosyringae","authors":"Martin S. Mullett, Anna R. Harris, Bruno Scanu, Kris Van Poucke, Jared LeBoldus, Elizabeth Stamm, Tyler B. Bourret, Petya K. Christova, Jonás Oliva, Miguel A. Redondo, Venche Talgø, Tamara Corcobado, Ivan Milenković, Marília Horta Jung, Joan Webber, Kurt Heungens, Thomas Jung","doi":"10.1111/mpp.13450","DOIUrl":"https://doi.org/10.1111/mpp.13450","url":null,"abstract":"<jats:italic>Phytophthora pseudosyringae</jats:italic> is a self‐fertile pathogen of woody plants, particularly associated with tree species from the genera <jats:italic>Fagus</jats:italic>, <jats:italic>Notholithocarpus</jats:italic>, <jats:italic>Nothofagus</jats:italic> and <jats:italic>Quercus</jats:italic>, which is found across Europe and in parts of North America and Chile. It can behave as a soil pathogen infecting roots and the stem collar region, as well as an aerial pathogen infecting leaves, twigs and stem barks, causing particular damage in the United Kingdom and western North America. The population structure, migration and potential outcrossing of a worldwide collection of isolates were investigated using genotyping‐by‐sequencing. Coalescent‐based migration analysis revealed that the North American population originated from Europe. Historical gene flow has occurred between the continents in both directions to some extent, yet contemporary migration is overwhelmingly from Europe to North America. Two broad population clusters dominate the global population of the pathogen, with a subgroup derived from one of the main clusters found only in western North America. Index of association and network analyses indicate an influential level of outcrossing has occurred in this preferentially inbreeding, homothallic oomycete. Outcrossing between the two main population clusters has created distinct subgroups of admixed individuals that are, however, less common than the main population clusters. Differences in life history traits between the two main population clusters should be further investigated together with virulence and host range tests to evaluate the risk each population poses to natural environments worldwide.","PeriodicalId":18763,"journal":{"name":"Molecular plant pathology","volume":null,"pages":null},"PeriodicalIF":4.9,"publicationDate":"2024-04-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140590009","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}
扫码关注我们
求助内容：
应助结果提醒方式：
京公网安备 11010802042870号