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{"title"=>"The RhoGAP SPIN6 Associates with SPL11 and OsRac1 and Negatively Regulates Programmed Cell Death and Innate Immunity in Rice", "type"=>"journal", "authors"=>[{"first_name"=>"Jinling", "last_name"=>"Liu", "scopus_author_id"=>"21739933400"}, {"first_name"=>"Chan Ho", "last_name"=>"Park", "scopus_author_id"=>"57198830087"}, {"first_name"=>"Feng", "last_name"=>"He", "scopus_author_id"=>"57199987000"}, {"first_name"=>"Minoru", "last_name"=>"Nagano", "scopus_author_id"=>"16233976900"}, {"first_name"=>"Mo", "last_name"=>"Wang", "scopus_author_id"=>"56480888200"}, {"first_name"=>"Maria", "last_name"=>"Bellizzi", "scopus_author_id"=>"36776444000"}, {"first_name"=>"Kai", "last_name"=>"Zhang", "scopus_author_id"=>"56542113400"}, {"first_name"=>"Xiaoshan", "last_name"=>"Zeng", "scopus_author_id"=>"57197046192"}, {"first_name"=>"Wende", "last_name"=>"Liu", "scopus_author_id"=>"55353457100"}, {"first_name"=>"Yuese", "last_name"=>"Ning", "scopus_author_id"=>"37665700600"}, {"first_name"=>"Yoji", "last_name"=>"Kawano", "scopus_author_id"=>"7201460639"}, {"first_name"=>"Guo Liang", "last_name"=>"Wang", "scopus_author_id"=>"7407144581"}], "year"=>2015, "source"=>"PLoS Pathogens", "identifiers"=>{"sgr"=>"84924363504", "doi"=>"10.1371/journal.ppat.1004629", "pui"=>"602902206", "pmid"=>"25658451", "scopus"=>"2-s2.0-84924363504", "issn"=>"15537374", "isbn"=>"1553-7374 (Electronic)\\r1553-7366 (Linking)"}, "id"=>"15c01f0e-9778-3942-8380-bc4189360a2e", "abstract"=>"The ubiquitin proteasome system in plants plays important roles in plant-microbe interactions and in immune responses to pathogens. We previously demonstrated that the rice U-box E3 ligase SPL11 and its Arabidopsis ortholog PUB13 negatively regulate programmed cell death (PCD) and defense response. However, the components involved in the SPL11/PUB13-mediated PCD and immune signaling pathway remain unknown. In this study, we report that SPL11-interacting Protein 6 (SPIN6) is a Rho GTPase-activating protein (RhoGAP) that interacts with SPL11 in vitro and in vivo. SPL11 ubiquitinates SPIN6 in vitro and degrades SPIN6 in vivo via the 26S proteasome-dependent pathway. Both RNAi silencing in transgenic rice and knockout of Spin6 in a T-DNA insertion mutant lead to PCD and increased resistance to the rice blast pathogen Magnaporthe oryzae and the bacterial blight pathogen Xanthomonas oryzae pv. oryzae. The levels of reactive oxygen species and defense-related gene expression are significantly elevated in both the Spin6 RNAi and mutant plants. Strikingly, SPIN6 interacts with the small GTPase OsRac1, catalyze the GTP-bound OsRac1 into the GDP-bound state in vitro and has GAP activity towards OsRac1 in rice cells. Together, our results demonstrate that the RhoGAP SPIN6 acts as a linkage between a U-box E3 ligase-mediated ubiquitination pathway and a small GTPase-associated defensome system for plant immunity.", "link"=>"http://www.mendeley.com/research/rhogap-spin6-associates-spl11-osrac1-negatively-regulates-programmed-cell-death-innate-immunity-rice", "reader_count"=>36, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>4, "Student > Doctoral Student"=>3, "Researcher"=>4, "Student > Ph. D. Student"=>12, "Student > Postgraduate"=>3, "Other"=>1, "Student > Master"=>4, "Student > Bachelor"=>3, "Lecturer"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>4, "Student > Doctoral Student"=>3, "Researcher"=>4, "Student > Ph. D. Student"=>12, "Student > Postgraduate"=>3, "Other"=>1, "Student > Master"=>4, "Student > Bachelor"=>3, "Lecturer"=>1}, "reader_count_by_subject_area"=>{"Engineering"=>1, "Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>3, "Agricultural and Biological Sciences"=>29, "Medicine and Dentistry"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>29}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Unspecified"=>{"Unspecified"=>2}}, "reader_count_by_country"=>{"France"=>1, "Germany"=>1}, "group_count"=>1}

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• http://doi.org/10.3389/fpls.2020.00716
• http://doi.org/10.1093/jxb/erx411
• http://doi.org/10.1186/s12864-019-5696-z
• http://doi.org/10.1111/mpp.12271
• http://doi.org/10.1093/jxb/erx136
• http://doi.org/10.1016/j.ygeno.2019.06.027
• http://doi.org/10.1111/jipb.12426
• http://doi.org/10.1002/cppb.20026
• http://doi.org/10.3390/cells9092016
• http://doi.org/10.1016/j.rsci.2020.05.004
• http://doi.org/10.1016/j.plantsci.2019.04.004
• http://doi.org/10.1371/journal.ppat.1005529
• http://doi.org/10.1038/srep23805
• http://doi.org/10.1111/mpp.12521
• http://doi.org/10.1007/s11738-019-2856-3
• http://doi.org/10.3389/fpls.2017.00016
• http://doi.org/10.1016/j.chom.2018.03.003
• http://doi.org/10.1016/j.chom.2016.10.023
• http://doi.org/10.1186/s12284-018-0220-7
• http://doi.org/10.1080/15592324.2015.1039212
• http://doi.org/10.1016/j.tplants.2020.08.001
• http://doi.org/10.1186/s12284-017-0153-6
• http://doi.org/10.1016/j.plaphy.2020.07.016
• http://doi.org/10.3390/ijms21041369
• http://doi.org/10.1093/pcp/pcv063
• http://doi.org/10.1080/17429145.2018.1528512
• http://doi.org/10.1186/s12870-020-2298-5
• http://doi.org/10.1016/j.molp.2016.06.015
• http://doi.org/10.1016/j.molp.2020.02.010
• http://doi.org/10.1186/s12870-019-2175-2
• http://doi.org/10.1146/annurev-arplant-010720-022215
• http://doi.org/10.3390/ijms20051191
• http://doi.org/10.1016/j.plantsci.2019.110182
• http://doi.org/10.1016/j.bbrc.2015.07.030
• http://doi.org/10.1371/journal.pgen.1006311
• http://doi.org/10.1038/s41598-017-03585-0
• http://doi.org/10.3389/fpls.2018.00615
• http://doi.org/10.1007/s11103-019-00933-8
• http://doi.org/10.1111/nph.14818
• http://doi.org/10.1038/s41467-018-04369-4
• http://doi.org/10.1016/j.xplc.2020.100020
• http://doi.org/10.1021/acs.jafc.9b07426
• http://doi.org/10.1093/jxb/eraa450
• http://doi.org/10.1007/s13205-016-0400-3

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• {"id"=>"563996863380979713", "text"=>"Our collaborative research was published in PLOS Pathogens. \nThis paper explores new \"OsRac1 world.\"\n\nhttp://t.co/nPINNKhGkg", "created_at"=>"2015-02-07T09:45:05Z", "user"=>"YojiKAWANO", "user_name"=>"Yoji Kawano", "user_profile_image"=>"http://pbs.twimg.com/profile_images/562230643749179392/Zv49_ldY_normal.jpeg"}
• {"id"=>"650067763440934912", "text"=>"#EditorPick: Function of RhoGAP SPIN6 in rice immunity http://t.co/fhqpep1EG2 #ppathturns10 http://t.co/aDeutvLcIc", "created_at"=>"2015-10-02T22:00:07Z", "user"=>"PLOSPathogens", "user_name"=>"PLOS Pathogens", "user_profile_image"=>"http://pbs.twimg.com/profile_images/459394339945197568/BuJQyL0D_normal.jpeg"}
• {"id"=>"650073451269619712", "text"=>"RT @PLOSPathogens: #EditorPick: Function of RhoGAP SPIN6 in rice immunity http://t.co/fhqpep1EG2 #ppathturns10 http://t.co/aDeutvLcIc", "created_at"=>"2015-10-02T22:22:43Z", "user"=>"ClaireDrurey", "user_name"=>"Claire Drurey", "user_profile_image"=>"http://pbs.twimg.com/profile_images/646725596358250497/Gf4WcEuQ_normal.jpg"}

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• {"files"=>["https://ndownloader.figshare.com/files/1884369", "https://ndownloader.figshare.com/files/1884370"], "description"=>"<div><p>The ubiquitin proteasome system in plants plays important roles in plant-microbe interactions and in immune responses to pathogens. We previously demonstrated that the rice U-box E3 ligase SPL11 and its <i>Arabidopsis</i> ortholog PUB13 negatively regulate programmed cell death (PCD) and defense response. However, the components involved in the SPL11/PUB13-mediated PCD and immune signaling pathway remain unknown. In this study, we report that SPL11-interacting Protein 6 (SPIN6) is a Rho GTPase-activating protein (RhoGAP) that interacts with SPL11 <i>in vitro</i> and <i>in vivo</i>. SPL11 ubiquitinates SPIN6 <i>in vitro</i> and degrades SPIN6 <i>in vivo</i> via the 26S proteasome-dependent pathway. Both RNAi silencing in transgenic rice and knockout of <i>Spin6</i> in a T-DNA insertion mutant lead to PCD and increased resistance to the rice blast pathogen <i>Magnaporthe oryzae</i> and the bacterial blight pathogen <i>Xanthomonas oryzae</i> pv. <i>oryzae</i>. The levels of reactive oxygen species and defense-related gene expression are significantly elevated in both the <i>Spin6</i> RNAi and mutant plants. Strikingly, SPIN6 interacts with the small GTPase OsRac1, catalyze the GTP-bound OsRac1 into the GDP-bound state <i>in vitro</i> and has GAP activity towards OsRac1 in rice cells. Together, our results demonstrate that the RhoGAP SPIN6 acts as a linkage between a U-box E3 ligase-mediated ubiquitination pathway and a small GTPase-associated defensome system for plant immunity.</p></div>", "links"=>[], "tags"=>["ubiquitin proteasome system", "RhoGAP SPIN 6 acts", "rice blast pathogen Magnaporthe oryzae", "degrades SPIN 6", "pcd", "OsRac 1", "Reactive oxygen species", "SPL 11 ubiquitinates SPIN 6", "Arabidopsis ortholog PUB 13", "RhoGAP SPIN 6 Associates", "Negatively Regulates Programmed Cell Death", "blight pathogen Xanthomonas oryzae pv", "SPL 11", "Spin 6 RNAi", "pathway"], "article_id"=>1303232, "categories"=>["Biological Sciences"], "users"=>["Jinling Liu", "Chan Ho Park", "Feng He", "Minoru Nagano", "Mo Wang", "Maria Bellizzi", "Kai Zhang", "Xiaoshan Zeng", "Wende Liu", "Yuese Ning", "Yoji Kawano", "Guo-Liang Wang"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1004629.s001", "https://dx.doi.org/10.1371/journal.ppat.1004629.s002"], "stats"=>{"downloads"=>11, "page_views"=>59, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_RhoGAP_SPIN6_Associates_with_SPL11_and_OsRac1_and_Negatively_Regulates_Programmed_Cell_Death_and_Innate_Immunity_in_Rice_/1303232", "title"=>"The RhoGAP SPIN6 Associates with SPL11 and OsRac1 and Negatively Regulates Programmed Cell Death and Innate Immunity in Rice", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2015-02-06 04:49:56"}
• {"files"=>["https://ndownloader.figshare.com/files/1884358"], "description"=>"<p><b>(A)</b> SPIN6 interacts with OsRac1 in yeast. The Mav203 yeast transformant diluted 10, 100, or 1000 times was plated on synthetic dextrose medium without Trp, Leu, or His (SD-LTH) and with 0 mM or 40 mM 3-amino-1,2,4,- triazole (3AT). EV-Empty Vector (<b>B</b>) The Co-IP assay of SPIN6 and OsRac1 in <i>N</i>. <i>benthamiana</i>. The <i>GFP</i>:<i>Spin6</i> and <i>Myc</i>:<i>OsRac1</i> plasmids were used for co-infiltration in <i>N</i>. <i>benthamiana</i>. (<b>C</b>) BiFC assay of SPIN6 and OsRac1 in <i>N</i>. <i>benthamiana</i>. The <i>Spin6</i>:<i>CeYFP</i> and <i>NeYFP</i>:<i>OsRac1</i> plasmids were used for co-infiltration. (<b>D</b>) <i>In vitro</i> GAP activity assay of SPIN6. SPIN6 refers to GST-fused SPIN6 protein. OsRac1 refers to MBP-fused OsRac1 protein. GST and MBP are controls. Values are means and standard errors of three replications.</p>", "links"=>[], "tags"=>["ubiquitin proteasome system", "RhoGAP SPIN 6 acts", "rice blast pathogen Magnaporthe oryzae", "degrades SPIN 6", "pcd", "OsRac 1", "Reactive oxygen species", "SPL 11 ubiquitinates SPIN 6", "Arabidopsis ortholog PUB 13", "RhoGAP SPIN 6 Associates", "Negatively Regulates Programmed Cell Death", "blight pathogen Xanthomonas oryzae pv", "SPL 11", "Spin 6 RNAi", "pathway"], "article_id"=>1303221, "categories"=>["Biological Sciences"], "users"=>["Jinling Liu", "Chan Ho Park", "Feng He", "Minoru Nagano", "Mo Wang", "Maria Bellizzi", "Kai Zhang", "Xiaoshan Zeng", "Wende Liu", "Yuese Ning", "Yoji Kawano", "Guo-Liang Wang"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004629.g005", "stats"=>{"downloads"=>1, "page_views"=>22, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_SPIN6_interacts_with_OsRac1_in_vitro_and_in_vivo_and_catalyzes_OsRac1_hydrolysis_in_vitro_/1303221", "title"=>"SPIN6 interacts with OsRac1 <i>in vitro</i> and <i>in vivo</i>, and catalyzes OsRac1 hydrolysis <i>in vitro</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-02-06 04:49:56"}
• {"files"=>["https://ndownloader.figshare.com/files/1884357"], "description"=>"<p>(A), (B) ROS accumulation dynamics of the <i>Spin6</i> RNAi lines (16–2 and 22–2) and the wild type NPB after the chitin or flg22 treatment. Water served as the control. (C)-(F) The relative expression level of defense-related genes <i>PBZ1</i> (C, F), <i>PAL</i> (D), and <i>PR1a</i> (E) in the <i>Spin6</i> RNAi line 22–2 and NPB after treatment with chitin and flg22. Values are means and standard errors of three replications. Significance was determined level at *P<0.05 and **P<0.01 (n = 3) with a <i>t</i>-test.</p>", "links"=>[], "tags"=>["ubiquitin proteasome system", "RhoGAP SPIN 6 acts", "rice blast pathogen Magnaporthe oryzae", "degrades SPIN 6", "pcd", "OsRac 1", "Reactive oxygen species", "SPL 11 ubiquitinates SPIN 6", "Arabidopsis ortholog PUB 13", "RhoGAP SPIN 6 Associates", "Negatively Regulates Programmed Cell Death", "blight pathogen Xanthomonas oryzae pv", "SPL 11", "Spin 6 RNAi", "pathway"], "article_id"=>1303220, "categories"=>["Biological Sciences"], "users"=>["Jinling Liu", "Chan Ho Park", "Feng He", "Minoru Nagano", "Mo Wang", "Maria Bellizzi", "Kai Zhang", "Xiaoshan Zeng", "Wende Liu", "Yuese Ning", "Yoji Kawano", "Guo-Liang Wang"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004629.g004", "stats"=>{"downloads"=>5, "page_views"=>24, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_ROS_generation_and_defense_related_gene_expression_of_the_Spin6_RNAi_lines_after_chitin_and_flg22_treatments_/1303220", "title"=>"ROS generation and defense-related gene expression of the <i>Spin6</i> RNAi lines after chitin and flg22 treatments.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-02-06 04:49:56"}
• {"files"=>["https://ndownloader.figshare.com/files/1884354"], "description"=>"<p><b>(A)</b><i>In vitro</i> ubiquitination of SPIN6 by SPL11. The ubiquitination of GST:SPIN6 by MBP:SPL11 and the E3 ligase activity of SPL11 were detected by immunoblot with the anti-GST antibody and anti-ubiquitin antibody, respectively, in the presence of Arabidopsis E1 (At5g06460), E2 (AtUBC10, At5g53300) and ubiquitin. MBP and mutated SPL11 without E3 ligase activity (SPL11m) fused with MBP were used as the negative controls. Immunoblot with anti-MBP antibody was conducted as a loading control. <b>(B)</b> Degradation of SPIN6 promoted by SPL11 in <i>N</i>. <i>benthamiana</i>. Either SPL11:Myc or SPL11m:Myc was co-expressed with GFP:SPIN6 by agro-infiltration in <i>N</i>. <i>benthamiana</i>. Tissues were harvested at 3 days after the infiltration. MG132 (50μM), an inhibitor of 26S proteasome system, was infiltrated at 18 h before sampling with DMSO (-) as a control. RFP was expressed as an internal control.</p>", "links"=>[], "tags"=>["ubiquitin proteasome system", "RhoGAP SPIN 6 acts", "rice blast pathogen Magnaporthe oryzae", "degrades SPIN 6", "pcd", "OsRac 1", "Reactive oxygen species", "SPL 11 ubiquitinates SPIN 6", "Arabidopsis ortholog PUB 13", "RhoGAP SPIN 6 Associates", "Negatively Regulates Programmed Cell Death", "blight pathogen Xanthomonas oryzae pv", "SPL 11", "Spin 6 RNAi", "pathway"], "article_id"=>1303217, "categories"=>["Biological Sciences"], "users"=>["Jinling Liu", "Chan Ho Park", "Feng He", "Minoru Nagano", "Mo Wang", "Maria Bellizzi", "Kai Zhang", "Xiaoshan Zeng", "Wende Liu", "Yuese Ning", "Yoji Kawano", "Guo-Liang Wang"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004629.g002", "stats"=>{"downloads"=>3, "page_views"=>88, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Ubiquitination_of_SPIN6_in_vitro_and_degradation_of_SPIN6_in_N_benthamiana_by_SPL11_/1303217", "title"=>"Ubiquitination of SPIN6 <i>in vitro</i> and degradation of SPIN6 in <i>N</i>. <i>benthamiana</i> by SPL11.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-02-06 04:49:56"}
• {"files"=>["https://ndownloader.figshare.com/files/1884352"], "description"=>"<p>(A) The protein structure of SPIN6, SPIN6.2 and SPIN6.3. The position of the Pleckstrin Homology (PH) domain (34–142), RhoGAP domain (192–383), and coiled coil (CC) motif (583–699) are indicated. (B) SPIN6 interacts with SPL11 in yeast. SPL11 represents the full-length SPL11; ARM is the ARM domain of SPL11; and SPL11m is the SPL11 mutant with a three amino-acid deletion at C314P315T316 in the U-box domain, resulting in a loss-of-function of E3 ligase activity (Zeng et al., 2004). After they were diluted 10, 100, and 1000 times with sterilized-distilled H₂O, the Mav203 yeast transformants were plated on synthetic dextrose medium without Trp, Leu, and His amino acids (SD-LTH) and with 0 mM or 40 mM 3-amino-1,2,4,-triazole (3AT), separately. (C) SPIN6 binds to SPL11 in the GST pull-down assay. His:SPIN6 and GST:SPL11, GST:ARM of SPL11 were used in the assay. (D) SPIN6 interacts with SPL11 in <i>N</i>. <i>benthamiana</i> in BiFC assay. SPIN6 was fused with the C-terminal of eYFP to make SPIN6:CeYFP. SPL11, ARM, and SPL11m were fused with the N-terminal eYFP to make NeYFP:SPL11, NeYFP:ARM, and NeYFP:SPL11m, respectively.</p>", "links"=>[], "tags"=>["ubiquitin proteasome system", "RhoGAP SPIN 6 acts", "rice blast pathogen Magnaporthe oryzae", "degrades SPIN 6", "pcd", "OsRac 1", "Reactive oxygen species", "SPL 11 ubiquitinates SPIN 6", "Arabidopsis ortholog PUB 13", "RhoGAP SPIN 6 Associates", "Negatively Regulates Programmed Cell Death", "blight pathogen Xanthomonas oryzae pv", "SPL 11", "Spin 6 RNAi", "pathway"], "article_id"=>1303214, "categories"=>["Biological Sciences"], "users"=>["Jinling Liu", "Chan Ho Park", "Feng He", "Minoru Nagano", "Mo Wang", "Maria Bellizzi", "Kai Zhang", "Xiaoshan Zeng", "Wende Liu", "Yuese Ning", "Yoji Kawano", "Guo-Liang Wang"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004629.g001", "stats"=>{"downloads"=>0, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_SPIN6_is_a_Rho_GTPase_activating_protein_RhoGAP_and_interacts_with_SPL11_in_vitro_and_in_vivo_/1303214", "title"=>"SPIN6 is a Rho GTPase-activating protein (RhoGAP) and interacts with SPL11 <i>in vitro</i> and <i>in vivo</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-02-06 04:49:56"}
• {"files"=>["https://ndownloader.figshare.com/files/1884360"], "description"=>"<p><b>(A)</b> Images of confocal laser-scanning micrographs of rice protoplasts expressing the <i>Raichu-OsRac1</i> constructs. Rice protoplasts were co-transfected with constructs expressing <i>Raichu-OsRac1</i> and individual constructs. The FRET images are shown in intensity-modulated display mode, which associates color hue with emission ratio values and the intensity of each hue with the brightness of the source image. <b>(B)</b> Normalized emission ratio of cFRET/CFP. Double asterisks indicate significant differences (P < 0.01). Error bars indicate SE (N≧30).</p>", "links"=>[], "tags"=>["ubiquitin proteasome system", "RhoGAP SPIN 6 acts", "rice blast pathogen Magnaporthe oryzae", "degrades SPIN 6", "pcd", "OsRac 1", "Reactive oxygen species", "SPL 11 ubiquitinates SPIN 6", "Arabidopsis ortholog PUB 13", "RhoGAP SPIN 6 Associates", "Negatively Regulates Programmed Cell Death", "blight pathogen Xanthomonas oryzae pv", "SPL 11", "Spin 6 RNAi", "pathway"], "article_id"=>1303223, "categories"=>["Biological Sciences"], "users"=>["Jinling Liu", "Chan Ho Park", "Feng He", "Minoru Nagano", "Mo Wang", "Maria Bellizzi", "Kai Zhang", "Xiaoshan Zeng", "Wende Liu", "Yuese Ning", "Yoji Kawano", "Guo-Liang Wang"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004629.g006", "stats"=>{"downloads"=>2, "page_views"=>32, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Analysis_of_RhoGAP_activity_of_SPIN6_toward_OsRac1_in_rice_protoplasts_/1303223", "title"=>"Analysis of RhoGAP activity of SPIN6 toward OsRac1 in rice protoplasts.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-02-06 04:49:56"}
• {"files"=>["https://ndownloader.figshare.com/files/1884361"], "description"=>"<p>By associating with RhoGAP protein SPIN6, the E3 ligase SPL11 negatively modulates OsRac1-mediated immune signaling. SPIN6 is ubiquitinated and degraded by the E3 ligase SPL11 via the 26S proteasome system. From the GDP state to the GTP state, OsRac1 is activated by the GEF protein OsRacGEF1, then associates with the NADPH oxidases OsRBOH/CDPK complex to trigger ROS generation. The activation of OsRac1 requires the phosphorylation by the kinase protein OsCERK1, a co-receptor of the PAMP effector chitin. OsCERK1 dimerizes with LysM protein CEBiP1 to perceive chitin signaling. The interaction between SPIN6 and OsRac1 may lead to the change of OsRac1 from the GTP state to the GDP state, which reduces the active form of OsRac1 in rice cells. Mutation in the <i>Spin6</i> gene may cause accumulation of ROS and PR proteins, i.e., PR1a, PR5 and PBZ1, that results in plant cell death and immunity.</p>", "links"=>[], "tags"=>["ubiquitin proteasome system", "RhoGAP SPIN 6 acts", "rice blast pathogen Magnaporthe oryzae", "degrades SPIN 6", "pcd", "OsRac 1", "Reactive oxygen species", "SPL 11 ubiquitinates SPIN 6", "Arabidopsis ortholog PUB 13", "RhoGAP SPIN 6 Associates", "Negatively Regulates Programmed Cell Death", "blight pathogen Xanthomonas oryzae pv", "SPL 11", "Spin 6 RNAi", "pathway"], "article_id"=>1303224, "categories"=>["Biological Sciences"], "users"=>["Jinling Liu", "Chan Ho Park", "Feng He", "Minoru Nagano", "Mo Wang", "Maria Bellizzi", "Kai Zhang", "Xiaoshan Zeng", "Wende Liu", "Yuese Ning", "Yoji Kawano", "Guo-Liang Wang"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004629.g007", "stats"=>{"downloads"=>0, "page_views"=>74, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Proposed_working_model_of_the_relationship_between_SPL11_SPIN6_and_OsRac1_/1303224", "title"=>"Proposed working model of the relationship between SPL11, SPIN6, and OsRac1.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-02-06 04:49:56"}
• {"files"=>["https://ndownloader.figshare.com/files/1884356"], "description"=>"<p><b>(A)</b> Cell death phenotypes of the <i>Spin6</i> RNAi silencing lines. Japonica rice Nipponbare (NPB) is the wild type, and 16–2 and 22–2 are <i>Spin6</i> RNAi lines. <b>(B)</b> The relative expression level of <i>Spin6</i> and <i>Spl11</i> in the wild type and <i>Spin6</i> RNAi lines as determined by real-time quantitative PCR. The data were normalized with ubiquitin. <b>(C)</b> Lesion-size of the <i>Spin6</i> RNAi lines and the wild type plants inoculated with <i>M</i>. <i>oryzae</i> isolate RO1–1. <b>(D)</b> Number of <i>M</i>. <i>oryzae</i> spores produced by lesions on the <i>Spin6</i> RNAi lines and the wild type. <b>(E)</b> Relative <i>M</i>. <i>oryzae</i> biomass in lesions in the <i>Spin6</i> RNAi lines and the wild type. <b>(F)</b> Lesion-size of the <i>Spin6</i> RNAi lines and the wild type infected with <i>Xoo</i> strain race 6. <b>(G)</b> Bacterial blight lesion length in the <i>Spin6</i> RNAi lines and the wild type. Values are means and standard errors of three replications. Significance was determined at *P<0.05 and **P<0.01 (n≥3) with a <i>t</i>-test.</p>", "links"=>[], "tags"=>["ubiquitin proteasome system", "RhoGAP SPIN 6 acts", "rice blast pathogen Magnaporthe oryzae", "degrades SPIN 6", "pcd", "OsRac 1", "Reactive oxygen species", "SPL 11 ubiquitinates SPIN 6", "Arabidopsis ortholog PUB 13", "RhoGAP SPIN 6 Associates", "Negatively Regulates Programmed Cell Death", "blight pathogen Xanthomonas oryzae pv", "SPL 11", "Spin 6 RNAi", "pathway"], "article_id"=>1303219, "categories"=>["Biological Sciences"], "users"=>["Jinling Liu", "Chan Ho Park", "Feng He", "Minoru Nagano", "Mo Wang", "Maria Bellizzi", "Kai Zhang", "Xiaoshan Zeng", "Wende Liu", "Yuese Ning", "Yoji Kawano", "Guo-Liang Wang"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004629.g003", "stats"=>{"downloads"=>3, "page_views"=>112, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Knock_down_of_Spin6_results_in_cell_death_phenotypes_and_enhanced_resistance_to_the_rice_blast_pathogen_M_oryzae_and_the_bacterial_blight_pathogen_Xoo_in_rice_/1303219", "title"=>"Knock-down of <i>Spin6</i> results in cell death phenotypes and enhanced resistance to the rice blast pathogen <i>M</i>. <i>oryzae</i> and the bacterial blight pathogen <i>Xoo</i> in rice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-02-06 04:49:56"}

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• {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"12"}
• {"unique-ip"=>"9", "full-text"=>"9", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"1"}
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• {"unique-ip"=>"14", "full-text"=>"13", "pdf"=>"10", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"3"}
• {"unique-ip"=>"13", "full-text"=>"14", "pdf"=>"7", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"1"}
• {"unique-ip"=>"8", "full-text"=>"9", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"5"}
• {"unique-ip"=>"14", "full-text"=>"20", "pdf"=>"11", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2018", "month"=>"4"}
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• {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"6", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
• {"unique-ip"=>"14", "full-text"=>"14", "pdf"=>"6", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
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• {"unique-ip"=>"11", "full-text"=>"10", "pdf"=>"6", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
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• {"unique-ip"=>"14", "full-text"=>"12", "pdf"=>"8", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"12", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
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• {"unique-ip"=>"11", "full-text"=>"14", "pdf"=>"6", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
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• {"unique-ip"=>"7", "full-text"=>"3", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"4", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}
• {"unique-ip"=>"5", "full-text"=>"3", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"8", "cited-by"=>"0", "year"=>"2020", "month"=>"2"}
• {"unique-ip"=>"15", "full-text"=>"21", "pdf"=>"15", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"4", "cited-by"=>"0", "year"=>"2020", "month"=>"3"}
• {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"4"}
• {"unique-ip"=>"12", "full-text"=>"10", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"7", "cited-by"=>"0", "year"=>"2020", "month"=>"5"}
• {"unique-ip"=>"10", "full-text"=>"9", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2020", "month"=>"6"}
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• {"unique-ip"=>"7", "full-text"=>"8", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"8"}
• {"unique-ip"=>"6", "full-text"=>"8", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2020", "month"=>"9"}
• {"unique-ip"=>"9", "full-text"=>"7", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"10"}
• {"unique-ip"=>"8", "full-text"=>"10", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2020", "month"=>"11"}
• {"unique-ip"=>"9", "full-text"=>"11", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"12"}

Relative Metric

{"start_date"=>"2015-01-01T00:00:00Z", "end_date"=>"2015-12-31T00:00:00Z", "subject_areas"=>[]}

F1000Prime