Characterization of a Ran gene from Puccinia striiformis f. sp. tritici involved in fungal growth and anti-cell death
Identifieur interne : 000747 ( Ncbi/Merge ); précédent : 000746; suivant : 000748Characterization of a Ran gene from Puccinia striiformis f. sp. tritici involved in fungal growth and anti-cell death
Auteurs : Yulin Cheng [République populaire de Chine] ; Juanni Yao [République populaire de Chine] ; Yanru Zhang [République populaire de Chine] ; Shumin Li [République populaire de Chine] ; Zhensheng Kang [République populaire de Chine]Source :
- Scientific Reports [ 2045-2322 ] ; 2016.
Abstract
Ran, an important family of small GTP-binding proteins, has been shown to regulate a variety of important cellular processes in many eukaryotes. However, little is known about Ran function in pathogenic fungi. In this study, we report the identification and functional analysis of a Ran gene (designated
Url:
DOI: 10.1038/srep35248
PubMed: 27734916
PubMed Central: 5062253
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Characterization of a Ran gene from <italic>Puccinia striiformis</italic> f. sp. <italic>tritici</italic> involved in fungal growth and anti-cell death</title><author><name sortKey="Cheng, Yulin" sort="Cheng, Yulin" uniqKey="Cheng Y" first="Yulin" last="Cheng">Yulin Cheng</name><affiliation wicri:level="1"><nlm:aff id="a1"><institution>State Key Laboratory of Crop Stress Biology for Arid Areas, College of Life Sciences, Northwest A&F University</institution>, Yangling 712100, Shaanxi,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Yao, Juanni" sort="Yao, Juanni" uniqKey="Yao J" first="Juanni" last="Yao">Juanni Yao</name><affiliation wicri:level="1"><nlm:aff id="a2"><institution>State Key Laboratory of Crop Stress Biology for Arid Areas, College of Plant Protection, Northwest A&F University</institution>, Yangling 712100, Shaanxi,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Zhang, Yanru" sort="Zhang, Yanru" uniqKey="Zhang Y" first="Yanru" last="Zhang">Yanru Zhang</name><affiliation wicri:level="1"><nlm:aff id="a2"><institution>State Key Laboratory of Crop Stress Biology for Arid Areas, College of Plant Protection, Northwest A&F University</institution>, Yangling 712100, Shaanxi,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Li, Shumin" sort="Li, Shumin" uniqKey="Li S" first="Shumin" last="Li">Shumin Li</name><affiliation wicri:level="1"><nlm:aff id="a2"><institution>State Key Laboratory of Crop Stress Biology for Arid Areas, College of Plant Protection, Northwest A&F University</institution>, Yangling 712100, Shaanxi,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Kang, Zhensheng" sort="Kang, Zhensheng" uniqKey="Kang Z" first="Zhensheng" last="Kang">Zhensheng Kang</name><affiliation wicri:level="1"><nlm:aff id="a2"><institution>State Key Laboratory of Crop Stress Biology for Arid Areas, College of Plant Protection, Northwest A&F University</institution>, Yangling 712100, Shaanxi,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">27734916</idno><idno type="pmc">5062253</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5062253</idno><idno type="RBID">PMC:5062253</idno><idno type="doi">10.1038/srep35248</idno><date when="2016">2016</date><idno type="wicri:Area/Pmc/Corpus">000093</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000093</idno><idno type="wicri:Area/Pmc/Curation">000093</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000093</idno><idno type="wicri:Area/Pmc/Checkpoint">000635</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">000635</idno><idno type="wicri:Area/Ncbi/Merge">000747</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Characterization of a Ran gene from <italic>Puccinia striiformis</italic> f. sp. <italic>tritici</italic> involved in fungal growth and anti-cell death</title><author><name sortKey="Cheng, Yulin" sort="Cheng, Yulin" uniqKey="Cheng Y" first="Yulin" last="Cheng">Yulin Cheng</name><affiliation wicri:level="1"><nlm:aff id="a1"><institution>State Key Laboratory of Crop Stress Biology for Arid Areas, College of Life Sciences, Northwest A&F University</institution>, Yangling 712100, Shaanxi,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Yao, Juanni" sort="Yao, Juanni" uniqKey="Yao J" first="Juanni" last="Yao">Juanni Yao</name><affiliation wicri:level="1"><nlm:aff id="a2"><institution>State Key Laboratory of Crop Stress Biology for Arid Areas, College of Plant Protection, Northwest A&F University</institution>, Yangling 712100, Shaanxi,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Zhang, Yanru" sort="Zhang, Yanru" uniqKey="Zhang Y" first="Yanru" last="Zhang">Yanru Zhang</name><affiliation wicri:level="1"><nlm:aff id="a2"><institution>State Key Laboratory of Crop Stress Biology for Arid Areas, College of Plant Protection, Northwest A&F University</institution>, Yangling 712100, Shaanxi,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Li, Shumin" sort="Li, Shumin" uniqKey="Li S" first="Shumin" last="Li">Shumin Li</name><affiliation wicri:level="1"><nlm:aff id="a2"><institution>State Key Laboratory of Crop Stress Biology for Arid Areas, College of Plant Protection, Northwest A&F University</institution>, Yangling 712100, Shaanxi,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Kang, Zhensheng" sort="Kang, Zhensheng" uniqKey="Kang Z" first="Zhensheng" last="Kang">Zhensheng Kang</name><affiliation wicri:level="1"><nlm:aff id="a2"><institution>State Key Laboratory of Crop Stress Biology for Arid Areas, College of Plant Protection, Northwest A&F University</institution>, Yangling 712100, Shaanxi,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author></analytic><series><title level="j">Scientific Reports</title><idno type="eISSN">2045-2322</idno><imprint><date when="2016">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Ran, an important family of small GTP-binding proteins, has been shown to regulate a variety of important cellular processes in many eukaryotes. However, little is known about Ran function in pathogenic fungi. In this study, we report the identification and functional analysis of a Ran gene (designated <italic>PsRan</italic>) from <italic>Puccinia striiformis</italic> f. sp. <italic>tritici (Pst</italic>), an important fungal pathogen affecting wheat production worldwide. The PsRan protein contains all conserved domains of Ran GTPases and shares more than 70% identity with Ran proteins from other organisms, indicating that Ran proteins are conserved in different organisms. <italic>PsRan</italic> shows a low level of intra-species polymorphism and is localized to the nucleus. qRT-PCR analysis showed that transcript level of <italic>PsRan</italic> was induced <italic>in planta</italic> during <italic>Pst</italic> infection. Silencing of <italic>PsRan</italic> did not alter <italic>Pst</italic> virulence phenotype but impeded fungal growth of <italic>Pst</italic>. In addition, heterologous overexpression of <italic>PsRan</italic> in plant failed to induce cell death but suppressed cell death triggered by a mouse BAX gene or a <italic>Pst</italic> Ras gene. Our results suggest that <italic>PsRan</italic> is involved in the regulation of fungal growth and anti-cell death, which provides significant insight into Ran function in pathogenic fungi.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Takai, Y" uniqKey="Takai Y">Y. Takai</name></author><author><name sortKey="Sasaki, T" uniqKey="Sasaki T">T. Sasaki</name></author><author><name sortKey="Matozaki, T" uniqKey="Matozaki T">T. Matozaki</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Jiang, S Y" uniqKey="Jiang S">S. Y. Jiang</name></author><author><name sortKey="Ramachandran, S" uniqKey="Ramachandran S">S. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Sci Rep</journal-id><journal-id journal-id-type="iso-abbrev">Sci Rep</journal-id><journal-title-group><journal-title>Scientific Reports</journal-title></journal-title-group><issn pub-type="epub">2045-2322</issn><publisher><publisher-name>Nature Publishing Group</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">27734916</article-id><article-id pub-id-type="pmc">5062253</article-id><article-id pub-id-type="pii">srep35248</article-id><article-id pub-id-type="doi">10.1038/srep35248</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article</subject></subj-group></article-categories><title-group><article-title>Characterization of a Ran gene from <italic>Puccinia striiformis</italic> f. sp. <italic>tritici</italic> involved in fungal growth and anti-cell death</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Cheng</surname><given-names>Yulin</given-names></name><xref ref-type="aff" rid="a1">1</xref><xref ref-type="author-notes" rid="n1">*</xref></contrib><contrib contrib-type="author"><name><surname>Yao</surname><given-names>Juanni</given-names></name><xref ref-type="aff" rid="a2">2</xref><xref ref-type="author-notes" rid="n1">*</xref></contrib><contrib contrib-type="author"><name><surname>Zhang</surname><given-names>Yanru</given-names></name><xref ref-type="aff" rid="a2">2</xref></contrib><contrib contrib-type="author"><name><surname>Li</surname><given-names>Shumin</given-names></name><xref ref-type="aff" rid="a2">2</xref></contrib><contrib contrib-type="author"><name><surname>Kang</surname><given-names>Zhensheng</given-names></name><xref ref-type="corresp" rid="c1">a</xref><xref ref-type="aff" rid="a2">2</xref></contrib><aff id="a1"><label>1</label><institution>State Key Laboratory of Crop Stress Biology for Arid Areas, College of Life Sciences, Northwest A&F University</institution>, Yangling 712100, Shaanxi,<country>China</country></aff><aff id="a2"><label>2</label><institution>State Key Laboratory of Crop Stress Biology for Arid Areas, College of Plant Protection, Northwest A&F University</institution>, Yangling 712100, Shaanxi,<country>China</country></aff></contrib-group><author-notes><corresp id="c1"><label>a</label><email>kangzs@nwsuaf.edu.cn</email></corresp><fn id="n1"><label>*</label><p>These authors contributed equally to this work.</p></fn></author-notes><pub-date pub-type="epub"><day>13</day><month>10</month><year>2016</year></pub-date><pub-date pub-type="collection"><year>2016</year></pub-date><volume>6</volume><elocation-id>35248</elocation-id><history><date date-type="received"><day>07</day><month>07</month><year>2016</year></date><date date-type="accepted"><day>23</day><month>09</month><year>2016</year></date></history><permissions><copyright-statement>Copyright © 2016, The Author(s)</copyright-statement><copyright-year>2016</copyright-year><copyright-holder>The Author(s)</copyright-holder><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/4.0/"><pmc-comment>author-paid</pmc-comment>
<license-p>This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link></license-p></license></permissions><abstract><p>Ran, an important family of small GTP-binding proteins, has been shown to regulate a variety of important cellular processes in many eukaryotes. However, little is known about Ran function in pathogenic fungi. In this study, we report the identification and functional analysis of a Ran gene (designated <italic>PsRan</italic>) from <italic>Puccinia striiformis</italic> f. sp. <italic>tritici (Pst</italic>), an important fungal pathogen affecting wheat production worldwide. The PsRan protein contains all conserved domains of Ran GTPases and shares more than 70% identity with Ran proteins from other organisms, indicating that Ran proteins are conserved in different organisms. <italic>PsRan</italic> shows a low level of intra-species polymorphism and is localized to the nucleus. qRT-PCR analysis showed that transcript level of <italic>PsRan</italic> was induced <italic>in planta</italic> during <italic>Pst</italic> infection. Silencing of <italic>PsRan</italic> did not alter <italic>Pst</italic> virulence phenotype but impeded fungal growth of <italic>Pst</italic>. In addition, heterologous overexpression of <italic>PsRan</italic> in plant failed to induce cell death but suppressed cell death triggered by a mouse BAX gene or a <italic>Pst</italic> Ras gene. Our results suggest that <italic>PsRan</italic> is involved in the regulation of fungal growth and anti-cell death, which provides significant insight into Ran function in pathogenic fungi.</p></abstract></article-meta></front><floats-group><fig id="f1"><label>Figure 1</label><caption><title>Sequence alignment and phylogenetic analysis of PsRan and other Ran proteins in different organisms.</title><p>(<bold>a</bold>) Sequence alignment of PsRan and Ran proteins in three other organisms, including <italic>Saccharomyces cerevisiae (Sc</italic>), <italic>Arabidopsis thaliana (At</italic>) and <italic>Homo sapiens (Hs</italic>). Lines indicated six conserved domains for Ran GTPases, including four guanine nucleotide-binding domains (I–IV), an effector domain (E), and an acidic C-terminal domain. (<bold>b</bold>) Phylogenic analysis of PsRan and other Ran proteins in several fungi, animals, and plants. <italic>P. graminis</italic> f. sp. <italic>tritici (Pg</italic>), <italic>P. triticina (Pt</italic>), <italic>Melampsora larici-populina (Ml</italic>), <italic>Cryptococcus neoformans (Cn</italic>), <italic>Ustilago maydis (Um</italic>), <italic>S. cerevisiae (Sc</italic>), <italic>Aspergillus fumigatus (Af</italic>), <italic>F. graminearum (Fg</italic>), and <italic>Magnaporthe oryzae (Mo</italic>) are grouped as fungi; <italic>Caenorhabditis elegans (Ce</italic>), <italic>Homo sapiens (Hs</italic>), and <italic>Drosophila melanogaster (Dm</italic>) are grouped as animals; <italic>Arabidopsis thaliana (At</italic>), <italic>Oryza sativa (Os</italic>), and <italic>Ricinus communis (Rc</italic>) are grouped as plants. Phylogenetic analysis was carried out with the MEGA5 software by the neighbor-joining method and the red arrow indicates PsRan.</p></caption><graphic xlink:href="srep35248-f1"></graphic></fig><fig id="f2"><label>Figure 2</label><caption><title>Subcellular localization of PsRan in <italic>N. benthamiana</italic> and <italic>S. pombe</italic>.</title><p> (<bold>a</bold>) Overexpression of PsRan-GFP fusion protein and only GFP (control) in <italic>N. benthamiana</italic> using <italic>A. tumefaciens</italic>. Bar = 20 μm. (<bold>b</bold>) Overexpression of PsRan-GFP fusion protein and only GFP (control) in <italic>S. pombe</italic> using the yeast expression vector pREP3X. Bar = 5 μm.</p></caption><graphic xlink:href="srep35248-f2"></graphic></fig><fig id="f3"><label>Figure 3</label><caption><title>Transcription profiles of <italic>PsRan</italic> in different <italic>Pst</italic> infection stages by qRT-PCR.</title><p><italic>Pst</italic> development in wheat can be divided into three major stages, penetration stage (gray), parasitic/biotrophic stage (yellow), and sporulation stage (red). U, urediniospores; GU, <italic>in vitro</italic> germinated urediniospores; 18 h–216 h, wheat leaves infected with <italic>Pst</italic> at 18–216 hpi. Relative transcript levels were calculated by the comparative 2<sup>−ΔΔCT</sup> method and values are expressed relative to an endogenous <italic>Pst</italic> reference gene <italic>EF1</italic>. Results are composed of the means ± standard errors of three biological replications (each done in triplicates). Asterisks indicate a significant difference (<italic>P</italic> < 0.05) verus uredinospores using Student’s t test.</p></caption><graphic xlink:href="srep35248-f3"></graphic></fig><fig id="f4"><label>Figure 4</label><caption><title>HIGS of <italic>PsRan</italic> did not alter <italic>Pst</italic> virulence phenotype.</title><p>(<bold>a</bold>) Two specific sequence regions for HIGS of <italic>PsRan</italic>. (<bold>b</bold>) Phenotypes of the fourth leaves of BSMV:00- (control), BSMV:PsRan-1as-, and BSMV:PsRan-2as-inoculated wheat plants at 14 dpi with <italic>Pst</italic>. (<bold>c</bold>) Quantification of uredinial density in BSMV:00-, BSMV:PsRan-1as-, and BSMV:PsRan-2as-inoculated wheat plants 14 dpi with <italic>Pst</italic>. Values represent mean ± standard errors of three biological replications (each done in triplicates). (<bold>d</bold>) Relative transcript levels of <italic>PsRan</italic> in BSMV:00-, BSMV:PsRan-1as-, and BSMV:PsRan-2as-inoculated wheat plants at 18 hpi, 24 hpi, 48 hpi, and 14 dpi with <italic>Pst</italic>. Values are expressed relative to endogenous <italic>Pst</italic> reference gene <italic>EF1</italic>, with the empty vector (BSMV:00) set at 1. Values represent mean ± standard errors of three biological replications (each done in triplicates). Differences were assessed using Student’s t-tests and asterisks indicate <italic>P</italic> < 0.05.</p></caption><graphic xlink:href="srep35248-f4"></graphic></fig><fig id="f5"><label>Figure 5</label><caption><title>HIGS of <italic>PsRan</italic> impeded fungal growth of <italic>Pst</italic>.</title><p>(<bold>a</bold>) The average length of infection hyphae (IH) per infection unit in control (BSMV:00-inoculated) and PsRan-silenced (BSMV:PsRan-1as- and BSMV:PsRan-2as-inoculated) wheat plants. The length of IH was measured from the substomatal vesicle to the apex of the longest infection hyphae. (<bold>b</bold>) The average number of haustoria (H) per infection unit at control and PsRan-silenced wheat plants. (<bold>c</bold>) Fungal biomass measurements using qRT-PCR analysis of total DNA extracted from control (BSMV:00-inoculated) and PsRan-silenced (BSMV:PsRan-1as- and BSMV:PsRan-2as-inoculated) wheat plants. Ratio of total <italic>Pst</italic> DNA to total wheat DNA was assessed using the <italic>Pst</italic> gene <italic>PsEF1</italic> and the wheat gene <italic>TaEF1</italic>. In (<bold>a</bold>–<bold>c</bold>), samples were taken at 18, 24, and 48 hpi with <italic>Pst</italic>, values represent mean ± standard errors of three biological replications (each done in triplicates), and differences were assessed using Student’s t-tests and asterisks indicate <italic>P</italic> < 0.05.</p></caption><graphic xlink:href="srep35248-f5"></graphic></fig><fig id="f6"><label>Figure 6</label><caption><title>Micrographs of fungal growth in control (BSMV:00-inoculated) and PsRan-silenced (BSMV:PsRan-1as- and BSMV:PsRan-2as-inoculated) wheat plants.</title><p>Infected wheat leaves were sampled at 18, 24, and 48 hpi with <italic>Pst</italic> and then were examined under an Olympus BX-53 microscope after staining with wheat germ agglutinin conjugated to the fluorophore Alexa-488. IH: infection hypha. Bar = 20 μm.</p></caption><graphic xlink:href="srep35248-f6"></graphic></fig><fig id="f7"><label>Figure 7</label><caption><title>Herologous overexpression of <italic>PsRan</italic> in plant failed to induce cell death but suppressed cell death triggered by <italic>BAX</italic> or PsRas1.</title><p>(<bold>a</bold>) Overexpression of <italic>PsRan</italic> and <italic>eGFP</italic> (negative control) could not trigger cell death in <italic>N. benthamiana</italic> as a mouse pro-apoptotic gene <italic>BAX</italic> and a <italic>Pst</italic> Ras gene <italic>PsRas1</italic> that can induce strong cell death in <italic>N. benthamiana</italic>. (<bold>b</bold>) Overexpression of <italic>PsRan</italic> in <italic>N. benthamiana</italic> suppressed cell death triggered by <italic>BAX</italic> and <italic>PsRas1. N. benthamiana</italic> leaves were infiltrated with <italic>A. tumefaciens</italic> cells containing PVX carrying <italic>PsRan</italic> or a control gene (<italic>eGFP</italic>), followed after 24 h by <italic>A. tumefaciens</italic> cells carrying PVX:BAX/PsRas1.</p></caption><graphic xlink:href="srep35248-f7"></graphic></fig></floats-group></pmc><affiliations><list><country><li>République populaire de Chine</li></country></list><tree><country name="République populaire de Chine"><noRegion><name sortKey="Cheng, Yulin" sort="Cheng, Yulin" uniqKey="Cheng Y" first="Yulin" last="Cheng">Yulin Cheng</name></noRegion><name sortKey="Kang, Zhensheng" sort="Kang, Zhensheng" uniqKey="Kang Z" first="Zhensheng" last="Kang">Zhensheng Kang</name><name sortKey="Li, Shumin" sort="Li, Shumin" uniqKey="Li S" first="Shumin" last="Li">Shumin Li</name><name sortKey="Yao, Juanni" sort="Yao, Juanni" uniqKey="Yao J" first="Juanni" last="Yao">Juanni Yao</name><name sortKey="Zhang, Yanru" sort="Zhang, Yanru" uniqKey="Zhang Y" first="Yanru" last="Zhang">Yanru Zhang</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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