Phytophthora capsici PcFtsZ2 Is Required for Asexual Development and Plant Infection.
Identifieur interne : 000337 ( Main/Exploration ); précédent : 000336; suivant : 000338Phytophthora capsici PcFtsZ2 Is Required for Asexual Development and Plant Infection.
Auteurs : Jing Li [République populaire de Chine] ; Congcong Ai [République populaire de Chine] ; Cancan Yang [République populaire de Chine] ; Weilin Jiang [République populaire de Chine] ; Hui Sheng [République populaire de Chine] ; Paul F. Morris [États-Unis] ; Xiuguo Zhang [République populaire de Chine]Source :
- Molecular plant-microbe interactions : MPMI [ 0894-0282 ] ; 2020.
Descripteurs français
- KwdFr :
- MESH :
- croissance et développement : Phytophthora.
- génétique : Phytophthora.
- microbiologie : Maladies des plantes, Plantes.
- pathogénicité : Phytophthora.
- Animaux, Escherichia coli.
English descriptors
- KwdEn :
- MESH :
- genetics : Phytophthora.
- growth & development : Phytophthora.
- microbiology : Plant Diseases, Plants.
- pathogenicity : Phytophthora.
- Animals, Escherichia coli.
Abstract
In bacteria, FtsZ proteins form a Z ring that is the initial step preceding septal fission. FtsZ proteins enable the division of mitochondria in early eukaryotes and are present in some kingdoms but have been lost in animals, fungi, and plants. Here, we have identified two Phytophthora capsici ortholog genes of Escherichia coli FtsZs, designated PcFtsZ1 and PcFtsZ2. Overexpression of PcFtsZ2 in E. coli fully complemented the overexpression phenotype of EcFtsZ. In contrast, overexpression of PcFtsZ1 in E. coli had minimal impact on cell division and separation. Thus, we focused on evaluating the impact of altered expression of PcFtsZ2 in P. capsici, as it exhibited the strongest phenotype. PcFtsZ2 was expressed at the highest levels in mycelia, sporangia, and germinating cysts, as well as in late infection. PcFtsZ2 mis-expression lines showed aberrant asexual growth and development of P. capsici. Alterations in the expression of PcFtsZ2 changed the distribution of mitochondria in hyphae and sporangia and, also, affected the number, size, and shape of actin plaques. Silencing of PcFtsZ2 restrained growth and development of invasive structures, especially cysts and sporangia, substantially inhibiting the ability of transformants to cause blight lesions. In overexpressed transformant lines, cyst and sporangial germination rates were only half that of controls, but hyphal growth from direct germination of sporangia was more rapid than controls. These transformant lines were only slightly impaired in virulence relative to controls. This study emphasizes the essential role of the evolutionarily conserved FtsZ2 proteins in affecting cytoskeleton dynamics.
DOI: 10.1094/MPMI-01-20-0002-R
PubMed: 32096689
Affiliations:
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Morris</name><affiliation wicri:level="2"><nlm:affiliation>Department of Biological Sciences, Bowling Green State University, Bowling Green, OH 43403, U.S.A.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biological Sciences, Bowling Green State University, Bowling Green, OH 43403</wicri:regionArea><placeName><region type="state">Ohio</region></placeName></affiliation></author><author><name sortKey="Zhang, Xiuguo" sort="Zhang, Xiuguo" uniqKey="Zhang X" first="Xiuguo" last="Zhang">Xiuguo Zhang</name><affiliation wicri:level="1"><nlm:affiliation>Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Tai'an, 271018, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong 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wicri:level="1"><nlm:affiliation>Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Tai'an, 271018, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Tai'an, 271018</wicri:regionArea><wicri:noRegion>271018</wicri:noRegion></affiliation></author><author><name sortKey="Ai, Congcong" sort="Ai, Congcong" uniqKey="Ai C" first="Congcong" last="Ai">Congcong Ai</name><affiliation wicri:level="1"><nlm:affiliation>Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Tai'an, 271018, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Tai'an, 271018</wicri:regionArea><wicri:noRegion>271018</wicri:noRegion></affiliation></author><author><name sortKey="Yang, Cancan" sort="Yang, Cancan" uniqKey="Yang C" first="Cancan" last="Yang">Cancan Yang</name><affiliation wicri:level="1"><nlm:affiliation>Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Tai'an, 271018, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Tai'an, 271018</wicri:regionArea><wicri:noRegion>271018</wicri:noRegion></affiliation></author><author><name sortKey="Jiang, Weilin" sort="Jiang, Weilin" uniqKey="Jiang W" first="Weilin" last="Jiang">Weilin Jiang</name><affiliation wicri:level="1"><nlm:affiliation>Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Tai'an, 271018, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Tai'an, 271018</wicri:regionArea><wicri:noRegion>271018</wicri:noRegion></affiliation></author><author><name sortKey="Sheng, Hui" sort="Sheng, Hui" uniqKey="Sheng H" first="Hui" last="Sheng">Hui Sheng</name><affiliation wicri:level="1"><nlm:affiliation>Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Tai'an, 271018, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Tai'an, 271018</wicri:regionArea><wicri:noRegion>271018</wicri:noRegion></affiliation></author><author><name sortKey="Morris, Paul F" sort="Morris, Paul F" uniqKey="Morris P" first="Paul F" last="Morris">Paul F. Morris</name><affiliation wicri:level="2"><nlm:affiliation>Department of Biological Sciences, Bowling Green State University, Bowling Green, OH 43403, U.S.A.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biological Sciences, Bowling Green State University, Bowling Green, OH 43403</wicri:regionArea><placeName><region type="state">Ohio</region></placeName></affiliation></author><author><name sortKey="Zhang, Xiuguo" sort="Zhang, Xiuguo" uniqKey="Zhang X" first="Xiuguo" last="Zhang">Xiuguo Zhang</name><affiliation wicri:level="1"><nlm:affiliation>Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Tai'an, 271018, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Tai'an, 271018</wicri:regionArea><wicri:noRegion>271018</wicri:noRegion></affiliation></author></analytic><series><title level="j">Molecular plant-microbe interactions : MPMI</title><idno type="ISSN">0894-0282</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Animals (MeSH)</term><term>Escherichia coli (MeSH)</term><term>Phytophthora (genetics)</term><term>Phytophthora (growth & development)</term><term>Phytophthora (pathogenicity)</term><term>Plant Diseases (microbiology)</term><term>Plants (microbiology)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Animaux (MeSH)</term><term>Escherichia coli (MeSH)</term><term>Maladies des plantes (microbiologie)</term><term>Phytophthora (croissance et développement)</term><term>Phytophthora (génétique)</term><term>Phytophthora (pathogénicité)</term><term>Plantes (microbiologie)</term></keywords><keywords scheme="MESH" qualifier="croissance et développement" xml:lang="fr"><term>Phytophthora</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Phytophthora</term></keywords><keywords scheme="MESH" qualifier="growth & development" xml:lang="en"><term>Phytophthora</term></keywords><keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Phytophthora</term></keywords><keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr"><term>Maladies des plantes</term><term>Plantes</term></keywords><keywords scheme="MESH" qualifier="microbiology" xml:lang="en"><term>Plant Diseases</term><term>Plants</term></keywords><keywords scheme="MESH" qualifier="pathogenicity" xml:lang="en"><term>Phytophthora</term></keywords><keywords scheme="MESH" qualifier="pathogénicité" xml:lang="fr"><term>Phytophthora</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Animals</term><term>Escherichia coli</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Animaux</term><term>Escherichia coli</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">In bacteria, FtsZ proteins form a Z ring that is the initial step preceding septal fission. FtsZ proteins enable the division of mitochondria in early eukaryotes and are present in some kingdoms but have been lost in animals, fungi, and plants. Here, we have identified two <i>Phytophthora capsici</i> ortholog genes of <i>Escherichia coli</i> FtsZs, designated <i>PcFtsZ</i>1 and <i>PcFtsZ</i>2. Overexpression of <i>PcFtsZ</i>2 in <i>E. coli</i> fully complemented the overexpression phenotype of <i>EcFtsZ</i>. In contrast, overexpression of <i>PcFtsZ</i>1 in <i>E. coli</i> had minimal impact on cell division and separation. Thus, we focused on evaluating the impact of altered expression of <i>PcFtsZ</i>2 in <i>P. capsici</i>, as it exhibited the strongest phenotype. <i>PcFtsZ</i>2 was expressed at the highest levels in mycelia, sporangia, and germinating cysts, as well as in late infection. <i>PcFtsZ</i>2 mis-expression lines showed aberrant asexual growth and development of <i>P. capsici</i>. Alterations in the expression of <i>PcFtsZ</i>2 changed the distribution of mitochondria in hyphae and sporangia and, also, affected the number, size, and shape of actin plaques. Silencing of <i>PcFtsZ</i>2 restrained growth and development of invasive structures, especially cysts and sporangia, substantially inhibiting the ability of transformants to cause blight lesions. In overexpressed transformant lines, cyst and sporangial germination rates were only half that of controls, but hyphal growth from direct germination of sporangia was more rapid than controls. These transformant lines were only slightly impaired in virulence relative to controls. This study emphasizes the essential role of the evolutionarily conserved FtsZ2 proteins in affecting cytoskeleton dynamics.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" IndexingMethod="Curated" Owner="NLM"><PMID Version="1">32096689</PMID><DateCompleted><Year>2020</Year><Month>09</Month><Day>03</Day></DateCompleted><DateRevised><Year>2020</Year><Month>09</Month><Day>03</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Print">0894-0282</ISSN><JournalIssue CitedMedium="Print"><Volume>33</Volume><Issue>5</Issue><PubDate><Year>2020</Year><Month>May</Month></PubDate></JournalIssue><Title>Molecular plant-microbe interactions : MPMI</Title><ISOAbbreviation>Mol Plant Microbe Interact</ISOAbbreviation></Journal><ArticleTitle><i>Phytophthora capsici PcFtsZ</i>2 Is Required for Asexual Development and Plant Infection.</ArticleTitle><Pagination><MedlinePgn>727-741</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1094/MPMI-01-20-0002-R</ELocationID><Abstract><AbstractText>In bacteria, FtsZ proteins form a Z ring that is the initial step preceding septal fission. FtsZ proteins enable the division of mitochondria in early eukaryotes and are present in some kingdoms but have been lost in animals, fungi, and plants. Here, we have identified two <i>Phytophthora capsici</i> ortholog genes of <i>Escherichia coli</i> FtsZs, designated <i>PcFtsZ</i>1 and <i>PcFtsZ</i>2. Overexpression of <i>PcFtsZ</i>2 in <i>E. coli</i> fully complemented the overexpression phenotype of <i>EcFtsZ</i>. In contrast, overexpression of <i>PcFtsZ</i>1 in <i>E. coli</i> had minimal impact on cell division and separation. Thus, we focused on evaluating the impact of altered expression of <i>PcFtsZ</i>2 in <i>P. capsici</i>, as it exhibited the strongest phenotype. <i>PcFtsZ</i>2 was expressed at the highest levels in mycelia, sporangia, and germinating cysts, as well as in late infection. <i>PcFtsZ</i>2 mis-expression lines showed aberrant asexual growth and development of <i>P. capsici</i>. Alterations in the expression of <i>PcFtsZ</i>2 changed the distribution of mitochondria in hyphae and sporangia and, also, affected the number, size, and shape of actin plaques. Silencing of <i>PcFtsZ</i>2 restrained growth and development of invasive structures, especially cysts and sporangia, substantially inhibiting the ability of transformants to cause blight lesions. In overexpressed transformant lines, cyst and sporangial germination rates were only half that of controls, but hyphal growth from direct germination of sporangia was more rapid than controls. These transformant lines were only slightly impaired in virulence relative to controls. This study emphasizes the essential role of the evolutionarily conserved FtsZ2 proteins in affecting cytoskeleton dynamics.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Li</LastName><ForeName>Jing</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Tai'an, 271018, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ai</LastName><ForeName>CongCong</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Tai'an, 271018, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Yang</LastName><ForeName>CanCan</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Tai'an, 271018, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Jiang</LastName><ForeName>WeiLin</ForeName><Initials>W</Initials><AffiliationInfo><Affiliation>Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Tai'an, 271018, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sheng</LastName><ForeName>Hui</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Tai'an, 271018, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Morris</LastName><ForeName>Paul F</ForeName><Initials>PF</Initials><AffiliationInfo><Affiliation>Department of Biological Sciences, Bowling Green State University, Bowling Green, OH 43403, U.S.A.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>XiuGuo</ForeName><Initials>X</Initials><Identifier Source="ORCID">http://orcid.org/0000-0001-9733-8494</Identifier><AffiliationInfo><Affiliation>Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Tai'an, 271018, China.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>04</Month><Day>02</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Mol Plant Microbe Interact</MedlineTA><NlmUniqueID>9107902</NlmUniqueID><ISSNLinking>0894-0282</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D004926" MajorTopicYN="N">Escherichia coli</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D010838" MajorTopicYN="N">Phytophthora</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName><QualifierName UI="Q000254" MajorTopicYN="N">growth & development</QualifierName><QualifierName UI="Q000472" MajorTopicYN="N">pathogenicity</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D010935" MajorTopicYN="N">Plant Diseases</DescriptorName><QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D010944" MajorTopicYN="N">Plants</DescriptorName><QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName></MeshHeading></MeshHeadingList><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">FtsZ proteins</Keyword><Keyword MajorTopicYN="N">oomycete-plant interactions</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>2</Month><Day>26</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>9</Month><Day>4</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>2</Month><Day>26</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">32096689</ArticleId><ArticleId IdType="doi">10.1094/MPMI-01-20-0002-R</ArticleId></ArticleIdList></PubmedData></pubmed><affiliations><list><country><li>République populaire de Chine</li><li>États-Unis</li></country><region><li>Ohio</li></region></list><tree><country name="République populaire de Chine"><noRegion><name sortKey="Li, Jing" sort="Li, Jing" uniqKey="Li J" first="Jing" last="Li">Jing Li</name></noRegion><name sortKey="Ai, Congcong" sort="Ai, Congcong" uniqKey="Ai C" first="Congcong" last="Ai">Congcong Ai</name><name sortKey="Jiang, Weilin" sort="Jiang, Weilin" uniqKey="Jiang W" first="Weilin" last="Jiang">Weilin Jiang</name><name sortKey="Sheng, Hui" sort="Sheng, Hui" uniqKey="Sheng H" first="Hui" last="Sheng">Hui Sheng</name><name sortKey="Yang, Cancan" sort="Yang, Cancan" uniqKey="Yang C" first="Cancan" last="Yang">Cancan Yang</name><name sortKey="Zhang, Xiuguo" sort="Zhang, Xiuguo" uniqKey="Zhang X" first="Xiuguo" last="Zhang">Xiuguo Zhang</name></country><country name="États-Unis"><region name="Ohio"><name sortKey="Morris, Paul F" sort="Morris, Paul F" uniqKey="Morris P" first="Paul F" last="Morris">Paul F. 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