De Novo Assembly and Phasing of Dikaryotic Genomes from Two Isolates of Puccinia coronata f. sp. avenae, the Causal Agent of Oat Crown Rust.
Identifieur interne : 000204 ( Main/Corpus ); précédent : 000203; suivant : 000205De Novo Assembly and Phasing of Dikaryotic Genomes from Two Isolates of Puccinia coronata f. sp. avenae, the Causal Agent of Oat Crown Rust.
Auteurs : Marisa E. Miller ; Ying Zhang ; Vahid Omidvar ; Jana Sperschneider ; Benjamin Schwessinger ; Castle Raley ; Jonathan M. Palmer ; Diana Garnica ; Narayana Upadhyaya ; John Rathjen ; Jennifer M. Taylor ; Robert F. Park ; Peter N. Dodds ; Cory D. Hirsch ; Shahryar F. Kianian ; Melania FigueroaSource :
- mBio [ 2150-7511 ] ; 2018.
English descriptors
- KwdEn :
- Avena (microbiology), Basidiomycota (classification), Basidiomycota (genetics), Basidiomycota (isolation & purification), Gene Expression Profiling (MeSH), Genetic Variation (MeSH), Genome, Fungal (MeSH), Genotype (MeSH), Molecular Sequence Annotation (MeSH), Plant Diseases (microbiology), Polymorphism, Single Nucleotide (MeSH).
- MESH :
- classification : Basidiomycota.
- genetics : Basidiomycota.
- isolation & purification : Basidiomycota.
- microbiology : Avena, Plant Diseases.
- Gene Expression Profiling, Genetic Variation, Genome, Fungal, Genotype, Molecular Sequence Annotation, Polymorphism, Single Nucleotide.
Abstract
Oat crown rust, caused by the fungus Pucinnia coronata f. sp. avenae, is a devastating disease that impacts worldwide oat production. For much of its life cycle, P. coronata f. sp. avenae is dikaryotic, with two separate haploid nuclei that may vary in virulence genotype, highlighting the importance of understanding haplotype diversity in this species. We generated highly contiguous de novo genome assemblies of two P. coronata f. sp. avenae isolates, 12SD80 and 12NC29, from long-read sequences. In total, we assembled 603 primary contigs for 12SD80, for a total assembly length of 99.16 Mbp, and 777 primary contigs for 12NC29, for a total length of 105.25 Mbp; approximately 52% of each genome was assembled into alternate haplotypes. This revealed structural variation between haplotypes in each isolate equivalent to more than 2% of the genome size, in addition to about 260,000 and 380,000 heterozygous single-nucleotide polymorphisms in 12SD80 and 12NC29, respectively. Transcript-based annotation identified 26,796 and 28,801 coding sequences for isolates 12SD80 and 12NC29, respectively, including about 7,000 allele pairs in haplotype-phased regions. Furthermore, expression profiling revealed clusters of coexpressed secreted effector candidates, and the majority of orthologous effectors between isolates showed conservation of expression patterns. However, a small subset of orthologs showed divergence in expression, which may contribute to differences in virulence between 12SD80 and 12NC29. This study provides the first haplotype-phased reference genome for a dikaryotic rust fungus as a foundation for future studies into virulence mechanisms in P. coronata f. sp. avenaeIMPORTANCE Disease management strategies for oat crown rust are challenged by the rapid evolution of Puccinia coronata f. sp. avenae, which renders resistance genes in oat varieties ineffective. Despite the economic importance of understanding P. coronata f. sp. avenae, resources to study the molecular mechanisms underpinning pathogenicity and the emergence of new virulence traits are lacking. Such limitations are partly due to the obligate biotrophic lifestyle of P. coronata f. sp. avenae as well as the dikaryotic nature of the genome, features that are also shared with other important rust pathogens. This study reports the first release of a haplotype-phased genome assembly for a dikaryotic fungal species and demonstrates the amenability of using emerging technologies to investigate genetic diversity in populations of P. coronata f. sp. avenae.
DOI: 10.1128/mBio.01650-17
PubMed: 29463655
PubMed Central: PMC5821079
Links to Exploration step
pubmed:29463655Le document en format XML
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Assembly and Phasing of Dikaryotic Genomes from Two Isolates of <i>Puccinia coronata</i>
f. sp. <i>avenae</i>
, the Causal Agent of Oat Crown Rust.</title>
<author><name sortKey="Miller, Marisa E" sort="Miller, Marisa E" uniqKey="Miller M" first="Marisa E" last="Miller">Marisa E. Miller</name>
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<author><name sortKey="Zhang, Ying" sort="Zhang, Ying" uniqKey="Zhang Y" first="Ying" last="Zhang">Ying Zhang</name>
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<author><name sortKey="Raley, Castle" sort="Raley, Castle" uniqKey="Raley C" first="Castle" last="Raley">Castle Raley</name>
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</affiliation>
</author>
<author><name sortKey="Dodds, Peter N" sort="Dodds, Peter N" uniqKey="Dodds P" first="Peter N" last="Dodds">Peter N. Dodds</name>
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</affiliation>
</author>
<author><name sortKey="Hirsch, Cory D" sort="Hirsch, Cory D" uniqKey="Hirsch C" first="Cory D" last="Hirsch">Cory D. Hirsch</name>
<affiliation><nlm:affiliation>Department of Plant Pathology, University of Minnesota, St. Paul, Minnesota, USA.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Kianian, Shahryar F" sort="Kianian, Shahryar F" uniqKey="Kianian S" first="Shahryar F" last="Kianian">Shahryar F. Kianian</name>
<affiliation><nlm:affiliation>Department of Plant Pathology, University of Minnesota, St. Paul, Minnesota, USA shahryar.kianian@ars.usda.gov figue031@umn.edu.</nlm:affiliation>
</affiliation>
<affiliation><nlm:affiliation>USDA-ARS Cereal Disease Laboratory, St. Paul, Minnesota, USA.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Figueroa, Melania" sort="Figueroa, Melania" uniqKey="Figueroa M" first="Melania" last="Figueroa">Melania Figueroa</name>
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<affiliation><nlm:affiliation>Stakman-Borlaug Center for Sustainable Plant Health, University of Minnesota, St. Paul, Minnesota, USA.</nlm:affiliation>
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<sourceDesc><biblStruct><analytic><title xml:lang="en"><i>De Novo</i>
Assembly and Phasing of Dikaryotic Genomes from Two Isolates of <i>Puccinia coronata</i>
f. sp. <i>avenae</i>
, the Causal Agent of Oat Crown Rust.</title>
<author><name sortKey="Miller, Marisa E" sort="Miller, Marisa E" uniqKey="Miller M" first="Marisa E" last="Miller">Marisa E. Miller</name>
<affiliation><nlm:affiliation>Department of Plant Pathology, University of Minnesota, St. Paul, Minnesota, USA.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Zhang, Ying" sort="Zhang, Ying" uniqKey="Zhang Y" first="Ying" last="Zhang">Ying Zhang</name>
<affiliation><nlm:affiliation>Supercomputing Institute for Advanced Computational Research, University of Minnesota, Minneapolis, Minnesota, USA.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Omidvar, Vahid" sort="Omidvar, Vahid" uniqKey="Omidvar V" first="Vahid" last="Omidvar">Vahid Omidvar</name>
<affiliation><nlm:affiliation>Department of Plant Pathology, University of Minnesota, St. Paul, Minnesota, USA.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Sperschneider, Jana" sort="Sperschneider, Jana" uniqKey="Sperschneider J" first="Jana" last="Sperschneider">Jana Sperschneider</name>
<affiliation><nlm:affiliation>Centre for Environment and Life Sciences, Commonwealth Scientific and Industrial Research Organization, Agriculture and Food, Perth, WA, Australia.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Schwessinger, Benjamin" sort="Schwessinger, Benjamin" uniqKey="Schwessinger B" first="Benjamin" last="Schwessinger">Benjamin Schwessinger</name>
<affiliation><nlm:affiliation>Research School of Biology, Australian National University, Canberra, ACT, Australia.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Raley, Castle" sort="Raley, Castle" uniqKey="Raley C" first="Castle" last="Raley">Castle Raley</name>
<affiliation><nlm:affiliation>Leidos Biomedical Research, Frederick, Maryland, USA.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Palmer, Jonathan M" sort="Palmer, Jonathan M" uniqKey="Palmer J" first="Jonathan M" last="Palmer">Jonathan M. Palmer</name>
<affiliation><nlm:affiliation>Center for Forest Mycology Research, Northern Research Station, USDA Forest Service, Madison, Wisconsin, USA.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Garnica, Diana" sort="Garnica, Diana" uniqKey="Garnica D" first="Diana" last="Garnica">Diana Garnica</name>
<affiliation><nlm:affiliation>Agriculture and Food, Commonwealth Scientific and Industrial Research Organization, Canberra, ACT, Australia.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Upadhyaya, Narayana" sort="Upadhyaya, Narayana" uniqKey="Upadhyaya N" first="Narayana" last="Upadhyaya">Narayana Upadhyaya</name>
<affiliation><nlm:affiliation>Agriculture and Food, Commonwealth Scientific and Industrial Research Organization, Canberra, ACT, Australia.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Rathjen, John" sort="Rathjen, John" uniqKey="Rathjen J" first="John" last="Rathjen">John Rathjen</name>
<affiliation><nlm:affiliation>Research School of Biology, Australian National University, Canberra, ACT, Australia.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Taylor, Jennifer M" sort="Taylor, Jennifer M" uniqKey="Taylor J" first="Jennifer M" last="Taylor">Jennifer M. Taylor</name>
<affiliation><nlm:affiliation>Agriculture and Food, Commonwealth Scientific and Industrial Research Organization, Canberra, ACT, Australia.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Park, Robert F" sort="Park, Robert F" uniqKey="Park R" first="Robert F" last="Park">Robert F. Park</name>
<affiliation><nlm:affiliation>Plant Breeding Institute, Faculty of Agriculture and Environment, School of Life and Environmental Sciences, University of Sydney, Narellan, NSW, Australia.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Dodds, Peter N" sort="Dodds, Peter N" uniqKey="Dodds P" first="Peter N" last="Dodds">Peter N. Dodds</name>
<affiliation><nlm:affiliation>Agriculture and Food, Commonwealth Scientific and Industrial Research Organization, Canberra, ACT, Australia.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Hirsch, Cory D" sort="Hirsch, Cory D" uniqKey="Hirsch C" first="Cory D" last="Hirsch">Cory D. Hirsch</name>
<affiliation><nlm:affiliation>Department of Plant Pathology, University of Minnesota, St. Paul, Minnesota, USA.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Kianian, Shahryar F" sort="Kianian, Shahryar F" uniqKey="Kianian S" first="Shahryar F" last="Kianian">Shahryar F. Kianian</name>
<affiliation><nlm:affiliation>Department of Plant Pathology, University of Minnesota, St. Paul, Minnesota, USA shahryar.kianian@ars.usda.gov figue031@umn.edu.</nlm:affiliation>
</affiliation>
<affiliation><nlm:affiliation>USDA-ARS Cereal Disease Laboratory, St. Paul, Minnesota, USA.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Figueroa, Melania" sort="Figueroa, Melania" uniqKey="Figueroa M" first="Melania" last="Figueroa">Melania Figueroa</name>
<affiliation><nlm:affiliation>Department of Plant Pathology, University of Minnesota, St. Paul, Minnesota, USA shahryar.kianian@ars.usda.gov figue031@umn.edu.</nlm:affiliation>
</affiliation>
<affiliation><nlm:affiliation>Stakman-Borlaug Center for Sustainable Plant Health, University of Minnesota, St. Paul, Minnesota, USA.</nlm:affiliation>
</affiliation>
</author>
</analytic>
<series><title level="j">mBio</title>
<idno type="eISSN">2150-7511</idno>
<imprint><date when="2018" type="published">2018</date>
</imprint>
</series>
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<profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Avena (microbiology)</term>
<term>Basidiomycota (classification)</term>
<term>Basidiomycota (genetics)</term>
<term>Basidiomycota (isolation & purification)</term>
<term>Gene Expression Profiling (MeSH)</term>
<term>Genetic Variation (MeSH)</term>
<term>Genome, Fungal (MeSH)</term>
<term>Genotype (MeSH)</term>
<term>Molecular Sequence Annotation (MeSH)</term>
<term>Plant Diseases (microbiology)</term>
<term>Polymorphism, Single Nucleotide (MeSH)</term>
</keywords>
<keywords scheme="MESH" qualifier="classification" xml:lang="en"><term>Basidiomycota</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Basidiomycota</term>
</keywords>
<keywords scheme="MESH" qualifier="isolation & purification" xml:lang="en"><term>Basidiomycota</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiology" xml:lang="en"><term>Avena</term>
<term>Plant Diseases</term>
</keywords>
<keywords scheme="MESH" xml:lang="en"><term>Gene Expression Profiling</term>
<term>Genetic Variation</term>
<term>Genome, Fungal</term>
<term>Genotype</term>
<term>Molecular Sequence Annotation</term>
<term>Polymorphism, Single Nucleotide</term>
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<front><div type="abstract" xml:lang="en">Oat crown rust, caused by the fungus <i>Pucinnia coronata</i>
f. sp. <i>avenae</i>
, is a devastating disease that impacts worldwide oat production. For much of its life cycle, <i>P. coronata</i>
f. sp. <i>avenae</i>
is dikaryotic, with two separate haploid nuclei that may vary in virulence genotype, highlighting the importance of understanding haplotype diversity in this species. We generated highly contiguous <i>de novo</i>
genome assemblies of two <i>P. coronata</i>
f. sp. <i>avenae</i>
isolates, 12SD80 and 12NC29, from long-read sequences. In total, we assembled 603 primary contigs for 12SD80, for a total assembly length of 99.16 Mbp, and 777 primary contigs for 12NC29, for a total length of 105.25 Mbp; approximately 52% of each genome was assembled into alternate haplotypes. This revealed structural variation between haplotypes in each isolate equivalent to more than 2% of the genome size, in addition to about 260,000 and 380,000 heterozygous single-nucleotide polymorphisms in 12SD80 and 12NC29, respectively. Transcript-based annotation identified 26,796 and 28,801 coding sequences for isolates 12SD80 and 12NC29, respectively, including about 7,000 allele pairs in haplotype-phased regions. Furthermore, expression profiling revealed clusters of coexpressed secreted effector candidates, and the majority of orthologous effectors between isolates showed conservation of expression patterns. However, a small subset of orthologs showed divergence in expression, which may contribute to differences in virulence between 12SD80 and 12NC29. This study provides the first haplotype-phased reference genome for a dikaryotic rust fungus as a foundation for future studies into virulence mechanisms in <i>P. coronata</i>
f. sp. <i>avenae</i>
<b>IMPORTANCE</b>
Disease management strategies for oat crown rust are challenged by the rapid evolution of <i>Puccinia coronata</i>
f. sp. <i>avenae</i>
, which renders resistance genes in oat varieties ineffective. Despite the economic importance of understanding <i>P. coronata</i>
f. sp. <i>avenae</i>
, resources to study the molecular mechanisms underpinning pathogenicity and the emergence of new virulence traits are lacking. Such limitations are partly due to the obligate biotrophic lifestyle of <i>P. coronata</i>
f. sp. <i>avenae</i>
as well as the dikaryotic nature of the genome, features that are also shared with other important rust pathogens. This study reports the first release of a haplotype-phased genome assembly for a dikaryotic fungal species and demonstrates the amenability of using emerging technologies to investigate genetic diversity in populations of <i>P. coronata</i>
f. sp. <i>avenae</i>
.</div>
</front>
</TEI>
<pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">29463655</PMID>
<DateCompleted><Year>2018</Year>
<Month>12</Month>
<Day>11</Day>
</DateCompleted>
<DateRevised><Year>2020</Year>
<Month>03</Month>
<Day>06</Day>
</DateRevised>
<Article PubModel="Electronic"><Journal><ISSN IssnType="Electronic">2150-7511</ISSN>
<JournalIssue CitedMedium="Internet"><Volume>9</Volume>
<Issue>1</Issue>
<PubDate><Year>2018</Year>
<Month>02</Month>
<Day>20</Day>
</PubDate>
</JournalIssue>
<Title>mBio</Title>
<ISOAbbreviation>mBio</ISOAbbreviation>
</Journal>
<ArticleTitle><i>De Novo</i>
Assembly and Phasing of Dikaryotic Genomes from Two Isolates of <i>Puccinia coronata</i>
f. sp. <i>avenae</i>
, the Causal Agent of Oat Crown Rust.</ArticleTitle>
<ELocationID EIdType="pii" ValidYN="Y">e01650-17</ELocationID>
<ELocationID EIdType="doi" ValidYN="Y">10.1128/mBio.01650-17</ELocationID>
<Abstract><AbstractText>Oat crown rust, caused by the fungus <i>Pucinnia coronata</i>
f. sp. <i>avenae</i>
, is a devastating disease that impacts worldwide oat production. For much of its life cycle, <i>P. coronata</i>
f. sp. <i>avenae</i>
is dikaryotic, with two separate haploid nuclei that may vary in virulence genotype, highlighting the importance of understanding haplotype diversity in this species. We generated highly contiguous <i>de novo</i>
genome assemblies of two <i>P. coronata</i>
f. sp. <i>avenae</i>
isolates, 12SD80 and 12NC29, from long-read sequences. In total, we assembled 603 primary contigs for 12SD80, for a total assembly length of 99.16 Mbp, and 777 primary contigs for 12NC29, for a total length of 105.25 Mbp; approximately 52% of each genome was assembled into alternate haplotypes. This revealed structural variation between haplotypes in each isolate equivalent to more than 2% of the genome size, in addition to about 260,000 and 380,000 heterozygous single-nucleotide polymorphisms in 12SD80 and 12NC29, respectively. Transcript-based annotation identified 26,796 and 28,801 coding sequences for isolates 12SD80 and 12NC29, respectively, including about 7,000 allele pairs in haplotype-phased regions. Furthermore, expression profiling revealed clusters of coexpressed secreted effector candidates, and the majority of orthologous effectors between isolates showed conservation of expression patterns. However, a small subset of orthologs showed divergence in expression, which may contribute to differences in virulence between 12SD80 and 12NC29. This study provides the first haplotype-phased reference genome for a dikaryotic rust fungus as a foundation for future studies into virulence mechanisms in <i>P. coronata</i>
f. sp. <i>avenae</i>
<b>IMPORTANCE</b>
Disease management strategies for oat crown rust are challenged by the rapid evolution of <i>Puccinia coronata</i>
f. sp. <i>avenae</i>
, which renders resistance genes in oat varieties ineffective. Despite the economic importance of understanding <i>P. coronata</i>
f. sp. <i>avenae</i>
, resources to study the molecular mechanisms underpinning pathogenicity and the emergence of new virulence traits are lacking. Such limitations are partly due to the obligate biotrophic lifestyle of <i>P. coronata</i>
f. sp. <i>avenae</i>
as well as the dikaryotic nature of the genome, features that are also shared with other important rust pathogens. This study reports the first release of a haplotype-phased genome assembly for a dikaryotic fungal species and demonstrates the amenability of using emerging technologies to investigate genetic diversity in populations of <i>P. coronata</i>
f. sp. <i>avenae</i>
.</AbstractText>
<CopyrightInformation>Copyright © 2018 Miller et al.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Miller</LastName>
<ForeName>Marisa E</ForeName>
<Initials>ME</Initials>
<AffiliationInfo><Affiliation>Department of Plant Pathology, University of Minnesota, St. Paul, Minnesota, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Zhang</LastName>
<ForeName>Ying</ForeName>
<Initials>Y</Initials>
<AffiliationInfo><Affiliation>Supercomputing Institute for Advanced Computational Research, University of Minnesota, Minneapolis, Minnesota, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Omidvar</LastName>
<ForeName>Vahid</ForeName>
<Initials>V</Initials>
<AffiliationInfo><Affiliation>Department of Plant Pathology, University of Minnesota, St. Paul, Minnesota, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Sperschneider</LastName>
<ForeName>Jana</ForeName>
<Initials>J</Initials>
<AffiliationInfo><Affiliation>Centre for Environment and Life Sciences, Commonwealth Scientific and Industrial Research Organization, Agriculture and Food, Perth, WA, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Schwessinger</LastName>
<ForeName>Benjamin</ForeName>
<Initials>B</Initials>
<Identifier Source="ORCID">0000-0002-7194-2922</Identifier>
<AffiliationInfo><Affiliation>Research School of Biology, Australian National University, Canberra, ACT, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Raley</LastName>
<ForeName>Castle</ForeName>
<Initials>C</Initials>
<AffiliationInfo><Affiliation>Leidos Biomedical Research, Frederick, Maryland, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Palmer</LastName>
<ForeName>Jonathan M</ForeName>
<Initials>JM</Initials>
<AffiliationInfo><Affiliation>Center for Forest Mycology Research, Northern Research Station, USDA Forest Service, Madison, Wisconsin, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Garnica</LastName>
<ForeName>Diana</ForeName>
<Initials>D</Initials>
<AffiliationInfo><Affiliation>Agriculture and Food, Commonwealth Scientific and Industrial Research Organization, Canberra, ACT, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Upadhyaya</LastName>
<ForeName>Narayana</ForeName>
<Initials>N</Initials>
<AffiliationInfo><Affiliation>Agriculture and Food, Commonwealth Scientific and Industrial Research Organization, Canberra, ACT, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Rathjen</LastName>
<ForeName>John</ForeName>
<Initials>J</Initials>
<AffiliationInfo><Affiliation>Research School of Biology, Australian National University, Canberra, ACT, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Taylor</LastName>
<ForeName>Jennifer M</ForeName>
<Initials>JM</Initials>
<AffiliationInfo><Affiliation>Agriculture and Food, Commonwealth Scientific and Industrial Research Organization, Canberra, ACT, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Park</LastName>
<ForeName>Robert F</ForeName>
<Initials>RF</Initials>
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