A membrane-bound ankyrin repeat protein confers race-specific leaf rust disease resistance in wheat

Plasma membrane-associated and intracellular proteins and protein complexes play a pivotal role in pathogen recognition and disease resistance signaling in plants and animals. The two predominant protein families perceiving plant pathogens are receptor-like kinases and nucleotide binding-leucine-ric...

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Published inNature communications Vol. 12; no. 1; pp. 956 - 12
Main Authors Kolodziej, Markus C., Singla, Jyoti, Sánchez-Martín, Javier, Zbinden, Helen, Šimková, Hana, Karafiátová, Miroslava, Doležel, Jaroslav, Gronnier, Julien, Poretti, Manuel, Glauser, Gaétan, Zhu, Wangsheng, Köster, Philipp, Zipfel, Cyril, Wicker, Thomas, Krattinger, Simon G., Keller, Beat
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 11.02.2021
Nature Publishing Group
Nature Portfolio
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Online AccessGet full text
ISSN2041-1723
2041-1723
DOI10.1038/s41467-020-20777-x

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Abstract Plasma membrane-associated and intracellular proteins and protein complexes play a pivotal role in pathogen recognition and disease resistance signaling in plants and animals. The two predominant protein families perceiving plant pathogens are receptor-like kinases and nucleotide binding-leucine-rich repeat receptors (NLR), which often confer race-specific resistance. Leaf rust is one of the most prevalent and most devastating wheat diseases. Here, we clone the race-specific leaf rust resistance gene Lr14a from hexaploid wheat. The cloning of Lr14a is aided by the recently published genome assembly of Arina LrFor , an Lr14a -containing wheat line. Lr14a encodes a membrane-localized protein containing twelve ankyrin (ANK) repeats and structural similarities to Ca 2+ -permeable non-selective cation channels. Transcriptome analyses reveal an induction of genes associated with calcium ion binding in the presence of Lr14a . Haplotype analyses indicate that Lr14a- containing chromosome segments were introgressed multiple times into the bread wheat gene pool, but we find no variation in the Lr14a coding sequence itself. Our work demonstrates the involvement of an ANK-transmembrane (TM)-like type of gene family in race-specific disease resistance in wheat. This forms the basis to explore ANK-TM-like genes in disease resistance breeding. Winter wheat cultivar Forno harbors a race-specific leaf rust resistance locus Lr14a , but the causative gene is unknown. Here, the authors show that Lr14a encodes a membrane-localized protein containing ankyrin repeats and Lr14a -containing segments have been introgressed into the bread wheat gene pool multiple times.
AbstractList Plasma membrane-associated and intracellular proteins and protein complexes play a pivotal role in pathogen recognition and disease resistance signaling in plants and animals. The two predominant protein families perceiving plant pathogens are receptor-like kinases and nucleotide binding-leucine-rich repeat receptors (NLR), which often confer race-specific resistance. Leaf rust is one of the most prevalent and most devastating wheat diseases. Here, we clone the race-specific leaf rust resistance gene Lr14a from hexaploid wheat. The cloning of Lr14a is aided by the recently published genome assembly of Arina LrFor , an Lr14a -containing wheat line. Lr14a encodes a membrane-localized protein containing twelve ankyrin (ANK) repeats and structural similarities to Ca 2+ -permeable non-selective cation channels. Transcriptome analyses reveal an induction of genes associated with calcium ion binding in the presence of Lr14a . Haplotype analyses indicate that Lr14a- containing chromosome segments were introgressed multiple times into the bread wheat gene pool, but we find no variation in the Lr14a coding sequence itself. Our work demonstrates the involvement of an ANK-transmembrane (TM)-like type of gene family in race-specific disease resistance in wheat. This forms the basis to explore ANK-TM-like genes in disease resistance breeding. Winter wheat cultivar Forno harbors a race-specific leaf rust resistance locus Lr14a , but the causative gene is unknown. Here, the authors show that Lr14a encodes a membrane-localized protein containing ankyrin repeats and Lr14a -containing segments have been introgressed into the bread wheat gene pool multiple times.
Plasma membrane-associated and intracellular proteins and protein complexes play a pivotal role in pathogen recognition and disease resistance signaling in plants and animals. The two predominant protein families perceiving plant pathogens are receptor-like kinases and nucleotide binding-leucine-rich repeat receptors (NLR), which often confer race-specific resistance. Leaf rust is one of the most prevalent and most devastating wheat diseases. Here, we clone the race-specific leaf rust resistance gene Lr14a from hexaploid wheat. The cloning of Lr14a is aided by the recently published genome assembly of ArinaLrFor, an Lr14a-containing wheat line. Lr14a encodes a membrane-localized protein containing twelve ankyrin (ANK) repeats and structural similarities to Ca2+-permeable non-selective cation channels. Transcriptome analyses reveal an induction of genes associated with calcium ion binding in the presence of Lr14a. Haplotype analyses indicate that Lr14a-containing chromosome segments were introgressed multiple times into the bread wheat gene pool, but we find no variation in the Lr14a coding sequence itself. Our work demonstrates the involvement of an ANK-transmembrane (TM)-like type of gene family in race-specific disease resistance in wheat. This forms the basis to explore ANK-TM-like genes in disease resistance breeding.Plasma membrane-associated and intracellular proteins and protein complexes play a pivotal role in pathogen recognition and disease resistance signaling in plants and animals. The two predominant protein families perceiving plant pathogens are receptor-like kinases and nucleotide binding-leucine-rich repeat receptors (NLR), which often confer race-specific resistance. Leaf rust is one of the most prevalent and most devastating wheat diseases. Here, we clone the race-specific leaf rust resistance gene Lr14a from hexaploid wheat. The cloning of Lr14a is aided by the recently published genome assembly of ArinaLrFor, an Lr14a-containing wheat line. Lr14a encodes a membrane-localized protein containing twelve ankyrin (ANK) repeats and structural similarities to Ca2+-permeable non-selective cation channels. Transcriptome analyses reveal an induction of genes associated with calcium ion binding in the presence of Lr14a. Haplotype analyses indicate that Lr14a-containing chromosome segments were introgressed multiple times into the bread wheat gene pool, but we find no variation in the Lr14a coding sequence itself. Our work demonstrates the involvement of an ANK-transmembrane (TM)-like type of gene family in race-specific disease resistance in wheat. This forms the basis to explore ANK-TM-like genes in disease resistance breeding.
Plasma membrane-associated and intracellular proteins and protein complexes play a pivotal role in pathogen recognition and disease resistance signaling in plants and animals. The two predominant protein families perceiving plant pathogens are receptor-like kinases and nucleotide binding-leucine-rich repeat receptors (NLR), which often confer race-specific resistance. Leaf rust is one of the most prevalent and most devastating wheat diseases. Here, we clone the race-specific leaf rust resistance gene Lr14a from hexaploid wheat. The cloning of Lr14a is aided by the recently published genome assembly of Arina LrFor , an Lr14a -containing wheat line. Lr14a encodes a membrane-localized protein containing twelve ankyrin (ANK) repeats and structural similarities to Ca 2+ -permeable non-selective cation channels. Transcriptome analyses reveal an induction of genes associated with calcium ion binding in the presence of Lr14a . Haplotype analyses indicate that Lr14a- containing chromosome segments were introgressed multiple times into the bread wheat gene pool, but we find no variation in the Lr14a coding sequence itself. Our work demonstrates the involvement of an ANK-transmembrane (TM)-like type of gene family in race-specific disease resistance in wheat. This forms the basis to explore ANK-TM-like genes in disease resistance breeding.
Plasma membrane-associated and intracellular proteins and protein complexes play a pivotal role in pathogen recognition and disease resistance signaling in plants and animals. The two predominant protein families perceiving plant pathogens are receptor-like kinases and nucleotide binding-leucine-rich repeat receptors (NLR), which often confer race-specific resistance. Leaf rust is one of the most prevalent and most devastating wheat diseases. Here, we clone the race-specific leaf rust resistance gene Lr14a from hexaploid wheat. The cloning of Lr14a is aided by the recently published genome assembly of ArinaLrFor, an Lr14a-containing wheat line. Lr14a encodes a membrane-localized protein containing twelve ankyrin (ANK) repeats and structural similarities to Ca2+-permeable non-selective cation channels. Transcriptome analyses reveal an induction of genes associated with calcium ion binding in the presence of Lr14a. Haplotype analyses indicate that Lr14a-containing chromosome segments were introgressed multiple times into the bread wheat gene pool, but we find no variation in the Lr14a coding sequence itself. Our work demonstrates the involvement of an ANK-transmembrane (TM)-like type of gene family in race-specific disease resistance in wheat. This forms the basis to explore ANK-TM-like genes in disease resistance breeding.Winter wheat cultivar Forno harbors a race-specific leaf rust resistance locus Lr14a, but the causative gene is unknown. Here, the authors show that Lr14a encodes a membrane-localized protein containing ankyrin repeats and Lr14a-containing segments have been introgressed into the bread wheat gene pool multiple times.
Plasma membrane-associated and intracellular proteins and protein complexes play a pivotal role in pathogen recognition and disease resistance signaling in plants and animals. The two predominant protein families perceiving plant pathogens are receptor-like kinases and nucleotide binding-leucine-rich repeat receptors (NLR), which often confer race-specific resistance. Leaf rust is one of the most prevalent and most devastating wheat diseases. Here, we clone the race-specific leaf rust resistance gene Lr14a from hexaploid wheat. The cloning of Lr14a is aided by the recently published genome assembly of ArinaLrFor, an Lr14a-containing wheat line. Lr14a encodes a membrane-localized protein containing twelve ankyrin (ANK) repeats and structural similarities to Ca -permeable non-selective cation channels. Transcriptome analyses reveal an induction of genes associated with calcium ion binding in the presence of Lr14a. Haplotype analyses indicate that Lr14a-containing chromosome segments were introgressed multiple times into the bread wheat gene pool, but we find no variation in the Lr14a coding sequence itself. Our work demonstrates the involvement of an ANK-transmembrane (TM)-like type of gene family in race-specific disease resistance in wheat. This forms the basis to explore ANK-TM-like genes in disease resistance breeding.
Winter wheat cultivar Forno harbors a race-specific leaf rust resistance locus Lr14a, but the causative gene is unknown. Here, the authors show that Lr14a encodes a membrane-localized protein containing ankyrin repeats and Lr14a-containing segments have been introgressed into the bread wheat gene pool multiple times.
ArticleNumber 956
Author Karafiátová, Miroslava
Zhu, Wangsheng
Poretti, Manuel
Zbinden, Helen
Keller, Beat
Wicker, Thomas
Krattinger, Simon G.
Gronnier, Julien
Zipfel, Cyril
Singla, Jyoti
Šimková, Hana
Sánchez-Martín, Javier
Doležel, Jaroslav
Glauser, Gaétan
Kolodziej, Markus C.
Köster, Philipp
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/33574268$$D View this record in MEDLINE/PubMed
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Snippet Plasma membrane-associated and intracellular proteins and protein complexes play a pivotal role in pathogen recognition and disease resistance signaling in...
Winter wheat cultivar Forno harbors a race-specific leaf rust resistance locus Lr14a, but the causative gene is unknown. Here, the authors show that Lr14a...
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SubjectTerms 14/19
38
38/91
42
45
631/208/8
631/449/2169
631/449/2491
631/449/2661/2666
Ankyrin Repeat - genetics
Ankyrins
Basidiomycota - pathogenicity
Binding
Bread
Calcium channels
Calcium ions
Calcium permeability
Chromosomes
Cloning
Cultivars
Disease
Disease resistance
Disease Resistance - genetics
Gene expression
Gene Expression Regulation, Plant
Gene Pool
Gene Silencing
Genes
Genes, Plant - genetics
Genomes
Haplotypes
Humanities and Social Sciences
Ion channels
Kinases
Leaf rust
Leaves
Leucine
Membrane proteins
Membrane Proteins - genetics
Membranes
multidisciplinary
Mutagenesis
Nicotiana - genetics
Nucleotides
Pathogens
Plant Breeding
Plant Diseases - genetics
Plant Proteins - genetics
Protein families
Proteins
Race
Receptors
Science
Science (multidisciplinary)
Segments
Transcriptomes
Triticum - genetics
Wheat
Winter wheat
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Title A membrane-bound ankyrin repeat protein confers race-specific leaf rust disease resistance in wheat
URI https://link.springer.com/article/10.1038/s41467-020-20777-x
https://www.ncbi.nlm.nih.gov/pubmed/33574268
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https://pubmed.ncbi.nlm.nih.gov/PMC7878491
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Volume 12
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