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 in | Nature communications Vol. 12; no. 1; pp. 956 - 12 |
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Main Authors | , , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
London
Nature Publishing Group UK
11.02.2021
Nature Publishing Group Nature Portfolio |
Subjects | |
Online Access | Get full text |
ISSN | 2041-1723 2041-1723 |
DOI | 10.1038/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 |
Author_xml | – sequence: 1 givenname: Markus C. orcidid: 0000-0003-3155-2935 surname: Kolodziej fullname: Kolodziej, Markus C. organization: University of Zurich, Department of Plant and Microbial Biology – sequence: 2 givenname: Jyoti surname: Singla fullname: Singla, Jyoti organization: University of Zurich, Department of Plant and Microbial Biology – sequence: 3 givenname: Javier orcidid: 0000-0002-0284-7219 surname: Sánchez-Martín fullname: Sánchez-Martín, Javier organization: University of Zurich, Department of Plant and Microbial Biology – sequence: 4 givenname: Helen surname: Zbinden fullname: Zbinden, Helen organization: University of Zurich, Department of Plant and Microbial Biology – sequence: 5 givenname: Hana orcidid: 0000-0003-4159-7619 surname: Šimková fullname: Šimková, Hana organization: Institute of Experimental Botany of the Czech Academy of Sciences, Centre of the Region Hana for Biotechnological and Agricultural Research – sequence: 6 givenname: Miroslava orcidid: 0000-0003-1177-6472 surname: Karafiátová fullname: Karafiátová, Miroslava organization: Institute of Experimental Botany of the Czech Academy of Sciences, Centre of the Region Hana for Biotechnological and Agricultural Research – sequence: 7 givenname: Jaroslav orcidid: 0000-0002-6263-0492 surname: Doležel fullname: Doležel, Jaroslav organization: Institute of Experimental Botany of the Czech Academy of Sciences, Centre of the Region Hana for Biotechnological and Agricultural Research – sequence: 8 givenname: Julien orcidid: 0000-0002-1429-0542 surname: Gronnier fullname: Gronnier, Julien organization: University of Zurich, Department of Plant and Microbial Biology – sequence: 9 givenname: Manuel orcidid: 0000-0001-6915-2238 surname: Poretti fullname: Poretti, Manuel organization: University of Zurich, Department of Plant and Microbial Biology – sequence: 10 givenname: Gaétan surname: Glauser fullname: Glauser, Gaétan organization: Neuchâtel Platform of Analytical Chemistry, Université de Neuchâtel – sequence: 11 givenname: Wangsheng orcidid: 0000-0001-7773-3438 surname: Zhu fullname: Zhu, Wangsheng organization: Department of Molecular Biology, Max Planck Institute for Developmental Biology, College of Plant Protection, China Agricultural University – sequence: 12 givenname: Philipp orcidid: 0000-0002-1359-822X surname: Köster fullname: Köster, Philipp organization: University of Zurich, Department of Plant and Microbial Biology – sequence: 13 givenname: Cyril orcidid: 0000-0003-4935-8583 surname: Zipfel fullname: Zipfel, Cyril organization: University of Zurich, Department of Plant and Microbial Biology – sequence: 14 givenname: Thomas orcidid: 0000-0002-6777-7135 surname: Wicker fullname: Wicker, Thomas email: wicker@botinst.uzh.ch organization: University of Zurich, Department of Plant and Microbial Biology – sequence: 15 givenname: Simon G. orcidid: 0000-0001-6912-7411 surname: Krattinger fullname: Krattinger, Simon G. email: simon.krattinger@kaust.edu.sa organization: King Abdullah University of Science and Technology (KAUST), Biological and Environmental Science and Engineering Division (BESE) – sequence: 16 givenname: Beat orcidid: 0000-0003-2379-9225 surname: Keller fullname: Keller, Beat email: bkeller@botinst.uzh.ch organization: University of Zurich, Department of Plant and Microbial Biology |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/33574268$$D View this record in MEDLINE/PubMed |
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DOI | 10.1038/s41467-020-20777-x |
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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 |
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