An unusual tandem kinase fusion protein confers leaf rust resistance in wheat

. 2023 Jun ; 55 (6) : 914-920. [epub] 20230522

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu dopisy, práce podpořená grantem, Research Support, U.S. Gov't, Non-P.H.S.

Perzistentní odkaz   https://www.medvik.cz/link/pmid37217716
Odkazy

PubMed 37217716
PubMed Central PMC10260399
DOI 10.1038/s41588-023-01401-2
PII: 10.1038/s41588-023-01401-2
Knihovny.cz E-zdroje

The introgression of chromosome segments from wild relatives is an established strategy to enrich crop germplasm with disease-resistance genes1. Here we use mutagenesis and transcriptome sequencing to clone the leaf rust resistance gene Lr9, which was introduced into bread wheat from the wild grass species Aegilops umbellulata2. We established that Lr9 encodes an unusual tandem kinase fusion protein. Long-read sequencing of a wheat Lr9 introgression line and the putative Ae. umbellulata Lr9 donor enabled us to assemble the ~28.4-Mb Lr9 translocation and to identify the translocation breakpoint. We likewise cloned Lr58, which was reportedly introgressed from Aegilops triuncialis3, but has an identical coding sequence compared to Lr9. Cytogenetic and haplotype analyses corroborate that the two genes originate from the same translocation event. Our work sheds light on the emerging role of kinase fusion proteins in wheat disease resistance, expanding the repertoire of disease-resistance genes for breeding.

Komentář v

PubMed

Zobrazit více v PubMed

Wulff BB, Moscou MJ. Strategies for transferring resistance into wheat: from wide crosses to GM cassettes. Front. Plant Sci. 2014;5:692. PubMed PMC

Sears, E. R. Brookhaven Symposia in Biology Vol. 9, pp. 1–21 (1956).

Kuraparthy V, et al. A cryptic wheat-Aegilops triuncialis translocation with leaf rust resistance gene Lr58. Crop Sci. 2007;47:1995–2003.

Tadesse W, et al. Genetic gains in wheat breeding and its role in feeding the world. Crop Breed. Genet. Genom. 2019;1:e190005.

Savary S, et al. The global burden of pathogens and pests on major food crops. Nat. Ecol. Evol. 2019;3:430–439. PubMed

Kolmer J. Leaf rust of wheat: pathogen biology, variation and host resistance. Forests. 2013;4:70–84.

Hafeez AN, et al. Creation and judicious application of a wheat resistance gene atlas. Mol. Plant. 2021;14:1053–1070. PubMed

Said M, et al. Development of DNA markers from physically mapped loci in Aegilops comosa and Aegilops umbellulata using single-gene FISH and chromosome sequences. Front. Plant Sci. 2021;12:689031. PubMed PMC

Molnar-Lang, M., Ceoloni, C. & Dolezel, J. Alien Introgression in Wheat (Springer, 2015).

Schachermayr G, et al. Identification and localization of molecular markers linked to the Lr9 leaf rust resistance gene of wheat. Theor. Appl. Genet. 1994;88:110–115. PubMed

Huerta-Espino J, Singh RP, Reyna-Martinez J. First detection of virulence to genes Lr9 and Lr25 conferring resistance to leaf rust of wheat caused by Puccinia triticina in Mexico. Plant Dis. 2008;92:311. PubMed

Brueggeman R, et al. The barley stem rust-resistance gene Rpg1 is a novel disease-resistance gene with homology to receptor kinases. Proc. Natl Acad. Sci. USA. 2002;99:9328–9333. PubMed PMC

Klymiuk V, et al. Cloning of the wheat Yr15 resistance gene sheds light on the plant tandem kinase-pseudokinase family. Nat. Commun. 2018;9:3735. PubMed PMC

Chen SS, et al. Wheat gene Sr60 encodes a protein with two putative kinase domains that confers resistance to stem rust. N. Phytol. 2020;225:948–959. PubMed

Lu P, et al. A rare gain of function mutation in a wheat tandem kinase confers resistance to powdery mildew. Nat. Commun. 2020;11:680. PubMed PMC

Gaurav K, et al. Population genomic analysis of Aegilops tauschii identifies targets for bread wheat improvement. Nat. Biotechnol. 2022;40:422–431. PubMed PMC

Yu G, et al. Aegilops sharonensis genome-assisted identification of stem rust resistance gene Sr62. Nat. Commun. 2022;13:1607. PubMed PMC

Arora S, et al. A wheat kinase and immune receptor form host-specificity barriers against the blast fungus. Nat. Plants. 2023;9:385–392. PubMed PMC

Liu JX, Jambunathan N, McNellis T. Transgenic expression of the von Willebrand A domain of the BONZAI1/COPINE1 protein triggers a lesion-mimic phenotype in Arabidopsis. Planta. 2005;221:85–94. PubMed

Whittaker CA, Hynes RO. Distribution and evolution of von Willebrand/integrin A domains: widely dispersed domains with roles in cell adhesion and elsewhere. Mol. Biol. Cell. 2002;13:3369–3387. PubMed PMC

Yin X, et al. Rice copine genes OsBON1 and OsBON3 function as suppressors of broad-spectrum disease resistance. Plant Biotechnol. J. 2018;16:1476–1487. PubMed PMC

Yang SH, Hua J. A haplotype-specific resistance gene regulated by BONZAI1 mediates temperature-dependent growth control in Arabidopsis. Plant Cell. 2004;16:1060–1071. PubMed PMC

Klymiuk V, Coaker G, Fahima T, Pozniak CJ. Tandem protein kinases emerge as new regulators of plant immunity. Mol. Plant Microbe Interact. 2021;34:1094–1102. PubMed PMC

Huang C, Yoshino-Koh K, Tesmer JJ. A surface of the kinase domain critical for the allosteric activation of G protein-coupled receptor kinases. J. Biol. Chem. 2009;284:17206–17215. PubMed PMC

Bajaj K, Chakrabarti P, Varadarajan R. Mutagenesis-based definitions and probes of residue burial in proteins. Proc. Natl Acad. Sci. USA. 2005;102:16221–16226. PubMed PMC

Hanks SK, Quinn AM, Hunter T. The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science. 1988;241:42–52. PubMed

Leslie ME, Lewis MW, Youn J-Y, Daniels MJ, Liljegren SJ. The EVERSHED receptor-like kinase modulates floral organ shedding in Arabidopsis. Development. 2010;137:467–476. PubMed PMC

International Wheat Genome Sequencing Consortium. Shifting the limits in wheat research and breeding through a fully annotated and anchored reference genome sequence. Science. 2018;361:eaar7191. PubMed

Walkowiak S, et al. Multiple wheat genomes reveal global variation in modern breeding. Nature. 2020;588:277–283. PubMed PMC

Zhu T, et al. Optical maps refine the bread wheat Triticum aestivum cv. Chinese Spring genome assembly. Plant J. 2021;107:303–314. PubMed PMC

Sato K, et al. Chromosome-scale genome assembly of the transformation-amenable common wheat cultivar ‘Fielder’. DNA Res. 2021;28:dsab008. PubMed PMC

Athiyannan N, et al. Long-read genome sequencing of bread wheat facilitates disease resistance gene cloning. Nat. Genet. 2022;54:227–231. PubMed PMC

Aury J-M, et al. Long-read and chromosome-scale assembly of the hexaploid wheat genome achieves high resolution for research and breeding. GigaScience. 2022;11:giac034. PubMed PMC

Maccaferri M, et al. Durum wheat genome highlights past domestication signatures and future improvement targets. Nat. Genet. 2019;51:885–895. PubMed

Zhou Y, et al. Introgressing the Aegilops tauschii genome into wheat as a basis for cereal improvement. Nat. Plants. 2021;7:774–786. PubMed

Li LF, et al. Genome sequences of five Sitopsis species of Aegilops and the origin of polyploid wheat B subgenome. Mol. Plant. 2022;15:488–503. PubMed

Rabanus-Wallace MT, et al. Chromosome-scale genome assembly provides insights into rye biology, evolution and agronomic potential. Nat. Genet. 2021;53:564–573. PubMed PMC

Li G, et al. A high-quality genome assembly highlights rye genomic characteristics and agronomically important genes. Nat. Genet. 2021;53:574–584. PubMed PMC

Studer AJ, et al. The draft genome of the C3 panicoid grass species Dichanthelium oligosanthes. Genome Biol. 2016;17:223. PubMed PMC

Hittalmani S, et al. Genome and transcriptome sequence of finger millet (Eleusine coracana (L.) Gaertn.) provides insights into drought tolerance and nutraceutical properties. BMC Genomics. 2017;18:465. PubMed PMC

Carballo J, et al. A high-quality genome of Eragrostis curvula grass provides insights into Poaceae evolution and supports new strategies to enhance forage quality. Sci. Rep. 2019;9:10250. PubMed PMC

VanBuren R, et al. Exceptional subgenome stability and functional divergence in the allotetraploid Ethiopian cereal teff. Nat. Commun. 2020;11:884. PubMed PMC

van der Hoorn RA, Kamoun S. From Guard to Decoy: a new model for perception of plant pathogen effectors. Plant Cell. 2008;20:2009–2017. PubMed PMC

Wenger AM, et al. Accurate circular consensus long-read sequencing improves variant detection and assembly of a human genome. Nat. Biotechnol. 2019;37:1155–1162. PubMed PMC

Edae EA, Olivera PD, Jin Y, Rouse MN. Genotyping-by-sequencing facilitates a high-density consensus linkage map for Aegilops umbellulata, a wild relative of cultivated wheat. G3 (Bethesda) 2017;7:1551–1561. PubMed PMC

Ortelli S, Winzeler M, Winzeler H, Nösberger J. Leaf rust resistance gene Lr9 and winter wheat yield reduction: II. Leaf gas exchange and root activity. Crop Sci. 1996;36:1595–1601.

Yu, G. et al. The wheat stem rust resistance gene Sr43 encodes an unusual protein kinase. Nat. Genet. 10.1038/s41588-023-01402-1 (2023). PubMed PMC

Fu D, et al. A kinase-START gene confers temperature-dependent resistance to wheat stripe rust. Science. 2009;323:1357–1360. PubMed PMC

Faris JD, et al. A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens. Proc. Natl Acad. Sci. USA. 2010;107:13544–13549. PubMed PMC

Zhang Z, et al. A protein kinase–major sperm protein gene hijacked by a necrotrophic fungal pathogen triggers disease susceptibility in wheat. Plant J. 2021;106:720–732. PubMed

Sánchez-Martín J, et al. Wheat Pm4 resistance to powdery mildew is controlled by alternative splice variants encoding chimeric proteins. Nat. Plants. 2021;7:327–341. PubMed PMC

Messmer MM, et al. Genetic analysis of durable leaf rust resistance in winter wheat. Theor. Appl. Genet. 2000;100:419–431.

Martinez F, Niks RE, Singh RP, Rubiales D. Characterization of Lr46, a gene conferring partial resistance to wheat leaf rust. Hereditas. 2001;135:111–114. PubMed

Kolmer JA. Virulence of Puccinia triticina, the wheat leaf rust fungus, in the United States in 2017. Plant Dis. 2019;103:2113–2120. PubMed

Wang Y, et al. Orthologous receptor kinases quantitatively affect the host status of barley to leaf rust fungi. Nat. Plants. 2019;5:1129–1135. PubMed

Watson A, et al. Speed breeding is a powerful tool to accelerate crop research and breeding. Nat. Plants. 2018;4:23–29. PubMed

Wicker T, Matthews DE, Keller B. TREP: a database for Triticeae repetitive elements. Trends Plant Sci. 2002;7:561–562.

Shen W, Le S, Li Y, Hu F. SeqKit: a cross-platform and ultrafast toolkit for FASTA/Q file manipulation. PLoS One. 2016;11:e0163962. PubMed PMC

Bushnell, B. BBMap: a fast, accurate, splice-aware aligner. Proceedings of 9th Annual Genomics of Energy & Environment Meeting (LBNL Department of Energy Joint Genome Institute, 2014).

Li H, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25:2078–2079. PubMed PMC

Sánchez-Martín J, et al. Rapid gene isolation in barley and wheat by mutant chromosome sequencing. Genome Biol. 2016;17:221. PubMed PMC

Chen C, et al. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol. Plant. 2020;13:1194–1202. PubMed

Green, M. R. & Sambrook, J. Nested polymerase chain reaction (PCR). Cold Spring Harb. Protoc. 2019, (2019). PubMed

Yuan C, et al. A high throughput barley stripe mosaic virus vector for virus induced gene silencing in monocots and dicots. PLoS One. 2011;6:e26468. PubMed PMC

Jumper J, et al. Highly accurate protein structure prediction with AlphaFold. Nature. 2021;596:583–589. PubMed PMC

Koo D-H, Liu W, Friebe B, Gill BS. Homoeologous recombination in the presence of Ph1 gene in wheat. Chromosoma. 2017;126:531–540. PubMed

Koo D-H, et al. Extrachromosomal circular DNA-based amplification and transmission of herbicide resistance in crop weed Amaranthus palmeri. Proc. Natl Acad. Sci. USA. 2018;115:3332–3337. PubMed PMC

Ma S, et al. WheatOmics: a platform combining multiple omics data to accelerate functional genomics studies in wheat. Mol. Plant. 2021;14:1965–1968. PubMed

Karkute SG, et al. Genome-wide analysis of von Willebrand factor A gene family in rice for its role in imparting biotic stress resistance with emphasis on rice blast disease. Rice Sci. 2022;29:375–384.

Driguez P, et al. LeafGo: Leaf to Genome, a quick workflow to produce high-quality de novo plant genomes using long-read sequencing technology. Genome Biol. 2021;22:256. PubMed PMC

Cheng H, Concepcion GT, Feng X, Zhang H, Li H. Haplotype-resolved de novo assembly using phased assembly graphs with hifiasm. Nat. Methods. 2021;18:170–175. PubMed PMC

Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics. 2013;29:1072–1075. PubMed PMC

Li H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics. 2018;34:3094–3100. PubMed PMC

Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010;26:841–842. PubMed PMC

Pedersen BS, Quinlan AR. Mosdepth: quick coverage calculation for genomes and exomes. Bioinformatics. 2018;34:867–868. PubMed PMC

Marcais, G. & Kingsford, C. Jellyfish: a fast k-mer counter. https://www.cbcb.umd.edu/software/jellyfish/jellyfish-manual-1.1.pdf (2012).

Gupta SK, Charpe A, Koul S, Prabhu KV, Haq QMR. Development and validation of molecular markers linked to an Aegilops umbellulata–derived leaf-rust-resistance gene, Lr9, for marker-assisted selection in bread wheat. Genome. 2005;48:823–830. PubMed

Kuraparthy V, Sood S, Guedira G-B, Gill BS. Development of a PCR assay and marker-assisted transfer of leaf rust resistance gene Lr58 into adapted winter wheats. Euphytica. 2011;180:227–234.

Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods. 2001;25:402–408. PubMed

Zobrazit více v PubMed

Dryad
10.5061/dryad.gxd2547pw

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace