Wheat Pm55 alleles exhibit distinct interactions with an inhibitor to cause different powdery mildew resistance

. 2024 Jan 13 ; 15 (1) : 503. [epub] 20240113

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid38218848
Odkazy

PubMed 38218848
PubMed Central PMC10787760
DOI 10.1038/s41467-024-44796-0
PII: 10.1038/s41467-024-44796-0
Knihovny.cz E-zdroje

Powdery mildew poses a significant threat to wheat crops worldwide, emphasizing the need for durable disease control strategies. The wheat-Dasypyrum villosum T5AL·5 V#4 S and T5DL·5 V#4 S translocation lines carrying powdery mildew resistant gene Pm55 shows developmental-stage and tissue-specific resistance, whereas T5DL·5 V#5 S line carrying Pm5V confers resistance at all stages. Here, we clone Pm55 and Pm5V, and reveal that they are allelic and renamed as Pm55a and Pm55b, respectively. The two Pm55 alleles encode coiled-coil, nucleotide-binding site-leucine-rich repeat (CNL) proteins, conferring broad-spectrum resistance to powdery mildew. However, they interact differently with a linked inhibitor gene, SuPm55 to cause different resistance to wheat powdery mildew. Notably, Pm55 and SuPm55 encode unrelated CNL proteins, and the inactivation of SuPm55 significantly reduces plant fitness. Combining SuPm55/Pm55a and Pm55b in wheat does not result in allele suppression or yield penalty. Our results provide not only insights into the suppression of resistance in wheat, but also a strategy for breeding durable resistance.

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Tian D, Traw MB, Chen JQ, Kreitman M, Bergelson J. Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature. 2013;423:74–77. doi: 10.1038/nature01588. PubMed DOI

Develey-Rivière MP, Galiana E. Resistance to pathogens and host developmental stage: a multifaceted relationship within the plant kingdom. New Phytol. 2007;175:405–416. doi: 10.1111/j.1469-8137.2007.02130.x. PubMed DOI

Adachi H, Derevnina L, Kamoun S. NLR singletons, pairs, and networks: evolution, assembly, and regulation of the intracellular immunoreceptor circuitry of plants. Curr. Opin. Plant Biol. 2019;50:121–131. doi: 10.1016/j.pbi.2019.04.007. PubMed DOI

Deng Y, et al. Epigenetic regulation of antagonistic receptors confers rice blast resistance with yield balance. Science. 2017;355:962–965. doi: 10.1126/science.aai8898. PubMed DOI

Whalen MC. Host defense in a developmental context. Mol. Plant Pathol. 2005;6:347–360. doi: 10.1111/j.1364-3703.2005.00286.x. PubMed DOI

Johnson R. A critical analysis of durable resistance. Annu. Rev. Phytopathol. 1984;22:309–330. doi: 10.1146/annurev.py.22.090184.001521. DOI

Fu D, et al. A kinase-START gene confers temperature-dependent resistance to wheat stripe rust. Science. 2009;323:1357–1360. doi: 10.1126/science.1166289. PubMed DOI PMC

Krattinger SG, et al. A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science. 2009;323:1360–1363. doi: 10.1126/science.1166453. PubMed DOI

Moore JW, et al. A recently evolved hexose transporter variant confers resistance to multiple pathogens in wheat. Nat. Genet. 2015;47:1494–1498. doi: 10.1038/ng.3439. PubMed DOI

Ellis JG, Lagudah ES, Spielmeyer W, Dodds PN. The past, present and future of breeding rust resistant wheat. Front. Plant Sci. 2014;5:641. doi: 10.3389/fpls.2014.00641. PubMed DOI PMC

Richard MMS, Gratias A, Meyers BC, Geffroy V. Molecular mechanisms that limit the costs of NLR-mediated resistance in plants. Mol. Plant Pathol. 2018;19:2516–2523. doi: 10.1111/mpp.12723. PubMed DOI PMC

Zhang RQ, et al. Pm55, a developmental-stage and tissue-specific powdery mildew resistance gene introgressed from Dasypyrum villosum into common wheat. Theor. Appl. Genet. 2016;129:975–1984. doi: 10.1007/s00122-016-2753-8. PubMed DOI

Zhang RQ, et al. Pm67, a new powdery mildew resistance gene transferred from Dasypyrum villosum chromosome 1V to common wheat (Triticum aestivum L.) Crop J. 2021;9:882–888. doi: 10.1016/j.cj.2020.09.012. DOI

Manser B, et al. Identification of specificity-defining amino acids of the wheat immune receptor Pm2 and powdery mildew effector AvrPm2. Plant J. 2021;106:993–1007. doi: 10.1111/tpj.15214. PubMed DOI

Bhullar NK, Street K, Mackay M, Yahiaoui N, Keller B. Unlocking wheat genetic resources for the molecular identification of previously undescribed functional alleles at the Pm3 resistance locus. Proc. Natl Acad. Sci. USA. 2009;106:9519–9524. doi: 10.1073/pnas.0904152106. PubMed DOI PMC

Lu X, et al. Allelic barley MLA immune receptors recognize sequence unrelated avirulence effectors of the powdery mildew pathogen. Proc. Natl Acad. Sci. USA. 2016;113:6486–6495. doi: 10.1073/pnas.1612947113. PubMed DOI PMC

Bourras S, et al. Multiple avirulence loci and allele-specific effector recognition control the Pm3 race-specific resistance of wheat to powdery mildew. Plant Cell. 2015;27:2991–3012. PubMed PMC

Brunner S, et al. Intragenic allele pyramiding combines different specificities of wheat Pm3 resistance alleles. Plant J. 2010;64:433–445. doi: 10.1111/j.1365-313X.2010.04342.x. PubMed DOI

Hiebert CW, et al. Stem rust resistance in wheat is suppressed by a subunit of the mediator complex. Nat. Commun. 2020;11:1123. doi: 10.1038/s41467-020-14937-2. PubMed DOI PMC

Stirnweis D, et al. Suppression among alleles encoding nucleotide binding-leucine-rich repeat resistance proteins interferes with resistance in F1 hybrid and allele-pyramided wheat plants. Plant J. 2014;79:893–903. doi: 10.1111/tpj.12592. PubMed DOI

Hurni S, et al. The powdery mildew resistance gene Pm8 derived from rye is suppressed by its wheat ortholog Pm3. Plant J. 2014;79:904–913. doi: 10.1111/tpj.12593. PubMed DOI

Xing LP, et al. Pm21 from Haynaldia villosa encodes a CC-NBS-LRR protein conferring powdery mildew resistance in wheat. Mol. Plant. 2018;11:874–878. doi: 10.1016/j.molp.2018.02.013. PubMed DOI

Zhang RQ, et al. Pm62, an adult-plant powdery mildew resistance gene introgressed from Dasypyrum villosum chromosome arm 2VL into wheat. Theor. Appl. Genet. 2018;131:2613–2620. doi: 10.1007/s00122-018-3176-5. PubMed DOI

Zhang RQ, et al. Fine mapping of powdery mildew and stripe rust resistance genes Pm5V/Yr5V transferred from Dasypyrum villosum into wheat without yield penalty. Theor. Appl. Genet. 2022;135:3629–3642. doi: 10.1007/s00122-022-04206-9. PubMed DOI

Zhang RQ, et al. The genetic effect of wheat-D. villosum T5VS·5DL translocated chromosome on agronomic characteristics, quality and powdery mildew resistance of common wheat. Sci. Agric. Sin. 2015;48:1041–1051.

Fu BS, et al. Development of molecular markers specific to 5VS chromosome arm of Dasypyrum villosum and their genetic effects in common wheat. J. Plant Gene. Res. 2022;23:195–208.

Zhang X, et al. A chromosome-scale genome assembly of Dasypyrum villosum provides insights into its application as a broad-spectrum disease resistance resource for wheat improvement. Mol. Plant. 2023;16:432–451. doi: 10.1016/j.molp.2022.12.021. PubMed DOI

Praz CR, et al. AvrPm2 encodes an RNase-like avirulence effector which is conserved in the two different specialized forms of wheat and rye powdery mildew fungus. New Phytol. 2017;213:1301–1314. doi: 10.1111/nph.14372. PubMed DOI PMC

Koo DH, Liu W, Friebe B, Gill BS. Homoeologous recombination in the presence of Ph1 gene in wheat. Chromosoma. 2017;126:531–540. doi: 10.1007/s00412-016-0622-5. PubMed DOI

Hurni S, et al. Rye Pm8 and wheat Pm3 are orthologous genes and show evolutionary conservation of resistance function against powdery mildew. Plant J. 2013;76:957–969. doi: 10.1111/tpj.12345. PubMed DOI

Zhu SY, et al. Orthologous genes Pm12 and Pm21 from two wild relatives of wheat show evolutionary conservation but divergent powdery mildew resistance. Plant Commun. 2022;9:100472. PubMed PMC

Xiao J, et al. Wheat genomic study for genetic improvement of traits in China. Sci. China Life Sci. 2022;65:1718–1775. doi: 10.1007/s11427-022-2178-7. PubMed DOI

Wang JZ, Han M, Liu YL. Diversity, structure and function of the coiled-coil domains of plant NLR immune receptors. J. Integr. Plant Biol. 2021;63:283–296. doi: 10.1111/jipb.13032. PubMed DOI

Césari S, et al. The NB-LRR proteins RGA4 and RGA5 interact functionally and physically to confer disease resistance. Embo. J. 2014;33:1941–1959. doi: 10.15252/embj.201487923. PubMed DOI PMC

Kourelis J, van der Hoorn RAL. Defended to the nines: 25 years of resistance gene cloning identifies nine mechanisms for R protein function. Plant Cell. 2018;30:285–299. doi: 10.1105/tpc.17.00579. PubMed DOI PMC

Luo M, et al. A five-transgene cassette confers broad-spectrum resistance to a fungal rust pathogen in wheat. Nat. Biotechnol. 2021;39:561–566. doi: 10.1038/s41587-020-00770-x. PubMed DOI

Koller T, Brunner S, Herren G, Hurni S, Keller B. Pyramiding of transgenic Pm3 alleles in wheat results in improved powdery mildew resistance in the field. Theor. Appl. Genet. 2018;131:861–871. doi: 10.1007/s00122-017-3043-9. PubMed DOI PMC

Zou SH, Wang H, Li Y, Kong ZS, Tang DZ. The NB-LRR gene Pm60 confers powdery mildew resistance in wheat. New Phytol. 2018;218:298–309. doi: 10.1111/nph.14964. PubMed DOI

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. doi: 10.1038/s41467-020-14294-0. PubMed DOI PMC

Said M, et al. Dissecting the complex genome of crested wheatgrass by chromosome flow sorting. Plant Genome. 2019;12:180096. doi: 10.3835/plantgenome2018.12.0096. PubMed DOI

Šimková H, et al. Coupling amplified DNA from flow-sorted chromosomes to high-density SNP mapping in barley. BMC Genomics. 2008;9:294. doi: 10.1186/1471-2164-9-294. PubMed DOI PMC

Cao WJ, et al. Construction and characterization of three wheat bacterial artificial chromosome libraries. Int. J. Mol. Sci. 2014;15:21896–21912. doi: 10.3390/ijms151221896. PubMed DOI PMC

Zeng, Q. D. et al. Novel high-accuracy genome assembly method utilizing a high-throughput workflow. Preprint 10.1101/2020.11.26.400507 (2020).

Allen GC, Flores-Vergara MA, Krasynanski S, Kumar S, Thompson WF. A modified protocol for rapid DNA isolation from plant tissues using cetyltrimethylammonium bromide. Nat. Protoc. 2006;1:2320–2325. doi: 10.1038/nprot.2006.384. PubMed DOI

Gao CY, Sun PW, Wang W, Tang DZ. Arabidopsis E3 ligase KEG associates with and ubiquitinates MKK4 and MKK5 to regulate plant immunity. J. Integr. Plant Biol. 2021;63:327–339. doi: 10.1111/jipb.13007. PubMed DOI

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. doi: 10.1006/meth.2001.1262. PubMed DOI

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. doi: 10.1371/journal.pone.0026468. PubMed DOI PMC

Ishida Y, Tsunashima M, Hiei Y, Komari T. Wheat (Triticum aestivum L.) transformation using immature embryos. Methods Mol. Biol. 2015;1223:189–198. doi: 10.1007/978-1-4939-1695-5_15. PubMed DOI

Li JH, et al. Dissecting conserved cis-regulatory modules of Glu-1 promoters which confer the highly active endosperm-specific expression via stable wheat transformation. Crop J. 2019;7:8–18. doi: 10.1016/j.cj.2018.08.003. DOI

Zhang SJ, et al. Targeted mutagenesis using the Agrobacterium tumefaciens-mediated CRISPR-Cas9 system in common wheat. BMC Plant Biol. 2018;18:302. doi: 10.1186/s12870-018-1496-x. PubMed DOI PMC

Zhang SJ, et al. CRISPR/Cas9-mediated genome editing for wheat grain quality improvement. Plant Biotechnol. J. 2021;19:1684–1686. doi: 10.1111/pbi.13647. PubMed DOI PMC

Wu XY, Li T. A casein kinase II phosphorylation site in AtYY1 affects its activity, stability, and function in the ABA response. Front. Plant Sci. 2017;8:323. PubMed PMC

Bracha-Drori K, et al. Detection of protein–protein interactions in plants using bimolecular fluorescence complementation. Plant J. 2004;40:419–427. doi: 10.1111/j.1365-313X.2004.02206.x. PubMed DOI

Bai SW, et al. Structure-function analysis of barley NLR immune receptor MLA10 reveals its cell compartment specific activity in cell death and disease resistance. PLoS Pathog. 2012;8:e1002752. doi: 10.1371/journal.ppat.1002752. PubMed DOI PMC

Lin J, et al. Histone acetyltransferase TaHAG1 interacts with TaNACL to promote heat stress tolerance in wheat. Plant Biotechnol. J. 2022;20:1645–1647. doi: 10.1111/pbi.13881. PubMed DOI PMC

Sievers F, et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 2011;7:539–539. doi: 10.1038/msb.2011.75. PubMed DOI PMC

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