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

. 2021 Feb 11 ; 12 (1) : 956. [epub] 20210211

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid33574268
Odkazy

PubMed 33574268
PubMed Central PMC7878491
DOI 10.1038/s41467-020-20777-x
PII: 10.1038/s41467-020-20777-x
Knihovny.cz E-zdroje

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.

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Kolmer J. Leaf Rust of Wheat: Pathogen Biology, Variation and Host Resistance. Forests. 2013;4:70–84. doi: 10.3390/f4010070. DOI

Schnurbusch T, et al. Dissection of quantitative and durable leaf rust resistance in Swiss winter wheat reveals a major resistance QTL in the Lr34 chromosomal region. Theor. Appl. Genet. 2004;108:477–484. doi: 10.1007/s00122-003-1444-4. PubMed DOI

Lagudah ES, et al. Gene-specific markers for the wheat gene Lr34/Yr18/Pm38 which confers resistance to multiple fungal pathogens. Theor. Appl. Genet. 2009;119:889–898. doi: 10.1007/s00122-009-1097-z. PubMed DOI

Singla J, et al. Characterization of Lr75: a partial, broad-spectrum leaf rust resistance gene in wheat. Theor. Appl .Genet. 2017;130:1–12. doi: 10.1007/s00122-016-2784-1. PubMed DOI

McIntosh, R. A., Wellings, C. R. & Park, R. F. Wheat Rusts: an Atlas of Resistance Genes (Springer, Netherlands, 1995).

Dyck P, Johnson R. Temperature sensitivity of genes for resistance in wheat to Puccinia recondita. Can. J. Plant Pathol. 1983;5:229–234. doi: 10.1080/07060668309501601. DOI

Dyck PL, Samborski DJ. The genetics of two alleles for leaf rust resistance at the Lr14 locus in wheat. Can. J. Genet. Cytol. 1970;12:689–694. doi: 10.1139/g70-091. DOI

Law CN, Johnson R. A genetic study of leaf rust resistance in wheat. Can. J. Genet. Cytol. 1967;9:805–822. doi: 10.1139/g67-086. DOI

Walkowiak S, et al. Multiple wheat genomes reveal global variation in modern breeding. Nature. 2020;588:277–283. doi: 10.1038/s41586-020-2961-x. PubMed DOI PMC

Sanchez-Martin J, et al. Rapid gene isolation in barley and wheat by mutant chromosome sequencing. Genome Biol. 2016;17:221. doi: 10.1186/s13059-016-1082-1. PubMed DOI PMC

Mosavi LK, Cammett TJ, Desrosiers DC, Peng ZY. The ankyrin repeat as molecular architecture for protein recognition. Protein Sci. 2004;13:1435–1448. doi: 10.1110/ps.03554604. PubMed DOI PMC

Li J, Mahajan A, Tsai MD. Ankyrin repeat: a unique motif mediating protein-protein interactions. Biochemistry. 2006;45:15168–15178. doi: 10.1021/bi062188q. PubMed DOI

Vo KTX, et al. Molecular insights into the function of ankyrin proteins in plants. J. Plant Biol. 2015;58:271–284. doi: 10.1007/s12374-015-0228-0. DOI

Singh RP, et al. Disease impact on wheat yield potential and prospects of genetic control. Annu. Rev. Phytopathol. 2016;54:303–322. doi: 10.1146/annurev-phyto-080615-095835. PubMed DOI

Zhang W, et al. Identification and characterization of Sr13, a tetraploid wheat gene that confers resistance to the Ug99 stem rust race group. Proc. Natl Acad. Sci. 2017;114:E9483–E9492. doi: 10.1073/pnas.1706277114. PubMed DOI PMC

Marone D, et al. Genetic analysis of durable resistance against leaf rust in durum wheat. Mol. Breed. 2009;24:25–39. doi: 10.1007/s11032-009-9268-9. DOI

Yahiaoui N, Kaur N, Keller B. Independent evolution of functional Pm3 resistance genes in wild tetraploid wheat and domesticated bread wheat. Plant J. 2009;57:846–856. doi: 10.1111/j.1365-313X.2008.03731.x. PubMed DOI

McFadden ES. A successful transfer of emmer characters to Vulgare wheat. Agron. J. 1930;12:1020–1034. doi: 10.2134/agronj1930.00021962002200120005x. DOI

Dong X. The role of membrane-bound ankyrin-repeat protein ACD6 in programmed cell death and plant defense. Sci. STKE. 2004;2004:pe6. PubMed

Sakamoto H, Matsuda O, Iba K. ITN1, a novel gene encoding an ankyrin-repeat protein that affects the ABA-mediated production of reactive oxygen species and is involved in salt-stress tolerance in Arabidopsis thaliana. Plant J. 2008;56:411–422. doi: 10.1111/j.1365-313X.2008.03614.x. PubMed DOI

Yang Y, et al. The ankyrin-repeat transmembrane protein BDA1 functions downstream of the receptor-like protein SNC2 to regulate plant immunity. Plant Physiol. 2012;159:1857–1865. doi: 10.1104/pp.112.197152. PubMed DOI PMC

Zhang Z, Guo J, Zhao Y, Chen J. Identification and characterization of maize ACD6-like gene reveal ZmACD6 as the maize orthologue conferring resistance to Ustilago maydis. Plant Signal. Behav. 2019;14:e1651604. doi: 10.1080/15592324.2019.1651604. PubMed DOI PMC

Todesco M, et al. Natural allelic variation underlying a major fitness trade-off in Arabidopsis thaliana. Nature. 2010;465:632–636. doi: 10.1038/nature09083. PubMed DOI PMC

Lu H, Liu Y, Greenberg JT. Structure-function analysis of the plasma membrane-localized Arabidopsis defense component ACD6. Plant J. 2005;44:798–809. doi: 10.1111/j.1365-313X.2005.02567.x. PubMed DOI

Zhang Z, Shrestha J, Tateda C, Greenberg JT. Salicylic acid signaling controls the maturation and localization of the arabidopsis defense protein ACCELERATED CELL DEATH6. Mol. Plant. 2014;7:1365–1383. doi: 10.1093/mp/ssu072. PubMed DOI PMC

Tateda C, et al. Salicylic acid regulates Arabidopsis microbial pattern receptor kinase levels and signaling. Plant Cell. 2014;26:4171–4187. doi: 10.1105/tpc.114.131938. PubMed DOI PMC

Lu H, Rate DN, Song JT, Greenberg JT. ACD6, a novel ankyrin protein, is a regulator and an effector of salicylic acid signaling in the Arabidopsis defense response. Plant Cell. 2003;15:2408–2420. doi: 10.1105/tpc.015412. PubMed DOI PMC

Suo Y, et al. Structural insights into electrophile irritant sensing by the human TRPA1 channel. Neuron. 2020;105:882–894 e5. doi: 10.1016/j.neuron.2019.11.023. PubMed DOI PMC

Leng L, et al. A subclass of HSP70s regulate development and abiotic stress responses in Arabidopsis thaliana. J. Plant Res. 2017;130:349–363. doi: 10.1007/s10265-016-0900-6. PubMed DOI

La Verde, V., Dominici, P. & Astegno, A. Towards understanding plant calcium signaling through calmodulin-like proteins: a biochemical and structural perspective. Int. J. Mol. Sci.19 1331 (2018). PubMed PMC

Tuteja N, Mahajan S. Calcium signaling network in plants: an overview. Plant Signal Behav. 2007;2:79–85. doi: 10.4161/psb.2.2.4176. PubMed DOI PMC

Dodd AN, Kudla J, Sanders D. The language of calcium signaling. Annu. Rev. Plant Biol. 2010;61:593–620. doi: 10.1146/annurev-arplant-070109-104628. PubMed DOI

Pitino M, Allen V, Duan Y. LasDelta5315 effector induces extreme starch accumulation and chlorosis as Ca. Liberibacter asiaticus infection in Nicotiana benthamiana. Front Plant Sci. 2018;9:113. doi: 10.3389/fpls.2018.00113. PubMed DOI PMC

Zhou B, Guo Z. Calcium is involved in the abscisic acid-induced ascorbate peroxidase, superoxide dismutase and chilling resistance in Stylosanthes guianensis. Biol. Plant. 2009;53:63–68. doi: 10.1007/s10535-009-0009-z. DOI

Lehtonen J. The significance of Ca2+ in the morphogenesis of Micrasterias studied with EGTA, verapamil, LaCl3 and calcium ionophore A 23187. Plant Sci. Lett. 1984;33:53–60. doi: 10.1016/0304-4211(84)90068-3. DOI

Zhu W, et al. Modulation of ACD6 dependent hyperimmunity by natural alleles of an Arabidopsis thaliana NLR resistance gene. PLoS Genet. 2018;14:e1007628. doi: 10.1371/journal.pgen.1007628. PubMed DOI PMC

Bogdanove AJ, Voytas DF. TAL effectors: customizable proteins for DNA targeting. Science. 2011;333:1843–1846. doi: 10.1126/science.1204094. PubMed DOI

Boch J, et al. Breaking the code of DNA binding specificity of TAL-type III effectors. Science. 2009;326:1509–1512. doi: 10.1126/science.1178811. PubMed DOI

Wang H, Zou S, Li Y, Lin F, Tang D. An ankyrin-repeat and WRKY-domain-containing immune receptor confers stripe rust resistance in wheat. Nat. Commun. 2020;11:1353. doi: 10.1038/s41467-020-15139-6. PubMed DOI PMC

Loutre C, et al. Two different CC-NBS-LRR genes are required for Lr10-mediated leaf rust resistance in tetraploid and hexaploid wheat. Plant J. 2009;60:1043–1054. doi: 10.1111/j.1365-313X.2009.04024.x. PubMed DOI

Messmer MM, et al. Genetic analysis of durable leaf rust resistance in winter wheat. Theor. Appl. Genet. 2000;100:419–431. doi: 10.1007/s001220050055. DOI

Peterson RF, Campbell AB, Hannah AE. A Diagrammatic scale for estimating rust intensity on leaves and stems of cereals. Can. J. Res. C: Botanical Sci. 1948;26:496–49. doi: 10.1139/cjr48c-033. DOI

Dolezel J, et al. Chromosomes in the flow to simplify genome analysis. Funct. Integr. Genomics. 2012;12:397–416. doi: 10.1007/s10142-012-0293-0. PubMed DOI PMC

Kubalakova M, Vrana J, Cihalikova J, Simkova H, Dolezel J. Flow karyotyping and chromosome sorting in bread wheat (Triticum aestivum L.) Theor. Appl Genet. 2002;104:1362–1372. doi: 10.1007/s00122-002-0888-2. PubMed DOI

Vrana J, et al. Flow sorting of mitotic chromosomes in common wheat (Triticum aestivum L.) Genetics. 2000;156:2033–2041. PubMed PMC

Giorgi D, et al. FISHIS: fluorescence in situ hybridization in suspension and chromosome flow sorting made easy. PLoS ONE. 2013;8:e57994. doi: 10.1371/journal.pone.0057994. PubMed DOI PMC

Simkova 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

Kubalakova M, et al. Analysis and sorting of rye (Secale cereale L.) chromosomes using flow cytometry. Genome. 2003;46:893–905. doi: 10.1139/g03-054. PubMed DOI

Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. J. 2011;17:10. doi: 10.14806/ej.17.1.200. DOI

Bhullar, N. K. & Keller, B. in (Pankaj K. Bhowmik Saikat K. Basu Aakash Goyal (eds.)) Advances in Biotechnology 185–203 (Bentham Science, 2009).

Holzberg S, Brosio P, Gross C, Pogue GP. Barley stripe mosaic virus-induced gene silencing in a monocot plant. Plant J. 2002;30:315–327. doi: 10.1046/j.1365-313X.2002.01291.x. PubMed DOI

Scofield SR, Brandt AS. Virus-induced gene silencing in hexaploid wheat using barley stripe mosaic virus vectors. Methods Mol. Biol. 2012;894:93–112. doi: 10.1007/978-1-61779-882-5_7. PubMed DOI

Scofield SR, Huang L, Brandt AS, Gill BS. Development of a virus-induced gene-silencing system for hexaploid wheat and its use in functional analysis of the Lr21-mediated leaf rust resistance pathway. Plant Physiol. 2005;138:2165–2173. doi: 10.1104/pp.105.061861. PubMed DOI PMC

Mosavi LK, Minor DL, Jr, Peng ZY. Consensus-derived structural determinants of the ankyrin repeat motif. Proc. Natl Acad. Sci. USA. 2002;99:16029–16034. doi: 10.1073/pnas.252537899. PubMed DOI PMC

Kallberg M, et al. Template-based protein structure modeling using the RaptorX web server. Nat. Protoc. 2012;7:1511–1522. doi: 10.1038/nprot.2012.085. PubMed DOI PMC

Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJ. The Phyre2 web portal for protein modeling, prediction and analysis. Nat. Protoc. 2015;10:845–858. doi: 10.1038/nprot.2015.053. PubMed DOI PMC

Zimmermann L, et al. A completely reimplemented MPI bioinformatics toolkit with a New HHpred server at its core. J. Mol. Biol. 2018;430:2237–2243. doi: 10.1016/j.jmb.2017.12.007. PubMed DOI

Buchmann JP, Matsumoto T, Stein N, Keller B, Wicker T. Inter-species sequence comparison of Brachypodium reveals how transposon activity corrodes genome colinearity. Plant J. 2012;71:550–563. doi: 10.1111/j.1365-313X.2012.05007.x. PubMed DOI

Ma J, Bennetzen JL. Rapid recent growth and divergence of rice nuclear genomes. Proc. Natl Acad. Sci. USA. 2004;101:12404–12410. doi: 10.1073/pnas.0403715101. PubMed DOI PMC

Rate DN, Cuenca JV, Bowman GR, Guttman DS, Greenberg JT. The gain-of-function Arabidopsis acd6 mutant reveals novel regulation and function of the salicylic acid signaling pathway in controlling cell death, defenses, and cell growth. Plant Cell. 1999;11:1695–1708. doi: 10.1105/tpc.11.9.1695. PubMed DOI PMC

Ronquist F, et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 2012;61:539–542. doi: 10.1093/sysbio/sys029. PubMed DOI PMC

Nakagawa T, et al. Improved Gateway binary vectors: high-performance vectors for creation of fusion constructs in transgenic analysis of plants. Biosci. Biotechnol. Biochem. 2007;71:2095–2100. doi: 10.1271/bbb.70216. PubMed DOI

Bucherl CA, et al. Plant immune and growth receptors share common signalling components but localise to distinct plasma membrane nanodomains. Elife. 2017;6:e25114. doi: 10.7554/eLife.25114. PubMed DOI PMC

Gronnier J, et al. Structural basis for plant plasma membrane protein dynamics and organization into functional nanodomains. Elife. 2017;6:e26404. doi: 10.7554/eLife.26404. PubMed DOI PMC

Bourras S, et al. The AvrPm3-Pm3 effector-NLR interactions control both race-specific resistance and host-specificity of cereal mildews on wheat. Nat. Commun. 2019;10:2292. doi: 10.1038/s41467-019-10274-1. PubMed DOI PMC

Himmelbach A, et al. A set of modular binary vectors for transformation of cereals. Plant Physiol. 2007;145:1192–1200. doi: 10.1104/pp.107.111575. PubMed DOI PMC

Voinnet O, Pinto YM, Baulcombe DC. Suppression of gene silencing: a general strategy used by diverse DNA and RNA viruses of plants. Proc. Natl Acad. Sci. USA. 1999;96:14147–14152. doi: 10.1073/pnas.96.24.14147. PubMed DOI PMC

Patro R, Duggal G, Love MI, Irizarry RA, Kingsford C. Salmon provides fast and bias-aware quantification of transcript expression. Nat. Methods. 2017;14:417–419. doi: 10.1038/nmeth.4197. PubMed DOI PMC

Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26:139–140. doi: 10.1093/bioinformatics/btp616. PubMed DOI PMC

Praz CR, et al. Non-parent of origin expression of numerous effector genes indicates a role of gene regulation in host adaption of the hybrid triticale powdery mildew pathogen. Front Plant Sci. 2018;9:49. doi: 10.3389/fpls.2018.00049. PubMed DOI PMC

Young MD, Wakefield MJ, Smyth GK, Oshlack A. goseq: gene ontology testing for RNA-seq datasets. R. Bioconductor. 2012;8:1–25.

Tian T, et al. agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update. Nucleic Acids Res. 2017;45:W122–W129. doi: 10.1093/nar/gkx382. PubMed DOI PMC

Ramirez-Gonzalez RH, et al. The transcriptional landscape of polyploid wheat. Science. 2018;361:eaar6089. doi: 10.1126/science.aar6089. PubMed DOI

Ma X, Keller B, McDonald BA, Palma-Guerrero J, Wicker T. Comparative transcriptomics reveals how wheat responds to infection by Zymoseptoria tritici. Mol. Plant Microbe Interact. 2018;31:420–431. doi: 10.1094/MPMI-10-17-0245-R. PubMed DOI

Glauser, G., Vallat, A. & Balmer, D. in (David B. Collinge (ed.)) Arabidopsis Protocols (Springer Protocols, 2014).

Clarke JD. Cetyltrimethyl ammonium bromide (CTAB) DNA miniprep for plant DNA isolation. Cold Spring Harb. Protoc. 2009;2009:pdb.prot5177. PubMed

Lang-Pauluzzi I. The behaviour of the plasma membrane during plasmolysis: a study by UV microscopy. J. Microsc. 2000;198:188–198. doi: 10.1046/j.1365-2818.2000.00677.x. PubMed DOI

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