Gene duplication and transposition of mobile elements drive evolution of the Rpv3 resistance locus in grapevine.

A wild grape haplotype (Rpv3-1) confers resistance to Plasmopara viticola. We mapped the causal factor for resistance to an interval containing a TIR-NB-LRR (TNL) gene pair that originated 1.6-2.6 million years ago by a tandem segmental duplication. Transient coexpression of the TNL pair in Vitis vinifera leaves activated pathogen-induced necrosis and reduced sporulation compared to control leaves. Even though transcripts of the TNL pair from the wild haplotype appear to be partially subject to nonsense-mediated mRNA decay, mature mRNA levels in a homozygous resistant genotype were individually higher than the mRNA trace levels observed for the orthologous single-copy TNL in sensitive genotypes. Allelic expression imbalance in a resistant heterozygote confirmed that cis-acting regulatory variation promotes expression in the wild haplotype. The movement of transposable elements had a major impact on the generation of haplotype diversity, altering the DNA context around similar TNL coding sequences and the CG content in their proximal 5' intergenic regions. The wild and domesticated haplotypes also diverged in conserved single-copy intergenic DNA, but the highest divergence was observed in intraspecific and not in interspecific comparisons. In this case, introgression breeding did not transgress the genetic boundaries of the domesticated species, because haplotypes present in modern varieties sometimes predate speciation events between wild and cultivated species.

[1]  M. Luo,et al.  An ancestral NB-LRR with duplicated 3′UTRs confers stripe rust resistance in wheat and barley , 2019, Nature Communications.

[2]  T. Rausch,et al.  Rpv3–1 mediated resistance to grapevine downy mildew is associated with specific host transcriptional responses and the accumulation of stilbenes , 2019, BMC Plant Biology.

[3]  D. Stainier,et al.  Genetic compensation triggered by mutant mRNA degradation , 2019, Nature.

[4]  M. Morgante,et al.  InDel markers for monitoring the introgression of downy mildew resistance from wild relatives into grape varieties , 2018, Molecular Breeding.

[5]  Emmanuel Paradis,et al.  ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R , 2018, Bioinform..

[6]  S. Cesari,et al.  Multiple strategies for pathogen perception by plant immune receptors. , 2018, The New phytologist.

[7]  T. Eulgem,et al.  Transcript-level expression control of plant NLR genes. , 2018, Molecular plant pathology.

[8]  M. Morgante,et al.  The genetic background modulates the intensity of Rpv3‐dependent downy mildew resistance in grapevine , 2018 .

[9]  Kenneth L. McNally,et al.  Genomes of 13 domesticated and wild rice relatives highlight genetic conservation, turnover and innovation across the genus Oryza , 2018, Nature Genetics.

[10]  M. Perazzolli,et al.  A multi-omics study of the grapevine-downy mildew (Plasmopara viticola) pathosystem unveils a complex protein coding- and noncoding-based arms race during infection , 2018, Scientific Reports.

[11]  S. Jackson,et al.  Genomic and epigenomic immunity in common bean: the unusual features of NB-LRR gene family , 2017, DNA research : an international journal for rapid publication of reports on genes and genomes.

[12]  W. Haerty,et al.  Dominant integration locus drives continuous diversification of plant immune receptors with exogenous domain fusions , 2017, Genome Biology.

[13]  B. Kobe,et al.  Multiple functional self-association interfaces in plant TIR domains , 2017, Proceedings of the National Academy of Sciences.

[14]  M. Bodén,et al.  Structure and Function of the TIR Domain from the Grape NLR Protein RPV1 , 2016, Front. Plant Sci..

[15]  S. Knapp,et al.  The Tomato (Solanum lycopersicum L., Solanaceae) and Its Botanical Relatives , 2016 .

[16]  Julien Gagneur,et al.  Measures of RNA metabolism rates: Toward a definition at the level of single bonds , 2016, Transcription.

[17]  M. Morgante,et al.  Characterization of the Poplar Pan-Genome by Genome-Wide Identification of Structural Variation , 2016, Molecular biology and evolution.

[18]  Daniel Mapleson,et al.  KAT: a K-mer analysis toolkit to quality control NGS datasets and genome assemblies , 2016, bioRxiv.

[19]  S. Carroll,et al.  Expression of tandem gene duplicates is often greater than twofold , 2016, Proceedings of the National Academy of Sciences.

[20]  L. Maquat,et al.  Nonsense-mediated mRNA decay in humans at a glance , 2016, Journal of Cell Science.

[21]  Christophe Malabat,et al.  Quality control of transcription start site selection by nonsense-mediated-mRNA decay , 2015, eLife.

[22]  Jonathan D. G. Jones,et al.  Two linked pairs of Arabidopsis TNL resistance genes independently confer recognition of bacterial effector AvrRps4 , 2015, Nature Communications.

[23]  J. Bogs,et al.  The transcription factor VvWRKY33 is involved in the regulation of grapevine (Vitis vinifera) defense against the oomycete pathogen Plasmopara viticola. , 2015, Physiologia plantarum.

[24]  T. Kroj,et al.  A novel conserved mechanism for plant NLR protein pairs: the “integrated decoy” hypothesis , 2014, Front. Plant Sci..

[25]  L. Hartmann,et al.  NMD: nonsense-mediated defense. , 2014, Cell host & microbe.

[26]  K. Ríha,et al.  Nonsense-mediated mRNA decay modulates immune receptor levels to regulate plant antibacterial defense. , 2014, Cell host & microbe.

[27]  M. Thomas,et al.  Genetic dissection of a TIR-NB-LRR locus from the wild North American grapevine species Muscadinia rotundifolia identifies paralogous genes conferring resistance to major fungal and oomycete pathogens in cultivated grapevine. , 2013, The Plant journal : for cell and molecular biology.

[28]  G. Zhong,et al.  A phylogenetic analysis of the grape genus (Vitis L.) reveals broad reticulation and concurrent diversification during neogene and quaternary climate change , 2013, BMC Evolutionary Biology.

[29]  M. Morgante,et al.  Historical Introgression of the Downy Mildew Resistance Gene Rpv12 from the Asian Species Vitis amurensis into Grapevine Varieties , 2013, PloS one.

[30]  Heng Li.  Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM , 2013, 1303.3997.

[31]  C. M. van der Weele,et al.  Removal of retained introns regulates translation in the rapidly developing gametophyte of Marsilea vestita. , 2013, Developmental cell.

[32]  Paul D. Shaw,et al.  Using Tablet for visual exploration of second-generation sequencing data , 2013, Briefings Bioinform..

[33]  Alexandra M. E. Jones,et al.  The Tomato Prf Complex Is a Molecular Trap for Bacterial Effectors Based on Pto Transphosphorylation , 2013, PLoS pathogens.

[34]  V. Beneš,et al.  DELLY: structural variant discovery by integrated paired-end and split-read analysis , 2012, Bioinform..

[35]  M. Morgante,et al.  Selective sweep at the Rpv3 locus during grapevine breeding for downy mildew resistance , 2012, Theoretical and Applied Genetics.

[36]  Gary Stacey,et al.  MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs. , 2011, Genes & development.

[37]  S. Kossida,et al.  Transcriptome map of mouse isochores , 2011, BMC Genomics.

[38]  R. Testolin,et al.  Defence responses in Rpv3-dependent resistance to grapevine downy mildew , 2011, Planta.

[39]  Ann A. Ferguson,et al.  Pack-MULEs , 2011, Mobile genetic elements.

[40]  M. DePristo,et al.  A framework for variation discovery and genotyping using next-generation DNA sequencing data , 2011, Nature Genetics.

[41]  Carl Kingsford,et al.  A fast, lock-free approach for efficient parallel counting of occurrences of k-mers , 2011, Bioinform..

[42]  W. Pirovano,et al.  Scaffolding pre-assembled contigs using SSPACE , 2011, Bioinform..

[43]  Edward S. Buckler,et al.  Genetic structure and domestication history of the grape , 2011, Proceedings of the National Academy of Sciences.

[44]  A. Gnirke,et al.  High-quality draft assemblies of mammalian genomes from massively parallel sequence data , 2010, Proceedings of the National Academy of Sciences.

[45]  K. Jena.  The species of the genus Oryza and transfer of useful genes from wild species into cultivated rice, O. sativa. , 2010 .

[46]  R. Testolin,et al.  Breakdown of resistance to grapevine downy mildew upon limited deployment of a resistant variety , 2010, BMC Plant Biology.

[47]  Aaron R. Quinlan,et al.  BIOINFORMATICS APPLICATIONS NOTE , 2022 .

[48]  M. Morgante,et al.  Resistance to Plasmopara viticola in grapevine ‘Bianca’ is controlled by a major dominant gene causing localised necrosis at the infection site , 2009, Theoretical and Applied Genetics.

[49]  Gonçalo R. Abecasis,et al.  The Sequence Alignment/Map format and SAMtools , 2009, Bioinform..

[50]  Steven J. M. Jones,et al.  Abyss: a Parallel Assembler for Short Read Sequence Data Material Supplemental Open Access , 2022 .

[51]  H. Dooner,et al.  Haplotype structure strongly affects recombination in a maize genetic interval polymorphic for Helitron and retrotransposon insertions , 2009, Proceedings of the National Academy of Sciences.

[52]  Lior Pachter,et al.  Sequence Analysis , 2020, Definitions.

[53]  Tamás B. Pálfy,et al.  Both introns and long 3′-UTRs operate as cis-acting elements to trigger nonsense-mediated decay in plants , 2006, Nucleic acids research.

[54]  Jerzy Jurka,et al.  Annotation, submission and screening of repetitive elements in Repbase: RepbaseSubmitter and Censor , 2006, BMC Bioinformatics.

[55]  V. Solovyev,et al.  Automatic annotation of eukaryotic genes, pseudogenes and promoters , 2006, Genome Biology.

[56]  Francisco Martinez-Murillo,et al.  Nonsense surveillance regulates expression of diverse classes of mammalian transcripts and mutes genomic noise , 2004, Nature Genetics.

[57]  Jianxin Ma,et al.  Rapid recent growth and divergence of rice nuclear genomes. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[58]  Robert C. Edgar,et al.  MUSCLE: a multiple sequence alignment method with reduced time and space complexity , 2004, BMC Bioinformatics.

[59]  Xue-Cheng Zhang,et al.  RPS4-Mediated Disease Resistance Requires the Combined Presence of RPS4 Transcripts with Full-Length and Truncated Open Reading Frames Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.013474. , 2003, The Plant Cell Online.

[60]  Blake C. Meyers,et al.  Genome-Wide Analysis of NBS-LRR–Encoding Genes in Arabidopsis Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.009308. , 2003, The Plant Cell Online.

[61]  P. Singh,et al.  Sequence architecture downstream of the initiator codon enhances gene expression and protein stability in plants. , 2001, Plant physiology.

[62]  M. A. Koch,et al.  Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). , 2000, Molecular biology and evolution.

[63]  S. Dinesh-Kumar,et al.  Alternatively spliced N resistance gene transcripts: their possible role in tobacco mosaic virus resistance. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[64]  H. Dooner,et al.  Recombination occurs uniformly within the bronze gene, a meiotic recombination hotspot in the maize genome. , 1997, The Plant cell.

[65]  M T Clegg,et al.  Substitution rate comparisons between grasses and palms: synonymous rate differences at the nuclear gene Adh parallel rate differences at the plastid gene rbcL. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[66]  R. Durbin,et al.  A dot-matrix program with dynamic threshold control suited for genomic DNA and protein sequence analysis. , 1995, Gene.

[67]  J. Possingham,et al.  Progress in grapevine breeding , 1988, Theoretical and Applied Genetics.

[68]  Florian Hahne,et al.  Visualizing Genomic Data Using Gviz and Bioconductor , 2016, Statistical Genomics.

[69]  Wen-Hsiung Li.  Unbiased estimation of the rates of synonymous and nonsynonymous substitution , 2006, Journal of Molecular Evolution.

[70]  M. Seidel,et al.  Inter-isolate variation of virulence of Plasmopara viticola on resistant vine varieties. , 2000 .