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


Foria, Serena; Copetti, Dario; Eisenmann, Birgit; Magris, Gabriele; Vidotto, Michele; Scalabrin, Simone; Testolin, Raffaele; Cipriani, Guido; Wiedemann‐Merdinoglu, Sabine; Bogs, Jochen; Di Gaspero, Gabriele; Morgante, Michele (2019). Gene duplication and transposition of mobile elements drive evolution of the Rpv3 resistance locus in grapevine. The Plant Journal, 101(3):529-542.

Abstract

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 with 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 GC-content in their proximal 50
-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.

Abstract

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 with 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 GC-content in their proximal 50
-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.

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Additional indexing

Item Type:Journal Article, refereed, original work
Communities & Collections:07 Faculty of Science > Institute of Evolutionary Biology and Environmental Studies
Dewey Decimal Classification:570 Life sciences; biology
590 Animals (Zoology)
Uncontrolled Keywords:Vitis vinifera, introgression breeding, disease resistance, grapevine, tandem gene duplicates
Language:English
Date:11 November 2019
Deposited On:07 Feb 2020 09:55
Last Modified:07 Feb 2020 10:14
Publisher:Wiley-Blackwell Publishing, Inc.
ISSN:0960-7412
OA Status:Closed
Free access at:Publisher DOI. An embargo period may apply.
Publisher DOI:https://doi.org/10.1111/tpj.14551
Project Information:
  • : FunderFP7
  • : Grant ID294780
  • : Project TitleNOVABREED - Novel variation in plant breeding and the plant pan-genomes

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