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Naturally Occurring Broad-Spectrum Powdery Mildew Resistance in a Central American Tomato Accession Is Caused by Loss of Mlo Function

January 2008 , Volume 21 , Number  1
Pages  30 - 39

Yuling Bai,1 Stefano Pavan,1,2 Zheng Zheng,1 Nana F. Zappel,3 Anja Reinstädler,3 Concetta Lotti,2 Claudio De Giovanni,2 Luigi Ricciardi,2 Pim Lindhout,1 Richard Visser,1 Klaus Theres,4 and Ralph Panstruga3

1Laboratory of Plant Breeding, Plant Sciences Group, Wageningen University, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands; 2Department of Agroforestry, Enviromental Biology and Chemistry, Section of Genetics and Plant Breeding, University of Bari, Via Amendola 165/A, 70126 Bari, Italy; 3Max-Planck Institute for Plant Breeding Research, Department of Plant-Microbe Interactions, Carl-von-Linné-Weg 10, D-50829 Köln, Germany; 4Max-Planck Institute for Plant Breeding Research, Department of Plant Breeding and Genetics, Carl-von-Linné-Weg 10, D-50829 Köln, Germany

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Accepted 18 September 2007.

The resistant cherry tomato (Solanum lycopersicum var. cerasiforme) line LC-95, derived from an accession collected in Ecuador, harbors a natural allele (ol-2) that confers broad-spectrum and recessively inherited resistance to powdery mildew (Oidium neolycopersici). As both the genetic and phytopathological characteristics of ol-2--mediated resistance are reminiscent of powdery mildew immunity conferred by loss-of-function mlo alleles in barley and Arabidopsis, we initiated a candidate-gene approach to clone Ol-2. A tomato Mlo gene (SlMlo1) with high sequence-relatedness to barley Mlo and Arabidopsis AtMLO2 mapped to the chromosomal region harboring the Ol-2 locus. Complementation experiments using transgenic tomato lines as well as virus-induced gene silencing assays suggested that loss of SlMlo1 function is responsible for powdery mildew resistance conferred by ol-2. In progeny of a cross between a resistant line bearing ol-2 and the susceptible tomato cultivar Moneymaker, a 19-bp deletion disrupting the SlMlo1 coding region cosegregated with resistance. This polymorphism results in a frameshift and, thus, a truncated nonfunctional SlMlo1 protein. Our findings reveal the second example of a natural mlo mutant that possibly arose post-domestication, suggesting that natural mlo alleles might be evolutionarily short-lived due to fitness costs related to loss of mlo function.

Additional keywords:comparative genetics, co-orthologs, introgression lines, pleiotropic effects.

© 2008 The American Phytopathological Society