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

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

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.