Loss of Function in Mlo Orthologs Reduces Susceptibility of Pepper and Tomato to Powdery Mildew Disease Caused by Leveillula taurica

Abstract

Powdery mildew disease caused by Leveillula taurica is a serious fungal threat to greenhouse tomato and pepper production. In contrast to most powdery mildew species which are epiphytic, L. taurica is an endophytic fungus colonizing the mesophyll tissues of the leaf. In barley, Arabidopsis, tomato and pea, the correct functioning of specific homologues of the plant Mlo gene family has been found to be required for pathogenesis of epiphytic powdery mildew fungi. The aim of this study was to investigate the involvement of the Mlo genes in susceptibility to the endophytic fungus L. taurica. In tomato (Solanum lycopersicum), a loss-of-function mutation in the SlMlo1 gene results in resistance to powdery mildew disease caused by Oidium neolycopersici. When the tomato Slmlo1 mutant was inoculated with L. taurica in this study, it proved to be less susceptible compared to the control, S. lycopersicum cv. Moneymaker. Further, overexpression of SlMlo1 in the tomato Slmlo1 mutant enhanced susceptibility to L. taurica. In pepper, the CaMlo2 gene was isolated by applying a homology-based cloning approach. Compared to the previously identified CaMlo1 gene, the CaMlo2 gene is more similar to SlMlo1 as shown by phylogenetic analysis, and the expression of CaMlo2 is up-regulated at an earlier time point upon L. taurica infection. However, results of virus-induced gene silencing suggest that both CaMlo1 and CaMlo2 may be involved in the susceptibility of pepper to L. taurica. The fact that overexpression of CaMlo2 restored the susceptibility of the tomato Slmlo1 mutant to O. neolycopersici and increased its susceptibility to L. taurica confirmed the role of CaMlo2 acting as a susceptibility factor to different powdery mildews, though the role of CaMlo1 as a co-factor for susceptibility cannot be excluded.

Genome-wide Identification, Classification and Expression Analysis of the Mildew Resistance Locus O ( MLO ) Gene Family in Sweet Orange ( Citrus sinensis )

“…Therefore, CisMLOs may play roles as an important cross-talk node in both stress and hormone signaling processes. The MLO genes are reported to take part in programmed cell death, and in the PM pathogen responses [ 12,24 ], the biotrophic oomycete pathogen Hyaloperonospora arabidopsidis, as well as the hemibiotrophic bacterial pathogens, for example, Pseudomonas syringae pv. tomato and Xanthomonas campestris pv.…”

Genetics and molecular mechanisms of resistance to powdery mildews in tomato (Solanum lycopersicum) and its wild relatives

“…The recessive ol-2 gene (Ciccarese et al 1998;Bai et al 2008) identified in S. lycopersicum var. cerasiforme confers incomplete resistance to L. taurica (Zheng et al 2013b). …”

Candidate Susceptibility Genes for Powdery and Downy Mildew in Watermelon and Squash

“…Inactivation of S-genes through gene-knockout, geneknockdown or virus induced gene-silencing has been proven a viable option for generating resistance genotypes against important diseases such as rice blast in rice (Oryza sativa) [7], citrus canker in citrus (Citrus paradisi) [8] and powdery mildew in grapevine (Vitis vinifera) [9], tomato and pepper [10]. Currently, two classes of PM S-genes are known, Mildew-Locus-O (MLO) genes and Powdery Mildew Resistance (PMR), both of which are loss-of-function genes [11][12].…”

“…Functional clade V MLO proteins negatively regulate defense pathways at the site of PM inoculation, thus allowing the pathogen to induce pathogenesis [11]. Therefore, a loss of function in MLO genes consequently induce resistance to PM [10,15]. PMR genes on the other hand are far less studied and most are putative, but some have been shown to play a role in PM susceptibility in Arabidopsis (AtPMR4, AtPMR5, and AtPMR6) and tomato (SlPMR4) [16][17][18][19].…”