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The Fusarium Wilt Resistance Locus Fom-2 of Melon Contains a Single Resistance Gene with Complex Features

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The Fusarium Wilt Resistance Locus Fom-2 of Melon Contains a Single Resistance Gene with Complex Features The Plant Journal (2004), 39, 283–297 doi: 10.1111/j.1365-313X.2004.02134.x The fusarium wilt resistance locus Fom-2 of melon contains a single resistance gene with complex features Tarek Joobeur1, Joseph J. King2, Shelly J. Nolin1, Claude E. Thomas3 and Ralph A. Dean1,* 1Department of Plant Pathology, Fungal Genomics Laboratory, North Carolina State University, Raleigh, NC 27965, USA, 2Seminis Vegetable Seeds, 37437 State Highway 16, Woodland, CA 95695, USA, and 3USDA-ARS, US Vegetable Laboratory, Charleston, SC 29414, USA Received 19 March 2004; revised 20 April 2004; accepted 10 May 2004. *For correspondence (fax þ1 919 513 0024; e-mail [email protected]). Summary The soil-borne fungus Fusarium oxysporum f.sp. melonis causes significant losses in the cultivated melon, a key member of the economically important family, the Cucurbitaceae. Here, we report the map-based cloning and characterization of the resistance gene Fom-2 that confers resistance to race 0 and 1 of this plant pathogen. Two recombination events, 75 kb apart, were found to bracket Fom-2 after screening approximately 1324 gametes with PCR-based markers. Sequence analysis of the Fom-2 interval revealed the presence of two candidate genes. One candidate gene showed significant similarity to previously characterized resistance genes. Sequence analysis of this gene revealed clear polymorphisms between resistant and susceptible materials and was therefore designated as Fom-2. Analysis of susceptible breeding lines (BL) presenting a haplotype very similar to the resistant cultivar MR-1 indicated that a gene conversion had occurred in Fom-2, resulting in a significant rearrangement of this gene. The second candidate gene which shared high similarity to an essential gene in Arabidopsis, presented an almost identical sequence in MR-1 and BL, further supporting Fom-2 identity. The gene conversion in Fom-2 produced a truncated R gene, revealing new insights into R gene evolution. Fom-2 was predicted to encode an NBS-LRR type R protein of the non-TIR subfamily. In contrast to most members of this class a coiled-coil structure was predicted within the LRR region rather than in the N-terminal. The Fom-2 physical region contained retroelement-like sequences and truncated genes, suggest- ing that this locus is complex. Keywords: Fom-2, melon, complex R locus, fine mapping, BAC end sequence, R gene evolution. Introduction The cultivated melon (Cucumis melo L.), an economically viable in the soil as chlamydospores for decades. An important member of the Cucurbitaceae family, includes a effective control for this pathogen is through host resist- diverse group of annual trailing-vine plants such as the ance (Martyn and Gordon, 1996). However, resistant vari- cantaloupe, honeydew, casaba, snake melon, pickling eties often lack the appropriate traits for the commercial melon, mango melon, and snap melon (McCreight et al., market. Traditional artificial inoculation used to evaluate 1993). In the US, over 120 000 acres of melons (cantaloupe resistance to fusarium wilt is a time consuming process and and honeydew) are grown annually, and in 1998 nearly susceptible plants may escape detection (Burger et al., 1 million tons of melons were produced with a total value 2003). Thus, molecular markers tightly linked to fusarium of over 500 million dollars (http://www.usda.gov/nass/). wilt resistance genes are highly valued in melon breeding. However, the full economic value of this crop has not been Currently, four races (0, 1, 2, and 1, 2) of the pathogen are achieved because of diseases caused primarily by fungi, defined by their capacity to incite disease in different vari- such as fusarium wilt, and powdery and downy mildews. eties of melons. Resistance to race 1 and race 2 is conferred Fusarium wilt, caused by Fusarium oxysporum f.sp. mel- by a single dominant gene Fom-2 and Fom-1, respectively. onis, is one of the most difficult diseases to control pri- Both genes also confer resistance to race 0 (Schreuder marily because the pathogen is soil-borne and remains et al., 2000; Zink and Thomas, 1990). ª 2004 Blackwell Publishing Ltd 283 284 Tarek Joobeur et al. Typically, race/cultivar-specific resistance is proposed to interval. A single candidate gene with significant similarity involve the recognition of the pathogen avirulence (avr) to previously characterized R genes was found and gene product by the complementary host resistance (R) designated as Fom-2. Evidence for this gene being gene protein. This recognition initiates a signal transduction Fom-2 was provided by the sequence analysis of alleles cascade and the defense response (Hammond-Kosack and from susceptible and resistant cultivars of the two iden- Jones, 1997; Martin et al., 2003). Several R-genes have been tified candidate genes. Sequence analysis of the two BAC isolated by map-based cloning and transposon-tagging clones encompassing Fom-2 showed the presence of strategies (Martin et al., 2003). Interestingly, R genes that several retroelement-like sequences as well as truncated confer resistance to different types of pathogens encode genes, typically found in complex loci. Comparison very similar proteins. A major class of R genes encodes between closely related resistant and susceptible haplo- proteins that contain leucine-rich (LRR) and nucleotide- types strongly indicated that truncated R genes could be binding site (NBS) domains and are likely located in the produced by gene conversion, revealing novel insights cytoplasm. This class can be divided into two subfamilies, into the R gene evolution. the TIR and the non-TIR, depending on the presence of a domain at the N-terminal with similarity to the Toll/interleu- Results kin-1 receptor (TIR) (Meyers et al., 1999). The former sub- family includes the resistance genes M and L6 from flax, N Fom-2 fine mapping from tobacco, and RPP5 from Arabidopsis. The non-TIR subfamily comprises RPS2 and RPM1 from Arabidopsis and In a previous work, we developed two co-dominant PCR- I2 and Prf from tomato. R proteins of the non-TIR class are based markers, FM and AM, that cosegregated with Fom-2 often predicted to have a coiled-coil (CC) structure near their (Wang et al., 2000). In addition, two AFLP markers ACT/CAT1 N-terminus and are referred to as the CC-NBS-LRR class. and AAC/CAT1 were found to flank Fom-2 at 1.7 and 3.3 cM, Other R genes, such as Xa21 in rice, encode a protein that is respectively. We used these markers to map Fom-2 using a likely located in the plasma membrane and presents an population (named Vad375) containing 159 RILs derived extracellular LRR domain and a cytoplasmic kinase domain. from the cultivar ‘Ve´ drantais’ and PI 161375. New primer The Cf proteins (Dixon et al., 1996) in tomato and the pairs were designed for FM and AM, producing smaller HS1Pro-1 (Cai et al., 1997) in sugar beet predominantly fragments that were suitable for analysis with ABI 377s consist of LRR domains. Few R proteins have been described (SSR154 for FM and STS178 for AM). SSR154 and STS178 to lack the LRR motif. One such example is the recently were found to flank Fom-2 at 2 and 4 recombination events, identified RPW8 protein in Arabidopsis that is predicted to respectively (Figure 1). The AFLP markers ACT/CAT1 and contain a CC structure (Xiao et al., 2001). AAC/CAT1 were used to create PCR-based markers for Resistance genes are continuously evolving to produce screening the Vad375 population. The AFLP fragments were new specificities in order to recognize mutated avr genes. isolated, cloned and sequenced. The resulting fragments Understanding the mechanisms governing R gene evolution were utilized to screen a HindIII BAC library of melon (Luo is therefore of major interest. Important insights were et al., 2001). The AAC/CAT fragment was considered repet- obtained from the sequence analysis of R genes loci from itive because several hundred BAC clones were identified. different species and haplotypes (Michelmore and Meyers, However, the ACT/CAT1 marker identified 23 BAC clones, 1998). New specificities are postulated to be the result of indicating this fragment was present as a single copy in the diversifying selection, interallelic recombination and gene genome. Restriction fragment analysis with the FPC pro- conversion. Resistance genes are often organized in tandem gram showed that all the clones belonged to the same repeats of paralogues and this structure is postulated to play contig. Two SSR markers SSR138 and SSR180 were derived a role in their evolution through additional mechanisms from the BAC end sequences. After screening the Vad375 such as unequal crossing-over (Chin et al., 2001; Parniske population, SSR138 was found to cosegregate with Fom-2 et al., 1997). (Figure 1). Interestingly, one recombination event was found Here, we report the map-based cloning and character- between SSR180 and Fom-2 indicating that Fom-2 is located ization of the first R gene in the Cucurbitaceae family, between SSR180 and STS178 (Figure 1). All markers and the Fom-2. Bacterial artificial chromosome (BAC) libraries resistance phenotype followed the expected segregation were screened with probes linked to Fom-2 and a physical ratio (1:1) for a co-dominant marker (P ¼ 0.93). The observed map of the interval was constructed. PCR-based markers frequency of heterozygous RILs was not significantly derived from the BAC end sequences were used to (P ¼ 0.29) different from the expected value, 4.20%. localize Fom-2 into two BAC clones. Fom-2 was further Screening additional populations (SF6 and IndF7; Table 1) delimited to 75 kb size-interval using additional markers with the Fom-2 flanking markers SSR154 and STS178 developed from the sequence of these BAC clones. revealed 15 recombinant plants (Figure 2a).
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