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Soybean Resistance Genes Specific for Different Pseudomonas Syringue Avirwlence Genes Are Auelic, Or Closely Linked, at the RPG1 Locus

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Soybean Resistance Genes Specific for Different Pseudomonas Syringue Avirwlence Genes Are Auelic, Or Closely Linked, at the RPG1 Locus Copyright 0 1995 by the Genetics Society of America Soybean Resistance Genes Specific for Different Pseudomonas syringue Avirwlence Genes are AUelic, or Closely Linked, at the RPG1 Locus Tom Ashfield,* Noel T. Keen,+ Richard I. Buzzell: and Roger W. Innes* *Department of Biology, Indiana University, Bloomington, Indiana 47405, $Department of Plant Pathology, University of California, Riverside, California 92521, and fAgriculture & Agri-food Canada, Research Station, Harrow, Ontario NOR lG0, Canada Manuscript received July6, 1995 Accepted for publication September 11, 1995 ABSTRACT RPGl and RPMl are disease resistance genes in soybean and Arabidopsis, respectively, that confer resistance to Pseudomonas syringae strains expressing the avirulence gene awB. RPMl has recently been demonstrated to have a second specificity, also conferring resistance to P. syringae strains expressing [email protected] we show that alleles, or closely linked genes, exist at the RPGl locus in soybean that are specific for either awB or awR@ml and thus can distinguish between these two avirulence genes. ESISTANCE displayed by particular plant cultivars genes specific to avirulence genes of both the soybean R to specific races of a pathogen is often mediated pathogen Psgand the tomato pathogen Pst. The inabil- by single dominant resistance genes (R-genes). Typi- ity of Pstto cause disease in any soybean cultivarcan be cally, these R-genes interact with single dominant “avir- explained, atleast in part, by the presence of a battery of ulence” (aw) genes in the pathogen. Such specific in- resistance genes in soybean that correspond to one or teractions between races of pathogens and cultivars of more avirulence genes present in all Pst strains. host plants are the basis of the “gene-for-gene” model There arenow severalexamples of bacterial avrgenes of disease resistance developed by H. H. FLOR over 50 detected by multiple plant species (WHALENet al. 1991; years ago (FLOR1955). This model states that resistance DANGL et al. 1992; FILLINGHAMet al. 1992; RONALDet of a plant cultivar to a specific pathogen race is con- al. 1992; INNESet al. 1993; SIMONICHand INNES1995). trolled by a single dominant resistance gene, the prod- These studies suggest that R-genes sharing the same uct of which specificallyinteracts (directly or indirectly) specificities are present in different plant species. This with the productof a “corresponding” avirulence gene. has been demonstrated genetically for interactions in- Thus, for each avirulence gene in the pathogen, there volving awB (KEEN and BUZZELL1991; INNESet al. is a corresponding resistance gene in a resistant plant, 1993), avrRpml (VIVIANet al. 1989; DEBENERet al. 1991; and resistance is observed only when both genes are FILLINGHAMet al. 1992) and awPph3 (JENNER et al. 1991; present. Often this resistance is associated with a “hy- SIMONICHand INNES 1995). Itis unclear as to whether persensitive resistance response” (HR) thatis visualized this phenomenon represents theconservation of ances- as rapid localized necrosis of plant tissue at theinfection tral R-genes through speciation or whether convergent site. The HR appears to be an important component evolution is responsible. If functionally analogous R- of the defense response in many plant species (GOOD- genes in different species represent the conservation of MAN and NOVACKY1994). ancestral genes during speciation, it seems paradoxical Recently, the “gene-for-gene” model has been ex- that they should be lost (or change specificity) at a high tended beyond race-cultivar interactions to include in- frequency within a species; however, multiple alleles of teractions between plant pathogens and “nonhosts.” differing specificities is a hallmark of R-geneloci For example, the tomato pathogen Pseudomonas syringue (PRYORand ELLIS1993). The cloning of R-genes shar- pv. tomato (Pst) possesses multiple avirulence genes that, ing common specificities will help address this question. when expressed in P. syringue pv. glycinea (Psg), induce Only recently have the first three R-genes specificfor an HR in various cultivars of soybean (KOBAYASHIet al. bacterial avrgenes been cloned.These are the Pto gene 1989). This interaction was shown to be a true gene- from tomato and RPS2 and RPMl from Arabidopsis for-gene interaction when KEEN and BUZZELL(1991) (-TIN et al. 1993; BENTet al. 1994; MINDRINOSet al. established that the resistance response in specific soy- 1994; GRANTet al. 1995). Pto and RPS2 interact with the bean cultivars was controlled by single dominant resis- P. syringue avirulence genes aurPto and avrRpt2, respec- tance genes corresponding to the individual Pst aviru- tively (RONALDet al. 1992; KUNJSELet al. 1993). RPMl lence genes. Thus, soybeancultivars carry resistance displays a dual specificity, responding to both awRpml and avrBand consequently is also known as RPS3(DEBE- Cmrespondzng author: Roger W. Innes, Department of Biology, Indi- ana University, Jordan Hall 142, Bloomington, IN 47405. NER et al. 1991; INNES et al. 1993; BISGROVEet al. 1994; E-mail: [email protected] GRANTet al. 1995). Sequence analysis has revealed that Genetics 141: 1597-1604 (December, 1995) 1598 T. Ashfield et al. TABLE 1 Bacterial strains and plasmids used Bacterial strain/ Description Reference plasmid Strain PsgR 4 PseudomonasglycineaPsgR4 pv.syringm race 4 LONGet al. (1985) (rifamycin resistant isolate) PsgR4 ( avrB) PsgR4 carrying the plasmid pVBO1 INNESet al. (1993) PsgR4 (aurB:: Q) PsgR4 carrying the plasmid pVl3Ol: :C2 INNESet a,Z. (1993) PsgR4 ( avrRpml) PsgR4 carrying the plasmid This paper pVSPGl/avrRprnl Plasmid pvBo1 awBin cloned the vector pVSP61 INNESet al. (1993) pvBo1::sz aurB disrupted by the insertion of an INNESet al. (1993) R fragment cloned in the vector pVSP61 pVSP6 1/ avrrPml avrRpml cloned in the vector pVSP61BISCROVE et al. (1994) Pto shows homology to known serine-threonine protein Bacterial strains and plasmids are described in Table 1. kinases, suggestive of a role in signal transduction. In Growth of bacteria and inoculumpreparation: Bacterial lawns were grown on King's medium B (KING et al. 1954) contrast, RPS2 and RPMl display no homology to pro- supplemented with the appropriate antibiotics at 30" over- tein kinases but contain leucine-rich-repeats, a putative night. Rifamycin (Sigma) was includedat 100 pg/mland leucine zipper and a potential nucleotide binding do- kanamycin (Sigma) at 50 pg/ml. Bacterial suspensions were main. These motifs are also present in other recently prepared from the lawns in 10 mM MgC12 and diluted to -1 cloned R-genes corresponding to viral and fungal X 10' cfu/ml (an OD600of 0.1) for the HR tests and -5 X lo5cfu/ml for in9lantagrowth analysis. The suspensions were pathogens,but their role in R-gene function is un- used within 4 hr of preparation. known (reviewed by BRICCS 1995;DANGL 1995; INNES HR hand-inoculation tests: Primary leaves were inoculated 1995; ST~~KAWICZet ul. 1995). Neither is it known 2-3 wk after planting. The undersides of the leaves were whether any of these R-gene products interact directly nicked with a razor blade before the inoculum was forced with pathogen-derived elicitors. into theapoplastwith a 1-ml disposable syringe with no needle We have been analyzing the R-genes RPMl and RPGl fitted. The inoculated panelswere scored 20-24 hr after injec- tion. Incompatible (hypersensitive) responses were observed from Arabidopsis and soybean, respectively. Bothgenes as areas of brown sunken tissue. Typically, no macroscopic confer resistance to P. syringae strains expressing the response was seen in compatible interactions at this time, avirulence gene aurB (MUKHERJEEet al. 1966; KEEN and although occasionally mild chlorosis was obsemed. At least BUZZEL1991; INNESet al. 1993). However, it was not five individuals were scored from each recombinant inbred known whether RPGl, like RPMl, also confers resis- family. Each FZ individual was injected twice with each bacte- rial strain being tested. tance to Psgstrains expressing avrRpml. Here we show In-planta growth analysis: Znplanta bacterial growth analysis that in most soybean cultivars, RPGl is specific only to was conducted essentially as described by BISGROVEet al. aurB. However an R-gene specific to aurRpml is present (1994). Primary leaves were inoculated when they were fully in some cultivars, and this gene isclosely linked, or expanded (2-3 wk after planting). The plants to be inocu- allelic, to RPGI. We also demonstrate that in a soybean lated were vacuum infiltrated with an inoculum containing 10 mM MgCI2, 0.001% Silwet L77 surfactant (Osi Specialties, cultivar responsive to both uur genes, both resistance Inc.) and 5 X 105cfu/ml bacteria. A cork borer was used to specificities are determined either by an allele of RPGl remove leaf-disc samples from the inoculated leaves 0, 2 and or by RPGl and a second closely linked gene. 4 days after inoculation. The bacterial titer in these samples was determined by homogenizing the leaf discs in 10 mM MgC12 and then plating serial dilutions of the homogenate MATERIALS AND METHODS on trypticase soy agar (Becton Dickinson, Cockeysville, MD) Plant lines and growth. All soybean [Glycine max (L.) Merr.] containing 100 pg/ml rifamycin and 50 pg/ml cyclohexa- seed used in this study was propagated at Harrow, Ontario, mide (Sigma). Colonies were counted after 48 hr. Each data- Canada. The Flambeau X Merit recombinant inbred lines point represents the average of four independent samples, were derived from a cross between these two cultivars followed and error bars represent one standard error. All in$Zanta by inbreeding to the F8 generation by single-seed descent. bacterial growth analyses were performed at least twice. All plants for pathogen tests were grown in clay pots (4 Linkage analysis: Map distances in the RI lines were cal- inch diam)containing a soi1:peat:vermiculite:perlite (2:l: culated using the Haldane and Waddington equation p = 0.5:0.5) mix supplemented with osmocote slow-release fertil- R/(2 - 2R), where p is the frequency of recombinant ga- izer. For the first 2-3 wk after planting, the seedlings were metes in a single meiosis and R is the proportion of recom- grown in a glasshouse.
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