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Vulgare-Rhynchosporium Secalis Pathosystem (Virulence/Resistance/Selection) B

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Vulgare-Rhynchosporium Secalis Pathosystem (Virulence/Resistance/Selection) B Proc. Natl. Acad. Sci. USA Vol. 86, pp. 3924-3927, May 1989 Population Biology Coevolution of host and pathogen populations in the Hordeum vulgare-Rhynchosporium secalis pathosystem (virulence/resistance/selection) B. A. MCDONALD*t, J. M. MCDERMOTT*, R. W. ALLARD*, AND R. K. WEBSTERt Departments of *Genetics and tPlant Pathology, University of California, Davis, CA 95616 Contributed by R. W. Allard, February 24, 1989 ABSTRACT Isolates of Rhynchosporium secalis collected The synthesis and evolutionary histories of CCII and CCV from two experimental barley populations were scored for have been described in detail (5, 6) and both populations are putative isozyme, colony color, and virulence loci. Allelic known to be polymorphic at many loci, including loci that frequencies, multilocus haplotype frequencies, and multilocus govern resistance vs. susceptibility to R. secalis. There have genetic structure differed in the two populations of R. secalis; also been a number of studies of the evolutionary responses haplotypes also differed widely from each other in virulence. of CCII and CCV to R. secalis (7-11) but much less infor- The average virulence of isolates collected from the more mation is available concerning the genetic structure of the resistant host population was greater than the average viru- populations ofR. secalis that have evolved on CCII and CCV lence of the isolates collected from the less resistant host (12). In this paper, we report the results of a study in which population; also the least virulent haplotype, which made up isozyme, colony color, and virulence variants were used to 19% ofthe pathogen population collected from the less resistant investigate the genetic composition and population structure host population, accounted for only 0.3% of the isolates of samples of R. secalis collected from generation 56 of CCII collected from the more resistant host population. It was and generation 44 of CCV during the 1985-1986 growing concluded that the genetic systems ofthe barley host and fungal season. pathogen interacted in a complementary fashion and that the genetic structures of both the host and pathogen populations were shaped by coevolutionary processes featuring interactions MATERIALS AND METHODS among loci affecting many different traits, including interac- Field Plantings. CCII and CCV were seeded in a pair of tions among host resistance genes and pathogen virulence plots (10 x 10 m), separated by a 4-m alley, in a field that had genes. not been seeded to barley for several years. For purposes of collecting fungal isolates, the two plots were each divided It is now widely accepted that the coevolution of plants and into 16 subplots measuring 1.25 m (width) x 5.0 m (length). their pathogens can be understood only in the context of Rainfall was above average (692 mm; 42% higher than the integrated host-pathogen systems (e.g., see refs. 1 and 2). normal of 492 mm) in 1985-1986, providing excellent condi- However, empirical studies of host-pathogen systems have tions for development of scald from seed-borne inoculum; usually focused on the host; this is partly because the host is conditions were particularly favorable for spread of the scald the partner of economic importance in the pathosystem and disease within the main plots during nine rainy periods, each partly because plant pathogens have often been perceived as ranging from 1 to 3 or 4 days and distributed throughout the less tractable to genetic analysis than their hosts. Rhyncho- growing season. sporium secalis (Oud.) Davis, the causal organism of the Collection of Leaf Tissue and Generation of Isolates. The scald disease of barley (Hordeum vulgare L.), is a haploid populations of R. secalis isolated from CCII and CCV were imperfect fungus, which is transmitted from generation to designated RSII and RSV, respectively. In an attempt to generation of the barley host through seed-borne mycelial obtain representative samples of R. secalis from both CCII inoculum; however, within single growing seasons it spreads and CCV, 20 or more scald-infected leaves were collected from plant to plant by short-distance rain-splashed dispersal from plants distributed throughout each of the 32 subplots. of R. This collection strategy allowed us to test for differences in of conidia (3). It is likely that occasional migrations the distribution of genetic variation within subplots, among secalis take place between barley populations (i) as a result subplots, and between RSII and RSV. Leaves from the of contamination of seeds by mycelium during harvesting, and al- cleaning, or planting operations; (ii) as a result of longer- different subplots were placed in paper envelopes distance dispersal of conidia by windswirling during rain- lowed to dry at room temperature (21°C) for 8 weeks. The or infected volun- dried leaves were then wet for 10 sec in 70% ethanol, surface storms; or (iii) from barley crop residues sterilized for 90 sec in a 0.5% sodium hypochlorite solution, teer plants in planting areas. Barley composite cross II (CCII) pressed dry between paper towels, and placed on a plastic and composite cross V (CCV) are closed experimental pop- screen that rested on rubber bands above damp filter paper ulations, which have been grown at Davis, California, since an incubator 1929 and 1941, respectively, in isolated plots that had not in a Petri dish. The Petri dishes were placed in it is (15°C) for 72 hr to induce sporulation, at which time isolates been seeded to barley for a number of years. Thus, likely were collected from distinct lesions that had produced mac- that the populations ofR. secalis that occur on CCII and CCV Small are, like their host populations, also tightly closed and that roscopically visible mycelium on their borders. pieces they have coevolved in intimate association with CCII and of mycelium were transferred to potato dextrose agar (PDA) CCV. R. secalis populations in California are highly variable for virulence as defined on a set of 14 barley differentials (4). Abbreviations: CCII, barley composite cross II; CCV, barley com- posite cross V; PDA, potato dextrose agar; PGI, phosphoglucoiso- merase; PGM, phosphoglucomutase; LAP, leucine aminopeptidase; The publication costs of this article were defrayed in part by page charge BGLU, ,3-glucosidase; COL, color. payment. This article must therefore be hereby marked "advertisement" tPresent address: Department of Plant Pathology and Microbiology, in accordance with 18 U.S.C. §1734 solely to indicate this fact. Texas A&M University, College Station, TX 77843. 3924 Downloaded by guest on September 29, 2021 Population Biology: McDonald et al. Proc. Natl. Acad. Sci. USA 86 (1989) 3925 Petri dishes with a sterile needle. An average of three clonal Table 1. Numbers (n) and frequencies (F) of the fast isozyme isolates per leaf were transferred to PDA culture tubes, which and black variants in populations RSII and RSV and probabilities were incubated at 15'C for 6 weeks and then transferred to a (P) that frequency differences between the two 40C cold room for storage until they were analyzed. A total populations are different of 1331 isolates were collected, 677 from RSII and 654 from RSII RSV RSV. Data Collection. Isolates were scored for three different Locus n F n F P types of characters: colony color, isozymes, and virulence vs. PGI 427 0.63 475 0.73 <0.001 avirulence (12). Colonies of the isolates were either black or PGM 520 0.77 530 0.81 0.239* cream-colored after 6 weeks of growth in PDA culture tubes. LAP 239 0.35 129 0.20 <0.001 Isolates were assayed on starch gels for four isozyme systems BGLU 493 0.73 557 0.85 <0.001 following methods described by McDermott et al. (12): phos- COL 609 0.90 469 0.72 <0.001 phoglucoisomerase (PGI; glucose-6-phosphate isomerase; D- *Not significant. glucose-6-phosphate ketol-isomerase, EC 5.3.1.9), phospho- glucomutase (PGM; a-D-glucose 1,6-phosphomutase, EC haplotype, 11121, was in high frequency in RSII but in low 5.4.2.2), leucine aminopeptidase [LAP; cytosol aminopeptid- frequency in RSV, whereas the opposite was the case for ase; a-aminoacyl-peptide hydrolase (cytosol), EC 3.4.11.1], haplotype 11212. Two haplotypes observed in low frequency and 0-glucosidase (BGLU; P-D-glucoside glucohydrolase, EC in RSII (12212, 12112) and one observed in low frequency in 3.2.1.21). Each enzyme system was dimorphic forfast vs. slow RSV were nonappearance of these rare variants. Both the color (COL) and the isozyme variants were (22211) private; transmitted stably through repeated transfers to fresh PDA haplotypes in our sample from the opposite population may medium. The black vs. cream-colored and the fast vs. slow have been due to (i) local founder effects during the period of isozyme variants were designated 1 and 2, respectively. These initial infection from seed-borne inoculum, (ii) subsequent numbers were combined in the order PGI, PGM, LAP, sampling accidents (genetic drift), or (iii) selection against BGLU, and COL in designating multilocus phenotypes; thus, some haplotypes. for example, phenotype 21211 is slow for PGI, fast for PGM, Multilocus Associations. Multilocus associations among the slow for LAP, fast for BGLU, and black colored. These five five markers were assessed using the discrete log-linear putative loci, each with two alternative allelic states, poten- procedure of Fienberg (13). Likelihood ratio tests were used tially identify 25 = 32 phenotypes (haploid genotypes), among in a series to identify and eliminate nonsignificant interaction which 14 were observed. Such multilocus phenotypes (geno- terms after which log-linear models were constructed to fit types) will hereafter be referred to as haplotypes. Because R. the remaining terms. Models were fit in a hierarchical manner secalis reproduces asexually in nature (12), the array of such that a higher-order term was included only when lower- haplotypes can be considered to be equivalent to an allelic order terms failed to fit the data; when a higher-order term series within which mutation (including somatic recombina- was included, all of its lower-order relatives were also tion) is expected to produce new haplotypes over time.
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