Stephen B. Goodwin

Historical and recent migrations of Phytophthora infestans: chronology, pathways, and implications.

The 1984 report of A2 mating types of Phytophthora infestans (Mont.) de Bary in western Europe (20) was the first indication of new and dramatic developments in populations ofthat Fungus. This discovery stimuiated plant pathologists aH over the world to analyze local populations, since previously only the A 1 mating type had been detected outside of central Mexico (Fig. I). The analyses of a large number of dispersed Eocal populations indicated, surprisingly, that the changes were not restricted to western Europe but, rather, were worldwide (Fig. 2) [3,10,23,26,36,41). The recent wortdwide changes in populations mOSK certainly result from migration. Indeed, migration has played an essential role in the entire history of potato late blight. In this article we illustrate that role. To provide context, however, we first present background concerning the basic biology/pathology of P. infestans, the genetic tools used to investigate populations of P. infesrons, and the char. acteristics of the source population of P. infestans.

Resurgence of the Irish Potato Famine Fungus

rope and led to the Irish potato famine, the plant pathogenic fungus Phytophthora infestans is again creating a major plant health problem. Migrations of virulent and fungicide-resistant strains in the past two decades have caused a worldwide resurgence of the potato (and tomato) late blight disease. Epidemics in parts of the United States and Canada during the early 1990s were locally devastating, sometimes causing total crop loss and severe economic hardship for many potato and tomato growers. This resurgence supports the view that introduced pathogens and new variants of old ones present a real and immediate threat for plants as well as for animals and humans.

Finished Genome of the Fungal Wheat Pathogen Mycosphaerella graminicola Reveals Dispensome Structure, Chromosome Plasticity, and Stealth Pathogenesis

The plant-pathogenic fungus Mycosphaerella graminicola (asexual stage: Septoria tritici) causes septoria tritici blotch, a disease that greatly reduces the yield and quality of wheat. This disease is economically important in most wheat-growing areas worldwide and threatens global food production. Control of the disease has been hampered by a limited understanding of the genetic and biochemical bases of pathogenicity, including mechanisms of infection and of resistance in the host. Unlike most other plant pathogens, M. graminicola has a long latent period during which it evades host defenses. Although this type of stealth pathogenicity occurs commonly in Mycosphaerella and other Dothideomycetes, the largest class of plant-pathogenic fungi, its genetic basis is not known. To address this problem, the genome of M. graminicola was sequenced completely. The finished genome contains 21 chromosomes, eight of which could be lost with no visible effect on the fungus and thus are dispensable. This eight-chromosome dispensome is dynamic in field and progeny isolates, is different from the core genome in gene and repeat content, and appears to have originated by ancient horizontal transfer from an unknown donor. Synteny plots of the M. graminicola chromosomes versus those of the only other sequenced Dothideomycete, Stagonospora nodorum, revealed conservation of gene content but not order or orientation, suggesting a high rate of intra-chromosomal rearrangement in one or both species. This observed “mesosynteny” is very different from synteny seen between other organisms. A surprising feature of the M. graminicola genome compared to other sequenced plant pathogens was that it contained very few genes for enzymes that break down plant cell walls, which was more similar to endophytes than to pathogens. The stealth pathogenesis of M. graminicola probably involves degradation of proteins rather than carbohydrates to evade host defenses during the biotrophic stage of infection and may have evolved from endophytic ancestors.

Diverse Lifestyles and Strategies of Plant Pathogenesis Encoded in the Genomes of Eighteen Dothideomycetes Fungi

The class Dothideomycetes is one of the largest groups of fungi with a high level of ecological diversity including many plant pathogens infecting a broad range of hosts. Here, we compare genome features of 18 members of this class, including 6 necrotrophs, 9 (hemi)biotrophs and 3 saprotrophs, to analyze genome structure, evolution, and the diverse strategies of pathogenesis. The Dothideomycetes most likely evolved from a common ancestor more than 280 million years ago. The 18 genome sequences differ dramatically in size due to variation in repetitive content, but show much less variation in number of (core) genes. Gene order appears to have been rearranged mostly within chromosomal boundaries by multiple inversions, in extant genomes frequently demarcated by adjacent simple repeats. Several Dothideomycetes contain one or more gene-poor, transposable element (TE)-rich putatively dispensable chromosomes of unknown function. The 18 Dothideomycetes offer an extensive catalogue of genes involved in cellulose degradation, proteolysis, secondary metabolism, and cysteine-rich small secreted proteins. Ancestors of the two major orders of plant pathogens in the Dothideomycetes, the Capnodiales and Pleosporales, may have had different modes of pathogenesis, with the former having fewer of these genes than the latter. Many of these genes are enriched in proximity to transposable elements, suggesting faster evolution because of the effects of repeat induced point (RIP) mutations. A syntenic block of genes, including oxidoreductases, is conserved in most Dothideomycetes and upregulated during infection in L. maculans, suggesting a possible function in response to oxidative stress.

The Population Genetics of Phytophthora

There are more than 60 species in the genus Phytophthora (94), and most are destructive plant pathogens. Extensive efforts are directed at the control of Phytophthora diseases each year, yet they still cause serious crop losses. For example, more than

Genetic Change Within Populations of Phytophthora infestans in the United States and Canada During 1994 to 1996: Role of Migration and Recombination

200 million in lost production annually is attributed to Phytophthora diseases in Australia alone (47). Late blight, caused by P. infestans, probably cost United States potato and tomato growers more than

Phylogenetic Analysis of Cercospora and Mycosphaerella Based on the Internal Transcribed Spacer Region of Ribosomal DNA

200 million during 1994:

The genomes of the fungal plant pathogens Cladosporium fulvum and Dothistroma septosporum reveal adaptation to different hosts and lifestyles but also signatures of common ancestry.

100 million in lost crop production and

Fueling the future with fungal genomics

100 million in additional control measures (30). Although usually remembered for the historical role played by P. infestans during the Irish potato famine of the 1840s, Phytophthora species still pose an immediate and real threat to world agriculture. Despite the huge economic costs of Phytophthora diseases, relatively little is known about the population genetics of the causal organisms. Genetic analyses in this genus were hindered until recently by the inability to perform genetic crosses, due to homothallism, poor germination of oospores, lack of suitable markers, or, simply, the limited availability of both mating types (91). Biochemical markers were first applied to analyze populations of P. cinnamomi (77) and P. infestans (99) in the mid-1980s. Progress accelerated during the 1990s with the addition of DNA-based markers and the inclusion of more species. Although much remains to be learned, some general patterns are beginning to emerge. The purpose of this paper is to review the literature on the population genetics of Phytophthora species and to formulate testable hypotheses that can explain many of the observed phenomena. Five main areas will be considered: sources of variation, migration, genetic drift, selection, and mating systems. Reviews of the genetics, systematics, and evolution of Phytophthora species have been published recently (9,10,48,50,91) and will not be duplicated here, except as needed to clarify particular points.

Meiosis Drives Extraordinary Genome Plasticity in the Haploid Fungal Plant Pathogen Mycosphaerella graminicola

ABSTRACT Dramatic changes occurred within populations of Phytophthora infestans in the United States and Canada from 1994 through 1996. Occurrence of the US-8 genotype, detected rarely during 1992 and 1993, increased rapidly and predominated in most regions during 1994 through 1996. US-7, which infected both potato and tomato and made up almost 50% of the sample during 1993, was detected only rarely among 330 isolates from the United States analyzed during 1994. It was not detected at all in more limited samples from 1996. Thus, ability to infect both potato and tomato apparently did not increase the fitness of this genotype relative to US-8, as predicted previously. US-1, the previously dominant genotype throughout the United States and Canada, made up 8% or less of the samples analyzed during 1994 through 1996. A few additional genotypes were detected, which could indicate the beginnings of sexual reproduction of P. infestans within the United States and Canada. However, clonal reproduction still predominated in all locations sampled; opportunities for sexual reproduction probably were limited, because the A1 and A2 mating types usually were separated geographically. The high sensitivity of the US-1 genotype to the fungicide metalaxyl also could have reduced opportunities for contact between the mating types in fields where this compound was applied. The previous correlation between metalaxyl sensitivity and genotype was confirmed and extended to a new genotype, US-17: all US-1 isolates tested were sensitive; all isolates of the US-7, US-8, and US-17 genotypes tested to date have been resistant. Isolates of P. capsici and P. erythroseptica, two other species often found on tomato and potato, could be easily distinguished from each other and from P. infestans using a simple allozyme assay for the enzyme glucose-6-phosphate isomerase. This technique could be useful for rapid identification of species, in addition to genotype of P. infestans. It generally was not possible to predict which genotypes would be present in a location from 1 year to the next. Long-distance movement of US-8 in seed tubers was documented, and this was probably the primary means for the rapid spread of this genotype from 1993 through 1996.