Despite many years of careful research, the factors determining the pathogenicity of fungi to their hosts remain, with few exceptions, elusive. What are the key differences between the saprophytic mould in your bread bin, and the pathogenic fungus causing a disease in the field next door, or perhaps infesting your feet? A lot of people would like to know the answer to this question.
This multiauthor volume should help. The aim of the book is to provide an overview of current research on fungal pathogenesis, with the main emphasis on insights gained from molecular genetic analyses of the disease process. Key topics include morphogenesis, virulence, avirulence and signalling during host–pathogen interaction. The advent of techniques for the isolation and manipulation of specific genes has provided a more robust test of their roles in disease. The editor points out that ‘we are on the verge of a revolution in our understanding of fungal pathogens because of the application of genomics’. This is a worthy claim, although for most of the fungi included in the book it is an expectation rather than a reality, and for others much of the information from genomics is in the commercial rather than the public domain.
The text comprises 12 chapters on different pathogens or types of pathogens, with the main emphasis on fungi infecting plants, but a chapter as well on a human mycosis and fungi-infecting insects. This selective approach means there are several notable exceptions, such as powdery and downy mildews, Fusarium and other major genera. No doubt some will be disappointed by the omission of their favourite pathogen, but I sympathize with the editor's dilemma. It all goes back to the well-worn debate about an E. coli (or perhaps an Arabidopsis) of plant pathology. Nice idea, but which one would you choose?
The opening chapter on the human pulmonary pathogen Aspergillus fumigatus highlights the problem and the hope. A. fumigatus is an opportunist pathogen that does not normally live in an animal host. Genetic fingerprinting and infection tests fail to discriminate between environmental isolates and those causing disease. The only factors so far implicated in pathogenicity are certain biosynthetic pathways needed for rapid growth, and melanin, which may play a role in evasion of host defence. The hope, of course, is that sequencing of the A. fumigatus genome, and analysis of the transcriptome under conditions relevant to infection, will reveal key processes involved in pathogenicity. In view of the very limited current choice of drugs effective against invasive aspergillosis, there is also a hope that novel fungicide targets may be identified by the genomic route.
The next five chapters all cover plant pathogenic fungi: Botrytis, Cladosporium, Cochliobolus, Colletotrichum and Cryphonectria. These reviews contain much of interest, not only from the published literature but also speculation about the evolution of the pathogenic habit. Cladosporium fulvum, for instance, is suggested to be a primitive pathogen possessing only basic pathogenicity factors. Other fungi with more sophisticated infection structures and specialized parasitic adaptations might have evolved from such basic species at the time of angiosperm radiation. Yet we know that mycorrhizal fungi can already be detected in the roots of the first land plants in the Devonian. How closely is the diversity of fungal parasitism to plants linked to host evolution? Botrytis cinerea attacks a very wide range of hosts, yet the majority of Botrytis species have narrow host ranges restricted to a few hosts in one plant family. These host-specific Botrytis species appear to have necrotrophic habits very similar to the ubiquitous B. cinerea. The genus Colletotrichum contains specialized hemibiotrophs and outright necrotrophs occurring on the same host species. How did this scenario come about? In the case of Cochliobolus, new, more virulent races of the pathogen may evolve by horizontal transfer of a gene cluster encoding toxin biosythesis. At least in this case we have a molecular genetic explanation for some of the contrasts in virulence and host range. The same goes for Cryphonectria, where attenuation of virulence by virus infection has now been linked to effects on G-protein-mediated signal pathways. The topic of G-protein-mediated effects on fungal development and pathogenicity recurs in later chapters dealing with rice blast and maize smut.
The chapter on insect pathogenic fungi sits, somewhat surprisingly, amidst all this plant pathology. There are parallels, of course, in basic processes such as adhesion to, and penetration of, the host surface, yet the internal host environment and the nature of host defence responses confronting the pathogen are very different. There are parallel questions about host specificity and the extent to which different entomopathogenic fungi depend on their hosts. The population dynamics of some species may be related as much to factors enabling saprophytic growth and survival as to the ability to infect a host. The imperative to understand disease caused by these fungi is the hope that their pathogenicity can actually be increased to create more effective biocontrol agents.
The remainder of the book returns to fungi colonizing plants. These chapters start with Magnaporthe grisea, arguably the most tractable and best defined fungal pathosystem to date. Most of the tools of molecular genetics and functional genomics are in place: a physical map, a concerted sequencing effort, ESTs, transformation and an efficient system for targeted mutagenesis of specific genes. A further bonus is that the host plant, rice, has a relatively small genome which was almost completely sequenced before this book was published. The next chapter on Phytophthora (still an honorary fungus) provides a contrast. Plans are in place to sequence large numbers of ESTs from both P. infestans and P. sojae, but targeted gene knockouts remain problematical. To date, gene silencing is the only proven technology to attenuate gene expression in these pathogens. The final chapters cover rust fungi, endophytes and another well-characterized model, the maize smut fungus Ustilago maydis. Progress is being made in the identification of stage-specific genes expressed during host colonization by rusts. This mainly concerns early development of the pathogen prior to host entry, but includes genes involved in haustorial function, for instance nutrient transporters. The intriguing relationship between mutualistic endophytes and their hosts provides another perspective on the diversity of plant–fungus interactions. Infection of grasses by a range of endophytic fungi apparently benefits the host through protection against grazing and other types of stress. How the grass host and the fungal parasites coevolved is again a subject for speculation. The book concludes with a fascinating account of the link between mating and pathogenicity in Ustilago. The B locus required for mating also appears to function as a master regulatory locus controlling pathogenicity. This discovery highlights the close relationship between fundamental developmental processes and those involved in disease causation. Several genes required for cAMP signalling as well as MAP kinase cascades have also been implicated in regulating pathogenic development. Analysis of a large collection of mutants compromised in pathogenicity following insertional mutagenesis reinforces this impression. Mutations in genes involved in amino acid metabolism, signalling, gene regulation and various enzymatic functions all affect pathogenicity. Interestingly, around 50% of the genes identified in this screen have no known homologues in databases, suggesting that even in this well-characterized system much remains to be discovered.
Overall this is a very stimulating collection of reviews that illustrate the diversity of the pathogenic habit amongst fungi. The book will be of great value to advanced students and researchers wishing to explore the background to fungal molecular pathology. The editor is right to emphasize the potential power of comparative genomics to provide fresh insights into the nature and evolution of pathogenicity. This has already proved to be the case with the successful genome sequencing projects targeting animal pathogenic bacteria. But herein lies a problem for any book entering this fast-moving territory – a type of instant obsolescence. Despite the fact that this volume appears to have been produced by a fast-track camera-ready system (variable fonts, layout, etc.) I found only one reference later than 1999. This does not undermine the value of review articles, but anyone really wanting to explore the latest action needs to search rapid-publication journals or surf the net. The second problem this book faces is the price tag. The production standards are acceptable, and the figures include a colour plate, but I still think any book crossing the £100 threshold needs to be more of a Rolls Royce than this one.