Micología Aplicada International ISSN: 1534-2581 [email protected] Colegio de Postgraduados México

Esser, K. Genetics of fungi: retrospect and perspective Micología Aplicada International, vol. 13, núm. 1, january, 2001, pp. 1-8 Colegio de Postgraduados Puebla, México

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GENETICS OF FUNGI: RETROSPECT AND PERSPECTIVE*

K. ESSER

Lehrstuhl für Allgmeine Botanik, Ruhr-Universität, D-44780 Bochum, Germany Tel.: +49-234-32-22211; Fax: +49-234-32-14211; E-mail: [email protected] http://homepage.ruhr-uni-bochum.de/Karl.Esser

Accepted for publication August 30, 2000

ABSTRACT

This short survey on fungal genetics in the 20th century reflects the course of development from classical to molecular genetics and its implication to biotechnology.

Key words: Progressions in classical and molecular fungal genetics, implications to biotechnology.

INTRODUCTION done in this domain, without a solid knowledge of Fundamental Mycology. This Applied Mycology comprises a broad again involves a wide array including spectrum ranging from agriculture via taxonomy, morphology, physiology and pharmacy to medicine. The foundation of a genetics of fungi. At present the latter is very new journal presents an occasion to reflect important, because it is the prerequisite for the state of art in the field which is covered improvement of fungal exploitation in by this journal. From the title MICOLOGIA biotechnology, an area in which the fungi APLICADA INTERNATIONAL, one may derive at have gained tremendous importance and a first sight, that the aim of this journal is to therewith a renaissance of mycology was publish mainly papers dealing with Applied initiated. Mycology. This is true to a certain extent Since in the time of computers and genetic only, because no serious research can be engineering there is a strong tendency, especially within the young generation, to wear blind folders: one knows all about * A circumstantial version of this paper was sequencing a gene or molecular MpublishedICOL. APL recently. INT., 1113(1),. 2001, PP. 1-8 transformation, but one is not anymore 2 K. ESSER aware where it all came about. Living in in which each step involved the general the presence and improving science requires interest of researchers being concentrated knowledge of the past. Otherwise on one with a circle of problems. Progress phenomena will be rediscovered, because was made in increments and, as soon as they slipped out of mind. elucidation on one given topic was In following this line of thoughts I shall exhausted, experimental studies led on to a try to show in a brief overview of fungal further new and more promising level. This genetics the close linkage, in the widest does not mean that the topics of earlier sense of the word, of Applied Mycology periods were abandoned or no longer of and Fungal Genetics. This will be not a interest. They also progressed, albeit with literature review in the classical sense. This less momentum; for example, even for paper is meant as an opening address for studies of molecular biology, mapping of this new journal, which hopefully will chromosomal genes is sometimes required. succeed and be the place where papers of all branches of Mycology will be found. Comprehensive literature covering the whole The mostly descriptive studies in area of fungal genetics may be found in the mycology at the beginning of the last century following books or reviews: Esser and Kuenen involved neither experimentation nor 1967; Burnett 1975; Fincham et al. 1978; inheritance studies with fungi. However, the Fincham 1983; Perkins 1992; Wessels and 1,5, first genetic experiments with fungi were Meinhardt 1994; Kück 1995; Bos 1996 12, 13, 14, 17, 18, 19. begun shortly after the rediscovery of Mendel’s work, with various unrelated species. RETROSPECT Crossing experiments were reported in the zygomycete Phycomyces blakesleeanus There is no question that in the different (Burgeff 1912, 1914, 1915); in the ascomyctes periods of fungal genetics, as summarized Glomerella cingulata (Edgerton 1912, 1914) in Fig. 1, the principal interest was and Ascobolus magnificus (Dodge 1920), and fundamental research. However, one in the basidiomycete Schizophyllum commune should not underestimate the significance (Kniep 1918, 1920) 2,3,4,6,7,8,15,16. of this field to underpin and supplement the results of molecular genetics, not only at Thus, fungal genetics was born. present but also in the future. Unfortunately, the interest of geneticists in Following the spirit of the time, the aim this domain of genetics was slight at that of the fungal geneticists was at first to use time, partially due to the tremendous the fungi as experimental model organisms progress having been made in genetics using to support and enlarge the knowledge of diploid organisms, such as higher plants and inheritance as predicted by the Mendelian the fruit fly Drosophila as model organisms. laws. This mainly concerned the location of Nevertheless, fungal genetics developed genes on the chromosomes and their mode concomitantly with increasing knowledge of transmission (chromosomal or formal in other areas of biology as well as in genetics). Only decades later did the fungi chemistry and physics. In retrospect, a become accessible to extrachromosomal or stepwise progression becomes apparent, molecular genetics.

MICOL. APL. INT., 13(1), 2001, PP. 1-8 GENETICS OF FUNGI 3

Genetic engineering Extra chromosomal Plasmids genetics

Mitochondria

Gene expression

Chromosomal Recombination genetics

Breeding systems

1910 1920 1930 1940 1950 1960 1970 1980 1990 2000

Fig. 1. Scheme showing the stepwise progression of fungal genetics during the 20th century. The beginning of the main research areas is indicated in each particular step, followed by its specific topic 5.

As may be further seen from Fig. 1, in together with studies on the mechanism of the early 1920th the interest of geneticists mutation. was directed toward the elucidation of the In the mid of the 1940th, a third platform breeding systems. At the end of the 1920th was attained and therewith an essential it became evident, that mating in most fungi breakthrough, namely the inclusion of is not controlled by sexual differences based physiology into fungal genetics. A direct on sexual chromosomes, but by sexual correlation between chromosomal genes and incompatibility expressed as mating types. enzymes became evident. This area of gene The next platform was attained, when expression or biochemical genetics was first initiated by the work of Lindegren with established in Neurospora crassa and is Neurospora crassa, it became possible to connected with the names of Beadle and exploit the possibility of tetrad analysis Tatum. (especially in Ascomycetes) in order to Almost concomitantly with the understand the phenomenon of understanding of gene expression another recombination. Crossing over platform was reached at the beginning of chromosomal and chromatid interference the 1950th, when Ephrussi identified in and the establishment of chromosomal Saccharomyces cerevisiae mitochondria as maps, corrected by mapping functions were genetic traits responsible for the brought up to date by the late 1950th extrachromosomal inheritance, a

MICOL. APL. INT., 13(1), 2001, PP. 1-8 4 K. ESSER phenomenon recognized already along with fungal genetics and biotechnology had the rediscovery of the mendelian laws. developed for a long time quite There is another step, not shown in Fig. independently without a direct connection. 1. During the late 1950th, the genetic studies In the 1950th, when fungi were used for the of morphogenesis gained interest in several conversion of biochemical compounds laboratories. In my laboratory the (biological conversion), and later in the differentiation of fruiting bodies in the 1960s, when also perfect fungi were Ascomycetes and later in the included in biotechnology, it became Basidiomycetes, was shown to be controlled obvious that breeding techniques needed by a chain of nuclear genes steering the steps improvement. The time was ready to of differentiation. perform strain improvement by making use The largest platform was attained in the of the knowledge meanwhile accumulated mid of the 1970th, when fungal genetics in fundamental research by chromosomal became integrated into the domain of genetics. molecular genetics. This was achieved not This was achieved by recognizing the only by the discovery of genetic value of recombination, now using three information in mitochondrial DNA, but parameters: mutation, recombination, and also by the detection of mitochondrial selection under controlled conditions plasmids either integrated in the (concerted breeding 9, 10). The general mitochondrial genome or in the cytosol. The procedure is to bring together in one latter involved my laboratory as well as other organism, by means of recombination, groups in the US and France. favorable properties found either in wild Due to the cumulative data concerning the strains or obtained following mutagenic structure of extrachromosomal DNA, treatment, and then select for favorable including plasmids in both filamentous strains. Beginning with the 1960s, concerted fungi and yeasts, it was possible to step on breeding was successfully applied to many another platform and to remove the “iron perfect and also imperfect yeasts and curtain” between prokaryotes and mycelial fungi of industrial use. eukaryotes in that it now became possible Since many of the industrially used fungi to manipulate fungi by genetic engineering. are imperfect, concerted breeding with The advantage of fungi as hosts for genetic chromosomal genetics is very time engineering becomes rather obvious, consuming. Thus, it was a convenient because in contrast to Escherichia coli, coincidence that molecular cloning was fungi do not produce toxic substances. ready for industrial application. This was Furthermore genetic engineering may also also favored by the fact that fungi are be supported in fungi by classical genetics competent to process and express eukaryotic in making use of the advantage of genes properly. In contrast to prokaryotes, chromosomal recombination. they are able to splice mosaic genes and Parallel to the increasing importance of recognize their eukaryotic transcription, fungal genetics for fundamental research, translation, and signal sequences. Thus, it as shown in Fig. 1, the importance of fungi is not surprising that the past years have been with respect to applied research, especially a worldwide boom in using heterologous in the domain of biotechnology, has also gene expression for strain improvement in increased. As may be seen from Fig. 2, industry and agriculture.

MICOL. APL. INT., 13(1), 2001, PP. 1-8 GENETICS OF FUNGI 5

Fungal genetics Biotechnology Time scale

Food and beverages Antiquity and later

Subconsciously

End of 19th century Primary metabolites

Selection

Chromosomal 20th century

Breeding systems

1940 Recombination Gene expression Secondary metabolites ≈ (penicillin)

1950 Extra-chromosomal Biological transformation ≈

Mutation and selection

≈ 1960

ä Concerted breeding

≈ 1970

mtDNA plasmids ä Genetic engineering

≈ 1980

Fig. 2. Connections between fungal genetics and biotechnology 11. For explanations see text.

MICOL. APL. INT., 13(1), 2001, PP. 1-8 6 K. ESSER

PERSPECTIVE What can and should be done at this juncture? Based on the data of classical What is the perspective for fungal genetics genetics, the host-parasite system seems to in the future? Apart from promoting more be ready for studies with molecular genetics, or less intensively the areas which have been i.e. transformation of the host by cloned already influenced by both classical and resistant genes which may be taken either molecular genetics, according to the from resistant hosts or from fungi not author’s view there are four topics which specified on this or that particular host. have a “future” and are involved in both At present, there are some strategies fundamental and applied research. These which have yielded noteworthy results: areas are: 1. Characterization of molecular signals 1. Mycorrhizae involved in pathogen recognition and of 2. Host-parasite relations the molecular events that specify the 3. Intra- and intergenomic gene transfer expression of resistance. 4. Molecular basis of morphogenesis 2.Targeted disruption of fungal genes The first two domains are related, involved in phytopathogenicity. because there is no principle difference 3. The biocontrol of the chestnut blight between a peaceful or symbiotic association fungus Cryptophonetria parasitica was of a higher plant with a fungus for the benefit achieved by integrating a cDNA copy of of both (mycorrhiza) and the infection of a an RNA virus that confers hypovirulence. higher plant by a pathogenic fungus, leading With respect to mycorrhizae, at first some in many cases to the death of the host. In classical genetic methods need to be both cases, the prerequisite for the employed because there is no fundamental association is recognition. genetic model available explaining the onset Apart from the fact that further of this particular association. elucidation of this interaction between quite One must not neglect the fact that even if unrelated living beings is of interest from the genetic prerequisite for the host/fungus the point of view of fundamental research, interaction is known on a molecular basis, it is also of very great importance for applied the mode of expression of these genetic traits research. Namely, if the recognition system still remains an open question. For instance, is understood, it should be possible to in what way are enzyme systems mobilized increase the establishment of mycorrhizae to encourage the fungus after having formed in higher plants. This should lead to an an appressorium to penetrate cuticula and increase in the economic value of plants, cell wall of the plant? with respect to the present worldwide There is another aspect: does a transfer ecological discussion. Further, the addition of genetic material exist from fungus to host of fertilizers can be drastically diminished. or vice versa by plasmids or other In a similar way, based on the knowledge extrachromosomal genetic traits? Since, in or the understanding of the recognition addition to the detection of plasmids in fungi system host-parasite, it will be possible by and higher plants, in both groups of concerted breeding to develop resistant organisms many other extrachromosomal plants, leading to higher yield, and also to elements, such as viruses, have been found, avoid treatments of the plants with this area seems to be promising for further herbicides. genetic research.

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The third domain: the transfer of genetic genetics with respect to fundamental and material seems to be also a promising area applied research, into the area of molecular for genetic research in the future. This is genetics. It will thereby contribute not only supported by the fact that, in both fungi and to a better general understanding, but also higher plants, plasmids and other to a more skillful manipulation and extrachromosomal elements such as viruses understanding of living beings. and transposons have been found. There is Fungal genetics is a young discipline in also firm experimental evidence for gene science as compared to biotechnology, transfer between the nucleus and cell which is correlated with the beginning of organelles. human civilization. It was at first almost Where the fourth domain is concerned: exclusively devoted to fundamental the molecular mechanisms underlying research and came only during the last two genetics and physiology of morphogenesis decades into close relation to biotechnology, are poorly understood in fungi; fundamental when it appeared meaningful to apply research is required. But again, if the chromosomal genetics in a concerted principle of differentiation becomes known, manner to improve the production or the application for practical purposes transformation capacities of industrial and becomes obvious, leading, for instance, to agriculturally important fungi. an increase in productivity when yield is A landmark in the young relationship linked with morphological genetic between fungal genetics and biotechnology, differentiation. was the discovery of fungal plasmids and Fungi may serve as model organisms. As their relationship to mitochondrial DNA. mentioned above, for more than 40 years it This allowed incorporating also the fungi has been known that sexual differentiation in the concept of genetic engineering, thus is under polygenic control. Chromosomal making fungal genetics part of the new genes were identified controlling the biology and therewith giving applied different steps of morphogenesis. The mycology a new aspect. cloning and identification of the DNA sequences of these genes certainly will create the possibility for molecular LITERATURE CITED transformation and also of identifying the gene products responsible for single steps 1. Bos, C. J. (ed). 1996. Fungal genetics, principles and of morphogenesis. Work with Neurospora practice. Marcel Dekker, New York. 442 pp. crassa and Podospora anserina has shown 2. Burgeff, H. 1912. Über Sexualität, Variabilität und that specific products encoded by genes of Vererbung bei Phycomyces nitens Kunze. Ber. Dtsch. Bot. Ges. 30: 679-685. the mating-type locus are prerequisites for 3. Burgeff, H. 1914. Untersuchungen über Variabilität, the completion of sexual reproduction. Sexualität und Erblichkeit bei Phycomyces nitens Kunze. I. Flora, NF, Jena 107: 259- 316. 4. Burgeff, H. 1915. Untersuchungen über Variabilität, CONCLUSION Sexualität und Erblichkeit bei Phycomyces nitens Kunze. II. Flora, NF, Jena 108: 353- This survey shows that fungal genetics is 448. 5. Burnett, J. H. 1975. Mycogenetics, an introduction braced to extend its position, obtained to the general genetics of fungi. John Wiley, during the period of classical chromosomal London. 375 pp.

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6. Dodge, B. O. 1920. The life history of Ascobolus magnificus. Mycologia 12: 115-134. 7. Edgerton, C. W. 1912. Plus and minus strains in an ascomycete. Science 35: 151. 8. Edgerton, C. W. 1914. Plus and minus strains in the genus Glomerella. Am. J. Bot. 1: 244-254. 9. Esser, K. 1977. Concerted breeding in fungi and its biotechnological application. Endeavour N Ss 1: 143-148. 10. Esser, K. 1992. Genetics of fungi, past and future. World J. Microbiol. Biotechnol. 8 (Suppl. 1): 28-30. 11. Esser, K. 1996. Fungal genetics: from fundamental research to biotechnology. Progress in Botany vol. 58. Pp. 1-38. Springer Verlag, Berlin-Heidelberg. * 12. Esser, K. and R. Kuenen. 1967. Genetik der Pilze. Springer, Berlin-Heidelberg-New York. Ergänzter Neudruck. 501 pp. 13. Fincham, J. R. S. 1983. Genetics. Wright, Bristol. 643 pp. 14. Fincham, J. R. S., P. R. Day and A. Radford. 1978. Fungal genetics. Botanical monographs, vol. 4, 4th edn. Blackwell, Oxford. 636 pp. 15. Kniep, H. 1918. Über die Bedingungen der Schnallenbildung bie den Basidiomyceten. Flora, NF, Jena 111: 380-395. 16. Kniep, H. 1920. Über morphologische und physiologische Geschlechtsdifferenzierung. Verh. Phys.-Med. Ges., NF 46: 1-18. 17. Kück, U. (ed.). 1995. Genetics and Biotechnology, vol. II. In: The Mycota. Series eds. K. Esser and P. A. Lemke. Springer, Berlin- Heidelberg-New York. 375 pp. 18. Perkins, D. D. 1992. Neurospora: the organism behind the molecular revolution. Genetics 130: 687- 701. 19. Wessels, J. and F. Meinhardt (eds.) (1994) Growth, differentiation and sexuality, vol. I. In: The Mycota. Series eds. K. Esser and P. A. Lemke. Springer, Berlin-Heidelberg-New York. 433 pp.

* This paper contains an extended and comprehensive list of references.

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