Abstract
We have investigated the horizontal transfer of two mitochondrial plasmids and the Kalilo senescence phenotype in the fungus Neurospora without the use of heterokaryon-forcing markers. The Kalilo senescent state was only transferred between fully-compatible N. crassa strains, but not between strains differing at any of the loci het-c, het-d, het-e or mating-type. However, the linear plasmid kalDNA and the circular plasmid Han-2 were transferred following incompatible vegetative interactions. Our data suggest that vegetative incompatibility due to allelic differences at het-c is more effective in preventing transfer than that due to het-d, het-e or mating-type. Based on these observations we have developed a novel test for assessing vegetative incompatibility between Kalilo and non-Kalilo field isolates of N. intermedia. In this procedure combinations of Kalilo and non-Kalilo field isolates of N. intermedia were grown together and tested for senescence. Compatibility is inferred if the young non-Kalilo strain dies along with the senescent Kalilo strain, whereas incompatibility is inferred when the Kalilo strain dies without imposing its senescent state onto the non-Kalilo strain. Our results suggest that each of the nine Kalilo strains tested is incompatible with each of 20 non-Kalilo isolates from the same N. intermedia population of the Hawaiian island of Kauai. However, the observed incompatibility did not completely prevent cytoplasmic exchange, and in several cases plasmid transfer could be detected.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Anagnostakis SL (1982) Biological control of chestnut blight. Science 215:466–471
Anagnostakis SL (1983) Conversion to curative morphology in Endothia parasitica and its restiction by vegetative compatibility. Mycologia 75:777–780
Beadle GW, Coonradt VL (1994) Heterocaryosis in Neurospora crassa. Genetics 29:291–307
Bertrand H, Chan BS-S, Griffiths AJF (1985) Insertion of a foreign nucleotide sequence into mitochondrial DNA causes senescence in Neurospora intermedia. Cell 41:877–884
Bertrand H, Griffiths AJF, Court DA, Cheng CK (1986) An extrachromosomal plasmid is the etiological precursor of kalDNA insertion sequences in the mitochondrial chromosome of senescent Neurospora. Cell 47:829–837
Buss LW, (1982) Somatic cell parasitism and the evolution of somatic tissue compatibility. Proc Natl Acad Sci USA 79:5337–5341
Caten CE (1972) Vegetative incompatibility and cytoplasmic infection in fungi. J Gen Microbiol 72:221–229
Collins RA, Saville BJ (1990) Independent transfer of mitochondrial chromosomes and plasmids during unstable vegetative fusion in Neurospora. Nature 345:177–179
Court DA, Griffiths AJF, Kraus SR, Russell PJ, Bertrand H (1991) A new senescence-inducing mitochondrial linear plasmid in fieldisolated Neurospora crassa strains from India. Curr Genet 19:129–137
Davis RH, DeSerres FJ (1970) Genetic and microbiological research techniques for Neurospora crassa. Methods in Enzymology 17A:79–143
Esser K, Blaich R (1973) heterogeneic incompatibility in plants and animals. Adv Genet 17:107–145
Garnjobst L (1953) Genetic control of heterocaryosis in Neurospora crassa. Am J Bot 40:607–614
Glass NL, Kuldau GA (1992) Mating type and vegetative incompatibility in filamentous fungi. Annu Rev Phytopathol 30:201–224
Griffiths AJF (1992) Fungal senescence. Annu Rev Genet 26:351–372
Griffiths AJF, Kraus SR, Barton R, Court DA, Bertrand H (1990) Heterokaryotic transmission of senescence plasmid DNA in Neurospora. Curr Genet 17:139–145
Hartl DL, Dempster ER, Brown SR (1975) Adaptive significance of vegetative incompatibility in Neurospora crassa. Genetics 81: 553–569
Marcou D (1961) Notion de longévité et nature cytoplasmique du dèterminant de sénescence chez quelques champignons. Ann Sci Nat Bot 11:653–764
Myers CJ, Griffiths AJF, Bertrand H (1989) Linear Kalilo DNA is a Neurospora mitochondrial plasmid that intergrates into the mitochondrial DNA. Mol Gen Genet 220:113–120
Mylyk OM (1975) Heterokaryon incompatibility genes in Neurospora crassa detected using duplication-producing chromosome rearrangements. Genetics 80:107–124
Mylyk OM (1976) Heteromorphism for heterokaryon incompatibility genes in natural populations of Neurospora crassa. Genetics 83:275–284
Nauta MJ, Hoekstra RF (1993) Evolution of vegetative incompatibility in filamentous ascomycetes. 1. Selection models. Evolution (in press)
Perkins DD (1975) The use of duplication-generating rearrangements for studying heterokaryon incompatibility genes in Neurospora. Genetics 80:87–105
Perkins DD (1988) Main features of vegetative incompatibility in Neurospora. Fungal Genet Newslett 35:44–46
Perkins DD, Radford A, Newmeyer D, Björkman M (1982) Chromosomal loci of Neurospora crassa. Microbiol Rev 46:426–570
Rieck A, Griffiths AJF, Bertrand H (1982) Mitochondrial variants of Neurospora intermedia from nature. Can J Genet Cytol 24: 741–759
Turcq B, Deleu C, Denayrolles M, Bègueret J (1991) Two allelic genes responsible for vegetative incompatibility in the fungus Podospora anserina are not essential for cell viability. Mol Gen Genet 228:265–269
Yang X, Griffiths AJF (1993a) Plasmid diversity in senescent and nonsenescent strains of Neurospora. Mol Gen Genet 237:177–186
Yang X, Griffiths AJF (1993b) Male transmission of linear plasmids and mitochondrial DNA in the fungus Neurospora. Genetics 134: 1055–1062
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Debets, F., Yang, X. & Griffiths, A.J. Vegetative incompatibility in Neurospora: its effect on horizontal transfer of mitochondrial plasmids and senescence in natural populations. Curr Genet 26, 113–119 (1994). https://doi.org/10.1007/BF00313797
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00313797