Finished Genome of the Fungal Wheat Pathogen Mycosphaerella graminicola Reveals Dispensome Structure, Chromosome Plasticity, and Stealth Pathogenesis
Goodwin, S.B. ; M'Barek, S. Ben; Dhillon, B. ; Wittenberg, A.H.J. ; Crane, C.F. ; Hane, J.K. ; Foster, A.J. ; Lee, T.A.J. van der; Grimwood, J. ; Aerts, A. ; Antoniw, J. ; Bailey, A. ; Bluhm, B. ; Bowler, J. ; Bristow, J. ; Burgt, A. van der; Canto-Canché, B. ; Churchill, A.C.L. ; Conde-Ferràez, L. ; Cools, H.J. ; Coutinho, P.M. ; Csukai, M. ; Dehal, P. ; Wit, P.J.G.M. de; Donzelli, B. ; Geest, H.C. van de; Ham, R.C.H.J. van; Hammond-Kosack, K.E. ; Henrissat, B. ; Kilian, A. ; Kobayashi, A.K. ; Koopmann, E. ; Kourmpetis, Y. ; Kuzniar, A. ; Lindquist, E. ; Lombard, V. ; Maliepaard, C.A. ; Martins, N. ; Mehrabi, A. ; Nap, J.P.H. ; Ponomarenko, A. ; Rudd, J.J. ; Salamov, A. ; Schmutz, J. ; Schouten, H.J. ; Shapiro, H. ; Stergiopoulos, I. ; Torriani, S.F.F. ; Tu, H. ; Vries, R.P. de; Waalwijk, C. ; Ware, S.B. ; Wiebenga, A. ; Zwiers, L.H. ; Oliver, R.P. ; Grigoriev, I.V. ; Kema, G.H.J. - \ 2011
Plos Genetics 7 (2011)6. - ISSN 1553-7404 - 17 p.
magnaporthe-grisea - b-chromosomes - gene - host - organization - annotation - resistance - neurospora - expression - symbiosis
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. Author Summary The plant-pathogenic fungus Mycosphaerella graminicola causes septoria tritici blotch, one of the most economically important diseases of wheat worldwide and a potential threat to global food production. Unlike most other plant pathogens, M. graminicola has a long latent period during which it seems able to evade host defenses, and its genome appears to be unstable with many chromosomes that can change size or be lost during sexual reproduction. To understand its unusual mechanism of pathogenicity and high genomic plasticity, the genome of M. graminicola was sequenced more completely than that of any other filamentous fungus. The finished sequence contains 21 chromosomes, eight of which were different from those in the core genome and appear to have originated by ancient horizontal transfer from an unknown donor. The dispensable chromosomes collectively comprise the dispensome and showed extreme plasticity during sexual reproduction. A surprising feature of the M. graminicola genome was a low number of genes for enzymes that break down plant cell walls; this may represent an evolutionary response to evade detection by plant defense mechanisms. The stealth pathogenicity of M. graminicola may involve degradation of proteins rather than carbohydrates and could have evolved from an endophytic ancestor.
The fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization
Cuomo, C.A. ; Güldener, U. ; Xu, J.R. ; Trail, F. ; Turgeon, B.G. ; Waalwijk, C. - \ 2007
Science 317 (2007)5843. - ISSN 0036-8075 - p. 1400 - 1402.
neurospora - dna
We sequenced and annotated the genome of the filamentous fungus Fusarium graminearum, a major pathogen of cultivated cereals. Very few repetitive sequences were detected, and the process of repeat-induced point mutation, in which duplicated sequences are subject to extensive mutation, may partially account for the reduced repeat content and apparent low number of paralogous (ancestrally duplicated) genes. A second strain of F. graminearum contained more than 10,000 single-nucleotide polymorphisms, which were frequently located near telomeres and within other discrete chromosomal segments. Many highly polymorphic regions contained sets of genes implicated in plant-fungus interactions and were unusually divergent, with higher rates of recombination. These regions of genome innovation may result from selection due to interactions of F. graminearum with its plant hosts
On the ecology and evolution of fungal senescence
Maas, M.F.P.M. - \ 2005
Wageningen University. Promotor(en): Rolf Hoekstra, co-promotor(en): Fons Debets. - [S.l.] : S.n. - ISBN 9789085042846 - 118
pezizomycotina - neurospora - veroudering - verouderen - ecologie - evolutie - mitochondria - plasmiden - celbiologie - mutaties - genetica - pezizomycotina - neurospora - senescence - aging - ecology - evolution - mitochondria - plasmids - cellular biology - mutations - genetics
Aging evolves in the shadow of natural selection: Since the efficiency of natural selection declines with age, organisms will over the course of generations accumulate intrinsic, genetic factors that have a negative effect only late in life. This is generally known as the 'mutation accumulation' theory of aging. Should these factors additionally have apleiotropic, positive effect early on in life, for example on fertility, they could even befavoredby natural selection. This is known as the 'antagonisticpleiotropy' theory of aging. Aging is thus expected to be a multi-causal process resulting from intrinsic factors with negative effects late in life and possibly additional, positive effects early in life. It can be seen as the result of a lack of investment in somatic maintenance, a legacy of an organism's evolutionary past.In contrast to unitary organisms like most animals, modular organisms like plants, fungi and colonial invertebrates should not be subject to aging: In these organisms, there is no clear distinction between germ line and soma. Because the germ line should be immortal, in modular organisms aging or senescence is generally not expected, though parts or modules may be subject to aging or senescence. Though this is rare, there are striking examples oforganismalsenescence in fungi and plants, in which all parts of an individual die at the same time.This thesis deals with aging in two genera of filamentous fungi:NeurosporaandPodospora. It deals with the question whether there are similarities, both at the proximate or mechanistic level and at the ultimate or evolutionary level, between aging processes in fungi and aging processes as we know them from animals. It is shown that, at least in the pseudo-homothallic filamentousascomycetePodosporaanserina, aging is an intrinsic andmulticausalprocess as may be expected. An analysis of natural variation in life span shows that the main source of variation in life span corresponds to the presence or absence of mitochondrial plasmids, molecular parasites that interfere with respiration. Variation that arises spontaneously in the laboratory often corresponds to mitochondrial mutations in the electron transport chain. The latter mutations are all associated with the induction of alternative; nuclear encoded respiratory pathways and this leads via a yet unknown route to a stabilization of the otherwise unstable mitochondrial genome, a reduced level of reactive oxygen species as well as a reduced energy level. These mutations hence confer longevity at the cost of fertility. In addition to spontaneous mutations and chemical modifications of the electron transport chain, a dietary reduction in the amount of glucose can extend life span in fungi. The latter effect is strongly reduced by the presence of a type of mitochondrial plasmid that interferes with respiration, which indicates that it is strongly dependent on properly functioning mitochondria. The latter underlines the critical role of mitochondria in the fungal senescence
Nonmendelian inheritance of the HET-s prion or HET-s prion domains determines the het-S spore killing system in Podospora anserina
Dalstra, H.J.P. ; Zee, R.I. van der; Swart, K. ; Hoekstra, R.F. ; Saupe, S.J. ; Debets, A.J.M. - \ 2005
Fungal Genetics and Biology 42 (2005)10. - ISSN 1087-1845 - p. 836 - 847.
meiotic drive - heterokaryon incompatibility - vegetative incompatibility - in-vivo - protein - neurospora - fungi - organization - analog - genes
Two alleles of the het-s/S locus occur naturally in the filamentous fungus Podospora anserina, het-s and het-S. The het-s encoded protein can form a prion that propagates a self-perpetuating amyloid aggregate, resulting in two phenotypes for the het-s strains. The prion-infected [Het-s] shows an antagonistic interaction to het-S whereas the prion-free [Het-s*] is neutral in interaction to het-S. The antagonism between [Het-s] and het-S is seen as heterokaryon incompatibility at the somatic level and as het-S spore killing in the sexual cycle. Two different domains of the HET-s and HET-S proteins have been identified, and a structure-function relationship has been established for interactions at the somatic level. In this study, we correlate accumulation of the HET-s and HET-S proteins (visualized using GFP) during the sexual cycle with timing of het-S spore abortion. Also, we present the structure-function relationship of the HET-s domains for interactions in the sexual cycle. We show that the constructs that ensure het-s incompatibility function in somatic mycelium are also active in het-S spore killing in the sexual cycle. In addition, paternal prion transmission and het-S spore killing has been found with the HET-s(157-289) truncated protein. The consequences of the unique transition from a coenocytic to a cellular state in the sexual phase and the timing, and localization of paternal and maternal HET-s and HET-S expression that are pertinent to prion transmission, and het-S spore killing are elaborated. These data further support our previously proposed model for het-S spore killing.
Spore killing in the fungus Podospora anserina: a possible connection between meiotic drive and vegetative incompatibility
Gaag, M. van der; Debets, A.J.M. ; Hoekstra, R.F. - \ 2003
Genetica 117 (2003)1. - ISSN 0016-6707 - p. 59 - 65.
heterokaryon incompatibility - natural-populations - neurospora - plasmids - dynamics
Fungi in which the haploid nuclei resulting from meiosis are linearly arranged in asci provide unique opportunities to analyse abnormal segregation. Any meiotic drive system in such fungi will be observed in a cross between a driving and a sensitive strain as spore killing: the degeneration of half the ascospores in a certain proportion of the asci. In a sample of some 100 strains isolated from a single natural population we have discovered at least six different meiotic drive elements (van der Gaag et al., 2000). Here we report results of research that was aimed at elucidating a possible correlation between meiotic drive and vegetative incompatibility in eight different Spore killer strains from this population. We show that there is a strong correlation between these two phenotypes, although the precise genetic nature of the correlation is not yet clear. We discuss the implications of our results for the understanding of the population genetics of meiotic drive in Podospora
Sexual transmission of the [Het-s] prion leads to meiotic drive in Podospora anserina
Dalstra, H.J.P. ; Swart, K. ; Debets, A.J.M. ; Saupe, S.J. ; Hoekstra, R.F. - \ 2003
Proceedings of the National Academy of Sciences of the United States of America 100 (2003). - ISSN 0027-8424 - p. 6616 - 6621.
fungus podospora-anserina - heterokaryon incompatibility - spore killer - filamentous fungi - neurospora - protein - elements - products - meiosis - analog
In the filamentous fungus Podospora anserina, two phenomena are associated with polymorphism at the het-s locus, vegetative incompatibility and ascospore abortion. Two het-s alleles occur naturally, het-s and het-S. The het-s encoded protein is a prion propagating as a self-perpetuating amyloid aggregate. When prion-infected [Het-s] hyphae fuse with [Het-S] hyphae, the resulting heterokaryotic cells necrotize. [Het-s] and [Het-S] strains are sexually compatible. When, however, a female [Het-s] crosses with [Het-S], a significant percentage of het-S spores abort, in a way similar to spore killing in Neurospora and Podospora. We report here that sexual transmission of the [Het-s] prion after nonisogamous mating in the reproductive cycle of Podospora is responsible for the killing of het-S spores. Progeny of crosses between isogenic strains with distinct wild-type or introduced, ectopic het-s/S alleles were cytologically and genetically analyzed. The effect of het-s/S overexpression, ectopic het-s/S expression, absence of het-s expression, loss of [Het-s] prion infection, and the distribution patterns of HET-s/S-GFP proteins were categorized during meiosis and ascospore formation. This study unveiled a het-S spore-killing system that is governed by dosage of and interaction between the [Het-s] prion and the HET-S protein. Due to this property of the [Het-s] prion, the het-s allele acts as a meiotic drive element favoring maintenance of the prion-forming allele in natural populations.