Limits...
Finished genome of the fungal wheat pathogen Mycosphaerella graminicola reveals dispensome structure, chromosome plasticity, and stealth pathogenesis.

Goodwin SB, M'barek SB, Dhillon B, Wittenberg AH, Crane CF, Hane JK, Foster AJ, Van der Lee TA, Grimwood J, Aerts A, Antoniw J, Bailey A, Bluhm B, Bowler J, Bristow J, van der Burgt A, Canto-Canché B, Churchill AC, Conde-Ferràez L, Cools HJ, Coutinho PM, Csukai M, Dehal P, De Wit P, Donzelli B, van de Geest HC, van Ham RC, Hammond-Kosack KE, Henrissat B, Kilian A, Kobayashi AK, Koopmann E, Kourmpetis Y, Kuzniar A, Lindquist E, Lombard V, Maliepaard C, Martins N, Mehrabi R, Nap JP, Ponomarenko A, Rudd JJ, Salamov A, Schmutz J, Schouten HJ, Shapiro H, Stergiopoulos I, Torriani SF, Tu H, de Vries RP, Waalwijk C, Ware SB, Wiebenga A, Zwiers LH, Oliver RP, Grigoriev IV, Kema GH - PLoS Genet. (2011)

Bottom Line: 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.The finished genome contains 21 chromosomes, eight of which could be lost with no visible effect on the fungus and thus are dispensable.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.

View Article: PubMed Central - PubMed

Affiliation: USDA-Agricultural Research Service, Purdue University, West Lafayette, Indiana, United States of America. Steve.Goodwin@ARS.USDA.gov

ABSTRACT
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.

Show MeSH

Related in: MedlinePlus

Features of chromosome 2 of Mycosphaerella graminicola and alignment to genetic linkage maps.A, Plot of GC content. Areas of low GC usually correspond to regions of repetitive DNA. B, Repetitive regions of the M. graminicola genome. C, Single-copy (red) regions of the M. graminicola genome. D, Locations of genes for proteins containing signal peptides. E, Locations of homologs involved in pathogenicity or virulence that have been experimentally verified in species pathogenic to plant, animal or human hosts. F, Approximate locations of quantitative trait loci (QTL) for pathogenicity to wheat. G, Alignments between the genomic sequence and two genetic linkage maps of crosses involving isolate IPO323. Top half, Genetic linkage map of the cross between IPO323 and the Algerian durum wheat isolate IPO95052. Bottom half, Genetic linkage map of the cross between bread wheat isolates IPO323 and IPO94269. The physical map represented by the genomic sequence is in the center. Lines connect mapped genetic markers in each linkage map to their corresponding locations on the physical map based on the sequences of the marker loci. Exceptions to the almost perfect alignment between the three maps are indicated by crossed lines, most likely due to occasional incorrect scorings of the marker alleles. Chromosome 2 was used for this illustration because no QTL mapped to chromosome 1.
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC3111534&req=5

pgen-1002070-g001: Features of chromosome 2 of Mycosphaerella graminicola and alignment to genetic linkage maps.A, Plot of GC content. Areas of low GC usually correspond to regions of repetitive DNA. B, Repetitive regions of the M. graminicola genome. C, Single-copy (red) regions of the M. graminicola genome. D, Locations of genes for proteins containing signal peptides. E, Locations of homologs involved in pathogenicity or virulence that have been experimentally verified in species pathogenic to plant, animal or human hosts. F, Approximate locations of quantitative trait loci (QTL) for pathogenicity to wheat. G, Alignments between the genomic sequence and two genetic linkage maps of crosses involving isolate IPO323. Top half, Genetic linkage map of the cross between IPO323 and the Algerian durum wheat isolate IPO95052. Bottom half, Genetic linkage map of the cross between bread wheat isolates IPO323 and IPO94269. The physical map represented by the genomic sequence is in the center. Lines connect mapped genetic markers in each linkage map to their corresponding locations on the physical map based on the sequences of the marker loci. Exceptions to the almost perfect alignment between the three maps are indicated by crossed lines, most likely due to occasional incorrect scorings of the marker alleles. Chromosome 2 was used for this illustration because no QTL mapped to chromosome 1.

Mentions: The finished genome of M. graminicola isolate IPO323 consists of 21 complete chromosomes, telomere to telomere (Figure S2), with the exceptions of one telomere of chromosome 21 and two internal gaps of unclonable DNA that are missing from chromosome 18 (Table 1). Alignments between the 21 chromosomes and two genetic linkage maps yielded an excellent correspondence (Figure 1 and Figure S3), representing the most complete and the first finished sequence of a filamentous fungus. The next most complete genome of a filamentous fungus is that of Aspergillus fumigatus, which did not include centromere sequences and contained 11 gaps in total [13]. The complete 43,960-bp mitochondrial genome also was obtained and has been described elsewhere [14].


Finished genome of the fungal wheat pathogen Mycosphaerella graminicola reveals dispensome structure, chromosome plasticity, and stealth pathogenesis.

Goodwin SB, M'barek SB, Dhillon B, Wittenberg AH, Crane CF, Hane JK, Foster AJ, Van der Lee TA, Grimwood J, Aerts A, Antoniw J, Bailey A, Bluhm B, Bowler J, Bristow J, van der Burgt A, Canto-Canché B, Churchill AC, Conde-Ferràez L, Cools HJ, Coutinho PM, Csukai M, Dehal P, De Wit P, Donzelli B, van de Geest HC, van Ham RC, Hammond-Kosack KE, Henrissat B, Kilian A, Kobayashi AK, Koopmann E, Kourmpetis Y, Kuzniar A, Lindquist E, Lombard V, Maliepaard C, Martins N, Mehrabi R, Nap JP, Ponomarenko A, Rudd JJ, Salamov A, Schmutz J, Schouten HJ, Shapiro H, Stergiopoulos I, Torriani SF, Tu H, de Vries RP, Waalwijk C, Ware SB, Wiebenga A, Zwiers LH, Oliver RP, Grigoriev IV, Kema GH - PLoS Genet. (2011)

Features of chromosome 2 of Mycosphaerella graminicola and alignment to genetic linkage maps.A, Plot of GC content. Areas of low GC usually correspond to regions of repetitive DNA. B, Repetitive regions of the M. graminicola genome. C, Single-copy (red) regions of the M. graminicola genome. D, Locations of genes for proteins containing signal peptides. E, Locations of homologs involved in pathogenicity or virulence that have been experimentally verified in species pathogenic to plant, animal or human hosts. F, Approximate locations of quantitative trait loci (QTL) for pathogenicity to wheat. G, Alignments between the genomic sequence and two genetic linkage maps of crosses involving isolate IPO323. Top half, Genetic linkage map of the cross between IPO323 and the Algerian durum wheat isolate IPO95052. Bottom half, Genetic linkage map of the cross between bread wheat isolates IPO323 and IPO94269. The physical map represented by the genomic sequence is in the center. Lines connect mapped genetic markers in each linkage map to their corresponding locations on the physical map based on the sequences of the marker loci. Exceptions to the almost perfect alignment between the three maps are indicated by crossed lines, most likely due to occasional incorrect scorings of the marker alleles. Chromosome 2 was used for this illustration because no QTL mapped to chromosome 1.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3111534&req=5

pgen-1002070-g001: Features of chromosome 2 of Mycosphaerella graminicola and alignment to genetic linkage maps.A, Plot of GC content. Areas of low GC usually correspond to regions of repetitive DNA. B, Repetitive regions of the M. graminicola genome. C, Single-copy (red) regions of the M. graminicola genome. D, Locations of genes for proteins containing signal peptides. E, Locations of homologs involved in pathogenicity or virulence that have been experimentally verified in species pathogenic to plant, animal or human hosts. F, Approximate locations of quantitative trait loci (QTL) for pathogenicity to wheat. G, Alignments between the genomic sequence and two genetic linkage maps of crosses involving isolate IPO323. Top half, Genetic linkage map of the cross between IPO323 and the Algerian durum wheat isolate IPO95052. Bottom half, Genetic linkage map of the cross between bread wheat isolates IPO323 and IPO94269. The physical map represented by the genomic sequence is in the center. Lines connect mapped genetic markers in each linkage map to their corresponding locations on the physical map based on the sequences of the marker loci. Exceptions to the almost perfect alignment between the three maps are indicated by crossed lines, most likely due to occasional incorrect scorings of the marker alleles. Chromosome 2 was used for this illustration because no QTL mapped to chromosome 1.
Mentions: The finished genome of M. graminicola isolate IPO323 consists of 21 complete chromosomes, telomere to telomere (Figure S2), with the exceptions of one telomere of chromosome 21 and two internal gaps of unclonable DNA that are missing from chromosome 18 (Table 1). Alignments between the 21 chromosomes and two genetic linkage maps yielded an excellent correspondence (Figure 1 and Figure S3), representing the most complete and the first finished sequence of a filamentous fungus. The next most complete genome of a filamentous fungus is that of Aspergillus fumigatus, which did not include centromere sequences and contained 11 gaps in total [13]. The complete 43,960-bp mitochondrial genome also was obtained and has been described elsewhere [14].

Bottom Line: 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.The finished genome contains 21 chromosomes, eight of which could be lost with no visible effect on the fungus and thus are dispensable.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.

View Article: PubMed Central - PubMed

Affiliation: USDA-Agricultural Research Service, Purdue University, West Lafayette, Indiana, United States of America. Steve.Goodwin@ARS.USDA.gov

ABSTRACT
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.

Show MeSH
Related in: MedlinePlus