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Population structure of Geosmithia morbida, the causal agent of thousand cankers disease of walnut trees in the United States.

Zerillo MM, Ibarra Caballero J, Woeste K, Graves AD, Hartel C, Pscheidt JW, Tonos J, Broders K, Cranshaw W, Seybold SJ, Tisserat N - PLoS ONE (2014)

Bottom Line: The disease was first reported in the western United States (USA) on several Juglans species, but has been found more recently in the eastern USA in the native range of the highly susceptible Juglans nigra.Most of the haplotypes isolated from the native range of J. major (Arizona and New Mexico) were found in those states only or present in distinct genetic clusters.The large number of haplotypes observed and the genetic complexity of G. morbida indicate that it evolved in association with at least one Juglans spp. and the walnut twig beetle long before the first reports of the disease.

View Article: PubMed Central - PubMed

Affiliation: Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, Colorado, United States of America.

ABSTRACT
The ascomycete Geosmithia morbida and the walnut twig beetle Pityophthorus juglandis are associated with thousand cankers disease of Juglans (walnut) and Pterocarya (wingnut). The disease was first reported in the western United States (USA) on several Juglans species, but has been found more recently in the eastern USA in the native range of the highly susceptible Juglans nigra. We performed a comprehensive population genetic study of 209 G. morbida isolates collected from Juglans and Pterocarya from 17 geographic regions distributed across 12 U.S. states. The study was based on sequence typing of 27 single nucleotide polymorphisms from three genomic regions and genotyping with ten microsatellite primer pairs. Using multilocus sequence-typing data, 197 G. morbida isolates were placed into one of 57 haplotypes. In some instances, multiple haplotypes were recovered from isolates collected on the same tree. Twenty-four of the haplotypes (42%) were recovered from more than one isolate; the two most frequently occurring haplotypes (H02 and H03) represented 36% of all isolates. These two haplotypes were abundant in California, but were not recovered from Arizona or New Mexico. G. morbida population structure was best explained by four genetically distinct groups that clustered into three geographic regions. Most of the haplotypes isolated from the native range of J. major (Arizona and New Mexico) were found in those states only or present in distinct genetic clusters. There was no evidence of sexual reproduction or genetic recombination in any population. The scattered distribution of the genetic clusters indicated that G. morbida was likely disseminated to different regions at several times and from several sources. The large number of haplotypes observed and the genetic complexity of G. morbida indicate that it evolved in association with at least one Juglans spp. and the walnut twig beetle long before the first reports of the disease.

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Unrooted phylogenetic tree of Geosmithia species based on ITS/BT sequences.A Bayesian analysis was performed for 1,500,000 generations by using a GTR-gamma distributed model of evolution (invariant sites). Bayesian percentages (≥50%) are depicted above each branch, and maximum likelihood bootstrap values (≥500) obtained by using PhyML (default parameters) are shown below most branches. Geosmithia morbida haplotypes are color coded according to their genetic cluster assignment (four-cluster-MLST-DAPC model, as in Figure 3) and haplotypes sharing the same ITS and BT sequences are co-located. Leaves pertaining to the same branch were arranged together according to their cluster assignment. GenBank accession numbers of other Geosmithia spp. are identified within parenthesis.
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pone-0112847-g002: Unrooted phylogenetic tree of Geosmithia species based on ITS/BT sequences.A Bayesian analysis was performed for 1,500,000 generations by using a GTR-gamma distributed model of evolution (invariant sites). Bayesian percentages (≥50%) are depicted above each branch, and maximum likelihood bootstrap values (≥500) obtained by using PhyML (default parameters) are shown below most branches. Geosmithia morbida haplotypes are color coded according to their genetic cluster assignment (four-cluster-MLST-DAPC model, as in Figure 3) and haplotypes sharing the same ITS and BT sequences are co-located. Leaves pertaining to the same branch were arranged together according to their cluster assignment. GenBank accession numbers of other Geosmithia spp. are identified within parenthesis.

Mentions: Phylogenetic analysis showing the relatedness of G. morbida haplotypes and other Geosmithia species was conducted by using two concatenated genomic regions (ITS/BT). MAP was not included because of the absence of sequence data for other species in public databases. Fifty-five sequences were compared, six of which corresponded to other species of Geosmithia downloaded from GenBank (accessions are shown in Figure 2); the others corresponded to G. morbida haplotypes. Because MAP was not considered, some of the haplotypes sharing the same ITS and BT sequences were combined in a single leaf (e.g., H32 and H33, Figure 2). Sequences were aligned by using ClustalW [46] and trimmed in MEGA 5.05 [47], with lengths of 520 bp and 406 bp for ITS and BT, respectively. We performed two analyses: a Bayesian inference of phylogeny with a variant of Markov chain Monte Carlo [48] in MrBayes v3.1.2 [49] by using a general time-reversible model with inverse-gamma rates of evolution for 1,500,000 generations and a burn-in of 0.25; and a maximum-likelihood analysis in PhyML 3.0 [50] (http://www.atgc-montpellier.fr/phyml/) with default values except for bootstrap of 1,000 replicates. The unrooted phylogenetic tree obtained in MrBayes was formatted in MEGA5 [47] and branches with bootstrap values equal or greater than 50% were shown. Bootstrap values greater than 500 obtained in maximum-likelihood analysis were also indicated in that tree.


Population structure of Geosmithia morbida, the causal agent of thousand cankers disease of walnut trees in the United States.

Zerillo MM, Ibarra Caballero J, Woeste K, Graves AD, Hartel C, Pscheidt JW, Tonos J, Broders K, Cranshaw W, Seybold SJ, Tisserat N - PLoS ONE (2014)

Unrooted phylogenetic tree of Geosmithia species based on ITS/BT sequences.A Bayesian analysis was performed for 1,500,000 generations by using a GTR-gamma distributed model of evolution (invariant sites). Bayesian percentages (≥50%) are depicted above each branch, and maximum likelihood bootstrap values (≥500) obtained by using PhyML (default parameters) are shown below most branches. Geosmithia morbida haplotypes are color coded according to their genetic cluster assignment (four-cluster-MLST-DAPC model, as in Figure 3) and haplotypes sharing the same ITS and BT sequences are co-located. Leaves pertaining to the same branch were arranged together according to their cluster assignment. GenBank accession numbers of other Geosmithia spp. are identified within parenthesis.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC4231075&req=5

pone-0112847-g002: Unrooted phylogenetic tree of Geosmithia species based on ITS/BT sequences.A Bayesian analysis was performed for 1,500,000 generations by using a GTR-gamma distributed model of evolution (invariant sites). Bayesian percentages (≥50%) are depicted above each branch, and maximum likelihood bootstrap values (≥500) obtained by using PhyML (default parameters) are shown below most branches. Geosmithia morbida haplotypes are color coded according to their genetic cluster assignment (four-cluster-MLST-DAPC model, as in Figure 3) and haplotypes sharing the same ITS and BT sequences are co-located. Leaves pertaining to the same branch were arranged together according to their cluster assignment. GenBank accession numbers of other Geosmithia spp. are identified within parenthesis.
Mentions: Phylogenetic analysis showing the relatedness of G. morbida haplotypes and other Geosmithia species was conducted by using two concatenated genomic regions (ITS/BT). MAP was not included because of the absence of sequence data for other species in public databases. Fifty-five sequences were compared, six of which corresponded to other species of Geosmithia downloaded from GenBank (accessions are shown in Figure 2); the others corresponded to G. morbida haplotypes. Because MAP was not considered, some of the haplotypes sharing the same ITS and BT sequences were combined in a single leaf (e.g., H32 and H33, Figure 2). Sequences were aligned by using ClustalW [46] and trimmed in MEGA 5.05 [47], with lengths of 520 bp and 406 bp for ITS and BT, respectively. We performed two analyses: a Bayesian inference of phylogeny with a variant of Markov chain Monte Carlo [48] in MrBayes v3.1.2 [49] by using a general time-reversible model with inverse-gamma rates of evolution for 1,500,000 generations and a burn-in of 0.25; and a maximum-likelihood analysis in PhyML 3.0 [50] (http://www.atgc-montpellier.fr/phyml/) with default values except for bootstrap of 1,000 replicates. The unrooted phylogenetic tree obtained in MrBayes was formatted in MEGA5 [47] and branches with bootstrap values equal or greater than 50% were shown. Bootstrap values greater than 500 obtained in maximum-likelihood analysis were also indicated in that tree.

Bottom Line: The disease was first reported in the western United States (USA) on several Juglans species, but has been found more recently in the eastern USA in the native range of the highly susceptible Juglans nigra.Most of the haplotypes isolated from the native range of J. major (Arizona and New Mexico) were found in those states only or present in distinct genetic clusters.The large number of haplotypes observed and the genetic complexity of G. morbida indicate that it evolved in association with at least one Juglans spp. and the walnut twig beetle long before the first reports of the disease.

View Article: PubMed Central - PubMed

Affiliation: Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, Colorado, United States of America.

ABSTRACT
The ascomycete Geosmithia morbida and the walnut twig beetle Pityophthorus juglandis are associated with thousand cankers disease of Juglans (walnut) and Pterocarya (wingnut). The disease was first reported in the western United States (USA) on several Juglans species, but has been found more recently in the eastern USA in the native range of the highly susceptible Juglans nigra. We performed a comprehensive population genetic study of 209 G. morbida isolates collected from Juglans and Pterocarya from 17 geographic regions distributed across 12 U.S. states. The study was based on sequence typing of 27 single nucleotide polymorphisms from three genomic regions and genotyping with ten microsatellite primer pairs. Using multilocus sequence-typing data, 197 G. morbida isolates were placed into one of 57 haplotypes. In some instances, multiple haplotypes were recovered from isolates collected on the same tree. Twenty-four of the haplotypes (42%) were recovered from more than one isolate; the two most frequently occurring haplotypes (H02 and H03) represented 36% of all isolates. These two haplotypes were abundant in California, but were not recovered from Arizona or New Mexico. G. morbida population structure was best explained by four genetically distinct groups that clustered into three geographic regions. Most of the haplotypes isolated from the native range of J. major (Arizona and New Mexico) were found in those states only or present in distinct genetic clusters. There was no evidence of sexual reproduction or genetic recombination in any population. The scattered distribution of the genetic clusters indicated that G. morbida was likely disseminated to different regions at several times and from several sources. The large number of haplotypes observed and the genetic complexity of G. morbida indicate that it evolved in association with at least one Juglans spp. and the walnut twig beetle long before the first reports of the disease.

Show MeSH
Related in: MedlinePlus