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Elite UK winter wheat cultivars differ in their ability to support the colonization of beneficial root-infecting fungi.

ABSTRACT: In numerous countries, Gaeumannomyces species, within the Magnaporthaceae family, have previously been implicated in the suppression of take-all root disease in wheat. A UK arable isolate collection (n=47) was gathered and shown to contain Gaeumannomyces hyphopodioides and an unnamed Magnaporthaceae species. A novel seedling pot bioassay revealed that both species had a similar ability to colonize cereal roots; however, rye (Secale cereale) was only poorly colonized by the Magnaporthaceae species. To evaluate the ability of 40 elite UK winter wheat cultivars to support soil inoculum of beneficial soil-dwelling fungi, two field experiments were carried out using a naturally infested arable site in south-east England. The elite cultivars grown in the first wheat situation differed in their ability to support G. hyphopodioides inoculum, measured by colonization on Hereward as the subsequent wheat in a seedling soil core bioassay. In addition, the root colonization ability of G. hyphopodioides was influenced by the choice of the second wheat cultivar. Nine cultivars supported the colonization of the beneficial root fungus. Our findings provide evidence of complex host genotype-G. hyphopodioides interactions occurring under field conditions. This new knowledge could provide an additional soil-based crop genetic management strategy to help combat take-all root disease.

SUBMITTER: Osborne SJ

PROVIDER: S-EPMC5972604 | biostudies-literature | 2018 May

REPOSITORIES: biostudies-literature

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Elite UK winter wheat cultivars differ in their ability to support the colonization of beneficial root-infecting fungi.

Osborne Sarah-Jane SJ McMillan Vanessa E VE White Rodger R Hammond-Kosack Kim E KE

Journal of experimental botany 20180501 12

In numerous countries, Gaeumannomyces species, within the Magnaporthaceae family, have previously been implicated in the suppression of take-all root disease in wheat. A UK arable isolate collection (n=47) was gathered and shown to contain Gaeumannomyces hyphopodioides and an unnamed Magnaporthaceae species. A novel seedling pot bioassay revealed that both species had a similar ability to colonize cereal roots; however, rye (Secale cereale) was only poorly colonized by the Magnaporthaceae specie ...[more]

PMID: 29648609

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Project description:BACKGROUND:Proteins in the Glycoside Hydrolase family 32 (GH32) are carbohydrate-active enzymes known as invertases that hydrolyse the glycosidic bonds of complex saccharides. Fungi rely on these enzymes to gain access to and utilize plant-derived sucrose. In fungi, GH32 invertase genes are found in higher copy numbers in the genomes of pathogens when compared to closely related saprophytes, suggesting an association between invertases and ecological strategy. The aim of this study was to investigate the distribution and evolution of GH32 invertases in the Ceratocystidaceae using a comparative genomics approach. This fungal family provides an interesting model to study the evolution of these genes, because it includes economically important pathogenic species such as Ceratocystis fimbriata, C. manginecans and C. albifundus, as well as saprophytic species such as Huntiella moniliformis, H. omanensis and H. savannae. RESULTS:The publicly available Ceratocystidaceae genome sequences, as well as the H. savannae genome sequenced here, allowed for the identification of novel GH32-like sequences. The de novo assembly of the H. savannae draft genome consisted of 28.54 megabases that coded for 7 687 putative genes of which one represented a GH32 family member. The number of GH32 gene family members appeared to be related to the ecological adaptations of these fungi. The pathogenic Ceratocystis species all contained two GH32 family genes (a putative cell wall and a putative vacuolar invertase), while the saprophytic Huntiella species had only one of these genes (a putative cell wall invertase). Further analysis showed that the evolution of the GH32 gene family in the Ceratocystidaceae involved transposable element-based retro-transposition and translocation. As an example, the activity of a Fot5-like element likely facilitated the assembly of the genomic regions harbouring the GH32 family genes in Ceratocystis. CONCLUSIONS:This study provides insight into the evolutionary history of the GH32 gene family in Ceratocystidaceae. Our findings suggest that transposable elements shaped the evolution of the GH32 gene family, which in turn determines the sucrolytic activities and related ecological strategies of the Ceratocystidaceae species that harbour them. The study also provides insights into the role of carbohydrate-active enzymes in plant-fungal interactions and adds to our understanding of the evolution of these enzymes and their role in the life style of these fungi.

Project description:Harnessing plant-microbe interactions to advance crop resistance to pathogens could be a keystone in sustainable agriculture. The breeding of crops to maximize yield in intensive agriculture might have led to the loss of traits that are necessary for beneficial plant-soil feedback. In this study, we tested whether the soil microbiome can induce a stronger plant defense against root-lesion nematodes in ancestral genotypes of barley than in elite cultivars. Plants were grown in a sterile substrate with or without the inoculation of rhizosphere microbiomes, and Pratylenchus neglectus was inoculated to the roots. Unexpectedly, elite cultivars profited significantly more from the microbiome than ancestral genotypes, by the reduction of nematodes in roots and the increased shoot weight relative to control plants. The elite cultivars had higher microbial densities in the rhizosphere, which were correlated with root weight. The structure of the bacterial and fungal community of elite and ancestral genotypes differed, as compared by 16S rDNA or internal transcribed spacer amplicon profiles in denaturing gradient gel electrophoresis. The elite cultivars differed in responsiveness to the microbiome. For the most responsive cultivars Beysehir and Jolgeh, the strong microbe-induced suppression of nematodes coincided with the strongest microbe-dependent increase in transcripts of salicylic acid-regulated defense genes after nematode invasion, while the jasmonate-regulated genes LOX2 and AOS were downregulated in roots with the inoculated microbiome. The microbe-triggered modulation of defense gene expression differed significantly between elite and ancestral genotypes of barley. Soil microbiomes conditioned by maize roots suppressed the nematodes in elite cultivars, while the corresponding bulk soil microbiome did not. In conclusion, cultivars Beysehir and Jolgeh harbor the genetic background for a positive plant-microbiome feedback. Exploiting these traits in breeding for responsiveness to beneficial soil microbiomes, accompanied by soil biome management for compatible plant-microbe interactions, will support low-input agriculture and sustainability.

Dataset Information

Elite UK winter wheat cultivars differ in their ability to support the colonization of beneficial root-infecting fungi.

Publications

Elite UK winter wheat cultivars differ in their ability to support the colonization of beneficial root-infecting fungi.

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