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A QTL analysis of host plant effects on fungal endophyte biomass and alkaloid expression in perennial ryegrass.

ABSTRACT: The association between perennial ryegrass (Loliumperenne L.) and its Epichloë fungal endophyte symbiont, Epichloëfestucae var. lolii, supports the persistence of ryegrass-based pastures principally by producing bioactive alkaloid compounds that deter invertebrate herbivory. The host plant genotype affects endophyte trait expression, and elucidation of the underlying genetic mechanisms would enhance understanding of the symbiosis and support improvement of inplanta endophyte performance through plant breeding. Rapid metabolite profiling and enzyme-linked immunosorbent assay were used to quantify endophyte alkaloids and mycelial mass (MM) in leaves harvested, in consecutive autumns, from an F1 mapping population hosting standard toxic endophyte. Co-aligned quantitative trait loci (QTL) on linkage groups (LG)2, LG4 and LG7 for MM and concentrations of alkaloids peramine and ergovaline confirmed host plant effects on both MM and alkaloid level and inferred the effect on alkaloids was modulated through the quantity of endophyte present in the leaf tissue. For ergovaline, host regulation independent of endophyte concentration was also indicated, by the presence of MM-independent ergovaline QTL on LG4 and LG7. Partitioning of host genetic influence between MM-dependent and MM-independent mechanisms was also observed for the alkaloid N-formylloline (NFL), in a second mapping population harbouring a tall fescue-sourced endophyte. Single-marker analysis on repeated MM and NFL measures identified marker-trait associations at nine genome locations, four affecting both NFL and MM but five influencing NFL concentration alone. Co-occurrence of QTL on LG3, LG4 and LG7 in both mapping populations is evidence for host regulatory loci effective across genetic backgrounds and independent of endophyte variant. Variation at these loci may be exploited using marker-assisted breeding to improve endophyte trait expression in different host population × endophyte combinations.

SUBMITTER: Faville MJ

PROVIDER: S-EPMC4506467 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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A QTL analysis of host plant effects on fungal endophyte biomass and alkaloid expression in perennial ryegrass.

Faville Marty J MJ Briggs Lyn L Cao Mingshu M Koulman Albert A Jahufer M Z Zulfi MZ Koolaard John J Hume David E DE

Molecular breeding : new strategies in plant improvement 20150718 8

The association between perennial ryegrass (Loliumperenne L.) and its Epichloë fungal endophyte symbiont, Epichloëfestucae var. lolii, supports the persistence of ryegrass-based pastures principally by producing bioactive alkaloid compounds that deter invertebrate herbivory. The host plant genotype affects endophyte trait expression, and elucidation of the underlying genetic mechanisms would enhance understanding of the symbiosis and support improvement ...[more]

PMID: 26203296

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Project description:BackgroundCommercial cultivars of perennial ryegrass infected with selected Epichloë fungal endophytes are highly desirable in certain pastures as the resulting mutualistic association has the capacity to confer agronomic benefits (such as invertebrate pest deterrence) largely due to fungal produced secondary metabolites (e.g., alkaloids). In this study, we investigated T2 segregating populations derived from two independent transformation events expressing diacylglycerol acyltransferase (DGAT) and cysteine oleosin (CO) genes designed to increase foliar lipid and biomass accumulation. These populations were either infected with Epichloë festucae var. lolii strain AR1 or Epichloë sp. LpTG-3 strain AR37 to examine relationships between the introduced trait and the endophytic association. Here we report on experiments designed to investigate if expression of the DGAT + CO trait in foliar tissues of perennial ryegrass could negatively impact the grass-endophyte association and vice versa. Both endophyte and plant characters were measured under controlled environment and field conditions.ResultsExpected relative increases in total fatty acids of 17-58% accrued as a result of DGAT + CO expression with no significant difference between the endophyte-infected and non-infected progeny. Hyphal growth in association with DGAT + CO expression appeared normal when compared to control plants in a growth chamber. There was no significant difference in mycelial biomass for both strains AR1 and AR37, however, Epichloë-derived alkaloid concentrations were significantly lower on some occasions in the DGAT + CO plants compared to the corresponding null-segregant progenies, although these remained within the reported range for bioactivity.ConclusionsThese results suggest that the mutualistic association formed between perennial ryegrass and selected Epichloë strains does not influence expression of the host DGAT + CO technology, but that endophyte performance may be reduced under some circumstances. Further investigation will now be required to determine the preferred genetic backgrounds for introgression of the DGAT + CO trait in combination with selected endophyte strains, as grass host genetics is a major determinant to the success of the grass-endophyte association in this species.

Project description:Perennial ryegrass (Lolium perenne L.) is one of the most important species for temperate pastoral agriculture, forming associations with genetically diverse groups of mutualistic fungal endophytes. However, only two taxonomic groups (E. festucae var. lolii and LpTG-2) have so far been described. In addition to these two well-characterised taxa, a third distinct group of previously unclassified perennial ryegrass-associated endophytes was identified as belonging to a putative novel taxon (or taxa) (PNT) in a previous analysis based on simple sequence repeat (SSR) marker diversity. As well as genotypic differences, distinctive alkaloid production profiles were observed for members of the PNT group.A detailed phylogenetic analysis of perennial ryegrass-associated endophytes using components of whole genome sequence data was performed using complete sequences of 7 nuclear protein-encoding genes. Three independently selected genes (encoding a DEAD/DEAH box helicase [Sbp4], a glycosyl hydrolase [family 92 protein] and a MEAB protein), none of which have been previously used for taxonomic studies of endophytes, were selected together with the frequently used 'house-keeping' genes tefA and tubB (encoding translation elongation factor 1-? and ?-tubulin, respectively). In addition, an endophyte-specific gene (perA for peramine biosynthesis) and the fungal-specific MT genes for mating-type control were included. The results supported previous phylogenomic inferences for the known species, but revealed distinctive patterns of diversity for the previously unclassified endophyte strains, which were further proposed to belong to not one but two distinct novel taxa. Potential progenitor genomes for the asexual endophytes among contemporary teleomorphic (sexual Epichloë) species were also identified from the phylogenetic analysis.Unique taxonomic status for the PNT was confirmed through comparison of multiple nuclear gene sequences, and also supported by evidence from chemotypic diversity. Analysis of MT gene idiomorphs further supported a predicted independent origin of two distinct perennial ryegrass-associated novel taxa, designated LpTG-3 and LpTG-4, from different members of a similar founder population related to contemporary E. festucae. The analysis also provided higher resolution to the known progenitor contributions of previously characterised perennial ryegrass-associated endophyte taxa.

Project description:Plants harbor complex and highly diverse fungal endophyte communities (FECs), making it difficult to evaluate the functional role of individual taxa, subsets of the community, or the FEC as a whole. To reduce the complexity of this system, we aimed to produce fungi-null wheat (Triticum aestivum) plants. To this end, we treated seeds with heat and fungicides and generated plants from rescued embryos and callus tissue. A culture-based approach and reverse transcription PCR analysis were negative, indicating that all treatments produced plants apparently free of fungi. However, the analysis of DNA using digital droplet PCR and next-generation sequencing revealed that tissues from all treatments retained low levels but diversity-rich FECs. While the FECs varied in composition across treatments and tissues, they all included core taxa of the mycobiome. The reduced fungal biomass, along with the changes in FEC composition, negatively affected plant development, supporting a FEC contribution to proper plant development and fitness. Our discovery that a large part of the FEC cannot be separated from plants and can be transmitted through seeds and tissue culture calls for reevaluation of particular microbiome paradigms, such as core taxa concepts, transmission modes, and functional species.IMPORTANCEThe native microbiome in a given plant must be considered when evaluating the effect of a single taxon or synthetic community. The pre-existing microbiome can interact with artificially added microbial cargo, which affects the final outcome. Such issues can be at least partially solved by the use of endophyte-free plants, which provide a clean background that should be useful in determining the effect of a single taxon, taxa combinations, or the entire microbiome on plant performance. Previous reports regarded plants as endophyte-free or axenic by the lack of fungal growth on culture media or the generation of plants from tissue cultures. We showed here that while fungi could not be isolated from fungicide-treated or tissue culture-regenerated plants, nevertheless, all plants contained rich fungal endophyte communities; namely, it was impossible to create fungi-free wheat plants. Our results call for rethinking fundamental microbiome-related concepts, such as core taxa, transmission mode, and functional species.

Dataset Information

A QTL analysis of host plant effects on fungal endophyte biomass and alkaloid expression in perennial ryegrass.

Publications

A QTL analysis of host plant effects on fungal endophyte biomass and alkaloid expression in perennial ryegrass.

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