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Different response of perennial ryegrass-Epichloe endophyte symbiota to the elevated concentration of heavy metals in soil.

ABSTRACT: The phenomenon of plant mutualistic symbiosis with microbes may have a positive effect on the improvement of plant tolerance to environmental stresses as well as on the ability of plants to accumulate heavy metal (HM) ions from soil. The influence of Epichloë fungal endophyte (Ascomycota, Clavicipitaceae) on perennial ryegrass (Lolium perenne L.) plants grown in the presence of elevated concentrations of HM ions (Cd²⁺, Pb²⁺, and Cu²⁺) in soil was studied. The presence of Epichloë in the host grass tissues resulted in different accumulation of HM ions in the aboveground parts of the plants. In some cases, endophyte infection positively affected ryegrass ability to accumulate HM ions from soil. In plants with (E +) and without (E -) endophytes, the hormesis effect was induced by the elevated concentration of Cu²⁺ ions, resulting in better growth and photosynthesis, as examined by measurements of Chl a fluorescence. The obtained results indicate that based on the laboratory evaluation of the efficiency of HM accumulation, we were able to choose the best associations of perennial ryegrass with endophytes for HM phytoremediation.

SUBMITTER: Zurek G

PROVIDER: S-EPMC8755660 | biostudies-literature | 2022 Feb

REPOSITORIES: biostudies-literature

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Different response of perennial ryegrass-Epichloë endophyte symbiota to the elevated concentration of heavy metals in soil.

Żurek Grzegorz G Wiewióra Barbara B Rybka Krystyna K Prokopiuk Kamil K

Journal of applied genetics 20210921 1

The phenomenon of plant mutualistic symbiosis with microbes may have a positive effect on the improvement of plant tolerance to environmental stresses as well as on the ability of plants to accumulate heavy metal (HM) ions from soil. The influence of Epichloë fungal endophyte (Ascomycota, Clavicipitaceae) on perennial ryegrass (Lolium perenne L.) plants grown in the presence of elevated concentrations of HM ions (Cd2+, Pb2+, and Cu2+) in soil was studied. The pre ...[more]

PMID: 34546560

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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) is the most cultivated cool-season grass worldwide with crucial roles in carbon fixation, turfgrass applications, and fodder for livestock. Lolium perenne forms a mutualism with the strictly vertically transmitted fungal endophyte, Epichloë festucae var lolii. The fungus produces alkaloids that protect the grass from herbivory, as well as conferring protection from drought and nutrient stress. The rising concentration of atmospheric CO2, a proximate cause of climatic change, is known to have many direct and indirect effects on plant growth. There is keen interest in how the nature of this plant-fungal interaction will change with climate change. Lolium perenne is an obligately outcrossing species, meaning that the genetic profile of the host is constantly being reshuffled. Meanwhile, the fungus is asexual implying both a relatively constant genetic profile and the potential for incompatible grass-fungus pairings. In this study, we used a single cultivar, "Alto", of L. perenne. Each plant was infected with one of four strains of the endophyte: AR1, AR37, NEA2, and Lp19 (the "common strain"). We outcrossed the Alto mothers with pollen from a number of individuals from different ryegrass cultivars to create more genetic diversity in the hosts. We collected seed such that we had replicate maternal half-sib families. Seed from each family was randomly allocated into the two levels of the CO2 treatment, 400 and 800 ppm. Elevated CO2 resulted in an c. 18% increase in plant biomass. AR37 produced higher fungal concentrations than other strains; NEA2 produced the lowest fungal concentrations. We did not find evidence of genetic incompatibility between the host plants and the fungal strains. We conducted untargeted metabolomics and quantitative proteomics to investigate the grass-fungus interactions between and within family and treatment groups. We identified a number of changes in both the proteome and metabalome. Taken together, our data set provides new understanding into the intricacy of the interaction between endophyte and host from multiple molecular levels and suggests opportunity to promote plant robustness and survivability in rising CO2 environmental conditions through application of bioprotective epichloid strains.

Project description:BackgroundPerennial 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.ResultsA 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-α and β-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.ConclusionsUnique 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.

Dataset Information

Different response of perennial ryegrass-Epichloe endophyte symbiota to the elevated concentration of heavy metals in soil.

Publications

Different response of perennial ryegrass-Epichloë endophyte symbiota to the elevated concentration of heavy metals in soil.

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