Epichloë seed transmission efficiency is influenced by plant defense response mechanisms

Abstract

Asexual Epichloë are endophytic fungi that form mutualistic symbioses with cool-season grasses, conferring to their hosts protection against biotic and abiotic stresses. Symbioses are maintained between grass generations as hyphae are vertically transmitted from parent to progeny plants through seed. However, endophyte transmission to the seed is an imperfect process where not all seeds become infected. The mechanisms underpinning the varying efficiencies of seed transmission are poorly understood. Host gene expression in response to Epichloë sp. LpTG-3 strain AR37 was examined within inflorescence primordia and ovaries of high and low endophyte transmission genotypes within a single population of perennial ryegrass. A genome-wide association study was conducted to identify population-level single nucleotide polymorphisms (SNPs) and associated genes correlated with vertical transmission efficiency. For low transmitters of AR37, upregulation of perennial ryegrass receptor-like kinases and resistance genes, typically associated with phytopathogen detection, comprised the largest group of differentially expressed genes (DEGs) in both inflorescence primordia and ovaries. DEGs involved in signaling and plant defense responses, such as cell wall modification, secondary metabolism, and reactive oxygen activities were also abundant. Transmission-associated SNPs were associated with genes for which gene ontology analysis identified “response to fungus” as the most significantly enriched term. Moreover, endophyte biomass as measured by quantitative PCR of Epichloë non-ribosomal peptide synthetase genes, was significantly lower in reproductive tissues of low-transmission hosts compared to high-transmission hosts. Endophyte seed-transmission efficiency appears to be influenced primarily by plant defense responses which reduce endophyte colonization of host reproductive tissues.

The fungus Clonostachys epichloë alters the influence of the Epichloë endophyte on seed germination and the biomass of Puccinellia distans grass

“…Thus, the final effect of the presence of C. epichloë in the P. distans population will depend on the percentage of seeds infected with Epichloë, which is influenced not only by the number of infected grass individuals but also by the effectiveness of vertical transmission. Endophyte seed-transmission efficiency is influenced by host genetics ( Gagic et al, 2018 ) and by plant defense responses, which reduce endophyte colonization of host reproductive tissues ( Zhang et al, 2022 ). According to Afkhami and Rudgers (2008) , Epichloë endophytes can be lost at all possible stages: within adult plants, from adult tillers to seeds, and from seeds to seedlings, and the type and degree of loss differed not only among species and endophyte genera but among host populations as well, which makes estimating the number of infected seeds very difficult.…”

Epichloë fungal endophyte interactions in perennial ryegrass (Lolium perenne L.) modified to accumulate foliar lipids for increased energy density

“…Following seed germination, the fungus spreads systemically throughout the aerial portions of the plant forming a permanent mutualistic association [ 23 ]. However, vertical transmission frequency in some strains is heavily influenced by the grass host genetics, which generates an often-imperfect process resulting in endophyte-free progeny possessing a reduced agronomic fitness in the presence of certain insect pests [ 24 , 25 ].…”