Seed Transmission of Epichloë Endophytes in Lolium perenne Is Heavily Influenced by Host Genetics

Abstract

Vertical transmission of symbiotic Epichloë endophytes from host grasses into progeny seed is the primary mechanism by which the next generation of plants is colonized. This process is often imperfect, resulting in endophyte-free seedlings which may have poor ecological fitness if the endophyte confers protective benefits to its host. In this study, we investigated the influence of host genetics and environment on the vertical transmission of Epichloë festucae var. lolii strain AR37 in the temperate forage grass Lolium perenne. The efficiency of AR37 transmission into the seed of over 500 plant genotypes from five genetically diverse breeding populations was determined. In Populations I–III, which had undergone previous selection for high seed infection by AR37, mean transmission was 88, 93, and 92%, respectively. However, in Populations IV and V, which had not undergone previous selection, mean transmission was 69 and 70%, respectively. The transmission values, together with single-nucleotide polymorphism data obtained using genotyping-by-sequencing for each host, was used to develop a genomic prediction model for AR37 seed transmission. The predictive ability of the model was estimated at r = 0.54. While host genotype contributed greatly to differences in AR37 seed transmission, undefined environmental variables also contributed significantly to seed transmission across different years and geographic locations. There was evidence for a small host genotype-by-environment effect; however this was less pronounced than genotype or environment alone. Analysis of endophyte infection levels in parent plants within Populations I and IV revealed a loss of endophyte infection over time in Population IV only. This population also had lower average tiller infection frequencies than Population I, suggesting that AR37 failed to colonize all the daughter tillers and therefore seeds. However, we also observed that infection of seed by AR37 may fail during or after initiation of floral development from plants where all tillers remained endophyte-infected over time. While the effects of environment and host genotype on fungal endophyte transmission have been evaluated previously, this is the first study that quantifies the relative impacts of host genetics and environment on endophyte vertical transmission.

A Simple LC–MS Method for the Quantitation of Alkaloids in Endophyte-Infected Perennial Ryegrass

“…In pastoral agriculture, perennial ryegrass is often infected with asexual Epichloë endophytes. In asymptomatic interactions, endophytes are transmitted vertically from host grass to seed [3,4], forming symbiotic relationships with their host. Systemic colonization then occurs throughout the aerial portions of the grass’ tissues [5].…”

The Impact of Alkaloid-Producing Epichloë Endophyte on Forage Ryegrass Breeding: A New Zealand Perspective

“…Does the breeder breed the host to fit the endophyte or breed the best ryegrass and find a compatible endophyte? The first scenario may limit the host grass germplasm to only those genotypes that fit an endophyte, e.g., work of Gagic [ 56 ]. The second strategy does not limit the host genotypes but may produce a grass that cannot sufficiently host a suitable endophyte.…”

“…Even crosses between two lines that do contain the desired endophyte may create a host with characteristics less conducive to stability and transmission, so testing is always required. Determining compatibility in such a system, using AR37, has been made easier by the development of a genomic estimated breeding value (GEBV) tool for host acceptance of an endophyte [ 56 ]. Whilst this is a great advance, care is still required as transmission and stability within a host is not all that needs to be considered.…”

“…As mentioned above, ryegrass breeding methods are improving, new phenotyping [ 64 ] and genotyping techniques [ 57 ] are starting to deliver cost effective genomic selection [ 58 , 60 , 100 ] and these are being applied to improve endophyte stability and transmission [ 56 ]. Addition of hybrid breeding [ 61 ], self-fertility [ 101 ], along with gene editing technologies [ 102 ] will likely reduce variation between genotypes within a host germplasm (cultivar or F1 hybrid).…”

A Tale of Two Grass Species: Temperature Affects the Symbiosis of a Mutualistic Epichloë Endophyte in Both Tall Fescue and Perennial Ryegrass

“…Failure in vertical endophyte transmission has been documented for many endophyte-grass associations, including novel and wild-type associations, with no single factor responsible (Gundel et al, 2008). As well as genetic factors (Ju, 2011;Gagic et al, 2018), some environmental factors can contribute to incompatibility issues between these endophytic fungi and their grass hosts that may culminate by inhibiting the endophyte's transmission pathway, with temperature suggested as one of the most important (Ju et al, 2006).…”