How and when fungal endophytes can eliminate the plant growth–defence trade-off: mechanistic perspectives

A central paradigm in plant biology is that there is a trade-off between growth and defence against biotic stresses (Herms & Mattson, 1992; Lind et al., 2013; Karasov et al., 2017; Zust & € Agrawal, 2017; Monson et al., 2022). This paradigm is based on recurrent observations that increased production of chemical defences is associated with compromised plant growth, and it provides obvious limits to increasing the productivity of plants that must also resist pests and pathogens (Ballare & Austin, 2019; Ha et al., 2021; Sestari & Campos, 2021).We have recently challenged this paradigm by proposing that fungal endophytes can simultaneously increase plant growth and defence against biotic stresses (Fig. 1) (Bastıas et al., 2021).Fil: Bastías, Daniel A.. Grasslands Research Centre; Nueva ZelandaFil: Gundel, Pedro Emilio. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; Argentina. Universidad de Talca; ChileFil: Johnson, Richard D.. Grasslands Research Centre; Nueva ZelandaFil: Gianoli, Ernesto. Universidad de La Serena; Chil

Epichloë Fungal Endophytes Influence Seed-Associated Bacterial Communities

Seeds commonly harbour diverse bacterial communities that can enhance the fitness of future plants. The bacterial microbiota associated with mother plant’s foliar tissues is one of the main sources of bacteria for seeds. Therefore, any ecological factor influencing the mother plant’s microbiota may also affect the diversity of the seed’s bacterial community. Grasses form associations with beneficial vertically transmitted fungal endophytes of genus Epichloë. The interaction of plants with Epichloë endophytes and insect herbivores can influence the plant foliar microbiota. However, it is unknown whether these interactions (alone or in concert) can affect the assembly of bacterial communities in the produced seed. We subjected Lolium multiflorum plants with and without its common endophyte Epichloë occultans (E+, E-, respectively) to an herbivory treatment with Rhopalosiphum padi aphids and assessed the diversity and composition of the bacterial communities in the produced seed. The presence of Epichloë endophytes influenced the seed bacterial microbiota by increasing the diversity and affecting the composition of the communities. The relative abundances of the bacterial taxa were more similarly distributed in communities associated with E+ than E- seeds with the latter being dominated by just a few bacterial groups. Contrary to our expectations, seed bacterial communities were not affected by the aphid herbivory experienced by mother plants. We speculate that the enhanced seed/seedling performance documented for Epichloë-host associations may be explained, at least in part, by the Epichloë-mediated increment in the seed-bacterial diversity, and that this phenomenon may be applicable to other plant-endophyte associations.Fil: Bastías, Daniel A.. Grasslands Research Centre; Nueva ZelandaFil: Bubica Bustos, Ludmila Micaela. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; ArgentinaFil: Jáuregui, Ruy. Grasslands Research Centre; Nueva ZelandaFil: Barrera, Andrea. Universidad de Talca; ChileFil: Acuña Rodríguez, Ian S.. Universidad de Talca; ChileFil: Molina Montenegro, Marco A.. Universidad de Talca; Chile. Universidad Católica del Norte; Chile. Universidad Católica del Maule; ChileFil: Gundel, Pedro Emilio. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; Argentina. Universidad de Talca; Chil

Antagonism to Plant Pathogens by Epichloë Fungal Endophytes—A Review

Epichloë is a genus of filamentous fungal endophytes that has co-evolved with cool-season grasses with which they form long-term, symbiotic associations. The most agriculturally important associations for pasture persistence for grazing livestock are those between asexual vertically transmitted Epichloë strains and the pasture species, perennial ryegrass, and tall fescue. The fungus confers additional traits to their host grasses including invertebrate pest deterrence and drought tolerance. Selected strains of these mutualistic endophytes have been developed into highly efficacious biocontrol products and are widely utilized within the Americas, Australia, and New Zealand for pasture persistence. Less publicized is the antagonism Epichloë endophytes display towards multiple species of saprophytic and pathogenic microbes. This opinion piece will review the current literature on antimicrobial properties exhibited by this genus of endophyte and discuss the reasons why this trait has historically remained a research curiosity rather than a trait of commercial significance

Environmental interference of plant-microbe interactions

Environmental stresses can compromise the interactions of plants with beneficial microbes. In the present review, experimental results showing that stresses negatively affect the abundance and/or functionality of plant beneficial microbes are summarized. It is proposed that the environmental interference of these plant-microbe interactions is explained by the stress-mediated induction of plant signalling pathways associated with defence hormones and reactive oxygen species. These plant responses are recognized to regulate beneficial microbes within plants. The direct negative effect of stresses on microbes may also contribute to the environmental regulation of these plant mutualisms. It is also posited that, in stress situations, beneficial microbes harbour mechanisms that contribute to maintain the mutualistic associations. Beneficial microbes produce effector proteins and increase the antioxidant levels in plants that counteract the detrimental effects of plant stress responses on them. In addition, they deliver specific stress-protective mechanisms that assist to their plant hosts to mitigate the negative effects of stresses. Our study contributes to understanding how environmental stresses affect plant-microbe interactions and highlights why beneficial microbes can still deliver benefits to plants in stressful environments.Peer reviewe

Vertically Transmitted Epichloë Systemic Endophyte Enhances Drought Tolerance of Achnatherum inebrians Host Plants through Promoting Photosynthesis and Biomass Accumulation

Achnatherum inebrians (drunken horse grass, DHG) plants, a dominant grass species in the arid and semi-arid regions of northwest China, symbiotic with an Epichloë fungal endophyte, is well adapted to drought. However, little is known about how the presence of the foliar Epichloë endophyte enhances the tolerance of DHG to drought at the molecular level. This study explored the positive effects of the presence of the Epichloë endophyte on plant growth, biomass, and photosynthetic efficiency and processes of DHG under non-drought and two drought (moderate and severe) treatments, using RNA sequencing to compare transcriptomes. The transcriptome results showed that 32 selected unigenes involved in the photosynthesis processes within Epichloë symbiotic plants were differently expressed (DEGs) versus non-symbiotic plants. The majority of these selected DEGs were upregulated in Epichloë symbiotic plants versus non-symbiotic plants, such as upregulated unigenes (c51525.graph_c1, c47798.graph_c0 & c64087.graph_c0) under drought conditions. In line with the transcriptomes data, the presence of the Epichloë endophyte promoted the photosynthetic rate and biomass accumulation of DHG plants, and the relationship between the photosynthetic rate and biomass is linear and significant. The presence of the endophyte only increased the biomass per tiller of DHG plants under drought. This study provides further insights into the molecular mechanisms that underlie the enhanced plant growth and drought tolerance of Epichloë-symbiotic DHG plants

Environmental interference of plant−microbe interactions

Environmental stresses can compromise the interactions of plants with beneficial microbes. In the present review, experimental results showing that stresses negatively affect the abundance and/or functionality of plant beneficial microbes are summarized. It is proposed that the environmental interference of these plant−microbe interactions is explained by the stress-mediated induction of plant signalling pathways associated with defence hormones and reactive oxygen species. These plant responses are recognized to regulate beneficial microbes within plants. The direct negative effect of stresses on microbes may also contribute to the environmental regulation of these plant mutualisms. It is also posited that, in stress situations, beneficial microbes harbour mechanisms that contribute to maintain the mutualistic associations. Beneficial microbes produce effector proteins and increase the antioxidant levels in plants that counteract the detrimental effects of plant stress responses on them. In addition, they deliver specific stress-protective mechanisms that assist to their plant hosts to mitigate the negative effects of stresses. Our study contributes to understanding how environmental stresses affect plant−microbe interactions and highlights why beneficial microbes can still deliver benefits to plants in stressful environments.</p

Concentration of defense hormones and lolines of L. multiflorum plants and S. frugiperda performance measurements

MeJA: methyl jasmonate; SA: salicylic acid; JA: jasmonic acid; nanl: N-acetylnorlolines; nfl: N-formyllolines; DW: dry weight

Plant species, nitrogen status and endophytes are drivers of soil microbial communities in grasslands

Context: There is concern that the introduction of ‘novel’ plant germplasm/traits could outpace our capacity to measure and so assess their impacts on soil microbial communities and function.Aim: This study aimed to investigate the effects of plant species/functional traits, nitrogen (N) fertilisation and endophyte infection on grassland soil microbial communities within a short time span of 2 years.Methods: Two field experiments with monoculture plots were conducted in a common soil. Experiment 1 compared grasses and legumes, using two cultivars of perennial ryegrass (Lolium perenne) that varied in fructan content, along with the legumes white clover (Trifolium repens) and bird’s-foot trefoil (Lotus pedunculatus) that varied in tannin content. Grass treatments received high and low N application levels. Experiment 2 compared the presence/absence of Epichloë strains in ryegrass, tall fescue (Schedonorus phoenix) and meadow fescue (Schedonorus pratensis). Soil microbial communities were analysed by using high-throughput sequencing of DNA isolated from bulk soil cores.Key results: Higher abundance of ligninolytic fungi was found in grass soils and pectinolytic fungi in legume soils. Levels of N fertilisation and fructan in ryegrass had only minor effects on soil fungal communities. By contrast, N fertilisation or fixation had a strong effect on bacterial communities, with higher abundance of nitrifiers and denitrifiers in high-N grass soils and in legume soils than in low-N grass soils. Epichloë affected soil microbiota by reducing the abundance of certain fungal phytopathogens, increasing mycorrhizal fungi and reducing N-fixing bacteria.Conclusions: Chemical composition of plant cell walls, which differs between grasses and legumes, and presence of Epichloë in grasses were the main drivers of shifts in soil microbial communities.Implications: Impacts of farming practices such as mono- or poly-culture, N fertilisation and presence of Epichloë in grasses on soil microbial communities should be considered in pasture management.</p

Surface Immunogenic Protein of Streptococcus Group B is an Agonist of Toll-Like Receptors 2 and 4 and a Potential Immune Adjuvant

Vaccine-induced protection against pathogens, especially subunit-based vaccines, are related to antigen properties but mainly in their ability to stimulate the immune system by the use of an adjuvant. Modern vaccines are formulated with a high level of antigen purity, where an efficient adjuvant is necessary. In this context, the use of protein Toll-Like Receptor (TLR) agonists as vaccine adjuvants has been highlighted because of their optimal immunogenicity and minimal toxicity. The Surface Immunogenic Protein (SIP) from Group B Streptococcus (GBS) has gained importance as a new potential protein-based vaccine. Recently, we reported that recombinant SIP (rSIP) expressed by E. coli and purified by High Performance Liquid Chromatography (HPLC) alone induces a protective humoral immune response. In this study, we present the immunomodulatory properties of rSIP as a protein-based adjuvant, as an agonist of TLR. To this end, we showed that C57BL/6 bone marrow-derived dendritic cells pulsed by rSIP resulted in enhanced CD40, CD80, CD86, and Major Histocompatibility Complex (MHC) class II as well as increased secretion proinflammatory cytokines Interleukin (IL)-6, Interferon (IFN)-gamma, Tumor Necrosis Factor (TNF)-alpha, and IL-10. Next, we investigated the in vivo effect of rSIP in the absence or presence of ovalbumin (OVA) on antigen-specific antibody secretion in C57BL/6 mice. Immunization with rSIP plus OVA showed that anti-OVA IgG2a and IgG1a increased significantly compared with OVA alone in C57BL/6 mice. Also, the immunization of rSIP plus OVA generates increased serum cytokines levels characterized by IL-12p70, IL-10, IL-4, and IFN-gamma. Interestingly, we observed that rSIP stimulate Toll Like Receptor (TLR)2 and TLR4, individually expressed by Human embryonic kidney (HEK) 293-derived TLR reporter cells. These findings suggest that rSIP is a new potential protein TLR agonist adjuvant and may be employed in the development of new vaccines.FONDEF D10i1202 Millennium Institute on Immunology and Immunotherapy P09/016-F Instituto de Salud Publica de Chile (Institute of Public Health in Santiago, Chile

Effect of Bacteriophages on the Growth of Flavobacterium psychrophilum and Development of Phage-Resistant Strains

The controlling effect of single and multiple phages on the density of Flavobacterium psychrophilum at different initial multiplicity of infection (MOI) was assessed in batch cultures to explore the potential for phage-based treatment of this important fish pathogen. A high initial phage concentration (MOI = 0.3–4) was crucial for efficient viral lysis, resulting in a 104–105-fold reduction of phage-sensitive cells (both single phages and phage cocktails), which was maintained throughout the incubation (&gt;10 days). Following cell lysis, regrowth of phage-resistant strains was examined and resistant strains were isolated for further characterization. The application of a mathematical model allowed simulation of phage-host interactions and resistance development, confirming indications from strain isolations that phage-sensitive strains dominated the regrowing population (&gt;99.8 %) at low MOI and phage-resistant strains (&gt;87.8 %) dominated at high MOI. A cross-infectivity test covering 68 isolated strains and 22 phages resulted in 23 different host susceptibility patterns, with 20 of the isolates being resistant to all the applied phages. Eleven isolated strains with different susceptibility patterns had lower growth rates (0.093 to 0.31 h−1) than the host strain (0.33 h−1), while 10 of 14 examined strains had lost the ability to take up specific substrates as shown by BIOLOG profiles. Despite increased selection for phage resistance at high MOI, the results emphasize that high initial MOI is essential for fast and effective control of F. psychrophilum infection and suggest that the small populations of resistant clones had reduced competitive abilities relative to the sensitive ancestral strain