Phosphorus source and Epichloë coenophiala strain interact over time to modify tall fescue rhizosphere microbial community structure and function
Introduction
Tall fescue (Lolium arundinaceum (Schreb.) S.J. Darbyshire) is a common cool-season cultivated forage grass found throughout the world with an estimated 14 million hectares in the United States alone (Young et al., 2014). The persistence of tall fescue over other pasture species has been a topic of many research articles (see Omacini et al., 2012 and references therein). Much of this persistence is attributed to the presence of the shoot and host specific fungal endophyte Epichloë coenophiala (formerly Neotyphodium coenophiala) (Clay et al., 2005). Tall fescue plants infected with Epichloë coenophiala have a competitive advantage over endophyte-free grasses due to the production of alkaloids that improve abiotic and biotic stress tolerance (Malinowski and Belesky, 2019; Wang et al., 2020). This relationship makes them interesting to study for their potential role in improving tall fescue's resilience to changing climate scenarios or for manipulation of rhizosphere processes vital for ecosystem function (e.g. nutrient cycling, soil formation, C stabilization). However, a disadvantage for animal producers is that some of the alkaloids are also toxic to grazing livestock causing a suite of conditions collectively termed fescue toxicosis. Livestock consuming endophyte infected grasses in large quantities are less tolerant to heat, make poor weight gains, can have reproductive issues, and can develop a condition known as fescue foot (Stuedemann and Hoveland, 1988). Prompted by fescue toxicosis, researchers introduced endophytes isolated from native grasses with known, non-toxic alkaloid profiles into different tall fescue cultivars producing varieties that retained the non-toxic class of alkaloids (i.e. lolines and paramine) while producing little to none of the toxic alkaloids (i.e. ergot alkaloids) detrimental to grazing animals (Stuedemann and Hoveland, 1988; Hunt and Newman, 2005). The introduced endophytes have since been called ‘novel’ and include varieties such as AR542 found commercially in Jesup and Georgia 5 MaxQ seed (Bouton et al., 2002) and AR584 found in Texoma MaxQII (Hopkins et al., 2010) and several others (Malinowski and Belesky, 2019).
Several studies have shown that common-toxic endophyte infection in tall fescue has some influence on soil microbial processes which may contribute to the competitive advantage of infected over uninfected grasses (Matthews and Clay, 2001; Buyer et al., 2011; Iqbal et al., 2012). Less attention has been given to how novel endophyte-host associations affect rhizosphere processes particularly under nutrient-limiting conditions. Phosphorus (P) is by far the least mobile and available macronutrient for plants in most soils (Hinsinger, 2001) because it easily forms insoluble complexes with Fe and Al in acidic soils and Ca in calcareous or alkaline soils (Bertrand et al., 2003; Akhtar et al., 2009). The primary constraints on the availability of soil P, especially in acidic or moderately weathered soils, are the strong complexes it forms with Fe and Al oxides which keeps soil solution P low and severely limits the diffusion of P to the roots. The processes plants rely on to acquire P from soils are complex, and include 1) rhizosphere acidification and release of organic anions, 2) release of enzymes (notably phosphatase) to mineralize organic P forms, 3) changes in root system architecture or growth of roots into unexploited soils (i.e. root foraging), or 4) support of soil microorganisms directly (e.g. mycorrhizae) or indirectly via proliferation of P-solubilizing microbes feeding on root exudate carbon. All of these processes work together to influence P use efficiency. The mechanisms underlying how endophytes influence these processes, how this changes access to sparingly soluble soil P, and how it might vary with endophyte strain or differences in soil P speciation and availability are still not known.
Host and shoot specific fungal endophyte-related adaptations involved in enhancing nutrient uptake include increased root surface area and root hair number which have been well documented in many growth conditions including agar (Ding et al., 2015), hydroponics, and soils (Malinowski et al., 1998a,b; Malinowski and Belesky, 1999). Host and shoot specific fungal endophytes have also been shown to influence root exudate composition (Guo et al., 2015) which can alter rhizosphere chemistry and microbial community structure (Guo et al., 2016; Rojas et al., 2016) which are implicated in improving P acquisition from soils (Malinowski and Belesky, 1999). The concept of microbial enhancement of P availability for plants is not new. Many microbes involved in soil P mobilization have been identified (Richardson, 2011). In addition, the microbial biomass itself contains a large pool of immobilized P that is potentially available to plants (Richardson et al., 2011). Therefore, investigating the influence of novel fungal endophyte infected tall fescue on microbial community composition has great implications for studying P cycling under P starvation conditions.
In a similar study (Ding et al., 2016) we grew these same tall fescue-endophyte infected varieties in soils with a wider variety of P forms and found that after 90 days endophyte infection affected soil P fractions, but had little significant influence on rhizosphere soil microbial community structure, function, or plant P uptake. We hypothesized that the lack of response was possibly due to only sampling at one time point during plant development. Shi et al. (2015) showed that bacterial community structure in the rhizosphere of the annual grass Avena fatua L. changed with plant development (Shi et al., 2015). Further, it was recently shown that growth of the systemic grass endophyte Epichloë festucae var. Lolii (Leuchtmann, 2014) and alkaloid biosynthesis were enhanced in Lolium perenne L. as the plants aged (Fuchs et al., 2017). Taken together, these studies highlight the possibility that sampling throughout plant development might be necessary to capture the influence of endophyte strain on P acquisition. It was therefore the objective of this study to evaluate how fungal endophyte strain influences rhizosphere processes and P acquisition over time when grown in soils differing in P speciation. We hypothesize that 1) host and shoot-specific fungal endophytes within tall fescue will alter rhizosphere microbial community structure and function relative to endophyte free plants, 2) that this response will change with plant development and soil P forms, and 3) that these interactions (P form, endophyte strain, time) will influence P uptake. Because P is a limited resource and recovery of fertilizer-P inputs is generally low (McLaughlin and James, 1991) determining the endophyte-mediated mechanisms for increased P utilization could be of great economic and ecological benefit for modern sustainable agronomic production systems (Kauppinen et al., 2016).
Section snippets
Glasshouse propagation
A Sadler silt loam soil (Soil Survey Staff, NRCS) was collected from the top 0–20 cm of a fallow (60 yrs) field dominated by mixed grasses and weeds at the University of Kentucky Research and Education Center, Princeton, KY, USA. Soils were air-dried and sieved (<2 mm) and a subsample sent to the University of Kentucky regulatory services soil testing laboratory where they determined total organic carbon (TOC) and total nitrogen, (TN), pH, and Mehlich 3 extractable P, K, Ca, Mg, Cu, Mn, Fe, and
Plant growth and P uptake
Endophyte infection and the interaction of stand age and P form had a significant effect on tall fescue shoot biomass production (Table 2). Shoot biomass in CTE + infected tall fescue was significantly greater than those infected with AR542E+ and AR584E + endophytes and greater but not significantly different from E−tall fescue irrespective of P form (Fig. 1). Infection with AR542E + resulted in shoot biomass similar to AR584E+, but significantly less than E− and CTE+. Over all stand ages,
Discussion
The specific aim of this study was to assess how shoot-specific endophyte strain influences P acquisition with tall fescue growth and development from soils with different P sources. Infection with E. coenophiala is thought to enhance tall fescue's ability to access sparingly soluble P from soils and is considered one of the reasons for increases in productivity of endophyte infected compared to endophyte-free grasses growing in nutrient-poor soils (Malinoski and Belesky, 2000). Clear from this
Conclusions
This study examined how tall fescue shoot-specific fungal endophyte strain effects rhizosphere microbial community structure and function, P uptake and plant growth over time when grown in soils with different P speciation. We observed that novel endophytes tended to produce lesser shoot biomass relative to CTE+ and E−tall fescue. Supporting our hypotheses, we found that rhizosphere microbial community structure and function changed with plant development and was influenced by endophyte strain
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
This work was supported by a grant awarded to DHMJ from the United States Department of Agriculture National Institute of Food and Agriculture (2011-67019-30392), a cooperative agreement with the Kentucky Agricultural Experiment Station (KY006045), and the University of Kentucky Department of Plant and Soil Sciences.
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