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Tall Fescue Cultivar and Fungal Endophyte Combinations Influence

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Tall Fescue Cultivar and Fungal Endophyte Combinations Influence ORIGINAL RESEARCH published: 09 April 2015 doi: 10.3389/fpls.2015.00183 Tall fescue cultivar and fungal endophyte combinations influence plant growth and root exudate composition Jingqi Guo 1*, Rebecca L. McCulley 2 and David H. McNear Jr. 1* 1 Rhizosphere Science Laboratory, Department of Plant and Soil Sciences, University of Kentucky, Lexington, KY, USA, 2 Edited by: Grassland Ecology Laboratory, Department of Plant and Soil Sciences, University of Kentucky, Lexington, KY, USA Simone Ferrari, Sapienza Università di Roma, Italy Tall fescue [Lolium arundinaceum (Schreb.)] is a cool-season perennial grass used Reviewed by: in pastures throughout the Southeastern United States. The grass can harbor a Chuansheng Mei, Institute for Advanced Learning and shoot-specific fungal endophyte (Epichloë coenophiala) thought to provide the plant Research, USA with enhanced resistance to biotic and abiotic stresses. Because alkaloids produced Kerrie Farrar, Aberystwyth University, UK by the common variety of the endophyte cause severe animal health issues, focus has *Correspondence: been on replacing the common-toxic strain with novel varieties that do not produce the Jingqi Guo, mammal-toxic alkaloids but maintain abiotic and biotic stress tolerance benefits. Little Texas A&M AgriLife Research & attention has been given to the influence of the plant-fungal symbiosis on rhizosphere Extension Center at Beaumont, 1509 Aggie Drive, Beaumont, processes. Therefore, our objective was to study the influence of this relationship on TX 77713, USA plant biomass production and root exudate composition in tall fescue cultivars PDF [email protected]; David H. McNear Jr., and 97TF1, which were either not infected with the endophyte (E-), infected with the Rhizosphere Science Laboratory, common toxic endophyte (CTE+) strain or with one of two novel endophytes (AR542E+, Department of Plant and Soil AR584E+). Plants were grown sterile for 3 weeks after which plant biomass, total organic Sciences, University of Kentucky, N122S Agricultural Sciences North carbon, total phenolic content and detailed chemical composition of root exudates were Building, 1100 Nicholasville Road, determined. Plant biomass production and exudate phenolic and organic carbon content Lexington, KY 40502, USA [email protected] were influenced by endophyte status, tall fescue cultivar, and their interaction. GC-TOF MS identified 132 compounds, including lipids, carbohydrates and carboxylic acids. Specialty section: Cluster analysis showed that the interaction between endophyte and cultivar resulted This article was submitted to Plant-Microbe Interaction, a section of in unique exudate profiles. This is the first detailed study to assess how endophyte the journal Frontiers in Plant Science infection, notably with novel endophytes, and tall fescue cultivar interact to influence root Received: 24 December 2014 exudate composition. Our results illustrate that tall fescue cultivar and endophyte status Paper pending published: can influence plant growth and root exudate composition, which may help explain the 26 January 2015 Accepted: 06 March 2015 observed influence of this symbiosis on rhizosphere biogeochemical processes. Published: 09 April 2015 Keywords: Epichloë coenophiala, fungal endophyte, root exudates, plant growth, tall fescue Citation: Guo J, McCulley RL and McNear DH Jr. (2015) Tall fescue cultivar and fungal endophyte combinations Introduction influence plant growth and root exudate composition. Tall fescue [Lolium arundinaceum (Schreb.) Darbysh. = Schedonorus arundinaceus (Schreb.) Front. Plant Sci. 6:183. Dumort., formerly Festuca arundinacea Schreb. var. arundinacea Schreb.] is a perennial, cool doi: 10.3389/fpls.2015.00183 season bunchgrass native to Eurasia and North Africa (Gibson and Newman, 2001), but now Frontiers in Plant Science | www.frontiersin.org 1 April 2015 | Volume 6 | Article 183 Guo et al. Fungal endophytes affect exudate composition also occurs in North America, Australia, and New Zealand the interaction of novel fungal genotypes and tall fescue cultivars (Young et al., 2013). The majority of commercial tall fescue cul- influence rhizosphere biogeochemical processes such as nutrient tivars are allohexaploid (2n = 6x = 42) (Humphreys et al., 1995). cycling, microbial community structure and function, and root Significant heterozygosity and high self-incompatibility result exudate production. in tall fescue cultivars being populations of genetically unique While it is clear that the alkaloids produced by E. coenophiala individuals (Xu et al., 1994). “Kentucky-31” is one of the most have biological activity, it is unlikely that they are solely responsi- common tall fescue varieties in the North America, and can ble for the wide range of below-ground biogeochemical effects host a shoot specific fungal endophyte (Epichloë coenophiala for- associated with endophyte infection, such as the observed merly Neotyphodium coenophialum). E. coenophiala is an asex- increases in soil C and N storage in highly endophyte infected ual species (heteroploid) transmitted vertically by infecting plant tall fescue pastures of the southeastern U.S. (Franzluebbers et al., seeds (Clay and Schardl, 2002). The hyphae of E. coenophiala 1999a; Franzluebbers, 2006; Iqbal et al., 2012). The alkaloids are grow into developing ovules and seeds on symbiotic tall fescue found only within the plant and have not been identified in exu- plants and then after seed germination colonize the plant leaf dates released from plant roots into the rhizosphere. There is only sheaths and stems via intercalary growth, but are sparse or not one study (Franzluebbers and Hill, 2005) where alkaloids were present in the roots (Clay, 1988; Tan and Zou, 2001; Timper et al., found in surface soils in pastures dominated by CTE+ tall fescue, 2005; Christensen et al., 2008; Schardl, 2010). E. coenophiala is an but this may have been due to alkaloids leaching from decompos- obligate symbiotic fungus, surviving by absorbing water, amino ing leaf litter (Assuero et al., 2006), in which they can persist in acids and sugars produced by the plant (Malinowski and Belesky, measurable concentrations for up to 50 days (Siegrist et al., 2010). 2000; Sabzalian and Mirlohi, 2010). In return, fungal-produced There are a few studies that have found differences in root exu- primary or secondary metabolites serve to protect the plant date composition resulting from infection of tall fescue with the from herbivores and enhance tolerance to climactic and edaphic CTE+ strain. Van Hecke et al. (2005) found more carbohydrates stresses, ultimately improving overall plant fitness (Bouton et al., and organic carbon in root exudates of CTE+ than endophyte- 1993; Malinowski and Belesky, 2000). free (E-) tall fescue (Van Hecke et al., 2005). Malinowski et al. Secondary metabolites, such as alkaloids and phenolic com- (1998); Malinowski and Belesky (1999a) also found that exudates pounds, are ecologically important components produced by the from CTE+ tall fescue contained higher amounts of phenolic endophyte and the host tall fescue plant, respectively. Epichloë compounds compared to E- tall fescue which they attributed species produce four main classes of alkaloids including ergot to increased P acquisition by CTE+ plants (Malinowski et al., alkaloids, indole diterpenes, 1-aminopyrrolizidines and peramine 1998; Malinowski and Belesky, 1999a). The effect of tall fescue (Bush et al., 1993, 1997; Schardl, 2009). N-formaylloline, ergova- genotype was also shown to be a significant factor influencing line and peramine are produced in most E. coenophiala infected root exudate composition based on the indirect observation that tall fescue (Schardl, 2009). The alkaloids (specifically the ergot exudates from Grassland Flecha (a Mediterranean tall fescue) alkaloids) are responsible for an estimated $600 million in annual had greater Cu2+—binding activity compared to a continental beef cattle losses due to animal weight loss and reduced calf type tall fescue—Jesup—regardless of endophyte status which births (Morgan et al., 2005)—an ailment commonly referred the authors attributed to cultivar differences in total phenolic to as “fescue toxicosis.” Fescue toxicosis has also been linked compound exudation (Malinowski et al., 2004). to animal health issues in horses (Putnam et al., 1991; Chris- Changes in root exudate amount and composition result- tiansen et al., 2007), sheep (Burke et al., 2002), goats (Smith ing from endophyte infection may contribute directly to endo- et al., 2004), and Canadian geese (Conover and Messmer, phyte associated differences in C and N quantities in pasture 1996). soils by altering inputs to these pools, or indirectly by alter- Because of the impact on animal production, efforts have been ing the structure and function of the soil microbial commu- made to replace common toxic strains of the endophyte (CTE+ – nity which controls the processing and turnover of these soil toxic to mammals and insects) with so-called “novel” non- pools. Root exudates are comprised of carbon compounds such mammal-toxic strains. For example, Novel endophyte AR542 as organic, fatty, and amino acids, sugars, phenolics, and pro- and AR584 have been inserted into tall fescue cultivar “Jesup” teins (Jones et al., 2004; Schmidtke, 2005; Broeckling et al., and “Texoma” and commercialized as “Jesup” MaxQ and “Tex- 2008). Many of these compounds have been positively correlated oma” MaxQ II, respectively Bouton et al., 2002; Hopkins et al., with microbial activity (Vale et
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