As hypothesized, we found that the fungal endophyte affects the decomposition of litter of their host grasses F. sinensis, S. purpurea and A. inebrians. Different species varied in their response to fungal endophyte infection in the rate of decomposition of litter and related factors, such as litter quality and the surrounding microbial mass.
Grasses infected with fungal endophytes can release allelochemicals and alter the area of soil in which they grow (Malinowski et al. 1999; Petroski et al. 1990). Most studies about the effect of endophytes on litter decomposition of their host showed that the endophyte played a negative role during the process of decomposition of litter. For example, Omacini et al. (2004) found that the rates of decomposition in E + litters were 18% lower on average than that in the E- litters in both a garden microcosm experiment and a greenhouse experiment. Lemons et al. (2005) also found that the rates of decomposition were 6% slower in E + litter than in E- litter in an agricultural field experiment. In this study, the speed of decomposition in E + A. inebrians litter was slower than that in the E- litter (Fig. 1c), which is similar to previous results. Other studies demonstrated that the enhanced accumulation of soil carbon in Festuca pastures that were highly infected with endophytes compared with those that had low levels of infection could be attributed to the reduction in decomposition rates of E + litters (Franzluebbers et al. 1999; Osono 2006; Schomberg et al. 2000).
However, in contrast with A. inebrians, the rate of decomposition of litter in F. sinensis and S. purpurea with endophytes was quicker and the period of decomposition was shorter compared with the litters that lacked endophytes (Fig. 1a, b, Table 1). These results are consistent with a previous study that found that the E. uncinatum fungal endophyte increased the rate of decomposition of Schedonorus pratensis litter when incubated in a garden (Gundel et al. 2016). Grass endophytes can utilize simple sugars, such as glucose, sucrose, and xylose, as a sole carbon source in tissues that had recently died (White et al. 1991). Thus, endophytes have an advantage in their ability to utilize these readily available components before the fungi that colonize after tissue death. Such an ecological advantage suggests that grass infected by endophytes will decompose at a quicker rate (Gundel et al. 2016; Osono 2006).
Within individual ecosystems or biome types, litter quality becomes a more effective determinant of the rate of decomposition than the climate (Aerts 1997; Meentemeyer 1978). At the ecosystem scale, litter quality is most often related to the chemical characteristics of the litter, for example, carbon : nitrogen ratios and/or lignin content (Aber et al. 1990; Aerts 1997). In this study, the content of nitrogen in the A. inebrians, F. sinensis and S. purpurea litters increased with the progression of time (Fig. 2a). The content of nitrogen or phosphorus in litter would gradually increase during the decomposition of litter because of the lower speed of release of nutrient elements compared with the rate of loss of litter mass (Gallardo and Merino 1993). This could also be reflected in the change in residual rate of nitrogen, which decreased with the progression of time of decomposition (Fig. 3a). However, the residual rates of total nitrogen in the litters of three species had no significant difference between the E + and E- plants during most of the time of decomposition. Omacini et al. (2004) and Lemons et al. (2005) found there was no significant difference in the total content of N between E + and E- Lolium litters. In this study, the total nitrogen content appeared to have a different status in varied host species with the progression of time. Thus, the content of nitrogen in litter might not play a decisive role in the relative progress of the process of decomposition (Gundel et al. 2016).
In addition to changes in the mineral content, endophytes have been associated with changes in plant structural parameters, such as the content of fibers and lignin, that could also be linked with the decomposition of litter (Gundel et al. 2017; Rogers et al. 2011; Soto-Barajas et al. 2016). In this study, there was no visible effect from fungal endophytes on the original contents of lignin and cellulose of host grass. However, the degradation of lignin and cellulose varied between E + and E- symbiont for different species. First, S. purpurea had a higher content of lignin in the E + litter compared with that of E- during the process of decomposition, but the residual rates of lignin did not differ significantly (Figs. 2e, 3e). This may be owing to the higher speed of rate of decomposition of the E + litter. The content and residual rate of lignin in the E + litter from A. inebrians were higher than those of the E- litter to some degree during the process of decomposition (Figs. 2f, 3f). Thus, the slower rate of decomposition of the E + A. inebrians litter compared with that of E- may be partly attributed to the slower decomposition of lignin. Secondly, the content and residual rate of cellulose in the E + S. purpurea litter were lower than those in the E- litter to some degree during the year of decomposition (Figs. 2h, 3h). Thus, the lower concentration of cellulose in the lower mass weight of E + litter could result from the faster degradation of cellulose compared with that of the E- S. purpurea litter. The lower residual rate of cellulose in E + F. sinensis compared with that of E- could also induce the quicker decomposition of E + litter (Fig. 3g). However, the lower concentration of cellulose in E + A. inebrians litter was mostly caused by the slower decomposition of the E + litter based on the lack of a significant difference in the residual rate of cellulose between the E + and E- litters (Fig. 2i). These results suggest that the effect of fungal endophytes on the decomposition of litter could be partly attributed to the influence of lignin degradation for A. inebrians and the influence of cellulose degradation for F. sinensis and S. purpurea.
Soil microbial biomass is the main driving force in the decomposition of organic materials and is frequently used as an early indicator of changes in the chemical and physical properties of soil (Baaru et al. 2007; Brookes 1995). The quicker rate of decomposition of organic materials related to the higher values of soil microbial biomass carbon that resulted from the ready supply of nutrients that provide for microbial growth (Baaru et al. 2007). Grasses infected with fungal endophytes can release allelochemicals and alter the area of soil in which they grow (Malinowski et al. 1999; Petroski et al. 1990). In this study, the lower rate of decomposition of A. inebrians litter was associated with a lower amount of soil microbial biomass carbon. This result is consistent with those of previous studies (Baaru et al. 2007; Franzluebbers et al. 1999; Lemons et al. 2005). Thus, the exit of fungal endophytes in litter could decrease the soil microbial biomass by decreasing the speed of decomposition of litter by A. inebrians. This could be related to the secondary metabolites synthesized by the endophyte in A. inebrians, which altered the composition of the soil microbial community (Malinowski et al. 1998; Ponce et al. 2009; Siegel et al. 1990). However, other studies have found that the endophyte in Italian ryegrass (Neotyphodium occultans) increased the activity of soil fungal community (Casas et al. 2011). The value of microbial biomass nitrogen in soil can represent the dynamic balance during the process of the mineralization and immobilization of nutrients through the reproduction and death of microorganisms (Li et al. 2004b). Thus, the higher microbial biomass nitrogen of the soil under E + F. sinensis and S. purpurea could be attributed to the promotion of endophytes on microbial activity. This could be one indirect explanation for the quicker decomposition of E + F. sinensis and S. purpurea litters compared with that of the E- litters. Therefore, different endophyte species may induce various changes in the soil microbial community, from amount to vitality, during the decomposition of litter.
Fungal endophytes can alter the contents of amino acids, water soluble carbohydrates, lipids, organic acids or chlorogenic acid in the host plant, which result in different chemical constitutions between the E + and E- plants (Rasmussen et al. 2007; Rasmussen et al. 2008). These differences may directly influence the decomposition of litter by the host plant or indirectly change soil physicochemical properties and microbial community (Gundel et al. 2017; Omacini et al. 2004). Our results suggest that the endophyte of A. inebrians could decrease the degradation of lignin in A. inebrians litter, reducing the microbial mass in soil, to slow the decomposition of host grass litter. We found that the endophyte of S. purpurea accelerated the degradation of cellulose in S. purpurea litter, enhanced the microbial activity of soil, and finally promoted the rate of decomposition of this litter. The fact that the promotion of rate of decomposition by the F. sinensis endophyte may be owing to the higher microbial biomass of nitrogen in the soil under E + litter, whose litter quality did not differ significantly between E + and E- during the process of decomposition. Accordingly, the endophytes in A. inebrians, F. sinensis and S. purpurea played different roles in the decomposition of litter from their host, resulting in varied litter quality and environment for decomposition. Our results on decomposition further demonstrate a role for endophyte–plant mutualisms in ecosystem processes under field conditions. To fully understand the mechanism by which one endophyte affects the decomposition of litter, a more solid conclusion must await further examination on the effects of endophytes on litter quality or microbial community composition and the effect of environmental conditions in the future.