Next Article in Journal
Dietary Organic Acids Modulate Gut Microbiota and Improve Growth Performance of Nursery Pigs
Previous Article in Journal
Helicobacter Infection and Gastric Adenoma
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Microorganisms
Volume 9
Issue 1
10.3390/microorganisms9010109
microorganisms-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

The Inhibitory Effect of Endophyte-Infected Tall Fescue on White Clover Can Be Alleviated by Glomus mosseae Instead of Rhizobia

by
Jinming Liu
,
Xiaoyu Ge
,
Xiaowen Fan
,
Hui Liu
,
Yubao Gao
and
Anzhi Ren
*
College of Life Sciences, Nankai University, Tianjin 300071, China
*
Author to whom correspondence should be addressed.
Microorganisms 2021, 9(1), 109; https://doi.org/10.3390/microorganisms9010109
Submission received: 8 December 2020 / Revised: 30 December 2020 / Accepted: 31 December 2020 / Published: 5 January 2021
(This article belongs to the Section Plant Microbe Interactions)
Browse Figures
Review Reports Versions Notes

Abstract

:
In artificial ecosystems, mixed planting of gramineous and leguminous plants can have obvious advantages and is very common. Due to their improved growth performances and stress tolerance, endophyte-infected grasses are considered to be ideal plant species for grasslands. However, endophytic fungi can inhibit the growth of neighboring nonhost leguminous plants. In this study, we chose endophyte-infected and endophyte-free tall fescue (Lolium arundinaceum Darbyshire ex. Schreb.) and clover (Trifolium repens) as the experimental materials to explore whether arbuscular mycorrhizal fungi and rhizobium can alleviate the inhibitory effect of endophyte infection on clover. The results showed that endophytic fungi significantly reduced clover biomass. Arbuscular mycorrhizal fungi inoculation significantly increased the biomass of clover in both endophyte-infected tall fescue/clover and endophyte-free tall fescue/clover systems but the beneficial contribution of arbuscular mycorrhizal fungi was more obvious in the endophyte-infected tall fescue/clover system. Rhizobia inoculation could alleviate the detrimental effect of tall fescue on the growth of clover but did not alleviate the detrimental effect of endophyte infection on the growth of clover.

1. Introduction

Plant to plant interactions have important effects on the productivity and composition of plant communities and even ecosystems [1,2,3,4]. In artificial cultivation, the mixed planting method of leguminous and gramineous plants is usually adopted to build grassland. Compared with monoculture grassland, the mixed planting of grassland not only has advantages in improving forage yield and quality [5,6,7] but also plays an obvious role in improving soil fertility and realizing systematic sustainable production [8]. In a grazing experiment in Canada, Chen et al. [9] found that total amounts of N2 fixed in Medicago sativa and Poa pratensis mixed pastures were sufficient to replace N fertilizer and sustain plant protein for grazing compared with grass-only pastures. Li et al. [10] reported that in intensive farming systems, leguminous and gramineous mixed cropping played an important role in alleviating the inhibitory effect of N fertilization on nodulation and N2 fixation and the productivity of intercropping could also be improved. In addition to the fact that leguminous plants and rhizobium can form root nodules [11,12], terrestrial plants can also develop other nutrient absorption strategies with microorganisms; for example, higher plants associate with mycorrhizal fungi [13,14,15,16,17] and grass and endophytic fungi form symbionts [18,19,20].
Endophytic fungi are a kind of fungi that usually inhabit the aboveground tissues of healthy plants and do not cause obvious diseases [21]. Mutual relationships have been found between endophytes and some important cultivated grasses such as tall fescue and perennial ryegrass [22,23,24]. The host plants can provide endophytic fungi with photosynthetic products, nutrients and habitats; moreover, secondary metabolites produced by endophytic fungi can promote the growth and development of host plants [25] and improve the host’s resistance to biotic [26,27,28,29,30] and abiotic stresses [31,32,33] such as drought [34,35,36], nutrient deficiency [37], herbivory [38,39,40,41] and pathogens [25,42,43], Given the higher growth advantages of endophyte-infected (E+) over endophyte-free (E−) plants, E+ grasses are considered to be ideal plant species for artificial grasslands. However, endophyte infection could change the interspecific relationship between host grasses and neighboring plants [44]. Endophytes may affect the competitiveness of the host grass by changing their shoot and root growth [45,46,47,48], physiological response to abiotic stresses [49,50] or production of allelopathic substances [44,51,52,53]. For example, Hoveland et al. [54] and Malinowski et al. [55] found that when tall fescue was mixed with clover or alfalfa, endophytic fungi significantly inhibited the growth of leguminous plants, thus improving the competitiveness of host plants. Over a four year period, Clay and Holah [56] found that species richness declined and tall fescue dominance increased in infected plots relative to uninfected plots. Thus, as tall fescue has been widely planted for forage and turf, the potential effect of the endophyte on interspecific relationships and communities is large. Therefore, it is urgent to consider how to make full use of the benefits of endophytic fungi while reducing its adverse effects on other key species such as leguminous plants in the establishment of lawn. However, only a few relevant reports are available.
In grassland ecosystems, arbuscular mycorrhizal fungi (AMF) and rhizobia are also common. Their beneficial effects on host plants have been widely demonstrated [57,58,59,60,61,62,63]. AMF are obligate symbionts, which are fully reliant on the host plants to obtain carbon sources. They provide nutrients such as phosphorus to their hosts in turn and they can become parasitic under certain conditions such as high P availability. AMF members of the genus Glomus can form symbiotic associations with the roots of many grass species and legumes. Endophyte-infected grasses can also be infected with AMF simultaneously [64,65,66,67]. Studies show that endophyte infection can reduce the AMF colonization rates in tall fescue and perennial ryegrass [68,69,70]. Mack and Rudgers [65] further found that there was a negative correlation between the endophytic hyphae density in the leaf sheath of tall fescue and the colonization rate of AMF (Glomus intraradices). Liu et al. [69] found that the inoculation of mycorrhizal Glomus fungi reduced the concentration of endophytic fungi in ryegrass leaves and meristem. These studies indicate that the beneficial effects of endophytic fungi on the host grass can be offset by AMF. Clover is an important green manure and turfgrass that can form a natural symbiosis with rhizobia and establish a symbiotic system with AMF such as Glomus mosseae and Glomus claroideum, which confer complementary resources such as P and N to their host plants [71]. Considering that endophyte-infected grasses cannot form symbionts with rhizobia and the beneficial effects of endophyte infection are negatively affected by AMF, we hypothesize that AMF or rhizobia inoculation can offset the inhibitory effect of endophyte-infected tall fescue on leguminous plants such as clover.
In the present study, endophyte-infected tall fescue and clover were chosen as experimental materials. We aimed to answer the following questions: (1) Can the inhibition of endophyte infection on clover be alleviated by inoculating AMF and/or rhizobia? (2) What is the relationship between endophytic fungi, AMF and rhizobia?

2. Materials and Methods

2.1. Planting Site and Soil Sampling

Soil was collected from local grassland with nitrogen and phosphorus concentrations of 0.17% and 0.028%, respectively. The soil was homogenized and sieved (passed through a 0.5 cm mesh) and autoclaved at 1 atm pressure, 121 °C, for 20 min, three times with 24 h interval before use, to eliminate the interference of other microorganisms in the soil. Each pot (24 cm diameter, 18 cm depth) contained 5 kg of sterilized soil. Eight seedlings were planted in each pot. For the mixed planting mode, the planting density ratio of clover to tall fescue was set as 4:4. The experiment was conducted in a greenhouse with a 10:14 h light/dark photoperiod at Nankai University. The starting time was January 2019 and lasted for four months with water provided as needed during the experiment. All pots were randomized weekly to reduce position effects.

2.2. Experimental Design

The mixed planting experiment was designed as a three-factor random setup. Factor one was the endophytic fungal state of tall fescue set at two levels: infected (E+) and uninfected (E−). Factor two was the inoculation of AMF, also set at two levels: inoculation of AMF (AMF+) and non-inoculation of AMF (AMF−). Factor three was the inoculation status of rhizobia; the two inoculation levels were the inoculation of rhizobia (R+) and non-inoculation of rhizobia (R−). Five plant combinations and four inoculation regimes were included. The plant combinations were: (1) eight E+ tall fescue per pot, (2) eight E− tall fescue per pot, (3) eight clover per pot, (4) four E+ tall fescue and four clover per pot and (5) four E− tall fescue and four clover per pot. Each treatment was repeated four times for a total of 80 pots.

2.3. Plant Materials

In this experiment, tall fescue (Lolium arundinaceum Darbyshire ex. Schreb.) and clover (Trifolium repens) were selected as the experimental materials. The tall fescue (Kentucky-31) can form a symbiotic relationship with only one endophytic fungus Epichloë coenophiala [72] The E+ and E− tall fescue seeds used in this experiment were originally provided by Professor Keith Clay at Indiana University and were multiplied in the growth chamber of Nankai University. The clover seeds were purchased from Jiangsu Earth Seedling base, China. Seeds were surface-sterilized in 5% sodium hypochlorite solution for 8 min before use. The tall fescue seeds used in this experiment and the seedlings that were subsequently grown were confirmed by the aniline blue staining method that endophytic fungi were present in the E+ plants but not in the E− plants. The seeds of the E+ and E− tall fescue were soaked in 5% (w/v) NaOH overnight before boiling in aniline blue for 5–8 min. For the seedlings, the leaf sheath epidermis was ripped and stained for 3–5 min. Both were then observed under a microscope to examine the endophytic fungi. Every pot of plants in this experiment was planted from seeds.

2.4. Mycorrhizal Fungi and Rhizobia

We chose Glomus mosseae (Gm), which was a broadly suitable strain and could colonize the two plant species mentioned above, for AMF inoculation. It belongs to the family of Glomeraceae and represents a unique Glomus group. The strains were provided by the Institute of Plant Nutrition and Resources, Beijing Academy of Agriculture and Forestry and the inoculum of Gm was propagated on Trifolium repens for three months in a greenhouse. The inoculum consisted of spores and mycelium, colonized root fragments and sand. A total of 135 g inoculum was added to the sterilized background soil per pot; the control group received the same amount of autoclaved inoculum and 75 mL of non-autoclaved inoculum filtrate to ensure the consistency of the microflora.
We chose Rhizobium leguminosarum (purchased from Beijing Beina Chuanglian biotechnology company) for the rhizobia inoculation because this species was originally isolated from wild white clover root nodules and was shown to successfully infect the white clover species used in our experiment. Before use, the tested strains were activated on YMA plates and incubated at 28 °C for three days and then transferred to triangular bottles containing 150 mL of liquid culture medium for the shaking bed culture (150 r·min−1, 28 °C, 30 h). The bacterial suspension (> 109 bacteria·mL−1) [73] was injected into the root of each seedling for the first three days (100 µL each time, once a day). Non-inoculated pots were injected with the same volume of sterile water.

2.5. Harvest and Measuring

The shoot and root dry weights of clover and tall fescue were determined separately after oven-drying at 80 °C for 48 h. The nodule numbers of clover were recorded before weighing.
A weighted subsample of fresh roots was randomly taken. The roots were cut into approximately 1 cm lengths and were then cleared in 10% (w/v) KOH and stained with 0.05% trypan blue. The AMF colonization rate was recorded referencing the method of Biermann and Linderman [74], using Equation (1):
AMF colonization rate (%) = 100 × Σ (0 × root segment number + 10 × root segment number + 20 × root segment number + 100 × root segment number)/total root segment number

2.6. Statistical Analyses

Variance was analyzed using SPSS 22.0 software. Three-way ANOVAs were used to analyze the biomass data as well as the nodule numbers, with the two-level factors set as ‘infected by endophytic fungi (E±)’ (endophytic-infected, endophytic-free), ‘inoculation of AMF (AMF±)’ (inoculated with AMF, inoculated without AMF) and ‘inoculation of rhizobia (R±)’ (inoculated with rhizobia, inoculated without rhizobia). Two-way ANOVAs were then conducted to analyze the mycorrhizal colonization rate data, the influence of the endophytic fungi and the inoculation of rhizobia and the interactions between them on the clover mycorrhizal colonization rate. The significance level for all tests was 0.05.

3. Results

3.1. Clover Nodule Number

Endophytic fungi, Gm and rhizobia had marked effects on the clover nodule number (Table 1). Endophyte infection reduced the nodule number of the neighboring clover (Figure 1A,D). Both Gm and rhizobia inoculation significantly increased the clover nodule number (Figure 1B,C).

3.2. Mycorrhizal Colonization Rate of Clover

Neither endophytic fungi nor rhizobia had a significant effect on the mycorrhizal colonization rate of clover and there was no interaction between the two factors (Table 1).

3.3. Biomass of Clover

Endophytic fungi significantly inhibited the growth of clover and Gm inoculation significantly increased the biomass of clover (Table 1, Figure 2A,B), though only the extent of increase was affected by endophyte infection. The higher extent of improvement occurred when clover was mixed with E+ tall fescue where the biomass of clover in AMF+ treatment was 4.77 times higher than in AMF− treatments (Figure 2D). When mixed with E−, the biomass of clover was 1.81 times higher in AMF+ treatment compared with AMF− treatment (Figure 2D). Rhizobia inoculation could enhance the biomass of clover but a significant effect occurred only when the clover was mixed with E− plants (Figure 2C,E).

3.4. Biomass of Tall Fescue

Endophytic fungi and Gm inoculation significantly affected the biomass of tall fescue (p < 0.001). Endophyte infection significantly increased the biomass of tall fescue (Figure 3A) while Gm inoculation significantly decreased the biomass of tall fescue (Figure 3B). The effect of rhizobia inoculation on the biomass of tall fescue was affected by endophyte infection and the beneficial effect of rhizobia inoculation occurred only in E+ plants (Figure 3C).

4. Discussion

4.1. AMF Inoculation Can Alleviate the Inhibition of Endophytic Fungi on Clover

In nature, grasses can establish multiple symbiotic relationships with endophytic fungi and AMF simultaneously [67,68,69,70]. To date, several studies have examined the interactions between endophytes and AMF and their combined impacts on host plants but have neglected their combined impacts on nonhost plants. For example, Guo et al. [75] found that the roots of endophyte-free tall fescue were colonized more limitedly than those of pearl millet seedlings by Gm and endophytic fungi infection caused a further reduction in the extent of colonization. Antunes et al. [76] conducted two experiments and explained that Neotyphodiurn coenophialum infection reduced AM fungal spore germination and colonization in tall fescue. This phenomenon also exists in other grass species; Omacini et al. [77] found that endophyte-infected Lolium multiflorum had a lower level of mycorrhizal colonization compared with non-endophyte infection. On the other hand, AMF inoculation reduced the density or concentration of endophytic fungi [65,69]. Regarding the effects on host grass growth, Müller [78] found that the effects of endophytes might be enhanced or counterbalanced in the presence of AMF in different grass-endophyte symbionts. Omacini et al. [74] and Mack and Rudgers [65] found that there was no significant interaction between beneficial endophytic fungi and neutral AMF on the growth of ryegrass or tall fescue.
In the present study, we found that the growth of tall fescue was improved by endophyte infection and inhibited by Gm inoculation; we also did not find significant interactions between endophytic fungi and Gm on the growth of the host tall fescue. However, regarding the neighboring plant clover, we found that its growth was inhibited by endophyte infection and improved by Gm inoculation and that the detrimental effect of endophyte infection could be alleviated by Gm inoculation. In a previous study, Wagg et al. [58] reported that AMF inoculation could alleviate the inhibitory effect of perennial ryegrass on clover. In the present study, we further found that AMF inoculation could alleviate the inhibitory effect of endophyte infection on clover.

4.2. Rhizobia Inoculation Can Alleviate the Detrimental Effect of Tall Fescue on the Growth of Clover but Not the Detrimental Effect of Endophyte Infection

Rhizobia are natural symbionts of leguminous plants and it is well known that the symbiosis is mutually beneficial. As endophyte-infected grasses are not infected by rhizobia, studies on the interaction between endophytes and rhizobia are limited. Omacini et al. [79] reported that rhizobia were sensitive to endophytic fungi. García Parisi et al. [80] found that endophytic fungi could inhibit the number of nodules in leguminous plants but did not affect their growth. Our study found that rhizobia inoculation could significantly increase clover biomass when mixed with E− tall fescue; however, when mixed with E+ plants, the beneficial effect of rhizobia inoculation on clover disappeared. That is, rhizobia inoculation could alleviate the detrimental effect of tall fescue on the growth of clover but did not alleviate the detrimental effect of endophyte infection on the growth of clover. The probable reason for this difference might be the rhizobia inoculation rate and, thus, its contribution was significantly inhibited by endophyte infection.
In conclusion, we found that the growth of clover was inhibited by endophyte infection and improved by Gm inoculation and that the detrimental effect of endophyte infection could be alleviated by Gm inoculation. Rhizobia inoculation could alleviate the detrimental effect of tall fescue on the growth of clover but did not alleviate the detrimental effect of endophyte infection on the growth of clover. Certainly, more AMF and rhizobia species should be tested to clearly explore the interaction among endophytes, AMF and rhizobia in affecting plant growth.

Author Contributions

Conceptualization, A.R. and J.L.; methodology, A.R. and J.L.; software, J.L. and X.F.; validation, J.L. and H.L.; formal analysis, A.R., J.L. and X.G.; investigation, J.L. and X.G.; resources, A.R.; data curation, J.L. and X.G.; writing—original draft preparation, J.L. and A.R.; writing—review and editing, J.L., Y.G. and A.R.; visualization, X.F. and Y.G.; supervision, J.L. and A.R.; project administration, A.R.; funding acquisition, A.R. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the National Natural Science Foundation of China (31971425).

Data Availability Statement

This data Saved in Mendeley Data.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Pugnaire, F.I.; Luque, M.T. Changes in plant interactions along a gradient of environmental stress. Oikos 2001, 93, 42–49. [Google Scholar] [CrossRef] [Green Version]
  2. Graff, P.; Aguiar, M.R.; Chaneton, E.J. Shifts in Positive and Negative Plant Interactions along A Grazing Intensity Gradient. Ecology 2007, 88, 188–199. [Google Scholar] [CrossRef]
  3. Kaisermann, A.; De Vries, F.T.; Griffiths, R.I.; Bardgett, R.D. Legacy effects of drought on plant-soil feedbacks and plant-plant interactions. New Phytol. 2017, 215, 1413–1424. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  4. Yu, L.; Song, M.; Xia, Z.; Korpelainen, H.; Li, C. Plant-plant interactions and resource dynamics of Abies fabri and Picea brachytyla as affected by phosphorus fertilization. Environ. Exp. Bot. 2019, 168, 103893. [Google Scholar] [CrossRef]
  5. Sheaffer, C.C.; Peterson, P.R.; Hall, M.H.; Stordahl, J.B. Drought Effects on Yield and Quality of Perennial Grasses in the North Central United States. J. Prod. Agric. 1992, 5, 556–561. [Google Scholar] [CrossRef]
  6. Berdahl, J.D.; Karn, J.F.; Hendrickson, J.R. Dry Matter Yields of Cool–Season Grass Monocultures and Grass–Alfalfa Binary Mixtures. Agron. J. 2001, 93, 463–467. [Google Scholar] [CrossRef] [Green Version]
  7. Coelho, J.J.; Hennessy, A.; Casey, I.; Woodcock, T.; Kennedy, N. Responses of ryegrass, white clover, soil plant primary macronutrients and microbial abundance to application of anaerobic digestates, cattle slurry and inorganic N-fertiliser. Appl. Soil Ecol. 2019, 144, 112–122. [Google Scholar] [CrossRef]
  8. McDonagh, J.; Gilliland, T.J.; McEvoy, M.; Delaby, L.; O’Donovan, M. Nitrogen and white clover impacts on the management of perennial ryegrass–clover swards for grazing cattle. J. Agric. Sci. 2017, 155, 1381–1393. [Google Scholar] [CrossRef]
  9. Chen, W.; McCaughey, W.; Grant, C. Pasture type and fertilization effects on N2 fixation, N budgets and external energy inputs in western Canada. Soil Biol. Biochem. 2004, 36, 1205–1212. [Google Scholar] [CrossRef]
  10. Li, Y.-Y.; Yu, C.-B.; Cheng, X.; Li, C.-J.; Sun, J.-H.; Zhang, F.-S.; Lambers, H.; Li, L. Intercropping alleviates the inhibitory effect of N fertilization on nodulation and symbiotic N2 fixation of faba bean. Plant Soil 2009, 323, 295–308. [Google Scholar] [CrossRef]
  11. Loi, A.; Howieson, J.G.; Cocks, P.S.; Carr, S.J. Genetic variation in populations of two Mediterranean annual pasture legumes (Biserrula pelecinus L. and Ornithopus compressus L.) and associated rhizobia. Aust. J. Agric. Res. 1999, 50, 303. [Google Scholar] [CrossRef]
  12. Kim, Y.-N.; Robinson, B.; Lee, K.-A.; Boyer, S.; Dickinson, N. Interactions between earthworm burrowing, growth of a leguminous shrub and nitrogen cycling in a former agricultural soil. Appl. Soil Ecol. 2017, 110, 79–87. [Google Scholar] [CrossRef]
  13. Smith, S.E.; Read, D.J. Arbutoid and monotropoid mycorrhizas. Mycorrhizal Symbiosis 2002, 301–322. [Google Scholar] [CrossRef]
  14. Ren, L.; Zhang, N.; Wu, P.; Huo, H.; Xu, G.; Wu, G. Arbuscular mycorrhizal colonization alleviates Fusarium wilt in watermelon and modulates the composition of root exudates. Plant Growth Regul. 2015, 77, 77–85. [Google Scholar] [CrossRef]
  15. Lin, G.; McCormack, M.L.; Guo, D. Arbuscular mycorrhizal fungal effects on plant competition and community structure. J. Ecol. 2015, 103, 1224–1232. [Google Scholar] [CrossRef]
  16. Ambrosino, M.L.; Cabello, M.; Busso, C.A.; Silvana, V.M.; Torres, Y.A.; Cardillo, D.S.; Ithurrart, L.S.; Montenegro, O.A.; Giorgetti, H.; Rodríguez, G. Communities of arbuscular mycorrhizal fungi associated with perennial grasses of different forage quality exposed to defoliation. J. Arid. Environ. 2018, 154, 61–69. [Google Scholar] [CrossRef] [Green Version]
  17. Lee, S.-J.; Kong, M.; St-Arnaud, M.; Hijri, M. Arbuscular Mycorrhizal Fungal Communities of Native Plant Species under High Petroleum Hydrocarbon Contamination Highlights Rhizophagus as a Key Tolerant Genus. Microorganisms 2020, 8, 872. [Google Scholar] [CrossRef] [PubMed]
  18. Clay, K. Effects of fungal endophytes on the seed and seedling biology of Lolium perenne and Festuca arundinacea. Oecologia 1987, 73, 358–362. [Google Scholar] [CrossRef]
  19. Rocha, A.C.S.; Garcia, D.; Uetanabaro, A.P.T.; Carneiro, R.T.O.; Araújo, I.S.; Mattos, C.R.R.; Góes-Neto, A. Foliar endophytic fungi from Hevea brasiliensis and their antagonism on Microcyclus ulei. Fungal Divers. 2010, 47, 75–84. [Google Scholar] [CrossRef]
  20. Maulana, A.F.; Turjaman, M.; Sato, T.; Hashimoto, Y.; Cheng, W.; Tawaraya, K. Isolation of endophytic fungi from tropical forest in Indonesia. Symbiosis 2018, 76, 151–162. [Google Scholar] [CrossRef]
  21. Arnold, A.; Maynard, Z.; Gilbert, G.; Coley, P.; Kursar, T. Are tropical fungal endophytes hyperdiverse? Ecol. Lett. 2000, 3, 267–274. [Google Scholar] [CrossRef]
  22. Hesse, U.; Hahn, H.; Andreeva, K.; Forster, K.; Warnstorff, K.; Schöberlein, W.; Diepenbrock, W. Investigations on the Influence of Neotyphodium Endophytes on Plant Growth and Seed Yield of Lolium perenne Genotypes. Crop. Sci. 2004, 44, 1689–1695. [Google Scholar] [CrossRef]
  23. Saikkonen, K.; Wäli, P.; Helander, M.; Faeth, S.H. Evolution of endophyte—Plant symbioses. Trends Plant Sci. 2004, 9, 275–280. [Google Scholar] [CrossRef] [PubMed]
  24. Clarke, B.B.; White, J.F.; Hurley, R.H.; Torres, M.S.; Sun, S.; Huff, D.R. Endophyte-Mediated Suppression of Dollar Spot Disease in Fine Fescues. Plant Dis. 2006, 90, 994–998. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. Rahman, M.H.; Saiga, S. Endophytic fungi (Neotyphodium coenophialum) affect the growth and mineral uptake, transport and efficiency ratios in tall fescue (Festuca arundinacea). Plant Soil 2005, 272, 163–171. [Google Scholar] [CrossRef]
  26. Bush, L.P.; Wilkinson, H.H.; Schardl, C.L. Bioprotective Alkaloids of Grass-Fungal Endophyte Symbioses. Plant Physiol. 1997, 114, 1–7. [Google Scholar] [CrossRef] [Green Version]
  27. Van Hecke, M.M.; Treonis, A.M.; Kaufman, J.R. How does the Fungal Endophyte Neotyphodium coenophialum Affect Tall Fescue (Festuca arundinacea) Rhizodeposition and Soil Microorganisms? Plant Soil 2005, 275, 101–109. [Google Scholar] [CrossRef]
  28. Burns, J.C.; Fisher, D.S.; Rottinghaus, G.E. Grazing Influences on Mass, Nutritive Value, and Persistence of Stockpiled Jesup Tall Fescue without and with Novel and Wild—Type Fungal Endophytes. Crop. Sci. 2006, 46, 1898–1912. [Google Scholar] [CrossRef]
  29. Aschehoug, E.T.; Metlen, K.L.; Callaway, R.M.; Newcombe, G. Fungal endophytes directly increase the competitive effects of an invasive forb. Ecology 2012, 93, 3–8. [Google Scholar] [CrossRef]
  30. Jia, C.; Ruan, W.; Zhu, M.-J.; Ren, A.; Gao, Y.-B. Potential antagnosim of cultivated and wild grass–endophyte associations towards Meloidogyne incognita. Biol. Control. 2013, 64, 225–230. [Google Scholar] [CrossRef]
  31. Malinowski, D.P.; Alloush, G.A.; Belesky, D.P. Leaf endophyte Neotyphodium coenophialum modifies mineral uptake in tall fescue. Plant Soil 2000, 227, 115–126. [Google Scholar] [CrossRef]
  32. Hesse, U.; Schöberlein, W.; Wittenmayer, L.; Forster, K.; Warnstorff, K.; Diepenbrock, W.; Merbach, W. Influence of water supply and endophyte infection (Neotyphodium spp.) on vegetative and reproductive growth of two Lolium perenne L. genotypes. Eur. J. Agron. 2005, 22, 45–54. [Google Scholar] [CrossRef]
  33. Ortega, H.E.; Torres-Mendoza, D.; Cubilla-Rios, L. Patents on Endophytic Fungi for Agriculture and Bio- and Phytoremediation Applications. Mycroorganisms 2020, 8, 1237. [Google Scholar] [CrossRef]
  34. Bayat, F.; Mirlohi, A.; Khodambashi, M. Effects of endophytic fungi on some drought tolerance mechanisms of tall fescue in a hydroponics culture. Russ. J. Plant Physiol. 2009, 56, 510–516. [Google Scholar] [CrossRef]
  35. Nagabhyru, P.; Dinkins, R.D.; Wood, C.L.; Bacon, C.W.; Schardl, C.L. Tall fescue endophyte effects on tolerance to water-deficit stress. BMC Plant Biol. 2013, 13, 127. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  36. Rahman, M.H.; Simpson, W.; Matthew, C.; Sabreen, S.; Okubo, A.; Islam, K.R. Response of Diploid Perennial Ryegrass to Fungal Endophyte AR29 Infections under Water Stress. Commun. Soil Sci. Plant Anal. 2015, 46, 845–860. [Google Scholar] [CrossRef]
  37. Ren, A.Z.; Li, X.; Han, R.; Yin, L.J.; Wei, M.Y.; Gao, Y.-B. Benefits of a symbiotic association with endophytic fungi are subject to water and nutrient availability in Achnatherum sibiricum. Plant Soil 2011, 346, 363–373. [Google Scholar] [CrossRef]
  38. Clay, K.; Cheplick, G.P. Effect of ergot alkaloids from fungal endophyte-infected grasses on fall armyworm (Spodoptera frugiperda). J. Chem. Ecol. 1989, 15, 169–182. [Google Scholar] [CrossRef]
  39. Parisi, P.G.; Grimoldi, A.; Omacini, M. Endophytic fungi of grasses protect other plants from aphid herbivory. Fungal Ecol. 2014, 9, 61–64. [Google Scholar] [CrossRef]
  40. Thom, E.R.; Popay, A.J.; Waugh, C.D.; Minneé, E.M.K. Impact of novel endophytes in perennial ryegrass on herbage production and insect pests from pastures under dairy cow grazing in northern New Zealand. Grass Forage Sci. 2013, 69, 191–204. [Google Scholar] [CrossRef]
  41. Fuchs, B.; Krischke, M.; Mueller, M.J.; Krauss, J. Herbivore–specific induction of defence metabolites in a grass–endophyte association. Funct. Ecol. 2016, 31, 318–324. [Google Scholar] [CrossRef]
  42. Tian, P.; Nan, Z.; Li, C.; Spangenberg, G. Effect of the endophyte Neotyphodium lolii on susceptibility and host physiological response of perennial ryegrass to fungal pathogens. Eur. J. Plant Pathol. 2008, 122, 593–602. [Google Scholar] [CrossRef]
  43. Khiralla, A.; Spina, R.; Varbanov, M.; Philippot, S.; Lemiere, P.; Slezack-Deschaumes, S.; André, P.; Mohamed, I.; Yagi, S.M.; Laurain-Mattar, D. Evaluation of Antiviral, Antibacterial and Antiproliferative Activities of the Endophytic Fungus Curvularia papendorfii, and Isolation of a New Polyhydroxyacid. Mycroorganisms 2020, 8, 1353. [Google Scholar] [CrossRef] [PubMed]
  44. De Aldana, B.R.V.; Romo, M.; Petisco-Rodríguez, C.; De Aldana, B.R.V.; García-Ciudad, A.; García-Criado, B. Infection with the fungal endophyte Epichloë festucae may alter the allelopathic potential of red fescue. Ann. Appl. Biol. 2011, 159, 281–290. [Google Scholar] [CrossRef]
  45. Malinowski, D.; Leuchtmann, A.; Schmidt, D.; Nösberger, J. Symbiosis with Neotyphodium uncinatum Endophyte May Increase the Competitive Ability of Meadow Fescue. Agron. J. 1997, 89, 833–839. [Google Scholar] [CrossRef]
  46. Takai, T.; Sanada, Y.; Yamada, T. Influence of the fungal endophyte Neotyphodium uncinatum on the persistency and competitive ability of meadow fescue (Festuca pratensis Huds.). Grassl. Sci. 2010, 56, 59–64. [Google Scholar] [CrossRef] [Green Version]
  47. Craig, S.; Kannadan, S.; Flory, S.L.; Seifert, E.K.; Whitney, K.D.; Rudgers, J.A. Potential for endophyte symbiosis to increase resistance of the native grass Poa alsodes to invasion by the non-native grass Microstegium vimineum. Symbiosis 2011, 53, 17–28. [Google Scholar] [CrossRef]
  48. Ren, A.; Li, X.; Gao, Y.; Liu, H.; Gao, Y.-B.; Van Der Heijden, M.; Ren, A.-Z. Plant endophytes and arbuscular mycorrhizal fungi alter plant competition. Funct. Ecol. 2018, 32, 1168–1179. [Google Scholar] [CrossRef]
  49. Saari, S.; Faeth, S.H. Hybridization of Neotyphodium endophytes enhances competitive ability of the host grass. New Phytol. 2012, 195, 231–236. [Google Scholar] [CrossRef] [Green Version]
  50. Wu, L.; Ren, A.; Jing, Y.; Zhou, Y.; Wang, X.; Qin, J.; Gao, Y. Endophytic benefit for a competitive host is neutralized by increasing ratios of infected plants. Acta Oecol. 2016, 70, 112–120. [Google Scholar] [CrossRef]
  51. Sutherland, B.L.; Hume, D.E.; Tapper, B.A. Allelopathic effects of endophyte infected perennial ryegrass extracts on white clover seedlings. N. Z. J. Agric. Res. 2010, 42, 19–26. [Google Scholar] [CrossRef]
  52. Aschehoug, E.T.; Callaway, R.M.; Newcombe, G.; Tharayil, N.; Chen, S. Fungal endophyte increases the allelopathic effects of an invasive forb. Oecologia 2014, 175, 285–291. [Google Scholar] [CrossRef] [PubMed]
  53. Bao, G.; Saikkonen, K.; Wang, H.; Zhou, L.; Chen, S.; Li, C.; Nan, Z. Does endophyte symbiosis resist allelopathic effects of an invasive plant in degraded grassland? Fungal Ecol. 2015, 17, 114–125. [Google Scholar] [CrossRef]
  54. Hoveland, C.S.; Bouton, J.H.; Durham, R.G. Fungal endophyte effects on production of legumes in association with tall fescue. Agron. J. 1999, 91, 897–902. [Google Scholar] [CrossRef]
  55. Malinowski, D.P.; Belesky, D.P.; Fedders, J.M. Endophyte Infection May Affect the Competitive Ability of Tall Fescue Grown with Red Clover. J. Agron. Crop. Sci. 1999, 183, 91–101. [Google Scholar] [CrossRef]
  56. Clay, K. Fungal Endophyte Symbiosis and Plant Diversity in Successional Fields. Science 1999, 285, 1742–1744. [Google Scholar] [CrossRef]
  57. Chen, B.-D.; Zhu, Y.-G.; Duan, J.; Xiao, X.; Smith, S. Effects of the arbuscular mycorrhizal fungus Glomus mosseae on growth and metal uptake by four plant species in copper mine tailings. Environ. Pollut. 2007, 147, 374–380. [Google Scholar] [CrossRef]
  58. Wagg, C.; Jansa, J.; Stadler, M.; Schmid, B.; Van Der Heijden, M.G.A. Mycorrhizal fungal identity and diversity relaxes plant–plant competition. Ecology 2011, 92, 1303–1313. [Google Scholar] [CrossRef] [Green Version]
  59. Smith, F.A.; Smith, S.E. What is the significance of the arbuscular mycorrhizal colonisation of many economically important crop plants? Plant Soil 2011, 348, 63–79. [Google Scholar] [CrossRef]
  60. Lee, B.-R.; Muneer, S.; Avice, J.-C.; Jung, W.-J.; Kim, T.H. Mycorrhizal colonisation and P-supplement effects on N uptake and N assimilation in perennial ryegrass under well-watered and drought-stressed conditions. Mycorrhiza 2012, 22, 525–534. [Google Scholar] [CrossRef]
  61. Mirshad, P.P.; Puthur, J.T. Arbuscular mycorrhizal association enhances drought tolerance potential of promising bioenergy grass (Saccharum arundinaceumretz.). Environ. Monit. Assess. 2016, 188, 1–20. [Google Scholar] [CrossRef] [PubMed]
  62. Thilakarathna, M.S.; Raizada, M.N. A meta-analysis of the effectiveness of diverse rhizobia inoculants on soybean traits under field conditions. Soil Biol. Biochem. 2017, 105, 177–196. [Google Scholar] [CrossRef]
  63. Ipsilantis, I.; Lotos, L.; Tsialtas, I.T. Diversity and nodulation effectiveness of rhizobia and mycorrhizal presence in climbing dry beans grown in Prespa lakes plain, Greece. Arch. Microbiol. 2019, 201, 1151–1161. [Google Scholar] [CrossRef]
  64. Novas, M.V.; Cabral, D.; Godeas, A.M. Interaction between grass endophytes and mycorrhizas in Bromus setifolius from Patagonia, Argentina. Symbiosis 2005, 40, 23–30. [Google Scholar]
  65. Mack, K.M.L.; Rudgers, J.A. Balancing multiple mutualists: Asymmetric interactions among plants, arbuscular mycorrhizal fungi, and fungal endophytes. Oikos 2008, 117, 310–320. [Google Scholar] [CrossRef]
  66. Novas, M.V.; Iannone, L.; Godeas, A.M.; Scervino, J.M. Evidence for leaf endophyte regulation of root symbionts: Effect of Neotyphodium endophytes on the pre-infective state of mycorrhizal fungi. Symbiosis 2011, 55, 19–28. [Google Scholar] [CrossRef]
  67. Arrieta, A.; Iannone, L.; Scervino, J.M.; Vignale, M.; Novas, M.V. A foliar endophyte increases the diversity of phosphorus-solubilizing rhizospheric fungi and mycorrhizal colonization in the wild grass Bromus auleticus. Fungal Ecol. 2015, 17, 146–154. [Google Scholar] [CrossRef]
  68. Chu-Chou, M.; Guo, B.; An, Z.; Hendrix, J.; Ferriss, R.; Siegel, M.; Dougherty, C.; Burrus, P. Suppression of mycorrhizal fungi in fescue by the acremonium coenophialum endophyte. Soil Biol. Biochem. 1992, 24, 633–637. [Google Scholar] [CrossRef]
  69. Liu, Q.; Parsons, A.J.; Xue, H.; Fraser, K.; Ryan, G.D.; Newman, J.A.; Rasmussen, S. Competition between foliar Neotyphodium lolii endophytes and mycorrhizal Glomus spp. fungi in Lolium perenne depends on resource supply and host carbohydrate content. Funct. Ecol. 2011, 25, 910–920. [Google Scholar] [CrossRef] [Green Version]
  70. Vignale, M.V.; Iannone, L.J.; Pinget, A.D.; De Battista, J.P.; Novas, M.V. Effect of epichloid endophytes and soil fertilization on arbuscular mycorrhizal colonization of a wild grass. Plant Soil 2015, 405, 279–287. [Google Scholar] [CrossRef]
  71. Larimer, A.L.; Clay, K.; Bever, J.D. Synergism and context dependency of interactions between arbuscular mycorrhizal fungi and rhizobia with a prairie legume. Ecology 2014, 95, 1045–1054. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  72. Marks, S.; Clay, K. Physiological responses of Festuca arundinacea to fungal endophyte infection. New Phytol. 1996, 133, 727–733. [Google Scholar] [CrossRef]
  73. García-Parisi, P.A.; Lattanzi, F.A.; Grimoldi, A.A.; Druille, M.; Omacini, M. Three symbionts involved in interspecific plant-soil feedback: Epichloid endophytes and mycorrhizal fungi affect the performance of rhizobia-legume symbiosis. Plant Soil 2016, 412, 151–162. [Google Scholar] [CrossRef]
  74. Biermann, B.; Linderman, R.G. Quantifying Vesicular-Arbuscular Mycorrhizae: A Proposed Method Towards Standardization. New Phytol. 1981, 87, 63–67. [Google Scholar] [CrossRef]
  75. Guo, B.Z.; Hendrix, J.W.; An, Z.; Ferriss, R.S. Role of Acremonium Endophyte of Fescue on Inhibition of Colonization and Reproduction of Mycorrhizal Fungi. Mycologia 1992, 84, 882. [Google Scholar] [CrossRef]
  76. Antunes, P.M.; Miller, J.; Carvalho, L.M.; Newman, J.N.K.A. Even after death the endophytic fungus of schedonorus phoenix reduces the arbuscular mycorrhizas of other plants. Funct. Ecol. 2008, 22, 912–918. [Google Scholar] [CrossRef] [Green Version]
  77. Omacini, M.; Eggers, T.; Bonkowski, M.; Gange, A.C.; Jones, T.H. Leaf endophytes affect mycorrhizal status and growth of co-infected and neighbouring plants. Funct. Ecol. 2006, 20, 226–232. [Google Scholar] [CrossRef]
  78. Müller, J. Artificial infection by endophytes affects growth and mycorrhizal colonisation of Lolium perenne. Funct. Plant Biol. 2003, 30, 419–424. [Google Scholar] [CrossRef]
  79. Omacini, M.; Semmartin, M.; Pérez, L.I.; Gundel, P.E. Grass–endophyte symbiosis: A neglected aboveground interaction with multiple belowground consequences. Appl. Soil Ecol. 2012, 61, 273–279. [Google Scholar] [CrossRef]
  80. García-Parisi, P.A.; Lattanzi, F.A.; Grimoldi, A.A.; Omacini, M. Multi-symbiotic systems: Functional implications of the coexistence of grass-endophyte and legume-rhizobia symbioses. Oikos 2014, 124, 553–560. [Google Scholar] [CrossRef]
Microorganisms 09 00109 g001 550
Figure 1. (A–D) The influence of endophytic fungi, AMF and rhizobia on the number of nodules. E+, endophyte-infected tall fescue; E−, endophyte-free tall fescue; AMF+, AMF-inoculated; AMF−, AMF-free; R+, rhizobia-inoculated; R−, rhizobia-free. Different small letters indicate significant differences between treatments (p < 0.05).
Figure 1. (A–D) The influence of endophytic fungi, AMF and rhizobia on the number of nodules. E+, endophyte-infected tall fescue; E−, endophyte-free tall fescue; AMF+, AMF-inoculated; AMF−, AMF-free; R+, rhizobia-inoculated; R−, rhizobia-free. Different small letters indicate significant differences between treatments (p < 0.05).
Microorganisms 09 00109 g001
Microorganisms 09 00109 g002 550
Figure 2. (A–E) The influence of endophytic fungi, AMF and rhizobia on the biomass of clover. E+, endophyte-infected tall fescue; E−, endophyte-free tall fescue; AMF+, AMF-inoculated; AMF−, AMF-free; R+, rhizobia-inoculated; R−, rhizobia-free. Different small letters indicate significant differences between treatments (p < 0.05).
Figure 2. (A–E) The influence of endophytic fungi, AMF and rhizobia on the biomass of clover. E+, endophyte-infected tall fescue; E−, endophyte-free tall fescue; AMF+, AMF-inoculated; AMF−, AMF-free; R+, rhizobia-inoculated; R−, rhizobia-free. Different small letters indicate significant differences between treatments (p < 0.05).
Microorganisms 09 00109 g002
Microorganisms 09 00109 g003a 550Microorganisms 09 00109 g003b 550
Figure 3. (A–C) The influence of endophytic fungi and rhizobia on the biomass of tall fescue. E−, endophyte-free tall fescue, E+, endophyte-infected tall fescue; AMF+, AMF-inoculated; AMF−, AMF-free; R+, rhizobia-inoculated; R−, rhizobia-free. Different small letters indicate significant differences between treatments (p < 0.05).
Figure 3. (A–C) The influence of endophytic fungi and rhizobia on the biomass of tall fescue. E−, endophyte-free tall fescue, E+, endophyte-infected tall fescue; AMF+, AMF-inoculated; AMF−, AMF-free; R+, rhizobia-inoculated; R−, rhizobia-free. Different small letters indicate significant differences between treatments (p < 0.05).
Microorganisms 09 00109 g003aMicroorganisms 09 00109 g003b
Table
Table 1. ANOVA of the influence of endophytic fungi, arbuscular mycorrhizal fungi (AMF) and rhizobia on nodule number, mycorrhizal colonization rate (%) and biomass of Trifolium repens.
Table 1. ANOVA of the influence of endophytic fungi, arbuscular mycorrhizal fungi (AMF) and rhizobia on nodule number, mycorrhizal colonization rate (%) and biomass of Trifolium repens.
VariableNodule NumberMycorrhizal Colonization Rate (%)Biomass
FpFpFp
Endophytic fungi (E)4.7040.040 *0.4190.53024.892<0.001 ***
AMF18.089<0.001 *** 28.531<0.001 ***
Rhizobia (R)25.524<0.001 ***0.0400.8444.3640.048 *
E × AMF0.4710.499 5.2380.032 *
E × R5.7640.024 *0.7200.4145.3290.005 **
AMF × R1.7800.195 5.6150.027 *
E × AMF × R0.0220.883 2.0050.944
* p < 0.05, ** p < 0.01, *** p < 0.001.
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Liu, J.; Ge, X.; Fan, X.; Liu, H.; Gao, Y.; Ren, A. The Inhibitory Effect of Endophyte-Infected Tall Fescue on White Clover Can Be Alleviated by Glomus mosseae Instead of Rhizobia. Microorganisms 2021, 9, 109. https://doi.org/10.3390/microorganisms9010109

AMA Style

Liu J, Ge X, Fan X, Liu H, Gao Y, Ren A. The Inhibitory Effect of Endophyte-Infected Tall Fescue on White Clover Can Be Alleviated by Glomus mosseae Instead of Rhizobia. Microorganisms. 2021; 9(1):109. https://doi.org/10.3390/microorganisms9010109

Chicago/Turabian Style

Liu, Jinming, Xiaoyu Ge, Xiaowen Fan, Hui Liu, Yubao Gao, and Anzhi Ren. 2021. "The Inhibitory Effect of Endophyte-Infected Tall Fescue on White Clover Can Be Alleviated by Glomus mosseae Instead of Rhizobia" Microorganisms 9, no. 1: 109. https://doi.org/10.3390/microorganisms9010109

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop