Effects of Epichloë endophyte and field management practices on the abundance and diversity of the soil fungal community

doi:10.11686/cyxb2022154

Abstract

Abstract:

Endophytic fungi in grasses affect soil chemistry and microbial communities in host plant habitats by affecting above-ground plant litter decomposition and root exudation. However， few detailed data are available on whether the effects of Epichlo? endophyte on the habitat soils of host plants are mainly caused by endophyte-mediated plant litter decomposition or root metabolism. In this study， the chemical properties and the abundance and diversity of the soil fungal community in endophyte-infected （E+） and -free （E-） sample soils were determined after three cycles of mowing with different treatment practices （mowing and return to the field， mowing and removal， and natural growth）. It was found that： 1） Endophyte fungi increased organic carbon， ammonium nitrogen and nitrate nitrogen in the soil of E+ sample plots under the treatment of mowing back to the field， and significantly increased ammonium nitrogen content in the naturally growing soil of the host plants. 2） Epichlo? endophyte significantly increased the alpha diversity of the soil fungal community under the treatment of mowing and return to the field， while beta diversity differed significantly among the three treatments. 3） Epichlo? endophyte and management practices affected the abundance and diversity of the soil fungal community directly， or indirectly by affecting soil chemical properties （organic carbon， carbon to nitrogen ratio and nitrate nitrogen）. In summary， both decomposition of above-ground plant parts and root metabolism mediated by endophyte infection affect soil chemistry and the abundance and diversity of soil fungal community， with endophyte-mediated decomposition of above-ground parts having a stronger effect than root metabolism.

Key words: field management practices, Epichlo? endophyte, soil fungi, root metabolism, plant litter decomposition

Yuan-yuan JIN, Zhen-jiang CHEN, Tian WANG, Chun-jie LI. Effects of Epichloë endophyte and field management practices on the abundance and diversity of the soil fungal community[J]. Acta Prataculturae Sinica, 2023, 32(4): 142-152.

Figures/Tables 7

References 53

1	Siegel M R， Latch G C M， Johnson M C. Fungal endophytes of grasses. Annual Review of Phytopathology， 1987， 25（1）： 293-315.
2	Kauppinen M， Saikkonen K， Helander M， et al. Epichloë grass endophytes in sustainable agriculture. Nature Plants， 2016， 2（2）： 15224-15231.
3	Tian P， Nan Z B. Signaling in the mutualistic symbiotic interaction between endophytes and their hosts. Acta Prataculturae Sinica， 2017， 26（4）： 196-210.
	田沛，南志标. 内生真菌与寄主互惠共生的分子机制. 草业学报， 2017， 26（4）： 196-210.
4	Wang R， Luo S， Clarke B B， et al. The Epichloë festucae antifungal protein Efe-AfpA is also a possible effector protein required for the interaction of the fungus with its host grass Festuca rubra subsp. rubra. Microorganisms， 2021， 9（1）： 140-155.
5	Xie F X， Ren A Z， Wang Y H， et al. A comparative study of the inhibitive effect of fungal endophytes on turf grass fungus pathogens. Acta Ecologica Sinica， 2008， 28（8）： 3913-3920.
	谢凤行，任安芝，王银华，等. 内生真菌对草坪植物病原真菌抑制作用的比较. 生态学报， 2008， 28（8）： 3913-3920.
6	Wang X， Qin J， Chen W， et al. Pathogen resistant advantage of endophyte-infected over endophyte-free Leymus chinensis is strengthened by pre-drought treatment. European Journal of Plant Pathology， 2016， 144（3）： 477-486.
7	Chen T， Richard J， Chen S， et al. Infection by the fungal endophyte Epichloë bromicola enhances the tolerance of wild barley （Hordeum brevisubulatum） to salt and alkali stresses. Plant and Soil， 2018， 428（1/2）： 1-18.
8	Chen Z， Jin Y Y， Yao X， et al. Fungal endophyte improves survival of Lolium perenne in low fertility soils by increasing root growth， metabolic activity and absorption of nutrients. Plant and Soil， 2020， 452（1）： 185-206.
9	Li C J， Lang M X， Chen Z J， et al. Advances in artificial inoculation technology for grass-endophytic fungi. Acta Prataculturae Sinica， 2021， 30（7）： 179-189.
	李春杰，郎鸣晓，陈振江，等. 禾草-内生真菌人工接种技术研究进展. 草业学报， 2021， 30（7）： 179-189.
10	Nan Z B， Li C J. Roles of the grass-Neotyphodium association in pastoral agriculture systems. Acta Ecologica Sinica， 2004， 24（3）： 605-616.
	南志标，李春杰. 禾草-内生真菌共生体在草地农业系统中的作用. 生态学报， 2004， 24（3）： 605-616.
11	Li C J， Wang Z F， Chen T X， et al. Creation of novel barley germplasm using an Epichloë endophyte. Chinese Science Bulletin， 2021， 66（20）： 2608-2617.
	李春杰，王正凤，陈泰祥，等. 利用禾草内生真菌创制大麦新种质. 科学通报， 2021， 66（20）： 2608-2617.
12	Helander M， Phillips T， Faeth S H， et al. Alkaloid quantities in endophyte-infected tall fescue are affected by the plant-fungus combination and environment. Journal of Chemical Ecology， 2016， 42（2）： 118-126.
13	Zhong R， Xia C， Ju Y， et al. A foliar Epichloë endophyte and soil moisture modified belowground arbuscular mycorrhizal fungal biodiversity associated with Achnatherum inebrians. Plant and Soil， 2021， 458（1）： 105-122.
14	Chen Z， Jin Y， Yao X， et al. Gene analysis reveals that leaf litter from Epichloë endophyte-infected perennial ryegrass alters diversity and abundance of soil microbes involved in nitrification and denitrification. Soil Biology and Biochemistry， 2021， 154： 108-123.
15	Rojas X， Guo J Q， Leff J W， et al. Infection with a shoot-specific fungal endophyte （Epichloë） alters tall fescue soil microbial communities. Microbial Ecology， 2016， 72（18）： 197-206.
16	Guo J Q， Mcculley R L， Mcnear D H. Tall fescue cultivar and fungal endophyte combinations influence plant growth and root exudate composition. Frontiers in Plant Science， 2015， 6： 183-196.
17	Wakelin S， Harrison S， Mander C， et al. Impacts of endophyte infection of ryegrass on rhizosphere metabolome and microbial community. Crop and Pasture Science， 2015， 66（10）： 1049-1057.
18	Iqbal J， Nelson J， Mcculley R. Fungal endophyte presence and genotype affect plant diversity and soil-to-atmosphere trace gas fluxes. Plant and Soil， 2013， 364（1/2）： 15-27.
19	Dalmannsdottir S， Jørgensen M， Rapacz M， et al. Cold acclimation in warmer extended autumns impairs freezing tolerance of perennial ryegrass （Lolium perenne） and timothy （Phleum pratense）. Physiologia Plantarum， 2017， 160（3）： 266-281.
20	Chen Z， Li C J， Nan Z B， et al. Segregation of Lolium perenne into a subpopulation with high infection by endophyte Epichloë festucae var. lolii results in improved agronomic performance. Plant and Soil， 2020， 446（1）： 595-612.
21	Tanveer S K， Zhang J L， Lu X L， et al. Effect of corn residue mulch and N fertilizer application on nitrous oxide （N₂O） emission and wheat crop productivity under rain-fed condition of Loess Plateau China. International Journal of Agriculture and Biology， 2014， 16（3）： 505-512.
22	Zhang L M， Duff A M， Smith C J. Community and functional shifts in ammonia oxidizers across terrestrial and marine （soil/sediment） boundaries in two coastal bay ecosystems. Environmental Microbiology， 2018， 20（8）： 2834-2853.
23	Siahmard O J， Pableo R M B， Novero A U. Molecular identification of rhizospheric fungi associated with ‘Saba’ banana via the amplification of internal transcribed spacer sequence of 5.8S ribosomal DNA. Asian Journal of Plant Sciences， 2017， 16（2）： 78-86.
24	Schmidt M W I， Torn M S， Abiven S， et al. Persistence of soil organic matter as an ecosystem property. Nature， 2011， 478： 49-56.
25	Wang Y Z， Zheng J Q， Boyd S E， et al. Effects of litter quality and quantity on chemical changes during eucalyptus litter decomposition in subtropical Australia. Plant and Soil， 2019， 442（1/2）： 65-78.
26	Zhang B， Wang H L， Yao S H， et al. Litter quantity confers soil functional resilience through mediating soil biophysical habitat and microbial community structure on an eroded bare land restored with mono Pinus massoniana. Soil Biology and Biochemistry， 2013， 57： 556-567.
27	Sun Y D， Zhang X X， Gu L J， et al. Antifungal activity of the crude extraction of endophyte-infected and endophyte-free drunken horse grass. Pratacultural Science， 2015， 32（4）： 508-514.
	孙一丹，张兴旭，古丽君，等. 醉马草-内生真菌共生体中生物碱的抑菌活性. 草业科学， 2015， 32（4）： 508-514.
28	Gundel P E， Helander M， Garibaldi L A， et al. Role of foliar fungal endophytes in litter decomposition among species and population origins. Fungal Ecology， 2016， 21： 50-56.
29	Purahong W， Hyde D. Effects of fungal endophytes on grass and non-grass litter decomposition rates. Fungal Diversity， 2011， 47（1）： 1-7.
30	Müller K， Marhan S， Kandeler E， et al. Carbon flow from litter through soil microorganisms： From incorporation rates to mean residence times in bacteria and fungi. Soil Biology and Biochemistry， 2017， 115： 187-196.
31	Don A， Kalbitz K. Amounts and degradability of dissolved organic carbon from foliar litter at different decomposition stages. Soil Biology and Biochemistry， 2005， 37（12）： 2171-2179.
32	Zhou W J， Sha L Q， Schaefer D Q， et al. Direct effects of litter decomposition on soil dissolved organic carbon and nitrogen in a tropical rainforest. Soil Biology and Biochemistry， 2015， 81： 255-258.
33	Lemons A， Clay K， Rudgers J A. Connecting plant-microbial inter-actions above and belowground： A fungal endophyte affects decomposition. Oecologia， 2005， 145（4）： 595-604.
34	Daniel A， Alejandra M， Carlos L， et al. Epichloë fungal endophytes and plant defenses： Not just alkaloids. Trends in Plant Science， 2017， 22（11）： 939-948.
35	Newman J A， Abner M L， Dado R G， et al. Effects of elevated CO₂， nitrogen and fungal endophyte-infection on tall fescue： Growth， photosynthesis， chemical composition and digestibility. Global Change Biology， 2010， 9（3）： 425-437.
36	Couteaux M M， Bottner P， Berg B. Litter decomposition， climate and litter quality. Trends in Ecology and Evolution， 1995， 10（2）： 63-66.
37	Slaughter L C， Nelson J A， Carlisle E， et al. Climate change and Epichloë coenophiala association modify belowground fungal symbioses of tall fescue host. Fungal Ecology， 2018， 31： 37-46.
38	Osono T， Ishii Y， Takeda H， et al. Fungal succession and lignin decomposition on Shorea obtusa leaves in a tropical seasonal forest in northern Thailand. Fungal Divers， 2009， 36（10）： 101-119.
39	Koide K， Osono T， Takeda H. Colonization and lignin decomposition of Camellia japonica leaf litter by endophytic fungi. Mycoscience， 2005， 46（5）： 280-286.
40	Koide K， Osono T， Takeda H. Fungal succession and decomposition of Camellia japonica leaf litter. Ecological Research， 2005， 20（5）： 599-609.
41	Malinowski D P， Belesky D P. Ecological importance of Neotyphodium spp. grass endophytes in agroecosystems. Grassland Science， 2006， 52（1）： 1-14
42	Mack K M L， Rudgers J A. Balancing multiple mutualists： Asymmetric interactions among plants， arbuscular mycorrhizal fungi， and fungal endophytes. Oikos， 2008， 117（2）： 310-320.
43	Slaughter L C， McCulley R L. Aboveground Epichloë coenophiala-grass associations do not affect belowground fungal symbionts or associated plant， soil parameters. Microbial Ecology， 2016， 72： 682-691.
44	Larimer A L， Bever J D， Clay K. Consequences of simultaneous interactions of fungal endophytes and arbuscular mycorrhizal fungi with a shared host grass. Oikos， 2012， 121（12）： 2090-2096.
45	Arrieta A， Iannone L， Scervino J， et al. A foliar endophyte increases the diversity of phosphorus-solubilizing rhizospheric fungi and mycorrhizal colonization in the wild grass Bromus auleticus. Fungal Ecology， 2015， 17： 146-154.
46	Malinowski D P， Belesky D P. Adaptations of endophyte-infected cool-season grasses to environmental stresses： Mechanisms of drought and mineral stress tolerance. Crop Science， 2000， 40（4）： 923-940.
47	Cesco S， Mimmo T， Tonon G， et al. Plant-borne flavonoids released into the rhizosphere： Impact on soil bio-activities related to plant nutrition. A review. Biology and Fertility of Soils， 2012， 48（2）： 123-149.
48	Rodríguez-Blanco A， Sicardi M， Frioni L. Plant genotype and nitrogen fertilization effects on abundance and diversity of diazotrophic bacteria associated with maize （Zea mays L.）. Biology and Fertility of Soils， 2015， 51（3）： 391-402.
49	Yao L， Wang D， Kang L， et al. Effects of fertilizations on soil bacteria and fungi communities in a degraded arid steppe revealed by high through-put sequencing. PeerJ， 2018， 6： 4623-4650.
50	Parmar D K， Thakur D R. Improvement in soil physical， chemical and microbiological properties during cropping cycles under different nutrient managements in western Himalayas. International Journal of Current Microbiology and Applied Sciences， 2017， 6（6）： 487-496.
51	Gai J P， Tian H， Yang F Y， et al. Arbuscular mycorrhizal fungal diversity along a Tibetan elevation gradient. Pedobiologia， 2012， 55（33）： 145-151.
52	Johannes R， Erland B. Fungal and bacterial growth in soil with plant materials of different C/N ratios. FEMS Microbiology Ecology， 2007， 62（3）： 258-267.
53	Hu Y L， Wang S L， Huang Y， et al. Effects of litter chemistry on soil biological property and enzymatic activity. Acta Ecologica Sinica. 2005， 25（10）： 2662-2668.
	胡亚林，汪思龙，黄宇，等. 凋落物化学组成对土壤微生物学性状及土壤酶活性的影响. 生态学报， 2005， 25（10）： 2662-2668.

处理 Treatment		pH	土壤有机碳 Soil organic carbon （g·kg^-1）	土壤全氮 Soil total nitrogen （g·kg^-1）	土壤全磷 Soil total phosphorus （g·kg^-1）	土壤铵态氮 Soil ammonium nitrogen （mg·kg^-1）	土壤硝态氮 Soil nitrate nitrogen （mg·kg^-1）	碳氮比 C/N
裸地 Bare ground		7.35±0.14c	8.65±0.17d	1.90±0.02c	0.36±0.07b	1.16±0.03d	19.09±0.31d	4.55±0.13a
刈割移除 Mowing removal	E+	7.67±0.23bc	9.45±0.34d	2.61±0.14c	0.68±0.06ab	3.01±0.23cd	27.14±0.66cd	3.62±0.30b
刈割移除 Mowing removal	E-	7.87±0.40bc	9.88±0.32d	2.78±0.24bc	0.69±0.14ab	3.13±0.17c	29.87±0.78c	3.55±0.28b
刈割返田Mowing back to the field	E+	8.41±0.65a	15.63±0.54b	4.20±0.23a	1.06±0.19a	4.87±0.06a	52.30±1.36a	3.72±0.50b
刈割返田Mowing back to the field	E-	8.39±0.57ab	12.20±0.12c	3.50±0.05ab	0.64±0.05ab	4.12±0.05b	41.90±0.31b	3.48±0.08b
自然生长 Nature growth	E+	7.93±0.13ab	17.13±0.13a	4.12±0.04a	1.02±0.34a	4.46±0.12a	49.32±0.33a	4.15±0.09a
自然生长 Nature growth	E-	7.67±0.32bc	14.87±0.23b	3.01±0.27bc	0.99±0.19a	4.21±0.20b	48.97±0.41a	4.93±0.19a

处理 Treatment		pH	土壤有机碳 Soil organic carbon （g·kg^-1）	土壤全氮 Soil total nitrogen （g·kg^-1）	土壤全磷 Soil total phosphorus （g·kg^-1）	土壤铵态氮 Soil ammonium nitrogen （mg·kg^-1）	土壤硝态氮 Soil nitrate nitrogen （mg·kg^-1）	碳氮比 C/N
裸地 Bare ground		7.35±0.14c	8.65±0.17d	1.90±0.02c	0.36±0.07b	1.16±0.03d	19.09±0.31d	4.55±0.13a
刈割移除 Mowing removal	E+	7.67±0.23bc	9.45±0.34d	2.61±0.14c	0.68±0.06ab	3.01±0.23cd	27.14±0.66cd	3.62±0.30b
刈割移除 Mowing removal	E-	7.87±0.40bc	9.88±0.32d	2.78±0.24bc	0.69±0.14ab	3.13±0.17c	29.87±0.78c	3.55±0.28b
刈割返田Mowing back to the field	E+	8.41±0.65a	15.63±0.54b	4.20±0.23a	1.06±0.19a	4.87±0.06a	52.30±1.36a	3.72±0.50b
刈割返田Mowing back to the field	E-	8.39±0.57ab	12.20±0.12c	3.50±0.05ab	0.64±0.05ab	4.12±0.05b	41.90±0.31b	3.48±0.08b
自然生长 Nature growth	E+	7.93±0.13ab	17.13±0.13a	4.12±0.04a	1.02±0.34a	4.46±0.12a	49.32±0.33a	4.15±0.09a
自然生长 Nature growth	E-	7.67±0.32bc	14.87±0.23b	3.01±0.27bc	0.99±0.19a	4.21±0.20b	48.97±0.41a	4.93±0.19a

处理 Treatment		链格孢属 Alternaria	缓霉菌属 Bradymyces	小毛盘菌属 Cistella	枝孢属 Cladosporium	鬼伞属 Coprinopsis	附球菌属 Epicoccum
裸地 Bare ground		1.34±0.52a	2.62±0.55a	3.22±1.10a	0.41±0.11a	0.07±0.03d	1.35±0.19a
刈割移除 Mowing removal	E+	0.39±0.04ab	0.70±0.36b	1.65±0.41b	0.23±0.13bc	0.48±0.24bc	0.21±0.03b
刈割移除 Mowing removal	E-	0.18±0.05b	0.98±0.18b	0.68±0.32c	0.09±0.02c	1.22±0.26b	0.26±0.05b
刈割返田 Mowing back to the field	E+	0.15±0.29b	1.05±0.15b	0.54±0.26c	0.31±0.09b	0.15±0.09c	0.31±0.02b
刈割返田 Mowing back to the field	E-	0.46±0.16ab	1.35±0.10ab	0.64±0.10c	0.40±0.02a	2.27±0.23a	0.48±0.08b
自然生长 Nature growth	E+	0.08±0.03b	0.84±0.22b	0.63±0.16c	0.06±0.02c	0.11±0.04c	0.62±0.07b
自然生长 Nature growth	E-	0.10±0.07b	1.63±0.21ab	0.87±0.15bc	0.05±0.27c	0.17±0.04c	0.18±0.01b
处理 Treatment		赤霉菌属 Gibberella	被孢霉属 Mortierella	异壳二孢属 Neoascochyta	光黑壳属 Preussia	茄子菌属 Solicoccozyma	Tetracladium
裸地 Bare ground		3.38±0.87ab	18.63±2.60b	2.69±0.79ab	2.55±0.55a	1.74±0.41a	0.38±0.08b
刈割移除 Mowing removal	E+	1.47±0.38c	16.74±5.44b	5.95±0.16a	2.72±0.81a	2.61±0.65a	2.54±0.14a
刈割移除 Mowing removal	E-	1.52±0.41c	28.76±1.87a	0.92±0.01ab	2.39±0.26a	2.23±0.25a	1.19±0.03ab
刈割返田 Mowing back to the field	E+	3.97±0.33a	17.06±1.47b	3.98±1.90ab	1.57±0.34a	2.49±0.39a	0.63±0.09b
刈割返田 Mowing back to the field	E-	3.47±0.31ab	17.80±3.15b	5.85±0.68a	2.33±0.28a	2.28±0.84a	0.54±0.15b
自然生长 Nature growth	E+	1.45±0.55c	24.96±1.61ab	0.33±0.07ab	2.00±0.31a	2.64±0.87a	0.43±0.18b
自然生长 Nature growth	E-	1.93±0.62bc	25.11±0.97ab	0.01±0.01b	2.68±0.41a	4.81±0.22a	0.29±0.06b

处理 Treatment		链格孢属 Alternaria	缓霉菌属 Bradymyces	小毛盘菌属 Cistella	枝孢属 Cladosporium	鬼伞属 Coprinopsis	附球菌属 Epicoccum
裸地 Bare ground		1.34±0.52a	2.62±0.55a	3.22±1.10a	0.41±0.11a	0.07±0.03d	1.35±0.19a
刈割移除 Mowing removal	E+	0.39±0.04ab	0.70±0.36b	1.65±0.41b	0.23±0.13bc	0.48±0.24bc	0.21±0.03b
刈割移除 Mowing removal	E-	0.18±0.05b	0.98±0.18b	0.68±0.32c	0.09±0.02c	1.22±0.26b	0.26±0.05b
刈割返田 Mowing back to the field	E+	0.15±0.29b	1.05±0.15b	0.54±0.26c	0.31±0.09b	0.15±0.09c	0.31±0.02b
刈割返田 Mowing back to the field	E-	0.46±0.16ab	1.35±0.10ab	0.64±0.10c	0.40±0.02a	2.27±0.23a	0.48±0.08b
自然生长 Nature growth	E+	0.08±0.03b	0.84±0.22b	0.63±0.16c	0.06±0.02c	0.11±0.04c	0.62±0.07b
自然生长 Nature growth	E-	0.10±0.07b	1.63±0.21ab	0.87±0.15bc	0.05±0.27c	0.17±0.04c	0.18±0.01b
处理 Treatment		赤霉菌属 Gibberella	被孢霉属 Mortierella	异壳二孢属 Neoascochyta	光黑壳属 Preussia	茄子菌属 Solicoccozyma	Tetracladium
裸地 Bare ground		3.38±0.87ab	18.63±2.60b	2.69±0.79ab	2.55±0.55a	1.74±0.41a	0.38±0.08b
刈割移除 Mowing removal	E+	1.47±0.38c	16.74±5.44b	5.95±0.16a	2.72±0.81a	2.61±0.65a	2.54±0.14a
刈割移除 Mowing removal	E-	1.52±0.41c	28.76±1.87a	0.92±0.01ab	2.39±0.26a	2.23±0.25a	1.19±0.03ab
刈割返田 Mowing back to the field	E+	3.97±0.33a	17.06±1.47b	3.98±1.90ab	1.57±0.34a	2.49±0.39a	0.63±0.09b
刈割返田 Mowing back to the field	E-	3.47±0.31ab	17.80±3.15b	5.85±0.68a	2.33±0.28a	2.28±0.84a	0.54±0.15b
自然生长 Nature growth	E+	1.45±0.55c	24.96±1.61ab	0.33±0.07ab	2.00±0.31a	2.64±0.87a	0.43±0.18b
自然生长 Nature growth	E-	1.93±0.62bc	25.11±0.97ab	0.01±0.01b	2.68±0.41a	4.81±0.22a	0.29±0.06b

[1]	Hong-jian WEI, Jie DING, Ju-ming ZHANG, Wen YANG, Yong-qi WANG, Tian-zeng LIU. Changes in soil fungal community structure under bermudagrass turf in response to traffic stress [J]. Acta Prataculturae Sinica, 2022, 31(4): 102-112.
[2]	QIAN Ya-li, WANG Xian-zhi, LAI Xing-fa, LI Jun-cheng, SHEN Yu-ying. Effects of perennial forage on characteristics of the soil fungal community in an apple orchard [J]. Acta Prataculturae Sinica, 2019, 28(11): 124-132.
[3]	LU Guang-xin, CHEN Xiu-rong, YANG Cheng-de, XUE Li, LIU Wen, BIAN Jing. Identification of cellulose decomposing fungi strain F₁ and decomposition activity to two kinds of lawn grass litter [J]. Acta Prataculturae Sinica, 2011, 20(6): 170-179.
[4]	ZHANG Jun-zhong, CHEN Xiu-rong, YANG Cheng-de, XUE Li. A study on the diversity of soil cultured fungi in the alpine grassland of Eastern Qilian Mountains [J]. Acta Prataculturae Sinica, 2010, 19(2): 124-132.