Effects of Epichloё endophytic fungi infection in wild barley (Hordeum brevisubulatum) on soil chemical properties and the soil microbial community

doi:10.11686/cyxb2018677

Abstract

Abstract: An 8-month greenhouse study was conducted to investigate the belowground effects of infection of wild barley by the foliar endophyte Epichloё bromicola. The effects of endophyte infection status (E+: endophyte infected; E-: endophyte free) on soil chemical and microbiological properties were tested in three soils collected from Maqu, Yuzhong, and Linze in Gansu province, China. We measured the dry matter production of plants at 3, 6, and 8 months after establishment. The soil carbon, nitrogen, and phosphorous contents, pH, and the abundance of bacteria, fungi, and key bacteria involved in the soil nitrogen cycle were determined at 6 and 8 months after plant establishment. The dry matter production of wild barley was significantly higher in E+ plants than in E- plants in all three soils. Irrespective of endophyte status, the dry matter production was highest in Linze soils and lowest in Maqu soils. The presence of the endophyte significantly increased soil total nitrogen content and the abundance of ammonia-oxidizing bacteria. The effects of endophyte status on total soil carbon, microbial biomass carbon, pH, abundance of bacteria, fungi, denitrifying bacteria, and nitrous oxide-reducing bacteria varied with soil type and plant age. The total phosphorus content in soil varied significantly with soil type and plant age but not with endophyte status. These results confirmed that E. bromicola infection of wild barley influences the chemical and microbiological properties of soil in a soil type- and plant age-dependent manner. We suggest that long-term field studies in the future would be beneficial for understanding the mechanisms driving these observed changes in soil properties.

Key words: wild barley, endophytic fungi, soil microbes

JIN Yuan-yuan, BOWATTE Saman, JIA Qian-min, HOU Fu-jiang, LI Chun-jie. Effects of Epichloё endophytic fungi infection in wild barley (Hordeum brevisubulatum) on soil chemical properties and the soil microbial community[J]. Acta Prataculturae Sinica, 2019, 28(10): 66-77.

References

[1] Siegel M R, Johnos M C, VarneyD R. A fungal endophyte in tall fescue: Incidence and dissemination. Phytopathology, 1984, 74(8): 932-937.
[2] Kauppinen M, Saikkonen K, Helander M.Epichloё grass endophytes in sustainable agriculture. Nature Plants, 2016, 2(2): 15224-15231.
[3] Franken P.The plant strengthening root endophyte Piriformospora indica: Potential application and the biology behind. Applied Microbiology and Biotechnology, 2012, 96(6): 1455-1464.
[4] Rodriguez R, Redman R.More than 400 million years of evolution and some plants still can’t make it on their own: Plant stress tolerance via fungal symbiosis. Journal of Experimental Botany, 2008, 59(5): 1109.
[5] Richmond D S, Cardina J, Grewal P S.Influence of grass species and endophyte infection on weed populations during establishment of low-maintenance lawns. Agriculture Ecosystems and Environment, 2006, 115(1): 27-33.
[6] Johnson L J, Briggs L R, Caradus J R, et al. The exploitation of Epichloё endophytes for agricultural benefit. Fungal Diversity, 2013, 60(1): 171-188.
[7] Kannadan S, Rudgers J A.Endophyte symbiosis benefits a rare grass under low water availability. Functional Ecology, 2010, 22: 706-713.
[8] 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: 923-940.
[9] Sabzalian M R, Mirlohi A.Neotyphodium endophytes trigger salt resistance in tall and meadow fescues. Journal of Plant Nutrition and Soil Science, 2010, 173(6): 952-957.
[10] Czarnoleski M, Olejniczak P, Mikołajczak P, et al. Fungal endophytes protect grass seedlings against herbivory and allow economical seed production. Evolutionary Ecology Research, 2010, 12(6): 769-777.
[11] Pérez L I, Gundel P E, Omacini M.Can the defensive mutualism between grasses and fungal endophytes protect non-symbiotic neighbours from soil pathogens. Plant and Soil, 2016, 405(1/2): 289-298.
[12] Fuchs B, Krischke M, Mueller M J, et al. Plant age and seasonal timing determine endophyte growth and alkaloid biosynthesis. Fungal Ecology, 2017, 29: 52-58.
[13] Chen T, Johnson R, Chen S, et al. Infection by the fungal endophyte Epichloё bromicola enhances the tolerance of wild barley (Hordeum brevisubulatum) to salt and alkali stresses. Plant and Soil, 2018, 428: 1-18.
[14] Song M, Chai Q, Li X, et al. An asexual Epichloё, endophyte modifies the nutrient stoichiometry of wild barley (Hordeum brevisubulatum) under salt stress. Plant and Soil, 2015, 387(1/2): 153-165.
[15] Song M, Li X, Saikkonen K, et al. An asexual Epichloё endophyte enhances waterlogging tolerance of Hordeum brevisubulatum. Fungal Ecology, 2015, 13: 44-52.
[16] Jenkins M B, Franzluebbers A J, Humayoun S B.Assessing short-term responses of prokaryotic communities in bulk and rhizosphere soils to tall fescue endophyte infection. Plant and Soil, 2006, 289(1/2): 309-320.
[17] Rojas, Xavier. Symbiosis between tall fescue and a fungal shoot endophyte affects soil microbial communities. Delta, 2014, 21(3): 167-182.
[18] Franzluebbers A J, Nazih N, Stuedemann J A, et al. Soil carbon and nitrogen pools under low-and high-endophyte-infected tall fescue. Soil Science Society of America Journal, 1999, 63(6): 1687-1694.
[19] Hosseini F, Mosaddeghi M R, Hajabbasi M A, et al. Influence of tall fescue endophyte infection on structural stability as quantified by high energy moisture characteristic in a range of soils. Geoderma, 2015, 249/250: 87-99.
[20] Franzluebbers A J, Hill N S.Soil carbon, nitrogen,and ergot alkaloids with short-and long-term exposure to endophyte-infected and endophyte-free tall fescue. Soil Science Society of America Journal, 2005, 69(2): 404-412.
[21] Handayani I P, Coyne M S, Phillips T D.Soil organic carbon fractions differ in two contrasting tall fescue systems. Plant and Soil, 2011, 338(1/2): 43-50.
[22] Hosseini F, Mosaddeghi M R, Hajabbasi M A, et al. Aboveground fungal endophyte infection in tall fescue alters rhizosphere chemical, biological, and hydraulic properties in texture-dependent ways. Plant and Soil, 2015, 388(1/2): 351-366.
[23] Van H M M, Treonis A M, Kaufman J R. How does the fungal endophyte Neotyphodium coenophialum affect tall fescue (Festuca arundinacea) rhizo deposition and soil microorganisms? Plant and Soil, 2005, 275(1/2): 101-109.
[24] Zhong R, Xia C, Ju Y W, et al. Effects of Epichloё gansuensis on root-associated fungal communities of Achnatherum inebrians under different growth conditions. Fungal Ecology, 2018, 31: 29-36.
[25] Bowatte S, Barrett B, Luscombe C, et al. Effect of grass species and fungal endophyte on soil nitrification potential. New Zealand Journal of Agricultural Research, 2011, 54(4): 275-284.
[26] Saha D C, Jackson M A, Johnson C J M. A rapid staining method for detection of endophytic fungi in turf and forage grasses. Phytopathology, 1988, 78(2): 237-239.
[27] Murphy J, Riley J, Murphy J, et al. A modified single solution for determination of phosphate in nature waters. Analytica Chimica Acta, 1962, 27(7): 31-36.
[28] Li X H, Wang Z H.Comparison of two soil organic carbon determination methods. Analytical Instrumentation, 2009, (5): 78-80.
李小涵, 王朝辉. 两种测定土壤有机碳方法的比较. 分析仪器, 2009, (5): 78-80.
[29] Vance E D, Brookes P C, Jenkinson D S.An extraction method for measuring soil microbial biomass C. Soil Biology & Biochemistry, 1987, 19: 703-707.
[30] Grosskopf R, Janssen P H, Liesack W.Diversity and structure of the methanogenic community in anoxic rice paddy soil microcosms as examined by cultivation and direct 16S rRNA gene sequence retrieval. Applied and Environmental Microbiology, 1998, 64(3): 960-969.
[31] Chu H, Neufeld J D, Walker V K, et al. The influence of vegetation type on the dominant soil bacteria, archaea, and fungi in a low arctic tundra landscape. Soil Science Society of America Journal, 2011, 75(5): 1756-1765.
[32] Chen X P, Zhu Y G, Xia Y, et al. Ammonia-oxidizing archaea: Important players in paddy rhizosphere soil. Environmental Microbiology, 2008, 10(8): 1978-1987.
[33] Casciotti K L, Ward B B.Dissimilatory nitrite reductase genes from autotrophic ammonia-oxidizing bacteria. Applied and Environmental Microbiology, 2001, 67(5): 2213-2221.
[34] Throbäck I N, Enwall K, Åsa Jarvis, et al. Reassessing PCR primers targeting nirS, nirK and nosZ genes for community surveys of denitrifying bacteria with DGGE. Fems Microbiology Ecology, 2010, 49(3): 401-417.
[35] Peng H L.Soil quality investigationand plant adaptability of Chenshan botanical garden in Shanghai. Harbin: Northeast Forestry University, 2008.
彭红玲. 上海辰山植物园土壤肥力质量评价及植物适宜性研究. 哈尔滨: 东北林业大学, 2008.
[36] Lu C.Measures to improve soil fertility in Shandong apple orchard. Agricultural Knowledge, 2011, 23: 15-16.
路超. 提高山东苹果园土壤肥力的措施. 农业知识, 2011, 23: 15-16.
[37] Latch G C M, Hunt W F, Musgrave D R. Endophytic fungi affect growth of perennial ryegrass. New Zealand Journal of Agricultural Research, 1985, 28(1): 165-168.
[38] Kfm R, Cunningham P J, Barrie J T, et al. Productivity and persistence of cultivars and Algerian introductions of perennial ryegrass (Lolium perenne L.) in Victoria. Australian Journal of Experimental Agriculture, 1987, 27(2): 267-274.
[39] Chen M M, Yin H B, O’Connor P, et al. C:N:P stoichiometry and specific growth rate of clover colonized by arbuscular mycorrhizal fungi. Plant and Soil, 2010, 326(1/2): 21-29.
[40] Kyle M, Watts T, Schade J, et al. A microfluorometric method for quantifying RNA and DNA in terrestrial insects. Journal of Insect Science, 2003, 3(1): 1-7.
[41] Kenworthy J W, Thayer G W.Production and decomposition of the rand rhizomes of seagrasses, zostera marina and thalassia testudinum, in temperate and subtropical marine ecosystems. Bulletin of Marine Science, 1984, 35(3): 364-379.
[42] Smith V C, Bradford M A.Litter quality impacts on grassland litter decomposition are differently dependent on soil fauna across time. Applied Soil Ecology, 2003, 24(2): 197-203.
[43] Malinowski D P, Belesky D P, Hill N S, et al. Influence of phosphorus on the growth and ergot alkaloid content of Neotyphodium coenophialum-infected tall fescue (Festuca arundinacea Schreb.). Plant and Soil, 1998, 198(1): 53-61.
[44] Azevedo M D, Welty R E.A study of the fungal endophyte Acremonium coenophialum in the roots of tall fescue seedlings. Mycologia, 1995, 87(3): 289-297.
[45] Ren A Z, Gao Y B, Zhou F, et al. Effects of endophyte infection on ecophysiological response of perennial ryegrass under phosphorus deficiency. Acta Ecologica Sinica, 2007, 27(12): 5433-5440.
任安芝, 高玉葆, 周芳, 等. 黑麦草-内生真菌共生体对磷缺乏的生理生态反应. 生态学报, 2007, 27(12): 5433-5440.
[46] Aldana V, Beatriz R, Criado G, et al. Influence of fungal endophyte infection on nutrient element content of tall fescue. Journal of Plant Nutrition, 1999, 22(1): 163-176.
[47] Malinowski D P, Alloush G A, Belesky D P.Leaf endophyte Neotyphodium coenophialum modifies mineral uptake in tall fescue. Plant and Soil, 2000, 227(1/2): 115-126.
[48] Inselsbacher E, Näsholm T.The below-ground perspective of forest plants: Soil provides mainly organic nitrogen for plants and mycorrhizal fungi. New Phytologist, 2012, 195(2): 329-334.
[49] Chen Z J, Liu J, Wei X K, et al. Effects of latosols extracts with different pH and endophytic fungi on growth and physiology of lolium perenne seedling. Acta Botanica Boreali-Occidentalia Sinica, 2017, 37(7): 1348-1356.
陈振江, 刘静, 魏学凯, 等. 不同pH砖红壤浸提液和内生真菌对黑麦草幼苗生长生理的影响. 西北植物学报, 2017, 37(7): 1348-1356.
[50] Khayamim F, Khademi H, Sabzalian M R.Effect of Neotyphodium endophyte-tall fescue symbiosis on mineralogical changes in clay-sized phlogopite and muscovite. Plant and Soil, 2011, 341(1/2): 473-484.
[51] Li G P, Gao Y, Liu L, et al. Effects of fungal endophytes on properties and microbial community structure of the rhizosphere soil of Achnatherum sibiricum in nitrogen addition conditions. Acta Ecologica Sinica, 2017, 37(13): 4299-4308.
李隔萍, 高远, 刘磊, 等. 内生真菌对氮添加羽茅根际土壤特性和微生物群落的影响. 生态学报, 2017, 37(13): 4299-4308.
[52] Needelman B A, Wander M M, Bollero G A, et al. Interaction of tillage and soil texture: Biologically active soil organic matter in illinois. Soil Science Society of America Journal, 1999, 63(5): 1326-1334.
[53] Fernández B, Jesús D, Achmon Y, et al. Comparison of soil biosolarization with mesophilic and thermophilic solid digestates on soil microbial quantity and diversity. Applied Soil Ecology, 2017, 119: 183-191.
[54] Buyer J S, Zuberer D A, Nichols K A, et al. Soil microbial community function, structure, and glomalin in response to tall fescue endophyte infection. Plant and Soil, 2011, 339(1/2): 401-412.
[55] Zhou Y, Zheng L Y, Zhu M J, et al. Effects of fungal endophyte infection on soil properties and microbial communities in the host grass habitat. Chinese Journal of Plant Ecology, 2014, 38(1): 54-61.
周勇, 郑璐雨, 朱敏杰, 等. 内生真菌侵染对禾草宿主生境土壤特性和微生物群落的影响. 植物生态学报, 2014, 38(1): 54-61.
[56] Huang X, Li X Z, Chai Q, et al. Effects of Achnatherum inebrians/Neotyphodium endophyte symbiont on microflora and nutrient of soil. Pratacultural Science, 2013, 30(3): 352-356.
黄玺, 李秀璋, 柴青, 等. 醉马草内生真菌共生体对土壤微生物和养分的影响. 草业科学, 2013, 30(3): 352-356.
[57] Yang B, Wang X M, Ma H Y, et al. Fungal endophyte Phomopsis liquidambari affects nitrogen transformation processes and related microorganisms in the rice rhizosphere. Frontiers in Microbiology, 2015, 6: 982-997.
[58] Domeignozhorta L A, Philippot L, Peyrard C, et al. Peaks of in situ N₂O emissions are influenced by N₂O producing and reducing microbial communities across arable soils. Global Change Biology, 2017, 24(1): 360-369.
[59] Philippot L, Andert J, Jones C M, et al. Importance of denitrifiers lacking the genes encoding the nitrous oxide reductase for N₂O emissions from soil. Global Change Biology, 2011, 17(3): 1497-1504.