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Growth and physiological responses of perennial ryegrass to an AMF and an Epichloë endophyte under different soil water contents

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Abstract

Arbuscular mycorrhizal fungi (AMF) and endophytic Epichloë are two important symbiotic microorganisms of perennial ryegrass (Lolium perenne). The present study evaluates the individual and combined effects of AMF and Epichloë on drought stress. Plant growth, phosphorus (P) uptake, chlorophyll content, net photosynthetic rate (Pn), soluble sugar concentration, malondialdehyde (MDA) concentration, and antioxidant enzyme activities were measured in a greenhouse experiment. Both AMF and Epichloë significantly increased Pn and total P content for each soil water content. In addition, the presence of AMF increased plant total dry weight, root activity, and soluble sugar concentration at each soil water content. Furthermore, catalase activity increased and MDA concentration decreased at 30% soil water content (SWC). Infection with Epichloë increased the polyphenol oxidase activity of plants for both non-AMF and AMF treatments at 30% SWC. AMF + Epichloë treatments increased plant P uptake, Pn, root activity, and soluble sugar concentration at each soil water content (SWC) (P < 0.001), and increased peroxidase (POD) activity at 30% SWC (P < 0.001). Plant-AMF-Epichloë symbiosis alleviated the damage caused by drought stress by promoting P uptake, photosynthesis, and the accumulation of osmoregulatory substances.

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References

  • Alam SM (1999) Nutrient uptake by plants under stress conditions. In: Pessarakli M (ed) Handbook of plant and crop stress. Marcel Dekker, New York, pp 285–314

    Google Scholar 

  • Amalric C, Sallanon H, Monnet F, Hitmi A, Coudret A (1999) Gas exchange and chlorophyll fluorescence in symbiotic and non-symbiotic ryegrass under water stress. Photosynthetica 37:107–112

    Google Scholar 

  • Andersen CP, Markhart AHIII, Dixon RK, Sucoff EI (1988) Root hydraulic conductivity of vesicular-arbuscular mycorrhizal green ash seedlings. New Phytol 109:465–471

    Google Scholar 

  • Atimanav G, Adholeya A (2002) AM inoculations of five tropical fodder crops and inoculum production in marginal soil amended with organic matter. Biol Fertil Soils 35:214–218

    Google Scholar 

  • Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42

    Google Scholar 

  • Avis TJ, Gravel V, Antoun H, Tweddell RJ (2008) Multifaceted beneficial effects of rhizosphere microorganisms on plant health and productivity. Soil Biol Biochem 40:1733–1740

    CAS  Google Scholar 

  • Azcón R, Barea J (1997) Mycorrhizal dependency of a representative plant species in mediterranean shrublands (Lavandula spica) as a key factor to its use for revegetation strategies in desertification-threatened areas. Appl Soil Ecol 7:83–92

    Google Scholar 

  • Beers RF, Sizer IW (1952) A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 195:133–140

    PubMed  CAS  Google Scholar 

  • Briggs L, Crush J, Ouyang L, Sprosen J (2013) Neotyphodium endophyte strain and superoxide dismutase activity in perennial ryegrass plants under water deficit. Acta Physiol Plant 35:1513–1520

    CAS  Google Scholar 

  • Carroll G (1988) Fungal endophytes in stems and leaves: from latent pathogen to mutualistic symbiont. Ecol 69:2–9

    Google Scholar 

  • Catalin SI, Ionut M (2013) Drought phenomena and groundwater scarcity in eastern Romania (Siret-Prut region). EGU General Assembly 15:6997

    Google Scholar 

  • Cheplick GP, Perera A, Koulouris K (2000) Effect of drought on the growth of Lolium perenne genotypes with and without fungal endophytes. Funct Ecol 14:657–667

    Google Scholar 

  • Clay K (2004) Fungi and the food of the gods. Nature 427:401–402

    PubMed  CAS  Google Scholar 

  • Corradi N, Buffner B, Croll D, Colard A, Horak A, Sanders IR (2009) High-level molecular diversity of copper-zinc superoxide dismutase genes amongand within species of arbuscular mycorrhizal fungi. Appl Environ Microbiol 75:1970–1978

    PubMed  PubMed Central  CAS  Google Scholar 

  • Craven KD (2012) Population studies of native grass-endophyte symbioses provide clues for the roles of host jumps and hybridization in driving their evolution. Mol Ecol 21:2562–2564

    PubMed  CAS  Google Scholar 

  • Duan T, Facelli E, Smith SE, Smith FA, Nan Z (2011) Differential effects of soil disturbance and plant residue retention on function of arbuscular mycorrhizal (AM) symbiosis are not reflected in colonization of roots or hyphal development in soil. Soil Biol Biochem 43:571–578

    CAS  Google Scholar 

  • Faeth SH, Sullivan TJ (2003) Mutualistic asexual endophytes in a native grass are usually parasitic. Am Nat 161:310–325

    PubMed  Google Scholar 

  • Fester T, Hause T (2005) Accumulation of reactive oxygen species in arbuscular mycorrhizal roots. Mycorrhiza 15:373–379

    PubMed  CAS  Google Scholar 

  • Florea S, Schardl CL, Hollin W (2015) Detection and isolation of Epichloë species, fungal endophytes of grasses. Curr Protoc Microbiol 38:19A.1.1–19A.1.24

    Google Scholar 

  • Frey B, Schüepp H (1993) Acquisition of nitrogen by external hyphae of arbuscular mycorrhizal fungi associated with Zea mays. New Phytol 124(2):221–230

    Google Scholar 

  • Gierczik K, Sasvári Z, Posta K (2012) Effects of pre and post inoculation by mycorrhizal fungi on growth and production of spice pepper. J Landscape Ecol 10:385–391

    Google Scholar 

  • Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500

    Google Scholar 

  • Gueta-Dahan Y, Yaniv Z, Zilinskas A, Ben Hayyim G (1997) Salt and oxidative stress; similar and specific responses and their relation to salt tolerance in Citrus. Planta 203:460–469

    PubMed  CAS  Google Scholar 

  • Hanson WC (1950) The photometric determination of phosphorus in fertilizers using the phosphovanado-molybdate complex. J Sci Food Agric 1:172–173

    CAS  Google Scholar 

  • Heidari M, Karami V (2014) Effects of different mycorrhiza species on grain yield, nutrient uptake and oil content of sunflower under water stress. J Saudi Soc Agric Sci 13:9–13

    Google Scholar 

  • Hesse U, Schoberlein W, Wittenmayer L, Forster K, Warnstorff K, Diepenbrock W, Merbach W (2005) Influence of water supply and endophyte infection (Neotyphodium) on vegetative and reproductive growth of two Lolium perenne genotypes. Eur J Agron 22:45–54

    Google Scholar 

  • Hohmann P, Messmer MM (2017) Breeding for mycorrhizal symbiosis: focus on disease resistance. Euphytica 213:113

    Google Scholar 

  • Huang RS, Smith WK, Yost RS (1985) Influence of vesicular arbuscular mycorrhiza on growth, water relations and leaf orientation in Leucaena leucocephala. New Phytol 99:229–243

    Google Scholar 

  • Hume DE, Popay AJ, Barker DJ (1993) Effects of Acremonium endophyte on growth of ryegrass and tall fescue under varying levels of soil moisture and argentine stem weevil attack. Proceedings of the 2nd international symposium on acremonium/grass interactions, AgResearch, Palmerston North, New Zealand, 161–164

  • Jaleel CA, Gopi R, Sankar B, Gomathinayagam M, Panneerselvam R (2008) Differential responses in water use efficiency in two varieties of Catharanthus roseus under drought stress. Comp Rend Biol 331:42–47

    Google Scholar 

  • Khalafallah AA, Abo-Ghalia HH (2008) Effect of arbuscular mycorrhizal fungi on the metabolic products and activity of antioxidant system in wheat plants subjected to short-term water stress, followed by recovery at different growth stages. J Appl Sci Res 4:559–569

    CAS  Google Scholar 

  • Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301

    Google Scholar 

  • Kumar KB, Khan P (1982) Peroxidase and polyphenol oxidase in excised ragi (Eleusine corocana) leaves during senescence. Indian J Exp Biol 20:412–416

    CAS  Google Scholar 

  • Lacan D, Baccou JC (1998) High levels of antioxidant enzymes correlate with delayed senescence in nonnetted muskmelon fruits. Planta 204:377–382

    CAS  Google Scholar 

  • Larimer AL, Bever JD, Clay K (2012) Consequences of simultaneous interactions of fungal endophytes and arbuscular mycorrhizal fungi with a shared host grass. Oikos 121:2090–2096

    Google Scholar 

  • Lenoir I, Fontaine J, Tisserant B, Laruelle F, Lounèshadj SA (2017) Beneficial contribution of the arbuscular mycorrhizal fungus, Rhizophagus irregularis, in the protection of Medicago truncatula roots against benzo[a]pyrene toxicity. Mycorrhiza 27:465–476

    PubMed  CAS  Google Scholar 

  • Li YP, Li YH (2017) Advances in adaptability of meteorological drought indices in China. J Arid Meteorol 35:709–723

    Google Scholar 

  • Li HS, Sun Q, Zhao SJ, Zhang WH (2000) Principle and techniques of botanic, chemical and physiological experiments, 1st edn. Senior Education Press, Beijing

    Google Scholar 

  • Li HQ, Wang JJ, Zhang GM, Lin WH, Tian P (2016) Effects of fungal endophytes on the growth of perennial ryegrass under drought condition. Pratacul Sci 33:599–607

    Google Scholar 

  • Li F, Guo YE, Christensen MJ, Gao P, Li YZ, Duan TY (2018) An arbuscular mycorrhizal fungus and Epichloë festucae var. lolii reduce Bipolaris sorokiniana disease incidence and improve perennial ryegrass growth. Mycorrhiza 28:159–169

    PubMed  Google Scholar 

  • Liu H, Zheng G, Guan J, Li G (2002) Changes of root activity and membrane permeability under drought stress in maize. Acta Agr B Sin 17:20–22

    CAS  Google Scholar 

  • Liu Q, Parsons AJ, Xue H, Fraser K, Ryan GD, Newman JA, Rasmussen S (2011) Competition between foliar Neotyphodium lolii endophytes and mycorrhizal Glomus spp. fungi in Lolium perenne depends on resource supply and host carbohydrate content. Funct Ecol 25:910–920

    Google Scholar 

  • Liu H, Chen W, Wu M, Wu RH, Zhou Y, Gao YB, Ren AZ (2017) Arbuscular mycorrhizal fungus inoculation reduces the drought-resistance advantage of endophyte-infected versus endophyte-free Leymus chinensis. Mycorrhiza 27:1–9

    Google Scholar 

  • Malinowski DP, Belesky DP (1999) Neotyphodium coenophialum-endophyte infection affects the ability of tall fescue to use sparingly available phosphorus. J Plant Nutr 22:835–853

    CAS  Google Scholar 

  • Müller CB, Krauss J (2005) Symbiosis between grasses and asexual fungal endophytes. Curr Opin Plant Biol 8:450–456

    PubMed  Google Scholar 

  • Nan ZB (1996) Incidence and distribution of endophytic fungi in seeds of some native and introduced grasses in China. Acta Pratacul Sin 5:1–8 (In Chinese with English Abstract)

    Google Scholar 

  • Novas MV, Cabral D, Godeas AM (2005) Interaction between grass endophytes and mycorrhizas in Bromus setifolius from Patagonia, Argentina. Symbiosis 40:23–30

    Google Scholar 

  • Omacini M, Eggers T, Bonkowski M, Gang AC, Jones TH (2006) Leaf endophytes affect mycorrhizal status and growth of co-infected and neighbouring plants. Funct Ecol 20:226–232

    Google Scholar 

  • Parvizi K, Dashti F (2015) The effect of in vitro mycorrhization on growth characteristics, changes in endogenous hormones and performance of microplants in potato (Solanum tuberosum). J Cent Eur Agric 16:445–462

    Google Scholar 

  • Peng QQ, Li CJ, Song ML, Nan ZB (2013) Effects of seed hydropriming on growth of Festuca sinensis, infected with Neotyphodium endophyte. Fungal Ecol 6:83–91

    Google Scholar 

  • Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. T British Mycol Soc 55:158–IN118

    Google Scholar 

  • Rahman MH, Simpson WR, Matthew C, Sabreen S (2015) Response of diploid perennial ryegrass to fungal endophyte AR29 infections under water stress. Commun Soil Sci Plan 46:845–860

    CAS  Google Scholar 

  • Ravel C, Charmet G, Balfourier F (1995) Influence of the fungal endophyte Acremonium lolii on agronomic traits of perennial ryegrass in France. Grass For Sci 50:75–80

    Google Scholar 

  • Reed KFM (1996) Improving the adaptation of perennial ryegrass, tall fescue, phalaris, and cocksfoot for Australia. New Zeal J Agr Res 39:457–464

    Google Scholar 

  • Ren AZ, Wei MY, Yin LJ, Wu LJ, Zhou Y, Li X, Gao YB (2014) Benefits of a fungal endophyte in Leymus chinensis depend more on water than on nutrient availability. Environ Exp Bot 108:71–78

    CAS  Google Scholar 

  • Renker C, Heinrichs J, Kaldorf M (2003) Combining nested PCR and restriction digest of the internal transcribed spacer region to characterize arbuscular mycorrhizal fungi on roots from the field. Mycorrhiza 13:191–198

    PubMed  CAS  Google Scholar 

  • Roldan A, Diaz-Vivancos P, Hernandez JA, Carrosco L, Caravaca F (2008) Superoxide dismutase and total peroxidase activities in relation to drought recovery performance of mycorrhizal shrub seedlings grown in an amended semiarid soil. J Plant Physiol 165:715–722

    PubMed  CAS  Google Scholar 

  • Ruizlozano JM, Azcon R, Gomez M (1995) Effects of arbuscular-mycorrhizal glomus species on drought tolerance: physiological and nutritional plant responses. Appl Environ Microbiol 61:456–460

    CAS  Google Scholar 

  • Schardl CL, Leuchtmann A, Spiering MJ (2004) Symbioses of grasses with seedborne fungal endophytes. Annu Rev Plant Biol 55:315–340

    PubMed  CAS  Google Scholar 

  • Shangguan Z, Shao M, Dyckmans J (1999) Interaction of osmotic adjustment and photosynthesis in winter wheat under soil drought. J Plant Physiol 154:753–758

    CAS  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, London

    Google Scholar 

  • Tintjer T, Leuchtmann A, Clay K (2008) Variation in horizontal and vertical transmission of the endophyte Epichloe elymi infecting the grass Elymus hystrix. New Phytol 179:236–246

    PubMed  Google Scholar 

  • Tobar R, Azcon R, Barea JM (1994) Improved nitrogen uptake and transport from 15N-labelled nitrate by external hyphae of arbuscular mycorrhiza under water-stressed conditions. New Phytol 126:119–122

    Google Scholar 

  • VanHeeswijck R, McDonald G (1992) Acremonium endophytes in perennial ryegrass and other pasture grasses in Australia and New Zealand. Aust J Agric Res 43:1683–1709

    Google Scholar 

  • Wang W, Vinour B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14

    PubMed  CAS  Google Scholar 

  • West CP (1994) Physiology and drought tolerance of endophyte-infected grasses. In: Bacon CW, White JF Jr (eds) Biotechnology of endophytic fungi of grasses. CRC Press, Boca Raton, pp 87–99

    Google Scholar 

  • West CP, Izekor E, Turner KE, Elmi AA (1993) Endophyte effects on growth and persistence of tall fescue along a water-supply gradient. Agron J 85:264–270

    Google Scholar 

  • White JF, Torres MS (2010) Is plant endophyte-mediated defensive mutualism the result of oxidative stress protection? Physiol Plant 138:440–446

    PubMed  CAS  Google Scholar 

  • Wiewióra B, Żurek G, Żurek M (2015) Endophyte-mediated disease resistance in wild populations of perennial ryegrass (Lolium perenne). Fungal Ecol 15:1–8

    Google Scholar 

  • Wu QS, Xia RX (2006) Arbuscular mycorrhizal fungi influence growth, osmotic adjustment and photosynthesis of citrus under well-watered and water stress conditions. J Plant Physiol 163:417–425

    PubMed  CAS  Google Scholar 

  • Wu QS, Zou YN, Xia RX (2006) Effects of water stress and arbuscular mycorrhizal fungi on reactive oxygen metabolism and antioxidant production by citrus (Citrus tangerine) roots. Eur J Soil Biol 42:166–172

    CAS  Google Scholar 

  • Wu QS, Srivastava AK, Zou YN (2013) AMF-induced tolerance to drought stress in citrus: a review. Sci Hortic 164:77–87

    CAS  Google Scholar 

  • Xu L, Li X, Han L, Li D, Song G (2017) Epichloë endophyte infection improved drought and heat tolerance of tall fescue through altered antioxidant enzyme activity. Eur J Hortic Sci 82:90–97

    Google Scholar 

  • Yang T, Ma S, Dai CC (2014) Drought degree constrains the beneficial effects of a fungal endophyte on Atractylodes lancea. J Appl Microbiol 117:1435–1449

    PubMed  CAS  Google Scholar 

  • Yordanov I, Velikova V, Tsonev T (2000) Plant responses to drought, acclimation, and stress tolerance. Photosynthetica 38:171–186

    CAS  Google Scholar 

  • Zaidi A, Khan MS, Amil M (2003) Interactive effect of rhizotrophic microorganisms on yield and nutrient uptake of chickpea (Cicer arietinum). Eur J Agron 19:15–21

    Google Scholar 

  • Zhang YP, Nan ZB (2010) Growth and anti-oxidative systems changes in Elymus dahuricus is affected by Neotyphodium endophyte under contrasting water availability. J Agron Crop Sci 193:377–386

    Google Scholar 

  • Zhang XX, Li CJ, Nan ZB (2009) Effects of cadmium stress on growth and anti-oxidative systems in Achnatherum inebrians symbiotic with Neotyphodium gansuense. J Hazard Mater 175:703–709

    PubMed  Google Scholar 

  • Zhang XX, Fan XM, Li CJ, Nan ZB (2010) Effects of cadmium stress on seed germination, seedling growth and antioxidative enzymes in Achnatherum inebrians plants infected with a Neotyphodium endophyte. Plant Growth Regul 60:91–97

    CAS  Google Scholar 

  • Zhang SS, Kang HM, Yang WZ, Xiang ZY (2016) Effects of arbuscular mycorrhizal fungi on growth and photosynthetic characteristics of Nyssa yunnanensis seedlings under drought stress. Acta Ecol Sin 36:6850–6862

    Google Scholar 

  • Zhang W, Card SD, Mace WJ, Christensen MJ, Mcgill CR, Matthew C (2017) Defining the pathways of symbiotic Epichloë colonization in grass embryos with confocal microscopy. Mycologia 109:153–161

    PubMed  CAS  Google Scholar 

  • Zhou Y, Li X, Qin J, Liu H, Chen W, Niu Y, Ren AZ, Gao YB (2016) Effects of simultaneous infections of endophytic fungi and arbuscular mycorrhizal fungi on the growth of their shared host grass Achnatherum sibiricum under varying N and P supply. Fungal Ecol 20:56–65

    Google Scholar 

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Acknowledgements

This research was supported by the China Agriculture Research System (CARS-22 Green Manure).

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Authors and Affiliations

  1. State Key Laboratory of Grassland Agro-ecosystems, Lanzhou University, Lanzhou, 730020, China

    Fang Li, Jie Deng, Clement Nzabanita, Yanzhong Li & Tingyu Duan

  2. Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs, Lanzhou University, Lanzhou, 730020, China

    Fang Li, Jie Deng, Clement Nzabanita, Yanzhong Li & Tingyu Duan

  3. College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou, 730020, China

    Fang Li, Jie Deng, Clement Nzabanita, Yanzhong Li & Tingyu Duan

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  1. Fang Li
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Supplementary Fig S1

Shoot height (a) and tiller number (b) of perennial ryegrass with (E+) and without (E-) Epichloë and colonized either with (AMF) and without (NM) AMF at 70%, 50%, and 30% SWC before harvested. Means ± SEM of four replicates are shown. (DOCX 102 kb)

Supplementary Fig S2

Shoot dry weight (a) and root dry weight (b) of perennial ryegrass with (E+) and without (E-) Epichloë and colonized with either (AMF) and without (NM) AMF at 70%, 50%, and 30% SWC at harvest. Means ± SEM of four replicates are shown. Bars with the same lowercase letter do not differ significant for AMF × soil water content interaction at P ≤ 0.05 by Tukey’s HSD. (DOCX 98 kb)

Supplementary Fig S3

Shoot P content (a) and root P content (b) of perennial ryegrass with (E+) and without (E-) Epichloë and colonized either with (AMF) and without (NM) AMF at 70%, 50%, and 30% SWC at harvest. Means ± SEM of four replicates are shown. Bars with the same lowercase letter do not differ significant for AMF × Epichloë × soil water content interaction at P ≤ 0.05 by Tukey’s HSD. (DOCX 94 kb)

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Li, F., Deng, J., Nzabanita, C. et al. Growth and physiological responses of perennial ryegrass to an AMF and an Epichloë endophyte under different soil water contents. Symbiosis 79, 151–161 (2019). https://doi.org/10.1007/s13199-019-00633-3

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