Skip to main content
Log in

Epichloë endophyte infection enhances the tolerance of Stipa purpurea to parasitic stress through the regulation of antioxidants and phytohormones

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Aims

Root hemiparasite infection is considered a potential biotic stress that affects the growth of cool-season grasses, and the damage caused by a hemiparasitic plant to host grasses is largely determined by the density of the hemiparasite. Epichloë endophytes have been shown to be mutualistic symbionts of cool-season grasses under most environmental conditions. Although cool-season grasses can be host to both Epichloë endophytes and hemiparasites, little attention has been given to how Epichloë infection regulates the physiological and phytohormone responses of host grasses under parasitic stress.

Methods

We performed a pot experiment with an endophyte-infected and endophyte-free host grass, Stipa purpurea, and a facultative hemiparasite, Pedicularis kansuensis. The grasses were grown together under different densities of the hemiparasite (control, one or three plants per pot). Grass growth as well as physiological and phytohormone parameters were determined following parasitic stress.

Results

Successful parasitism increased the biomass and survival of P. kansuensis while suppressing the growth of S. purpurea. The reduction in the growth of S. purpurea was dependent on the density of P. kansuensis. Epichloë infection of S. purpurea improved the tolerance of this grass to parasitic stress, resulting in more tillers, longer roots, higher shoot and root biomasses and a higher root:shoot ratio compared with those of the endophyte-free grass. Interestingly, Epichloë infection increased proline, indole-3-acetic acid and abscisic acid production as well as superoxide dismutase, peroxidase and catalase activities and reduced the malondialdehyde content, root vitality and zeatin riboside content under root hemiparasitic stress.

Conclusions

Our results demonstrate that the growth of the host grass was severely reduced under parasitic stress; the negative effects of hemiparasitic plants on the host grass were largely determined by the density of the hemiparasite. The findings also indicate that the Epichloë endophytes greatly alleviated the damage caused by the hemiparasite to the cool-season grass by producing more antioxidant enzymes, enhancing root viability, synthesizing certain phytohormones and suppressing haustorium formation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

E + :

Endophyte infected

E − :

Endophyte free

NH:

Without host plant

MDA:

Malondialdehyde

SOD:

Superoxide dismutase

CAT:

Catalase

POD:

Peroxidase

TTC:

Triphenyltetrazolium chloride

IAA:

Indole-3-acetic acid

ABA:

Abscisic acid

ZR:

Zeatin riboside

HPLC–MS/MS:

High-performance liquid chromatography tandem mass spectrometry

MRM:

Multiple reaction monitoring

ANOVA:

Analysis of variance

ROS:

Reactive oxygen species

References

  • Bailly C, Benamar A, Corbineau F, Come D (1996) Changes in malondialdehyde content and in superoxide dismutase, catalase and glutathione reductase activities in sunflower seeds as related to deterioration during accelerated aging. Physiol Plantarum 97:104–110

    Article  CAS  Google Scholar 

  • Bao GS, Li CJ (2015) Isolation and identification endophytes infecting Stipa purpurea, a dominant grass in meadows of the Qinghai-Tibet Plateau. Acta Pratacul Sin 25:32–42 (in Chinese with English abstract)

    Google Scholar 

  • Bao GS, Saikkonen K, Wang HS, Zhou LY, Chen SH, Li CJ, Nan Z (2015a) Does endophyte symbiosis resist allelopathic effects of an invasive plant in degraded grassland? Fungal Ecol 17:114–125

    Article  Google Scholar 

  • Bao GS, Suetsugu K, Wang HS, Yao X, Liu L, Ou J, Li CJ (2015b) Effects of the hemiparasitic plant Pedicularis kansuensis on plant community structure in a degraded grassland. Ecol Res 30:507–515

    Article  Google Scholar 

  • Bao GS, Zhang XX, Li XZ, Wei XX, Li CJ (2015c) Incidence and isolation of endophyte in native grasses of Qinghai Plateau. Pratacultural Science 32:1997–2007 (in Chinese with English abstract)

    Google Scholar 

  • Bao GS, Song ML, Wang YQ, Saikkonen K, Li CJ (2020) Does Epichloё endophyte enhance host tolerance to root hemiparasite? Miciob Ecol. https://doi.org/10.1007/s00248-020-01496-8

    Article  Google Scholar 

  • Bar-Nun N, Sachs T, Mayer AM (2007) A role for IAA in the infection of Arabidopsis thaliana by Orobanche aegyptiaca. Ann Bot-London 101:261–265

    Article  CAS  Google Scholar 

  • Bardgett RD, Smith RS, Shiel RS, Peacock S, Simkin JM, Quirk H, Hobbs PJ (2006) Parasitic plants indirectly regulate below-ground properties in grassland ecosystems. Nature 439:969–972

    Article  CAS  PubMed  Google Scholar 

  • Bastías DA, Martínez-Ghersa MA, Ballaré CL, Gundel PE (2017) Epichloë Fungal endophytes and plant defenses: not just alkaloids. Trends Plant Sci 22:939–948

    Article  PubMed  CAS  Google Scholar 

  • Bastías DA, Martínez-Ghersa MA, Newman JA, Card SD, Mace WJ, Gundel PE (2018a) Jasmonic acid regulation of the anti-herbivory mechanism conferred by fungal endophytes in grasses. J Ecol 106:2365–2379

    Article  CAS  Google Scholar 

  • Bastías DA, Martínez-Ghersa MA, Newman JA, Card SD, Mace WJ, Gundel PE (2018b) The plant hormone salicylic acid interacts with the mechanism of anti-herbivory conferred by fungal endophytes in grasses. Plant Cell Environ 41:395–405

    Article  PubMed  CAS  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  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

    Article  CAS  PubMed  Google Scholar 

  • Bernhard RH, Jensen JE, Andreasen C (1998) Prediction of yield loss caused by Orobanche spp. in carrot and pea crops based on the soil seedbank. Weed Res 38:191–197

    Article  Google Scholar 

  • Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161:559–566

    Article  CAS  PubMed  Google Scholar 

  • Bonfante P, Genre A (2010) Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis. Nat Commun 1:48

    Article  PubMed  CAS  Google Scholar 

  • Cameron DD, Coats AM, Seel WE (2006) Differential resistance among host and non-host species underlies the variable success of the hemi-parasitic plant Rhinanthus minor. Ann Bot-London 98:1289–1299

    Article  Google Scholar 

  • Cameron DD, Geniez J-M, Seel WE, Irving LJ (2008) Suppression of host photosynthesis by the parasitic plant Rhinanthus minor. Ann Bot-London 101:573–578

    Article  CAS  Google Scholar 

  • Chance B, Maehly AC (1955) Assay of catalases and peroxidases. Methods Enzymol 2:764–775

    Article  Google Scholar 

  • Chen TX, Johnson R, Chen SH, Lv H, Zhou JL, Li CJ (2018) Infection by the fungal endophyte Epichloë bromicola enhances the tolerance of wild barley (Hordeum brevisubulatum) to salt and alkali stresses. Plant Soil 428:353–370

    Article  CAS  Google Scholar 

  • Chen TX, White JF, Li CJ (2021) Fungal endophyte Epichloë bromicola infection regulates anatomical changes to account for salt stress tolerance in wild barley (Hordeum brevisubulatum). Plant Soil. https://doi.org/10.1007/s11104-021-04828-w

    Article  Google Scholar 

  • Cheng X, Floková K, Bouwmeester H, Ruyter-Spira C (2017) The role of endogenous strigolactones and their interaction with ABA during the infection process of the parasitic weed phelipanche ramosa in tomato plants. Front Plant Sci 8:392

    Article  PubMed  PubMed Central  Google Scholar 

  • Clay K (1988) Fungal endophytes of grasses: a defensive mutualism between plants and fungi. Ecology 69:10–16

    Article  Google Scholar 

  • Clay K (1990) fungal endophytes of grasses. Annu Rev Ecol Syst 21:275–297

    Article  Google Scholar 

  • Clemensson-Lindell A (1994) Triphenyltetrazolium chloride as an indicator of fine-root vitality and environmental stress in coniferous forest stands: applications and limitations. Plant Soil 159:297–300

    Article  CAS  Google Scholar 

  • Davey JE, van Staden J (1976) Cytokinin translocation: changes in zeatin and zeatin-riboside levels in the root exudate of tomato plants during their development. Planta 130:69–72

    Article  CAS  PubMed  Google Scholar 

  • De Battista JP, Bacon CW, Severson R, Plattner RD, Bouton JH (1990) Indole acetic acid production by the fungal endophyte of tall fescue. Agron J 82:878–880

    Article  Google Scholar 

  • Drennan DSH, EI Hiweris SO (1979) Changes in growth regulating substances in Sorghum vulgare infected by Striga hermonthica. In: Musselman LJ, Worsham AD, Eplee RE (eds) Proceedings of the second symposium of parasitic weeds. North Carolina State University, Raleigh

  • Dupont PY, Eaton CJ, Wargent JJ, Fechtner S, Solomon P, Schmid J, Day RC, Scott B, Cox MP (2015) Fungal endophyte infection of ryegrass reprograms host metabolism and alters development. New Phytol 208:1227–1240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eaton CJ, Cox MP, Scott B (2011) What triggers grass endophytes to switch from mutualism to pathogenism? Plant Sci 180:190–195

    Article  CAS  PubMed  Google Scholar 

  • Fer A, Russo N, Simier P, Arnaud M-C, Thalouarn P (1994) Physiological changes in a root hemiparasitic angiosperm, Thesium humile (Santalaceae), before and after attachment to the host plant (Triticum vulgare). J Plant Physiol 143:704–710

    Article  CAS  Google Scholar 

  • Fuchs B, Krauss J (2019) Can Epichloë endophytes enhance direct and indirect plant defence? Fungal Ecol 38:98–103

    Article  Google Scholar 

  • Gibson CC, Watkinson AR (1992) The role of the hemiparasitic annual Rhinanthus minor in determining grassland community structure. Oecologia 89:62–68

    Article  CAS  PubMed  Google Scholar 

  • Goldwasser Y, Hershenhorn J, Plakhine D, Kleifeld Y, Rubin B (1999) Biochemical factors involved in vetch resistance to Orobanche aegyptiaca. Physiol Mol Plant Pathol 54:87–96

    Article  CAS  Google Scholar 

  • Gundel PE, Martínez-Ghersa MA, Ghersa CM (2012) Threshold modelling Lolium multiflorum seed germination: effects of Neotyphodium endophyte infection and storage environment. Seed Sci Technol 40:51–62

    Article  Google Scholar 

  • Hamilton CE, Gundel PE, Helander M, Saikkonen K (2012) Endophytic mediation of reactive oxygen species and antioxidant activity in plants: a review. Fungal Divers 54:1–10

    Article  Google Scholar 

  • Heer N, Klimmek F, Zwahlen C, Fischer M, Hölzel N, Klaus VH, Kleinebecker T, Prati D, Boch S (2018) Hemiparasite-density effects on grassland plant diversity, composition and biomass. Perspect Plant Ecol 32:22–29

    Article  Google Scholar 

  • Hegenauer V, Körner M, Albert M (2017) Plants under stress by parasitic plants. Curr Opin Plant Biol 38:34–41

    Article  PubMed  Google Scholar 

  • Hibberd JM, Quick WP, Press MC, Scholes JD (1996) The influence of the parasitic angiosperm Striga gesnerioides on the growth and photosynthesis of its host, Vigna unguiculata. J Exp Bot 47:507–512

    Article  CAS  Google Scholar 

  • Jiang F, Jeschke WD, Hartung W (2003) Water flows in the parasitic association Rhinanthus minor/Hordeum vulgare. J Exp Bot 54:1985–1993

    Article  CAS  PubMed  Google Scholar 

  • Jiang F, Jeschke WD, Hartung W (2004) Abscisic acid (ABA) flows from Hordeum vulgare to the hemiparasite Rhinanthus minor and the influence of infection on host and parasite abscisic acid relations. J Exp Bot 55:2323–2329

    Article  CAS  PubMed  Google Scholar 

  • Jiang F, Veselova S, Veselov D, Kudoyarova G, Jeschke WD, Hartung W (2005) Cytokinin flows from Hordeum vulgare to the hemiparasite Rhinanthus minor and the influence of infection on host and parasite cytokinins relations. Funct Plant Biol 32:619–629

    Article  CAS  PubMed  Google Scholar 

  • Jiang F, Jeschke WD, Hartung W, Cameron DD (2010) Interactions between Rhinanthus minor and its hosts: a review of water, mineral nutrient and hormone flows and exchanges in the hemiparasitic association. Folia Geobot 45:369–385

    Article  Google Scholar 

  • Joel DM, Gressel J, Musselman LJ (eds) (2015) Parasitic Orobanchaceae: parasitic mechanisms and control strategies. Springer-Verlag, Berlin Heidelberg

    Google Scholar 

  • Laitinen RK, Hellström KO, Wäli PR (2016) Context-dependent outcomes of subarctic grass-endophyte symbiosis. Fungal Ecol 23:66–74

    Article  Google Scholar 

  • Lam CK, Belanger FC, WhiteJr JF, Daie J (1995) Invertase activity in Epichloë/Acremonium fungal endophytes and its possible role in choke disease. Mycol Res 99(7):867–873

    Article  CAS  Google Scholar 

  • Lechowski Z (1997) Stomatal response to exogenous cytokinin treatment of the hemiparasite Melampyrum arvense L. before and after attachment to the host. Biol Plantarum 39:13–21

    Article  CAS  Google Scholar 

  • Lechowski Z, Bialczyk J (1996) Cytokinins in the hemiparasite Melampyrum arvense L. before and after attachment to the host. Biol Plantarum 38:481–488

    CAS  Google Scholar 

  • Lehtonen P, Helander M, Wink M, Sporer F, Saikkonen K (2005) Transfer of endophyte-origin defensive alkaloids from a grass to a hemiparasitic plant. Ecol Lett 8:1256–1263

    Article  Google Scholar 

  • Li HS (ed) (2000) Principle and techniques of botanic, chemical and physiological experiments. Senior Education Press, Beijing (in Chinese)

    Google Scholar 

  • Li AR, Guan KY (2008) Arbuscular mycorrhizal fungi may serve as another nutrient strategy for some hemiparasitic species of Pedicularis (Orobanchaceae). Mycorrhiza 18:429–436

    Article  CAS  PubMed  Google Scholar 

  • Li CJ, Nan ZB, Paul VH, Dapprich PD, Liu Y (2004) A new Neotyphodium species symbiotic with drunken horse grass (Achnatherum inebrians) in China. Mycotaxon 90:141–147

    Google Scholar 

  • Li X, Ma YQ, Song YX, Shui JF, Li XW (2009) Effects of Cistanche deserticola parasitization on Haloxylon ammodendron seedlings protective enzyme activities and osmotic adjustment substance contents. Chin J Ecol 28:1531–1536 (in Chinese with English abstract)

    CAS  Google Scholar 

  • Li AR, Smith SE, Smith FA, Guan KY (2012) Inoculation with arbuscular mycorrhizal fungi suppresses initiation of haustoria in the root hemiparasite Pedicularis tricolor. Ann Bot-London 109:1075–1080

    Article  Google Scholar 

  • Li AR, Li YJ, Smith SE, Smith FA, Guan KY (2013) Nutrient requirements differ in two Pedicularis species in the absence of a host plant: implication for driving forces in the evolution of host preference of root hemiparasitic plants. Ann Bot-London 112:1099–1106

    Article  CAS  Google Scholar 

  • Liu WS, Dong M, Song ZP, Wei W (2009) Genetic diversity pattern of Stipa purpurea populations in the hinterland of Qinghai-Tibet Plateau. Ann Appl Biol 154:57–65

    Article  CAS  Google Scholar 

  • Markhart AH, Fiscus EL, Naylor AW, Kramer PJ (1979) Effect of abscisic acid on root hydraulic conductivity. Plant Physiol 64:611–614

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matthies D (1995a) Host-parasite relations in the root hemiparasite Melampyrum arvense. Flora 190:383–394

    Article  Google Scholar 

  • Matthies D (1995b) Parasitic and competitive interactions between the hemiparasites Rhinanthus serotinus and Odontites rubra and their host Medicago sativa. J Ecol 83:245–251

    Article  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  Google Scholar 

  • Niones JT, Takemoto D (2014) An isolate of Epichloë festucae, an endophytic fungus of temperate grasses, has growth inhibitory activity against selected grass pathogens. J Gen Plant Pathol 80:337–347

    Article  CAS  Google Scholar 

  • Peterson RK, Higley LG (eds) (2000) Biotic stress and yield loss. CRC Press, Boca Raton

    Google Scholar 

  • Phoenix GK, Press MC (2005) Linking physiological traits to impacts on community structure and function: the role of root hemiparasitic Orobanchaceae (ex-Scrophulariaceae). J Ecol 93:67–78

    Article  Google Scholar 

  • Press MC, Phoenix GK (2005) Impacts of infection by parasitic angiosperms on host photosynthesis. Plant Biol 166:737–751

    Google Scholar 

  • Reigosa MJ, Pedrol N, González L (eds) (2006) Allelopathy: a physiological process with ecological implications. Springer, Dordrecht

    Google Scholar 

  • Rodenburg J, Bastiaans L, Kropff MJ (2006) Characterization of host tolerance to Striga hermonthica. Euphytica 147:353–365

    Article  Google Scholar 

  • Rodriguez R, Redman R (2008) More than 400 million years of evolution and some plants still can’t make it on their own: plant stress tolerance via fungal symbiosis. J Exp Bot 59:1109–1114

    Article  CAS  PubMed  Google Scholar 

  • Runyon JB, Mescher MC, Felton GW, De Moraes CM (2010) Parasitism by Cuscuta pentagona sequentially induces JA and SA defence pathways in tomato. Plant Cell Environ 33:290–303

    Article  CAS  PubMed  Google Scholar 

  • Saikkonen K, Faeth SH, Helander M, Sullivan TJ (1998) Fungal endophytes: a continuum of interactions with host plants. Annu Rev Ecol Syst 29:319–343

    Article  Google Scholar 

  • Saikkonen K, Wäli P, Helander M, Faeth SH (2004) Evolution of endophyte-plant symbioses. Trends Plant Sci 9:275–280

    Article  CAS  PubMed  Google Scholar 

  • Saikkonen K, Lehtonen P, Helander M, Koricheva J, Faeth SH (2006) Model systems in ecology: dissecting the endophyte-grass literature. Trends Plant Sci 11:428–433

    Article  CAS  PubMed  Google Scholar 

  • Saikkonen K, Gundel PE, Helander M (2013) Chemical ecology mediated by fungal endophytes in grasses. J Chem Ecol 39:962–968

    Article  CAS  PubMed  Google Scholar 

  • Saikkonen K, Young CA, Helander M, Schardl CL (2016) Endophytic Epichloë species and their grass hosts: from evolution to applications. Plant Mol Biol 90:665–675

    Article  CAS  PubMed  Google Scholar 

  • Santino A, Taurino M, De Domenico S, Bonsegna S, Poltronieri P, Pastor V, Flors V (2013) Jasmonate signaling in plant development and defense response to multiple (a)biotic stresses. Plant Cell Rep 32:1085–1098

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Schmid J, Day R, Zhang NX, Dupont P-Y, Cox MP, Schardl CL, Minards N, Truglio M, Moore N, Harris DR, Zhou YF (2017) Host tissue environment directs activities of an Epichloë endophyte, while it induces systemic hormone and defense responses in its native perennial ryegrass host. Mol Plant Microbe in 30:138–149

    Article  CAS  Google Scholar 

  • Scott B, Takemoto D, Tanaka A (2007) Fungal endophyte production of reactive oxygen species is critical for maintaining the mutualistic symbiotic interaction between Epichloë festucae and perennial ryegrass. Plant Signal Behav 2:171–173

    Article  PubMed  PubMed Central  Google Scholar 

  • Scott B, Green K, Berry D (2018) The fine balance between mutualism and antagonism in the Epichloë festucae–grass symbiotic interaction. Curr Opin Plant Biol 44:32–38

    Article  PubMed  Google Scholar 

  • Shang ZH, Yang SH, Shi JJ, Wang YL, Long RJ (2013) Seed rain and its relationship with above-ground vegetation of degraded Kobresia meadows. J Plant Res 126:63–72

    Article  PubMed  Google Scholar 

  • Smith JL, De Moraes CM, Mescher MC (2009) Jasmonate- and salicylate-mediated plant defense responses to insect herbivores, pathogens and parasitic plants. Pest Manag Sci 65:497–503

    Article  CAS  PubMed  Google Scholar 

  • Song ML, Li XZ, Saikkonen K, Li CJ, Nan ZB (2015) An asexual Epichloë endophyte enhances waterlogging tolerance of Hordeum brevisubulatum. Fungal Ecol 13:44–52

    Article  Google Scholar 

  • Sui XL, Li AR, Chen Y, Guan KY, Zhuo L, Liu YY (2014) Arbuscular mycorrhizal fungi: potential biocontrol agents against the damaging root hemiparasite Pedicularis kansuensis? Mycorrhiza 24:187–195

    Article  PubMed  Google Scholar 

  • Sui XL, Huang W, Li YJ, Guan KY, Li AR (2015) Host shoot clipping depresses the growth of weedy hemiparasitic Pedicularis kansuensis. J Plant Res 128:563–572

    Article  PubMed  Google Scholar 

  • Sui XL, Zhang T, Tian YQ, Xue RJ, Li AR (2019) A neglected alliance in battles against parasitic plants: arbuscular mycorrhizal and rhizobial symbioses alleviate damage to a legume host by root hemiparasitic Pedicularis species. New Phytol 221:470–481

    Article  PubMed  Google Scholar 

  • Taylor A, Martin J, Seel WE (1996) Physiology of the parasitic association between maize and witchweed (Striga hermonthica): is ABA involved? J Exp Bot 47:1057–1065

    Article  CAS  Google Scholar 

  • Těšitel J (2016) Functional biology of parasitic plants: a review. Plant Ecol Evol 149:5–20

    Article  Google Scholar 

  • Těšitel J, Těšitelová T, Fisher JP, Lepš J, Cameron DD (2015) Integrating ecology and physiology of root-hemiparasitic interaction: interactive effects of abiotic resources shape the interplay between parasitism and autotrophy. New Phytol 205:350–360

    Article  PubMed  Google Scholar 

  • Thorogood CJ, Rumsey FJ, Hiscock SJ (2009) Host-specific races in the holoparasitic angiosperm Orobanche minor: implications for speciation in parasitic plants. Ann Bot-London 103:1005–1014

    Article  CAS  Google Scholar 

  • Tian ZP, Wang RY, Ambrose KV, Clarke BB, Belanger FC (2017) The Epichloë festucae antifungal protein has activity against the plant pathogen Sclerotinia homoeocarpa, the causal agent of dollar spot disease. Sci Rep 7:5643

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tomilov AA, Tomilova NB, Yoder JI (2004) In vitro haustorium development in roots and root cultures of the hemiparasitic plant Triphysaria versicolor. Plant Cell Tiss Org 77:257–265

    Article  Google Scholar 

  • Tomilov AA, Tomilova NB, Abdallah I, Yoder JI (2005) Localized hormone fluxes and early haustorium development in the hemiparasitic plant Triphysaria versicolourcolor. Plant Physiol 138:1469–1480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vadassery J, Ritter C, Venus Y, Camehl I, Varma A, Shahollari B, Novák O, Strnad M, Ludwig-Müller J, Oelmüller R (2008) The role of auxins and cytokinins in the mutualistic interaction between Arabidopsis and Piriformospora indica. Mol Plant Microbe in 21:1371–1383

    Article  CAS  Google Scholar 

  • Wäli PR, Helander M, Saloniemi I, Ahlholm J, Saikkonen K (2009) Variable effects of endophytic fungus on seedling establishment of fine fescues. Oecologia 159:49–57

    Article  PubMed  Google Scholar 

  • Wang XY, Qin JH, Chen W, Zhou Y, Ren AZ, Gao YB (2016) Pathogen resistant advantage of endophyte-infected over endophyte-free Leymus chinensis is strengthened by pre-drought treatment. Eur J Plant Pathol 144:477–486

    Article  CAS  Google Scholar 

  • Wang JJ, Zhou YP, Lin WH, Li MM, Wang MN, Wang ZG, Kuang Y, Tian P (2017) Effect of an Epichloё endophyte on adaptability to water stress in Festuca sinensis. Fungal Ecol 30:39–47

    Article  Google Scholar 

  • Wang JF, Hou WP, Christensen MJ, Li XZ, Xia C, Li CJ, Nan ZB (2020) Role of Epichloë endophytes in improving host grass resistance ability and soil properties. J Agric Food Chem 68:6944–6955

    Article  CAS  PubMed  Google Scholar 

  • Watling JR, Press MC (2001) Impacts of infection by parasitic angiosperms on host photosynthesis. Plant Biol 3:244–250

    Article  CAS  Google Scholar 

  • Westerman PR, Hemerik L, van der Werf W, Stomph TJ (2018) Density-independent reproductive success of the hemiparasitic plant Striga hermonthica, despite positive and negative density-dependent phases. Ann Appl Biol 172:74–87

    Article  CAS  Google Scholar 

  • Westwood JH, Yoder JI, Timko MP, dePamphilis CW (2010) The evolution of parasitism in plants. Trends Plant Sci 15(4):227–235

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • You CC, Zhu HL, Xu BB, Huang WX, Wang SH, Ding YF, Liu ZH, Li GH, Chen L, Ding CQ (2016) Effect of removing superior spikelets on grain filling of inferior spikelets in rice. Front Plant Sci 7:1161

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang XX, Li CJ, Nan ZB (2010) Effects of cadmium stress on growth and anti-oxidative systems in Achnatherum inebrians symbiotic with Neotyphodium gansuense. J Hazard Mater 175:703–709

    Article  CAS  PubMed  Google Scholar 

  • Zhou LY, Li CJ, Zhang XX, Johnson R, Bao GS, Yao X, Chai Q (2015) Effects of cold shocked Epichloë infected Festuca sinensis on ergot alkaloid accumulation. Fungal Ecol 14:99–104

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank Professor Hongsheng Wang and Professor Wenhui Liu for their constructive comments on the manuscript. This research was financially supported by the Key Laboratory of Superior Forage Germplasm on the Qinghai-Tibetan Plateau (2020-ZJ-Y03), the Natural Science Foundation of China (Grants 32060398 and 31660690 and 31700098) and the Program for Qinghai Province Thousand Talent Innovative Plan.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gensheng Bao.

Additional information

Reponsible Editor: Birgit Mitter.

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bao, G., Song, M., Wang, Y. et al. Epichloë endophyte infection enhances the tolerance of Stipa purpurea to parasitic stress through the regulation of antioxidants and phytohormones. Plant Soil 466, 239–256 (2021). https://doi.org/10.1007/s11104-021-05046-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-021-05046-0

Keywords

Navigation