NaCl stress modifies the concentrations of endophytic fungal hyphal and peramine in Hordeum brevisubulatum seedlings
Taixiang Chen A , Wayne R. Simpson
B , Zhibiao Nan A and Chunjie Li A *
+ Author Affiliations
- Author Affiliations
A State Key Laboratory of Grassland Agro-ecosystems; Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs; Engineering Research Center of Grassland Industry, Ministry of Education; Gansu Tech Innovation Centre of Western China Grassland Industry; Center for Grassland Microbiome, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730020, China.
B AgResearch, Grasslands Research Centre, Palmerston North 4442, New Zealand.
Crop & Pasture Science 73(3) 214-221 https://doi.org/10.1071/CP21343
Submitted: 30 March 2021 Accepted: 19 September 2021 Published: 10 February 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Context: Infecting grasses with an Epichloë endophyte contribute significantly to host plant salt tolerance. The Epichloë endophyte alkaloid peramine is primarily responsible for feeding deterrence against some herbivorous insects. Infection by an Epichloë is required for peramine production in the host grass. Limited information is available regarding the effects of salinity stress on Epichloë endophyte colonisation and associated production of peramine metabolites.
Aims and methods: In this study, we determined the effects of NaCl stress on the concentration of endophytic hyphae and peramine in wild barley (Hordeum brevisubulatum (Trin.) Link) seedlings infected with Epichloë bromicola.
Key results: Seedings dry weight at 4 weeks declined from 7.05 to 4.27 g/plant over the range, 0–300 mM NaCl. The hyphal concentration, as well as the peramine concentration, increased in response to high NaCl concentrations, hyphae and peramine concentration at 4 weeks increased from 13.29 to 264.60 copies/ng gDNA and from 26.75 to 43.19 μg/g DW, respectively. Peramine concentration was positively correlated with the concentration of hyphae (R2 = 0.4012, P < 0.001).
Conclusions and implications: It seems that peramine concentration was mostly explained by the in-planta variation in endophyte hyphae concentration in wild barley infected with Epichloë species under highly saline conditions.
Keywords: alkaloid, endophyte, Epichloë bromicola, hyphal concentration, Hordeum brevisubulatum, peramine, salt stress, wild barley.
References
Ball OJ, Christensen MJ, Prestidge RA (1994) Effect of selected isolates of Acremonium endophyte on adult black beetle (Heteronychus arator) feeding. In ‘Proceedings of the 47th New Zealand Plant Protection Conference, 8–10 January 1994, Rotorua, New Zealand’. (Ed. A Popay) pp. 227–231. (New Zealand Plant Protection Society: Rotorua, New Zealand)Ball OJ, Prestidge RA, Sprosen JM (1995) Interrelationships between Acremonium lolii, peramine, and lolitrem B in perennial ryegrass. Applied and Environmental Microbiology 61, 1527–1533.
| Interrelationships between Acremonium lolii, peramine, and lolitrem B in perennial ryegrass.Crossref | GoogleScholarGoogle Scholar | 16535001PubMed |
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 and Soil 428, 353–370.
| Infection by the fungal endophyte Epichloë bromicola enhances the tolerance of wild barley (Hordeum brevisubulatum) to salt and alkali stresses.Crossref | GoogleScholarGoogle Scholar |
Chen TX, Simpson WR, Song QY, Chen SH, Li CJ, Ahmad RZ (2019) Identification of Epichloë endophytes associated with wild barley (Hordeum brevisubulatum) and characterisation of their alkaloid biosynthesis. New Zealand Journal of Agricultural Research 62, 131–149.
| Identification of Epichloë endophytes associated with wild barley (Hordeum brevisubulatum) and characterisation of their alkaloid biosynthesis.Crossref | GoogleScholarGoogle Scholar |
Christensen MJ, Bennett RJ, Ansari HA, Koga H, Johnson RD, Bryan GT, Simpson WR, Koolaard JP, Nickless EM, Voisey CR (2008) Epichloë endophytes grow by intercalary hyphal extension in elongating grass leaves. Fungal Genetics and Biology 45, 84–93.
| Epichloë endophytes grow by intercalary hyphal extension in elongating grass leaves.Crossref | GoogleScholarGoogle Scholar | 17919950PubMed |
Easton HS, Latch GCM, Tapper BA, Ball OJ-P (2002) Ryegrass host genetic control of concentrations of endophyte-derived alkaloids. Crop Science 42, 51–57.
| Ryegrass host genetic control of concentrations of endophyte-derived alkaloids.Crossref | GoogleScholarGoogle Scholar | 11756253PubMed |
Faeth SH, Bush LP, Sullivan TJ (2002) Peramine alkaloid variation in Neotyphodium-infected Arizona fescue: effects of endophyte and host genotype and environment. Journal of Chemical Ecology 28, 1511–1526.
| Peramine alkaloid variation in Neotyphodium-infected Arizona fescue: effects of endophyte and host genotype and environment.Crossref | GoogleScholarGoogle Scholar | 12371807PubMed |
Faville MJ, Briggs L, Cao M, Koulman A, Zulfi Jahufer MZ, Koolaard J, Hume DE (2015) A QTL analysis of host plant effects on fungal endophyte biomass and alkaloid expression in perennial ryegrass. Molecular Breeding 35, 161
| A QTL analysis of host plant effects on fungal endophyte biomass and alkaloid expression in perennial ryegrass.Crossref | GoogleScholarGoogle Scholar | 26203296PubMed |
Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytologist 179, 945–963.
| Salinity tolerance in halophytes.Crossref | GoogleScholarGoogle Scholar |
Fuchs B, Krischke M, Mueller MJ, Krauss J, Biere A (2017) Herbivore-specific induction of defence metabolites in a grass–endophyte association. Functional Ecology 31, 318–324.
| Herbivore-specific induction of defence metabolites in a grass–endophyte association.Crossref | GoogleScholarGoogle Scholar |
Graff P, Gundel PE, Salvat A, Cristos D, Chaneton EJ, Emery N (2020) Protection offered by leaf fungal endophytes to an invasive species against native herbivores depends on soil nutrients. Journal of Ecology 108, 1592–1604.
| Protection offered by leaf fungal endophytes to an invasive species against native herbivores depends on soil nutrients.Crossref | GoogleScholarGoogle Scholar |
Gundel PE, Seal CE, Biganzoli F, Molina-Montenegro MA, Vázquez-de-Aldana BR, Zabalgogeazcoa I, Bush LP, Martínez-Ghersa MA, Ghersa CM (2018) Occurrence of alkaloids in grass seeds symbiotic with vertically-transmitted Epichloë fungal endophytes and its relationship with antioxidants. Frontiers in Ecology and Evolution 6, 211
| Occurrence of alkaloids in grass seeds symbiotic with vertically-transmitted Epichloë fungal endophytes and its relationship with antioxidants.Crossref | GoogleScholarGoogle Scholar |
Helander M, Phillips T, Faeth SH, Bush LP, McCulley R, Saloniemi I, Saikkonen K (2016) Alkaloid quantities in endophyte-infected tall fescue are affected by the plant-fungus combination and environment. Journal of Chemical Ecology 42, 118–126.
| Alkaloid quantities in endophyte-infected tall fescue are affected by the plant-fungus combination and environment.Crossref | GoogleScholarGoogle Scholar | 26815170PubMed |
Hettiarachchige IK, Elkins AC, Reddy P, Mann RC, Guthridge KM, Sawbridge TI, Forster JW, Spangenberg GC (2019) Genetic modification of asexual Epichloë endophytes with the perA gene for peramine biosynthesis. Molecular Genetics and Genomics 294, 315–328.
| Genetic modification of asexual Epichloë endophytes with the perA gene for peramine biosynthesis.Crossref | GoogleScholarGoogle Scholar | 30443676PubMed |
Hewitt KG, Mace WJ, McKenzie CM, Matthew C, Popay AJ (2020) Fungal alkaloid occurrence in endophyte-infected perennial ryegrass during seedling establishment. Journal of Chemical Ecology 46, 410–421.
| Fungal alkaloid occurrence in endophyte-infected perennial ryegrass during seedling establishment.Crossref | GoogleScholarGoogle Scholar | 32125583PubMed |
Kuang Y (2016) Characteristics of Epichloë endophyte-festuca sinensis symbiote. Master’s Dissertation, Lanzhou University, Lanzhou, Gansu, China.
Mahmood T, Gergerich RC, Milus EA, West CP, Darcy CJ (1993) Barley yellow dwarf viruses in wheat, endophyte-infected and endophyte-free tall fescue, and other hosts in Arkansas. Plant Disease 77, 225–228.
| Barley yellow dwarf viruses in wheat, endophyte-infected and endophyte-free tall fescue, and other hosts in Arkansas.Crossref | GoogleScholarGoogle Scholar |
Malinowski DP, Belesky DP (2000) Adaptations of endophyte-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Science 40, 923–940.
| Adaptations of endophyte-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance.Crossref | GoogleScholarGoogle Scholar |
Moon CD, Miles CO, Järlfors U, Schardl CL (2002) The evolutionary origins of three new Neotyphodium endophyte species from grasses indigenous to the Southern Hemisphere. Mycologia 94, 694–711.
| The evolutionary origins of three new Neotyphodium endophyte species from grasses indigenous to the Southern Hemisphere.Crossref | GoogleScholarGoogle Scholar | 21156542PubMed |
Nagabhyru P, Dinkins RD, Wood CL, Bacon CW, Schardl CL (2013) Tall fescue endophyte effects on tolerance to water-deficit stress. BMC Plant Biology 13, 127
| Tall fescue endophyte effects on tolerance to water-deficit stress.Crossref | GoogleScholarGoogle Scholar | 24015904PubMed |
Popay AJ, Wyatt RT (1995) Resistance to argentine stem weevil in perennial ryegrass infected with endophytes producing different alkaloids. In ‘Proceedings of the 48th New Zealand Plant Protection Conference, 8–10 August 1995, Angus Inn, Hastings, New Zealand’. (Ed. AJ Popay) pp. 229–236. (New Zealand Plant Protection Society: Rotorua, New Zealand)
Rasmussen S, Parsons AJ, Bassett S, Christensen MJ, Hume DE, Johnson LJ, Johnson RD, Simpson WR, Stacke C, Voisey CR, Xue H, Newman JA (2007) High nitrogen supply and carbohydrate content reduce fungal endophyte and alkaloid concentration in Lolium perenne. New Phytologist 173, 787–797.
| High nitrogen supply and carbohydrate content reduce fungal endophyte and alkaloid concentration in Lolium perenne.Crossref | GoogleScholarGoogle Scholar |
Rowan DD, Dymock JJ, Brimble MA (1990) Effect of fungal metabolite peramine and analogs on feeding and development of argentine stem weevil (Listronotus bonariensis). Journal of Chemical Ecology 16, 1683–1695.
| Effect of fungal metabolite peramine and analogs on feeding and development of argentine stem weevil (Listronotus bonariensis).Crossref | GoogleScholarGoogle Scholar | 24263837PubMed |
Roy SJ, Negrão S, Tester M (2014) Salt resistant crop plants. Current Opinion in Biotechnology 26, 115–124.
| Salt resistant crop plants.Crossref | GoogleScholarGoogle Scholar | 24679267PubMed |
Ryan GD, Rasmussen S, Xue H, Parsons AJ, Newman JA (2014) Metabolite analysis of the effects of elevated CO2 and nitrogen fertilization on the association between tall fescue (Schedonorus arundinaceus) and its fungal symbiont Neotyphodium coenophialum. Plant, Cell Environment 37, 204–212.
| Metabolite analysis of the effects of elevated CO2 and nitrogen fertilization on the association between tall fescue (Schedonorus arundinaceus) and its fungal symbiont Neotyphodium coenophialum.Crossref | GoogleScholarGoogle Scholar | 23742115PubMed |
Schardl CL, Leuchtmann A, Spiering MJ (2004) Symbioses of grasses with seedborne fungal endophytes. Annual Review of Plant Biology 55, 315–340.
| Symbioses of grasses with seedborne fungal endophytes.Crossref | GoogleScholarGoogle Scholar | 15377223PubMed |
Schardl CL, Young CA, Faulkner JR, Florea S, Pan J (2012) Chemotypic diversity of epichloae, fungal symbionts of grasses. Fungal Ecology 5, 331–344.
| Chemotypic diversity of epichloae, fungal symbionts of grasses.Crossref | GoogleScholarGoogle Scholar |
Song ML, Chai Q, Li XZ, Yao X, Li CJ, Christensen MJ, Nan ZB (2015) An asexual Epichloë endophyte modifies the nutrient stoichiometry of wild barley (Hordeum brevisubulatum) under salt stress. Plant and Soil 387, 153–165.
| An asexual Epichloë endophyte modifies the nutrient stoichiometry of wild barley (Hordeum brevisubulatum) under salt stress.Crossref | GoogleScholarGoogle Scholar |
Spiering MJ, Elizabeth D, Tapper BA, Jan S, Lane GA (2002) Simplified extraction of ergovaline and peramine for analysis of tissue distribution in endophyte-infected grass tillers. Journal of Agricultural and Food Chemistry 50, 5856–5862.
| Simplified extraction of ergovaline and peramine for analysis of tissue distribution in endophyte-infected grass tillers.Crossref | GoogleScholarGoogle Scholar | 12358450PubMed |
Spiering MJ, Lane GA, Christensen MJ, Schmid J (2005) Distribution of the fungal endophyte Neotyphodium lolii is not a major determinant of the distribution of fungal alkaloids in Lolium perenne plants. Phytochemistry 66, 195–202.
| Distribution of the fungal endophyte Neotyphodium lolii is not a major determinant of the distribution of fungal alkaloids in Lolium perenne plants.Crossref | GoogleScholarGoogle Scholar | 15652576PubMed |
Vázquez-de-Aldana BR, García-Ciudad A, García-Criado B, Vicente-Tavera S, Zabalgogeazcoa I (2013) Fungal endophyte (Epichloë festucae) alters the nutrient content of Festuca rubra regardless of water availability. PLoS One 8, e84539
| Fungal endophyte (Epichloë festucae) alters the nutrient content of Festuca rubra regardless of water availability.Crossref | GoogleScholarGoogle Scholar | 24367672PubMed |
Wang CM, Xia ZR, Wu GQ, Yuan HJ, Wang XR, Li JH, Tian FP, Zhang Q, Zhu XQ, He JJ, Kumar T, Wang XL, Zhang JL (2016) The coordinated regulation of Na+ and K+ in Hordeum brevisubulatum responding to time of salt stress. Plant Science 252, 358–366.
| The coordinated regulation of Na+ and K+ in Hordeum brevisubulatum responding to time of salt stress.Crossref | GoogleScholarGoogle Scholar | 27717472PubMed |
Zhang YL, Li TY, Ma YS, Wu DR, Liu J, Wu DB (2015) Study on adaptability of different alfalfa varieties to saline-alkali soil in Hexi Corridor, Gansu Province. Grassland and Turf 35, 32–37.
