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Plant and Soil

, Volume 424, Issue 1–2, pp 555–571 | Cite as

Effect of Epichloë gansuensis endophyte and transgenerational effects on the water use efficiency, nutrient and biomass accumulation of Achnatherum inebrians under soil water deficit

  • Chao Xia
  • Michael J. Christensen
  • Xingxu Zhang
  • Zhibiao Nan
Regular Article

Abstract

Background and aims

This study explored the effects of Epichloë gansuensis endophyte on water use efficiency (WUE), nutrient content and biomass accumulation of Achnatherum inebrians (drunken horse grass, DHG) under varying water availability. It also examined possible transgenerational effects (TGE) on above indicators.

Methods

DHG with (EI) and without endophyte (EF), from seed of plants of the same seed-line that had been grown in Yuzhong (YZ-D, relatively dry) and Xiahe (XH-W, relatively wet), were grown under limited water conditions (LWC). Plant height, leaf number and chlorophyll content were monitored dynamically. After 10 weeks, the biomass, photosynthetic indexes and C, N, P content of plants was determined.

Results

The endophyte increased plant height and chlorophyll content, but decreased plant leaf number, and the CO2 concentration, while increasing other photosynthetic indexes. The biomass, N and P content were higher in EI than EF plants of the YZ-D DHG, but not the C content and root weight. However, there were almost no significant affects on these factors between EI and EF plants of the XH-W DHG.

Conclusions

The endophyte enhanced WUE and maintained the growth of plants under LWC by improving photosynthetic efficiency and promoting nutrient absorption. However, TGE also affected this process.

Keywords

Epichloid endophyte Drought tolerance Environment-linked plant adaptation Water use efficiency 

Notes

Acknowledgements

We wish to thank Professor Hong Zhang of Texas Tech University for providing related literatures, Dr. Wei Tang and Dr. Rui Li for sharing their meteorological data, Dr. Hui Song of Shandong Academy of Agricultural Science, Jinan, China for his benefit suggestions and the anonymous reviewers for reviewing the manuscript. This research was financially supported by the National Basic Research Program of China (2014CB138702), the National Nature Science Foundation of China (31402132 and 31772665), and the Fundamental Research Funds for the Central Universities (lzujbky-2016-12; lzujbky-2016-177).

Supplementary material

11104_2018_3561_MOESM1_ESM.docx (13 kb)
Supplementary Table 1 (DOCX 12 kb)
11104_2018_3561_Fig9_ESM.gif (176 kb)
Supplementary Fig. 1 The relationship among the traits measured in the present study (GIF 175 kb)
11104_2018_3561_MOESM2_ESM.tiff (7.9 mb)
High Resolution (TIFF 8039 kb)

References

  1. Arrieta AM, Iannone LJ, Scervino JM, Vignale MV, Novas MV (2015) A foliar endophyte increases the diversity of phosphorus-solubilizing rhizospheric fungi and mycorrhizal colonization in the wild grass Bromus auleticus. Fungal Ecol 17:146–154CrossRefGoogle Scholar
  2. Bacon CW (1993) Abiotic stress tolerances (moisture, nutrients) and photosynthesis in endophyte-infected tall fescue. Agric Ecosyst Environ 44:123–141CrossRefGoogle Scholar
  3. Bastias DA, Martinez-Ghersa MA, Ballaré CL, Gundel PE (2017) Epichloë fungal endophytes and plant defenses: not just alkaloids. Trends Plant Sci 22(11):939–948CrossRefPubMedGoogle Scholar
  4. Berman-Frank I, Dubinsky Z (1999) Balanced growth in aquatic plants: myth or reality? Phytoplankton use the imbalance between carbon assimilation and biomass production to their strategic advantage. Bioscience 49(1):29–37CrossRefGoogle Scholar
  5. Blum A (2009) Effective use of water (EUW) and not water-use efficiency (WUE) is the target of crop yield improvement under drought stress. Field Crop Res 112(2–3):119–123CrossRefGoogle Scholar
  6. Brundrett MC (2002) Coevolution of roots and mycorrhizas of land plants. New Phytol 154(2):275–304CrossRefGoogle Scholar
  7. Centritto M, Lauteri M, Monteverdi MC, Serraj R, Flexas J, Loreto F, Niinemets U, Sharkey T (2009) Leaf gas exchange, carbon isotope discrimination, and grain yield in contrasting rice genotypes subjected to water deficits during the reproductive stage. J Exp Bot 60(8):2325–2339CrossRefPubMedGoogle Scholar
  8. Chen L, Li X, Swoboda GA, Young CA, Sugawara K, Leuchtmann A, Schardl CL (2015) Two distinct Epichloë species symbiotic with Achnatherum inebrians, drunken horse grass. Mycologia 107(4):863–873CrossRefPubMedGoogle Scholar
  9. Chen N, He R, Chai Q, Li C, Nan Z (2016) Transcriptomic analyses giving insights into molecular regulation mechanisms involved in cold tolerance by Epichloë endophyte in seed germination of Achnatherum inebrians. Plant Growth Regul 80(3):367–375CrossRefGoogle Scholar
  10. Cheplick GP (2004) Recovery from drought stress in Lolium perenne (Poaceae): are fungal endophytes detrimental? Am J Bot 91(12):1960–1968CrossRefPubMedGoogle Scholar
  11. 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(6):657–667CrossRefGoogle Scholar
  12. 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 Genet Biol 45(2):84–93CrossRefPubMedGoogle Scholar
  13. Davitt AJ, Chen C, Rudgers JA (2011) Understanding context-dependency in plant-microbe symbiosis: the influence of abiotic and biotic contexts on host fitness and the rate of symbiont transmission. Environ Exp Bot 71(2):137–145CrossRefGoogle Scholar
  14. Elbersen HW, West CP (1996) Growth and water relations of field-grown tall fescue as influenced by drought and endophyte. Grass Forage Sci 51:333–342CrossRefGoogle Scholar
  15. Elmi AA, West CP (1995) Endophyte infection effects on stomatal conductance, osmotic adjustment and drought recovery of tall fescue. New Phytol 131(1):61–67CrossRefGoogle Scholar
  16. Elser JJ, O'Brien W, Dobberfuhl D, Dowling T (2000) The evolution of ecosystem processes: growth rate and elemental stoichiometry of a key herbivore in temperate and arctic habitats. J Evol Biol 13(5):845–853CrossRefGoogle Scholar
  17. Faeth SH, Fagan WF (2002) Fungal endophytes: common host plant symbionts but uncommon mutualists. Integr Comp Biol 42(2):360–368CrossRefPubMedGoogle Scholar
  18. Faeth SH, Sullivan TJ (2003) Mutualistic asexual endophytes in a native grass are usually parasitic? Am Nat 161(2):310–325CrossRefPubMedGoogle Scholar
  19. Fatichi S, Leuzinger S (2014) Moving beyond photosynthesis: from carbon source to sink-driven vegetation modeling. New Phytol 201(4):1086–1095CrossRefPubMedGoogle Scholar
  20. Freitak DH, Schmidtberg H, Dickel F, Lochnit G, Vogel H, Vilcinska A (2014) The maternal transfer of bacteria can mediate trans-generational immune priming in insects. Virulence 5:547–554CrossRefPubMedPubMedCentralGoogle Scholar
  21. Fujita Y, Robroek BJM, Ruiter PCD, Heil GW, Wassen MJ (2010) Increased N affects P uptake of eight grassland species: the role of root surface phosphatase activity. Oikos 119(10):1665–1673CrossRefGoogle Scholar
  22. Gundel PE, Irisarri JGN, Fazio L, Casas C, Pérez LI (2016) Inferring field performance from drought experiments can be misleading: the case of symbiosis between grasses and Epichloë fungal endophytes. J Arid Environ 132:60–62CrossRefGoogle Scholar
  23. Gundel PE, Rudgers JA, Ghersa CM (2011) Incorporating the process of vertical transmission into understanding of host-symbiont dynamics. Oikos 120(8):1121–1128CrossRefGoogle Scholar
  24. Gundel PE, Rudgers JA, Whitney KD (2017) Vertically transmitted symbionts as mechanisms of transgenerational effects. Am J Bot 104(5):787–792CrossRefPubMedGoogle Scholar
  25. Haerri SA, Krauss J, Mueller CB (2009) Extended larval development time for aphid parasitoids in the presence of plant endosymbionts. Ecol Entomol 34(1):20–25CrossRefGoogle Scholar
  26. Hamilton CE, Bauerle TL (2012) A new currency for mutualism? Fungal endophytes alter antioxidant activity in hosts responding to drought. Fungal Divers 54(1):39–49CrossRefGoogle Scholar
  27. Herman JJ, Sultan SE (2011) Adaptive transgenerational plasticity in plants: case studies, mechanisms, and implications for natural populations. Front Plant Sci 2:1–10CrossRefGoogle Scholar
  28. Hesse U, Schöberlein W, Wittenmayer L, Förster K, Warnstorff K, Diepenbrock W, Merbach W (2005) Influence of water supply and endophyte infection (Neotyphodium spp.) on vegetative and reproductive growth of two Lolium perenne L. genotypes. Eur J Agron 22(1):45–54CrossRefGoogle Scholar
  29. Hesse U, Schoberlein W, Wittenmayert L, Forster K, Warnstorn K, Diepenbrock W, Merbacht W (2003) Effect of Neotyphodium endophytes on growth reproduction and drought-stress tolerance of three Lolium perenne L. genotypes. Grass Forage Sci 58(4):407–415CrossRefGoogle Scholar
  30. Hessen DO, Jensen TC, Kyle M, Elser JJ (2007) RNA responses to N- and P-limitation; reciprocal regulation of stoichiometry and growth rate in Brachionus. Funct Ecol 21(5):956–962CrossRefGoogle Scholar
  31. Hosseini F, Mosaddeghi MR, Hajabbasi MA, Sabzalian MR (2016) Role of fungal endophyte of tall fescue (Epichloë coenophiala) on water availability, wilting point and integral energy in texturally-different soils. Agr water. Manage 163:197–211Google Scholar
  32. Iannone LJ, Irisarri JGN, Mc Cargo PD, Pérez LI, Gundel PE (2015) Occurrence of Epichloë fungal endophytes in the sheep-preferred grass Hordeum comosum from Patagonia. J Arid Environ 115:19–26CrossRefGoogle Scholar
  33. Jia T, Shymanovich T, Gao Y, Faeth SH (2015) Plant population and genotype effects override the effects of Epichloë endophyte species on growth and drought stress response of Achnatherum robustum plants in two natural grass populations. J Plant Ecol 41(6):3067–3075Google Scholar
  34. Johnson LJ, de Bonth ACM, Briggs LR, Caradus JR, Finch SC, Fleetwood DJ, Fletcher LR, Hume DE, Johnson RD, Popay AJ, Tapper BA, Simpson WR, Voisey CR, Card SD (2013) The exploitation of epichloae endophytes for agricultural benefit. Fungal Divers 60(1):171–188CrossRefGoogle Scholar
  35. Kannadan S, Rudgers JA (2008) Endophyte symbiosis benefits a rare grass under low water availability. Funct Ecol 22(4):706–713CrossRefGoogle Scholar
  36. Karcher DE, Richardson MD, Hignight K, Rush D (2008) Drought tolerance of tall fescue populations selected for high root/shoot ratios and summer survival. Crop Sci 48(2):771–777CrossRefGoogle Scholar
  37. Khan MH, Meghvansi MK, Gupta R, Veer V, Singh L, Kalita MC (2014) Foliar spray with vermiwash modifies the arbuscular mycorrhizal dependency and nutrient stoichiometry of bhut jolokia (Capsicum assamicum). PLoS One 9(3):e92318CrossRefPubMedPubMedCentralGoogle Scholar
  38. Kuldau G, Bacon C (2008) Clavicipitaceous endophytes: their ability to enhance resistance of grasses to multiple stresses. Biol Control 46(1):57–71CrossRefGoogle Scholar
  39. Leuchtmann A, Bacon CW, Schardl CL, White JF, Tadych M (2014) Nomenclatural realignment of Neotyphodium speices with genus Epichloë. Mycologia 106(2):202–215CrossRefPubMedGoogle Scholar
  40. Li C, Gao J, Nan Z (2007) Interactions of Neotyphodium gansuense, Achnatherum inebrians, and plant-pathogenic fungi. Mycol Res 111(10):1220–1227CrossRefPubMedGoogle Scholar
  41. Li C, Li F, Gou X, Nan Z (2008) Effects of abiotic stresses on Achnatherum inebrians by symbiotic endophyte of Neotyphodium gansuense. Multifunctional grasslands in changing world. Guangzhou, ChinaGoogle Scholar
  42. Li C, Nan Z, Gao J, Tian P (2004) Detection and distribution of Neotyphodium-Achnatherum inebrians association in China. Proceedings of 5th international Neotyphodium/grass interactions symposium, Arkansas, USAGoogle Scholar
  43. Li F (2007) Effects of endophyte infection on drought resistance to drunken horse grass (Achnatherum inebrians) MSc dissertation, Lanzhou University, Lanzhou, China (in Chinese, with English abstract)Google Scholar
  44. Li X, Ren A, Han R, Yin L, Wei M, Gao Y (2012) Endophyte-mediated effects on the growth and physiology of Achnatherum sibiricum are conditional on both N and P availability. PLoS One 7(11):e48010CrossRefPubMedPubMedCentralGoogle Scholar
  45. Lowman S, Kim-Dura S, Mei C, Nowak J (2016) Strategies for enhancement of swichgrass (e L.) performance under limited nitrogen supply based on utilization of N-fixing bacterial endophytes. Plant Soil 1-2:47–63CrossRefGoogle Scholar
  46. Malinowski DP, Belesky DP (2000) Adaptations of endophyte-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Sci 40(4):923–940CrossRefGoogle Scholar
  47. Malinowski DP, Leuchtmann A, Schmidt D, Nösberger J (1997) Growth and water status in meadow fescue is affected by Neotyphodium and Phialophora species endophytes. Agron J 89(4):673–678CrossRefGoogle Scholar
  48. Marks S, Clay K (1996) Physiological responses of Festuca arundinacea to fungal endophyte infection. New Phytol 133(4):727–733CrossRefGoogle Scholar
  49. McDonald A, Davies WJ (1996) Keeping in touch: responses of the whole plant to deficits. Adv Bot Res 22:229CrossRefGoogle Scholar
  50. Meister B, Krauss J, Härri SA, Victoria Schneider M, Müller CB (2006) Fungal endosymbionts affect aphid population size by reduction of adult life span and fecundity. Basic Appl Ecol 7(3):244–252CrossRefGoogle Scholar
  51. Miles CO, Lane GA, di Menna ME, Garthwaite I, Piper EL, Ball OJ, Latch GC, Allen JM, Hunt MB, Bush LP, Min FK, Fletcher I, Harris PS (1996) High levels of ergonovine and lysergic acid amide in toxic Achnatherum inebrians accompany infection by an Acremonium-like endophytic fungus. J Agric Food Chem 44(5):1285–1290CrossRefGoogle Scholar
  52. Morse LJ, Faeth SH, Day TA (2007) Neotyphodium interactions with a wild grass are driven mainly by endophyte haplotype. Funct Ecol 21:813–822CrossRefGoogle Scholar
  53. Müller CB, Krauss J (2005) Symbiosis between grasses and asexual fungal endophytes. Curr Opin Plant Biol 8(4):450–456CrossRefPubMedGoogle Scholar
  54. Nagabhyru P, Dinkins RD, Wood CL, Bacon CW, Schardl CL (2013) Tall fescue endophyte effects on tolerance to water-deficit stress. BMC Plant Biol 13:127CrossRefPubMedPubMedCentralGoogle Scholar
  55. Nan Z, Li C (2000) Neotyphodium in native grasses in China and observations on endophyte/host interactions. Proceedings of the 4th international Neotyphodium/grass interactions symposium, Soest, GermanyGoogle Scholar
  56. Nippert JB, Knapp AK (2007) Soil water partitioning contributes to species coexistence in tallgrass prairie. Oikos 116(6):1017–1029CrossRefGoogle Scholar
  57. Oberhofer M, Güsewell S, Leuchtmann A (2014) Effects of natural hybrid and non-hybrid Epichloë endophytes on the response of Hordelymus europaeus to drought stress. New Phytol 201(1):242–253CrossRefPubMedGoogle Scholar
  58. Odokonyero K, Acuña TB, Cardoso JA, de la Cruz Jimenez J, Rao IM (2016) Fungal endophyte association with Brachiaria grasses and its influence on plant water status, total non-structural carbohydrates and biomass production under drought stress. Plant Soil 409(1–2):273–282CrossRefGoogle Scholar
  59. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421(6918):37–42CrossRefPubMedGoogle Scholar
  60. Piao S, Ciais P, Yao H, Shen ZH, Peng SS, Li JS, Zhou LP, Liu HY, Ma YC, Ding YH (2010) The impacts of climate change on water resources and agriculture in China. Nature 467(7311):43CrossRefPubMedGoogle Scholar
  61. Pradhan N, Sukla LB (2006) Solubilization of inorganic phosphates by fungi isolated from agriculture soil. Afr J Biotechnol 5(10):850–854Google Scholar
  62. Rahman MH, Simpson WR, Matthew C, Sabreen S, Okubo A, Islam KR (2015) Response of diploid perennial ryegrass to fungal endophyte AR29 infections under water stress. Commun Soil Sci Plan Anal 46(7):845–860CrossRefGoogle Scholar
  63. Ren A, Gao Y, Wei W, Wang J (2006) Photosynthetic pigments and photosynthetic products of endophyte-infected and endophyte-free Lolium perenne L. under drought strees conditions. Front Biol China 1(2):168–173CrossRefGoogle Scholar
  64. Rozpądek P, Wężowicz K, Nosek M, Ważny R, Tokarz K, Lembicz M, Miszalski Z, Turnau K (2015) The fungal endophyte Epichloë typhina improves photosynthesis efficiency of its host orchard grass (Dactylis glomerata). Planta 242(4):1025–1035CrossRefPubMedPubMedCentralGoogle Scholar
  65. Saari S, Helander M, Faeth SH, Saikkonen K (2010) The effects of endophytes on seed production and seed predation of tall fescue and meadow fescue. Microb Ecol 60(4):928–934CrossRefPubMedGoogle Scholar
  66. Saikkonen K, Lehtonen P, Helander M, Koricheva J, Faeth SH (2006) Model systems in ecology: dissecting the endophyte-grass literature. Trends Plant Sci 11(9):428–433CrossRefPubMedGoogle Scholar
  67. Schardl CL, Grossman RB, Nagabhyru P, Faulkner JR, Mallik UP (2007) Loline alkaloids: currencies of mutualism. Phytochemistry 68(7):980–996CrossRefPubMedGoogle Scholar
  68. Schardl CL, Leuchtmann A, Spiering MJ (2004) Symbioses of grasses with seedborne fungal endophytes. Annu Rev Plant Biol 55:315–340CrossRefPubMedGoogle Scholar
  69. Smith SE, Jakobsen I, Grønlund M, Smith A (2011) Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol 156(3):1050–1057CrossRefPubMedPubMedCentralGoogle Scholar
  70. Song M, Chai Q, Li X, Yao X, Li C, Christensen MJ, Nan Z (2015) An asexual Epichloë endophyte modifies the nutrient stoichiometry of wild barley (Hordeum brevisubulatum) under salt stress. Plant Soil 387:153–165CrossRefGoogle Scholar
  71. Spiering MJ, Greer DH, Schmid J (2006) Effects of the fungal ndophyte, Neotyphodium lolii, on net photosynthesis and growth rates of perennial ryegrass (Lolium perenne) are independent of in planta endophyte concentration. Ann Bot-London 98(2):379–387CrossRefGoogle Scholar
  72. Swarthout D, Harper E, Judd S, Gonthier D, Shyne R, Stowe T, Bultman T (2009) Measures of leaf-level water-use efficiency in drought stressed endophyte infected and non-infected tall fescue grasses. Environ Exp Bot 66(1):88–93CrossRefGoogle Scholar
  73. Thom ER, Popay AJ, Waugh CD, Minne EE (2014) Impact of novel endophytes in perennial ryegrass on herbage production and insect pests from pastures under dairy cow grazing in northern New Zealand. Grass Forage Sci 69(1):191–204CrossRefGoogle Scholar
  74. 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:e84539CrossRefPubMedPubMedCentralGoogle Scholar
  75. Vignale MV, Astiz-Gassó MM, Novas MV, Iannone LJ (2013) Epichloid endophytes confer resistance to the smut Ustilago bullata in the wild grass Bromus auleticus (Trin.) Biol Control 67(1):1–7CrossRefGoogle Scholar
  76. White RH, Engelke MC, Morton SJ, Johnson CJM, Ruemmele BA (1992) Acremonium endophyte effects on tall fescue drought tolerence. Crop Sci 32:1392–1396CrossRefGoogle Scholar
  77. Xia C, Zhang X, Christensen MJ, Nan Z, Li C (2015) Epichloë endophyte affects the ability of powdery mildew (Blumeria graminis) to colonise drunken horse grass (Achnatherum inebrians). Fungal Ecol 16:26–33CrossRefGoogle Scholar
  78. Xin Z, Franks C, Payton P, Burke JJ (2008) A simple method to determine transpiration efficiency in sorghum. Field Crop Res 107(2):180–183CrossRefGoogle Scholar
  79. Ye W, Hu S, Wu L, Ge C, Cui Y, Chen P, Xu J, Dong G, Guo L, Qian Q (2017) Fine mapping a major QTL qFCC7L for chlorophyll content in rice (Oryza Sativa L.) cv. PA64s. Plant Growth Regul 81(1):81–90CrossRefGoogle Scholar
  80. Zaidi A, Khan MS (2007) Stimulatory effects of dual inoculation with phosphate solubilising microorganisms and arbuscular mycorrhizal fungus on chickpea. Aust J Exp Agric 47(8):1016–1022CrossRefGoogle Scholar
  81. Zhang X, Li C, Nan Z (2010) Effects of cadmium stress on growth and anti-oxidative systems in Achnatherum inebrians symbiotic with Neotyphodium gansuense. J Hazard Mater 175(1–3):703–709CrossRefPubMedGoogle Scholar
  82. Zhang X, Li C, Nan Z (2011) Effects of salt and drought stress on alkaloid production in endophyte-infected drunken horse grass (Achnatherum inebrians). Biochem Syst Ecol 39(4):471–476CrossRefGoogle Scholar
  83. Zhang X, Li C, Nan Z, Matthew C (2012) Neotyphodium endophyte increases Achnatherum inebrians (drunken horse grass) resistance to herbivores and seed predators. Weed Res 52(1):70–78CrossRefGoogle Scholar
  84. Zhang X, Nan Z, Li C, Gao K (2014) Cytotoxic effect of ergot alkaloids in Achnatherum inebrians infected by the Neotyphodium gansuense endophyte. J Agric Food Chem 62(30):7419–7422CrossRefPubMedGoogle Scholar
  85. Zhang Y, Nan Z (2007) Growth and anti-oxidative systems changes in Elymus dahuricus is affected by Neotyphodium endophyte under contrasting water availability. J Agron Crop Sci 193(6):377–386CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.State key Laboratory of Grassland Agro-ecosystems, Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture, College of Pastoral Agricultural Science and TechnologyLanzhou UniversityLanzhouPeople’s Republic of China
  2. 2.Grasslands Research CentrePalmerston NorthNew Zealand

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