Endophytic fungi and drought tolerance: ecophysiological adjustment in shoot and root of an annual mesophytic host grass
Milena E. Manzur
A B , Fabián A. Garello B C , Marina Omacini C D , Hans Schnyder E , Moira R. Sutka F and Pablo A. García-Parisi C G *
+ Author Affiliations
- Author Affiliations
A IIBIO-CONICET-UNSAM, Avenida 25 de Mayo y Francia, San Martín, CPA B1650HMP Buenos Aires, Argentina.
B Departamento de Biología Aplicada y Alimentos, Cátedra de Fisiología Vegetal, Facultad de Agronomía, Universidad de Buenos Aires, Avenida San Martín 4453, C1417DSE Buenos Aires, Argentina.
C IFEVA-CONICET, Facultad de Agronomía, Universidad de Buenos Aires, Avenida San Martín 4453, C1417DSE Buenos Aires, Argentina.
D Departamento de Recursos Naturales y Ambiente, Cátedra de Ecología, Facultad de Agronomía, Universidad de Buenos Aires, Avenida San Martín 4453, C1417DSE Buenos Aires, Argentina.
E Lehrstuhl für Grünlandlehre, Technische Universität München, D-85354 Freising-Weihenstephan, Germany.
F DBBE-IBBEA, CONICET, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Intendente Güiraldes 2160, Ciudad Universitaria, C1428EGA, Buenos Aires, Argentina.
G Departamento de Producción Animal, Cátedra de Forrajicultura, Facultad de Agronomía, Universidad de Buenos Aires, Avenida San Martín 4453, C1417DSE Buenos Aires, Argentina.
Functional Plant Biology 49(3) 272-282 https://doi.org/10.1071/FP21238
Submitted: 19 January 2021 Accepted: 20 December 2021 Published: 8 February 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Epichloid endophytic fungi, vertically transmitted symbionts of grasses, can increase plant tolerance to biotic and abiotic stress. Our aim was to identify ecophysiological mechanisms by which the endophyte Epichloë occultans confers drought tolerance to the annual grass Lolium multiflorum Lam. Endophyte-associated or endophyte-free plants were either well-watered or subjected to water deficit. We evaluated plant biomass, root length and nitrogen concentration, and we assessed intrinsic water use efficiency (iWUE) and its components net photosynthesis and stomatal conductance, by carbon and oxygen isotope analysis of shoot tissues. Endophyte-free plants produced more biomass than endophyte-associated ones at field capacity, while water deficit strongly reduced endophyte-free plants biomass. As a result, both types of plants produced similar biomass under water restriction. Based on oxygen isotope composition of plant cellulose, stomatal conductance decreased with water deficit in both endophyte-associated and endophyte-free plants. Meanwhile, carbon isotope composition indicated that iWUE increased with water deficit only in endophyte-associated plants. Thus, the isotope data indicated that net photosynthesis decreased more strongly in endophyte-free plants under water deficit. Additionally, endophyte presence reduced root length but increased its hydraulic conductivity. In conclusion, endophytic fungi confer drought tolerance to the host grass by adjusting shoot and root physiology.
Keywords: ecophysiology, fungal infection, mutualism, plant stresses, root, symbiosis, water stress physiology, water use efficiency.
References
Arechavaleta M, Bacon CW, Plattner RD, Hoveland CS, Radcliffe DE (1992) Accumulation of ergopeptide alkaloids in symbiotic tall fescue grown under deficits of soil water and nitrogen fertilizer. Applied and Environmental Microbiology 58, 857–861.| Accumulation of ergopeptide alkaloids in symbiotic tall fescue grown under deficits of soil water and nitrogen fertilizer.Crossref | GoogleScholarGoogle Scholar | 16348675PubMed |
Baca Cabrera JC, Hirl RT, Schäufele R, Macdonald A, Schnyder H (2021) Stomatal conductance limited the CO2 response of grassland in the last century. BMC Biology 19, 50
| Stomatal conductance limited the CO2 response of grassland in the last century.Crossref | GoogleScholarGoogle Scholar | 33757496PubMed |
Bacon CW, White JFJ (1994) ‘Biotechnology of endophytic fungi of grasses.’ (CRC Press: Boca Raton, USA)
Brendel O, Iannetta PPM, Stewart D (2000) A rapid and simple method to isolate pure alpha-cellulose. Phytochemical Analysis 11, 7–10.
| A rapid and simple method to isolate pure alpha-cellulose.Crossref | GoogleScholarGoogle Scholar |
Cheplick GP, Faeth SH (2009) ‘Ecology and evolution of the grass-endophyte symbiosis.’ Oxford Scholarship Online Monographs. (Oxford University Press: New York)
Clay K (1988) Fungal endophytes of grasses: a defensive mutualism between plants and fungi. Ecology 69, 10–16.
| Fungal endophytes of grasses: a defensive mutualism between plants and fungi.Crossref | GoogleScholarGoogle Scholar |
Condon AG, Richards RA, Rebetzke GJ, Farquhar GD (2004) Breeding for high water-use efficiency. Journal of Experimental Botany 55, 2447–2460.
| Breeding for high water-use efficiency.Crossref | GoogleScholarGoogle Scholar | 15475373PubMed |
Dastogeer KMG (2018) Influence of fungal endophytes on plant physiology is more pronounced under stress than well-watered conditions: a meta-analysis. Planta 248, 1403–1416.
| Influence of fungal endophytes on plant physiology is more pronounced under stress than well-watered conditions: a meta-analysis.Crossref | GoogleScholarGoogle Scholar | 30121874PubMed |
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. Environmental and Experimental Botany 71, 137–145.
| Understanding context-dependency in plant–microbe symbiosis: the influence of abiotic and biotic contexts on host fitness and the rate of symbiont transmission.Crossref | GoogleScholarGoogle Scholar |
De Battista JP, Bouton JH, Bacon CW, Siegel MR (1990) Rhizome and herbage production of endophyte-removed tall fescue clones and populations. Agronomy Journal 82, 651–654.
| Rhizome and herbage production of endophyte-removed tall fescue clones and populations.Crossref | GoogleScholarGoogle Scholar |
Douglas AE (2010) ‘The symbiotic habitat.’ (Princeton University Press: New Jersey, USA)
Easterling DR, Evans JL, Groisman PY, Karl TR, Kunkel KE, Ambenje P (2000) Observed variability and trends in extreme climate events: a brief review. Bulletin of the American Meteorological Society 81, 417–426.
| Observed variability and trends in extreme climate events: a brief review.Crossref | GoogleScholarGoogle Scholar |
Elmi AA, West CP (1995) Endophyte infection effects on stomatal conductance, osmotic adjustment and drought recovery of tall fescue. New Phytologist 131, 61–67.
| Endophyte infection effects on stomatal conductance, osmotic adjustment and drought recovery of tall fescue.Crossref | GoogleScholarGoogle Scholar |
Farquhar GD, Cernusak LA, Barnes B (2007) Heavy water fractionation during transpiration. Plant Physiology 143, 11–18.
| Heavy water fractionation during transpiration.Crossref | GoogleScholarGoogle Scholar | 17210909PubMed |
Farquhar GD, O’Leary MH, Berry JA (1982) On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Australian Journal of Plant Physiology 13, 281–292.
| On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves.Crossref | GoogleScholarGoogle Scholar |
Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 40, 503–537.
| Carbon isotope discrimination and photosynthesis.Crossref | GoogleScholarGoogle Scholar |
Fox J, Weisberg S (2019). An R Companion to Applied Regression. Third edition. Sage, Thousand Oaks CA. https://socialsciences.mcmaster.ca/jfox/Books/Companion/.
Gaudinski JB, Dawson TE, Quideau S, Schuur EAG, Roden JS, Trumbore SE, Sandquist DR, Oh S-W, Wasylishen RE (2005) Comparative analysis of cellulose preparation techniques for use with 13C, 14C, and 18O isotopic measurements. Analytical Chemistry 77, 7212–7224.
| Comparative analysis of cellulose preparation techniques for use with 13C, 14C, and 18O isotopic measurements.Crossref | GoogleScholarGoogle Scholar | 16285668PubMed |
Gundel PE, Batista WB, Texeira M, Martinez-Ghersa MA, Omacini M, Ghersa CM (2008) Neotyphodium endophyte infection frequency in annual grass populations: relative importance of mutualism and transmission efficiency. Proceedings of the Royal Society B: Biological Sciences 275, 897–905.
| Neotyphodium endophyte infection frequency in annual grass populations: relative importance of mutualism and transmission efficiency.Crossref | GoogleScholarGoogle Scholar | 18198146PubMed |
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. Journal of Arid Environments 132, 60–62.
| Inferring field performance from drought experiments can be misleading: the case of symbiosis between grasses and Epichloë fungal endophytes.Crossref | GoogleScholarGoogle Scholar |
Jaramillo VJ, Detling JK (1988) Grazing history, defoliation, and competition: effects on shortgrass production and nitrogen accumulation. Ecology 69, 1599–1608.
| Grazing history, defoliation, and competition: effects on shortgrass production and nitrogen accumulation.Crossref | GoogleScholarGoogle Scholar |
Kaschuk G, Kuyper TW, Leffelaar PA, Hungria M, Giller KE (2009) Are the rates of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbioses? Soil Biology and Biochemistry 41, 1233–1244.
| Are the rates of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbioses?Crossref | GoogleScholarGoogle Scholar |
Kiers ET, West SA (2015) Evolving new organisms via symbiosis. Science 348, 392–394.
| Evolving new organisms via symbiosis.Crossref | GoogleScholarGoogle Scholar | 25908807PubMed |
Klein T (2014) The variability of stomatal sensitivity to leaf water potential across tree species indicates a continuum between isohydric and anisohydric behaviours. Functional Ecology 28, 1313–1320.
| The variability of stomatal sensitivity to leaf water potential across tree species indicates a continuum between isohydric and anisohydric behaviours.Crossref | GoogleScholarGoogle Scholar |
Knapp AK, Smith MD (2001) Variation among biomes in temporal dynamics of aboveground primary production. Science 291, 481–484.
| Variation among biomes in temporal dynamics of aboveground primary production.Crossref | GoogleScholarGoogle Scholar | 11161201PubMed |
Latch GCM, Hunt WF, Musgrave DR (1985) Endophytic fungi affect growth of perennial ryegrass. New Zealand Journal of Agricultural Research 28, 165–168.
| Endophytic fungi affect growth of perennial ryegrass.Crossref | GoogleScholarGoogle Scholar |
Leuchtmann A, Bacon CW, Schardl CL, White JF, Tadych M (2014) Nomenclatural realignment of Neotyphodium species with genus Epichloë. Mycologia 106, 202–215.
| Nomenclatural realignment of Neotyphodium species with genus Epichloë.Crossref | GoogleScholarGoogle Scholar | 24459125PubMed |
Li T, Blande JD, Gundel PE, Helander M, Saikkonen K (2014) Epichloë endophytes alter inducible indirect defences in host grasses. PLoS ONE 9, e101331
| Epichloë endophytes alter inducible indirect defences in host grasses.Crossref | GoogleScholarGoogle Scholar | 24978701PubMed |
Ma WT, Tcherkez G, Wang XM, Schäufele R, Schnyder H, Yang Y, Gong XY (2021) Accounting for mesophyll conductance substantially improves 13C-based estimates of intrinsic water-use efficiency. New Phytologist 229, 1326–1338.
| Accounting for mesophyll conductance substantially improves 13C-based estimates of intrinsic water-use efficiency.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 |
Malinowski D, Leuchtmann A, Schmidt D, Nösberger J (1997) Growth and water status in meadow fescue is affected by Neotyphodium and Phialophora species endophytes. Agronomy Journal 89, 673–678.
| Growth and water status in meadow fescue is affected by Neotyphodium and Phialophora species endophytes.Crossref | GoogleScholarGoogle Scholar |
Malinowski DP, Alloush GA, Belesky DP (2000) Leaf endophyte Neotyphodium coenophialum modifies mineral uptake in tall fescue. Plant and Soil 227, 115–126.
| Leaf endophyte Neotyphodium coenophialum modifies mineral uptake in tall fescue.Crossref | GoogleScholarGoogle Scholar |
Martínez-Vilalta J, Poyatos R, Aguadé D, Retana J, Mencuccini M (2014) A new look at water transport regulation in plants. New Phytologist 204, 105–115.
| A new look at water transport regulation in plants.Crossref | GoogleScholarGoogle Scholar |
Matsuo N, Ozawa K, Mochizuki T (2009) Genotypic differences in root hydraulic conductance of rice (Oryza sativa L.) in response to water regimes. Plant and Soil 316, 25–34.
| Genotypic differences in root hydraulic conductance of rice (Oryza sativa L.) in response to water regimes.Crossref | GoogleScholarGoogle Scholar |
Miranda MI, Omacini M, Chaneton EJ (2011) Environmental context of endophyte symbioses: interacting effects of water stress and insect herbivory. International Journal of Plant Sciences 172, 499–508.
| Environmental context of endophyte symbioses: interacting effects of water stress and insect herbivory.Crossref | GoogleScholarGoogle Scholar |
Miyamoto N, Steudle E, Hirasawa T, Lafitte R (2001) Hydraulic conductivity of rice roots. Journal of Experimental Botany 52, 1835–1846.
| Hydraulic conductivity of rice roots.Crossref | GoogleScholarGoogle Scholar | 11520872PubMed |
Moreno-Gutiérrez C, Dawson TE, Nicolás E, Querejeta JI (2012) Isotopes reveal contrasting water use strategies among coexisting plant species in a Mediterranean ecosystem. New Phytologist 196, 489–496.
| Isotopes reveal contrasting water use strategies among coexisting plant species in a Mediterranean ecosystem.Crossref | GoogleScholarGoogle Scholar |
Moshelion M, Halperin O, Wallach R, Oren R, Way DA (2015) Role of aquaporins in determining transpiration and photosynthesis in water-stressed plants: crop water-use efficiency, growth and yield. Plant, Cell & Environment 38, 1785–1793.
| Role of aquaporins in determining transpiration and photosynthesis in water-stressed plants: crop water-use efficiency, growth and yield.Crossref | GoogleScholarGoogle Scholar |
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 |
Omacini M, Eggers T, Bonkowski M, Gange AC, Jones TH (2006) Leaf endophytes affect mycorrhizal status and growth of co-infected and neighbouring plants. Functional Ecology 20, 226–232.
| Leaf endophytes affect mycorrhizal status and growth of co-infected and neighbouring plants.Crossref | GoogleScholarGoogle Scholar |
Pinheiro JC, Bates D, DebRoy S, Sarkar D, Team RC (2015) {nlme}: linear and nonlinear mixed effects models. http://cran.r-project.org/package=nlme
R Core Team (2018) ‘R: a language and environment for statistical computing.’ (R Foundation for Statistical Computing). Available at https://www.r-project.org/
Redman RS, Kim YO, Woodward CJDA, Greer C, Espino L, Doty SL, Rodriguez RJ (2011) Increased fitness of rice plants to abiotic stress via habitat adapted symbiosis: a strategy for mitigating impacts of climate change. PLoS ONE 6, e14823
| Increased fitness of rice plants to abiotic stress via habitat adapted symbiosis: a strategy for mitigating impacts of climate change.Crossref | GoogleScholarGoogle Scholar | 21750695PubMed |
Richardson MD, Chapman GW, Hoveland CS, Bacon CW (1992) Sugar alcohols in endophyte-infected tall fescue under drought. Crop Science 32, 1060–1061.
| Sugar alcohols in endophyte-infected tall fescue under drought.Crossref | GoogleScholarGoogle Scholar |
Rodriguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L, Beckwith F, Kim Y-O, Redman RS (2008) Stress tolerance in plants via habitat-adapted symbiosis. The ISME Journal 2, 404–416.
| Stress tolerance in plants via habitat-adapted symbiosis.Crossref | GoogleScholarGoogle Scholar | 18256707PubMed |
Scheidegger Y, Saurer M, Bahn M, Siegwolf R (2000) Linking stable oxygen and carbon isotopes with stomatal conductance and photosynthetic capacity: a conceptual model. Oecologia 125, 350–357.
| Linking stable oxygen and carbon isotopes with stomatal conductance and photosynthetic capacity: a conceptual model.Crossref | GoogleScholarGoogle Scholar | 28547329PubMed |
Sheffield J, Wood EF (2007) Characteristics of global and regional drought, 1950–2000: analysis of soil moisture data from off-line simulation of the terrestrial hydrologic cycle. Journal of Geophysical Research: Atmospheres 112, D17115
| Characteristics of global and regional drought, 1950–2000: analysis of soil moisture data from off-line simulation of the terrestrial hydrologic cycle.Crossref | GoogleScholarGoogle Scholar |
Simms EL (2000) Defining tolerance as a norm of reaction. Evolutionary Ecology 14, 563–570.
| Defining tolerance as a norm of reaction.Crossref | GoogleScholarGoogle Scholar |
Stowe KA, Marquis RJ, Hochwender CG, Simms EL (2000) The evolutionary ecology of tolerance to consumer damage. Annual Review of Ecology and Systematics 31, 565–595.
| The evolutionary ecology of tolerance to consumer damage.Crossref | GoogleScholarGoogle Scholar |
Sultan SE (2000) Phenotypic plasticity for plant development, function and life history. Trends in Plant Science 5, 537–542.
| Phenotypic plasticity for plant development, function and life history.Crossref | GoogleScholarGoogle Scholar | 11120476PubMed |
Sutka MR, Manzur ME, Vitali VA, Micheletto S, Amodeo G (2016) Evidence for the involvement of hydraulic root or shoot adjustments as mechanisms underlying water deficit tolerance in two Sorghum bicolor genotypes. Journal of Plant Physiology 192, 13–20.
| Evidence for the involvement of hydraulic root or shoot adjustments as mechanisms underlying water deficit tolerance in two Sorghum bicolor genotypes.Crossref | GoogleScholarGoogle Scholar | 26803215PubMed |
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. Environmental and Experimental Botany 66, 88–93.
| Measures of leaf-level water-use efficiency in drought stressed endophyte infected and non-infected tall fescue grasses.Crossref | GoogleScholarGoogle Scholar |
Vile D, Pervent M, Belluau M, Vasseur F, Bresson J, Muller B, Granier C, Simonneau T (2012) Arabidopsis growth under prolonged high temperature and water deficit: independent or interactive effects? Plant Cell & Environment 35, 702–718.
| Arabidopsis growth under prolonged high temperature and water deficit: independent or interactive effects?Crossref | GoogleScholarGoogle Scholar |
Walder F, van der Heijden MGA (2015) Regulation of resource exchange in the arbuscular mycorrhizal symbiosis. Nature Plants 1, 15159
| Regulation of resource exchange in the arbuscular mycorrhizal symbiosis.Crossref | GoogleScholarGoogle Scholar | 27251530PubMed |
Wang J, Zhou Y, Lin W, Li M, Wang M, Wang Z, Kuang Y, Tian P (2017) Effect of an Epichloë endophyte on adaptability to water stress in Festuca sinensis. Fungal Ecology 30, 39–47.
| Effect of an Epichloë endophyte on adaptability to water stress in Festuca sinensis.Crossref | GoogleScholarGoogle Scholar |
White RH, Engelke MC, Morton SJ, Johnson-Cicalese JM, Ruemmele BA (1992) Acremonium endophyte effects on tall fescue drought tolerance. Crop Science 32, 1392–1396.
| Acremonium endophyte effects on tall fescue drought tolerance.Crossref | GoogleScholarGoogle Scholar |
Xia C, Christensen MJ, Zhang X, Nan Z (2018) Effect of Epichloë gansuensis endophyte and transgenerational effects on the water use efficiency, nutrient and biomass accumulation of Achnatherum inebrians under soil water deficit. Plant and Soil 424, 555–571.
| Effect of Epichloë gansuensis endophyte and transgenerational effects on the water use efficiency, nutrient and biomass accumulation of Achnatherum inebrians under soil water deficit.Crossref | GoogleScholarGoogle Scholar |
Xu Z, Jiang Y, Jia B, Zhou G (2016) Elevated-CO2 response of stomata and its dependence on environmental factors. Frontiers in Plant Science 7, 657
| Elevated-CO2 response of stomata and its dependence on environmental factors.Crossref | GoogleScholarGoogle Scholar | 27242858PubMed |
Yang Z, Liu J, Tischer S V., Christmann A, Windisch W, Schnyder H, Grill E (2016) Leveraging abscisic acid receptors for efficient water use in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 113, 6791–6796.
| Leveraging abscisic acid receptors for efficient water use in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 27247417PubMed |
