Effects of root endophytic fungi on response of Chenopodium quinoa to drought stress

M. González-Teuber, A. Urzúa, P. Plaza, L. Bascuñán-Godoy

Research output: Contribution to journalArticle

  • 2 Citations

Abstract

Symbiotic associations with microbes can help plants to respond to environmental changes. In this study, we investigated how colonization by root endophytic fungi enhances performance of Chenopodium quinoa and its ability to cope with extended periods of drought. The fungus Penicillium minioluteum, which was isolated from quinoa naturally occurring in the Atacama Desert, was used for endophyte colonization. We developed a greenhouse experiment, subjecting endophyte-infected (E+) and endophyte-free (E−) plants to two treatments: water deficit and abundant water availability. Differences in plant performance, photosynthesis, water-use efficiency and photochemical efficiency between E+ and E− plants under both water treatments were examined. We assessed the nature of the plant–symbiont interaction (parasitic or mutualistic) under both treatment conditions. We found that P. minioluteum initially affected radicle growth, subsequently triggering improvements in root formation, with the latter particularly evident under drought conditions. Under low water, E+ plants demonstrated a 40% improvement in root formation relative to E− plants; however, physiological responses to drought were not demonstrably enhanced by the presence of endophytic fungi. The nature of the interaction appeared to be positive, but only under conditions of water stress. Our study demonstrates that, in C. quinoa, P. minioluteum assists in coping with water stress primarily by affecting substantial root biomass adjustments, and that host benefits in this relationship are conferred in conditions of stress only. © 2017, Springer Science+Business Media B.V., part of Springer Nature.
LanguageEnglish
Pages231-240
Number of pages10
JournalPlant Ecology
Volume219
Issue number3
DOIs
Publication statusPublished - 2018

Fingerprint

Chenopodium quinoa
drought stress
water stress
fungus
fungi
endophyte
endophytes
drought
water treatment
colonization
physiological response
effect
symbiont
water use efficiency
Penicillium
greenhouse experimentation
water availability
symbionts
deserts
environmental change

Keywords

  • Plant tolerance
  • Quinoa
  • Root formation
  • Root-associated fungi
  • Water deficit
  • biomass
  • colonization
  • drought stress
  • endophyte
  • fungus
  • herb
  • physiological response
  • root system
  • water availability
  • water stress
  • Atacama Desert
  • Chile
  • Chenopodium quinoa
  • Fungi
  • Penicillium minioluteum

Cite this

Effects of root endophytic fungi on response of Chenopodium quinoa to drought stress. / González-Teuber, M.; Urzúa, A.; Plaza, P.; Bascuñán-Godoy, L.

In: Plant Ecology, Vol. 219, No. 3, 2018, p. 231-240.

Research output: Contribution to journalArticle

González-Teuber, M. ; Urzúa, A. ; Plaza, P. ; Bascuñán-Godoy, L. / Effects of root endophytic fungi on response of Chenopodium quinoa to drought stress. In: Plant Ecology. 2018 ; Vol. 219, No. 3. pp. 231-240.
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title = "Effects of root endophytic fungi on response of Chenopodium quinoa to drought stress",
abstract = "Symbiotic associations with microbes can help plants to respond to environmental changes. In this study, we investigated how colonization by root endophytic fungi enhances performance of Chenopodium quinoa and its ability to cope with extended periods of drought. The fungus Penicillium minioluteum, which was isolated from quinoa naturally occurring in the Atacama Desert, was used for endophyte colonization. We developed a greenhouse experiment, subjecting endophyte-infected (E+) and endophyte-free (E−) plants to two treatments: water deficit and abundant water availability. Differences in plant performance, photosynthesis, water-use efficiency and photochemical efficiency between E+ and E− plants under both water treatments were examined. We assessed the nature of the plant–symbiont interaction (parasitic or mutualistic) under both treatment conditions. We found that P. minioluteum initially affected radicle growth, subsequently triggering improvements in root formation, with the latter particularly evident under drought conditions. Under low water, E+ plants demonstrated a 40{\%} improvement in root formation relative to E− plants; however, physiological responses to drought were not demonstrably enhanced by the presence of endophytic fungi. The nature of the interaction appeared to be positive, but only under conditions of water stress. Our study demonstrates that, in C. quinoa, P. minioluteum assists in coping with water stress primarily by affecting substantial root biomass adjustments, and that host benefits in this relationship are conferred in conditions of stress only. {\circledC} 2017, Springer Science+Business Media B.V., part of Springer Nature.",
keywords = "Plant tolerance, Quinoa, Root formation, Root-associated fungi, Water deficit, biomass, colonization, drought stress, endophyte, fungus, herb, physiological response, root system, water availability, water stress, Atacama Desert, Chile, Chenopodium quinoa, Fungi, Penicillium minioluteum",
author = "M. Gonz{\'a}lez-Teuber and A. Urz{\'u}a and P. Plaza and L. Bascu{\~n}{\'a}n-Godoy",
note = "Export Date: 11 April 2018 CODEN: PLECF Correspondence Address: Gonz{\'a}lez-Teuber, M.; Max Planck Partner Group, Facultad de Qu{\'i}mica y Biolog{\'i}a, Universidad de Santiago de ChileChile; email: marcia.gonzalez.t@usach.cl Funding details: Usach, Universidad de Santiago de Chile Funding details: MPG, Max-Planck-Gesellschaft Funding text: Acknowledgements We thank Carolina Murciano and Andrea Morales for their valuable help in the laboratory. MGT is also very grateful to Convenio de Desempe{\~n}o Proyecto Basal, Universidad de Santiago de Chile. This work was supported by the Max Planck Society through the Max Planck Partner Group. References: Adams, A.E., Kazenel, M.R., Rudgers, J.A., Does a foliar endophyte improve plant fitness under flooding? (2017) Plant Ecol, 218, pp. 711-723; Alvarez-Flores, R., Winkel, T., Nguyen-Thi-Truc, A., Joffre, R., Root foraging capacity depends on root system architecture and ontogeny in seedlings of three Andean Chenopodium species (2014) Plant Soil, 380, pp. 415-428. , COI: 1:CAS:528:DC{\%}2BC2cXmtlWhtLg{\%}3D; Armas, C., Ordiales, R., Pugnaire, F.I., Measuring plant interactions: a new comparative index (2004) Ecology, 85, pp. 2682-2686; Arnold, A.E., Engelbrecht, B.M.J., Fungal endophytes double minimum leaf conductance in seedlings of a tropical tree (2007) J Trop Ecol, 23, pp. 369-372; Arnold, A.E., Maynard, Z., Gilbert, G.S., Coley, P.D., Kursar, T.A., Are tropical fungal endophytes hyperdiverse? (2000) Ecol Lett, 3, pp. 267-274; Bascu{\~n}{\'a}n-Godoy, L., Sanhueza, C., Cuba, M., Zu{\~n}iga, G.E., Corcuera, L.J., Bravo, L., Cold-acclimation limits low temperature induced photoinhibition by promoting a higher photochemical quantum yield and a more effective PSII restoration in darkness in the Antarctic rather than the Andean ecotype of Colobanthus quitensis Kunt Bartl (Cariophyllaceae) (2012) BMC Plant Biol, 12, p. 114. , PID: 22827966; Bascu{\~n}{\'a}n-Godoy, L., Reguera, M., Blumwald, Y.M., Blumwald, E., Water deficit stress-induced changes in carbon and nitrogen partitioning in Chenopodium quinoa willd (2016) Planta, 243, pp. 591-603. , PID: 26560134; Bertero, H.D., Ruiz, R.A., Reproductive partitioning in sea level quinoa (Chenopodium quinoa Willd.) cultivars (2010) Field Crops Res, 118, pp. 94-101; Bhargava, A., Shukla, S., Ohri, D., Chenopodium quinoa—an Indian perspective (2006) Ind Crops Prod, 23, pp. 73-87. , COI: 1:CAS:528:DC{\%}2BD28XotVChtw{\%}3D{\%}3D; Bray, E.A., Plant responses to water deficit (2007) Trends Plant Sci, 2, pp. 48-54; Chaves, M.M., Oliveira, M.M., Mechanisms underlying plant resilience to water deficits—prospects for water-saving agriculture (2004) J Exp Bot, 55, pp. 2365-2384. , COI: 1:CAS:528:DC{\%}2BD2cXovVOisr0{\%}3D, PID: 15475377; Chaves, M.M., Maroco, J.P., Pereira, J.S., Understanding plant responses to drought—from genes to the whole plant (2003) Funct Plant Biol, 30, pp. 239-264. , COI: 1:CAS:528:DC{\%}2BD3sXjtVKlt7o{\%}3D; Cheplick, G.P., Conceptual model for the analysis of plant-endophyte symbiosis in relation to abiotic stress (2009) Defensive mutualism in microbial symbiosis, pp. 322-323. , White JF, Torres MS, (eds), CRC Press, Boca Raton; Cheplick, G.P., Faeth, S.H., (2009) Ecology and evolution of the grass-endophyte symbiosis, , Oxford University Press, Oxford; Clay, K., Schardl, C., Evolutionary origins and ecological consequences of endophyte symbiosis with grasses (2002) Am Nat, 160, pp. 99-127; Contreras-Cornejo, H.A., Mac{\'i}as-Rodriguez, L., Cort{\'e}s-Penagos, C., L{\'o}pez-Bucio, J., Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxindependent mechanism in (2009) Plant Physiol, 149, pp. 1579-1592. , COI: 1:CAS:528:DC{\%}2BD1MXlsFCiu7w{\%}3D, PID: 19176721; Cusack, D., Quinoa: grain of the Incas (1984) Ecologist, 14, pp. 21-31; Dai, C.-C., Yu, B.-Y., Li, X., Screening of endophytic fungi that promote the growth of Euphorbia pekinensis (2008) Afr J Biotechnol, 7, pp. 3505-3510. , COI: 1:CAS:528:DC{\%}2BD1cXhtlygsL3J; Davitt, A.J., Chen, C., Rudgers, J.A., Understanding context-dependency in plant–microbe symbiosis: the influence of abiotic and biotic contexts on host fitness and the rate of symbiont transmission (2011) Environ Exp Bot, 71, pp. 137-145. , COI: 1:CAS:528:DC{\%}2BC3MXhvFWitr8{\%}3D; De Micco, V., Aronne, G., Morpho-anatomical traits for plant adaptation to drought (2012) Plant responses to drought stress: from morphological to molecular features, pp. 37-61. , Aroca R, (ed), Springer, Heidelberg; Elmi, A.A., West, C.P., Endophyte effects on tall fescue stomatal response, osmotic adjustment and tiller survival (1995) New Phytol, 131, pp. 61-67; Fuentes, F., Bhargava, A., Morphological analysis of quinoa germplasm grown under lowland desert conditions (2011) J Agron Crop Sci, 197, pp. 124-134; Gonz{\'a}lez-Teuber, M., Vilo, C., Bascu{\~n}{\'a}n-Godoy, L., Molecular characterization of endophytic fungi associated with the roots of Chenopodium quinoa inhabiting the Atacama Desert, Chile (2017) Genom Data, 11, pp. 109-112. , PID: 28116242; Houston, J., Hartley, A.J., The central andean west-slope rainshadow and its potential contribution to the origin of hyperaridity in the Atacama Desert (2003) Int J Climatol, 23, pp. 1453-1464; Hubbard, M., Germida, J., Vujanovic, V., Fungal endophytes enhance wheat heat and drought tolerance in terms of grain yield and second generation seed viability (2013) J Appl Microbiol, 116, pp. 109-122. , PID: 23889706; (2014) Bolet{\'i}n nacional de an{\'a}lisis de riesgos agroclim{\'a}ticos para las principales especies frutales y cultivos, y la ganader{\'i}a, , http://newsflash.asoex.cl/userfiles/file/269; Jankovic, S., Popovic, V., Ikanovic, J., Rakic, S., Kuzevski, J., Gavrilovic, M., Productivity traits of rye (Secale cereale), khorasan wheat (Triticum turgidum. ssp. Taranicum Mckey) and quinoa (Chenopodium quinoa Willd) grown on degraded soil (2016) Rom Agric Res, 33, pp. 283-290; Junges, E., Bri{\~a}o Muniz, M.F., de Oliveira, B.B., Oruoski, P., Biopriming in bean seeds (2015) Acta Agric Scand B; Kane, K.H., Effects of endophyte infection on drought stress tolerance of Lolium perenne accessions from the Mediterranean region (2011) Environ Exp Bot, 71, pp. 337-344; Kannadan, S., Rudgers, J.A., Endophyte symbiosis benefits a rare grass under low water availability (2008) Funct Ecol, 4, pp. 706-713; Khan, A.L., Hamayun, M., Ahmad, N., Hussain, J., Kang, S.M., Kim, Y.H., Adnan, M., Lee, I.J., Salinity stress resistance offered by endophytic fungal interaction between Penicillium minioluteum LHL09 and Glycine max. 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year = "2018",
doi = "10.1007/s11258-017-0791-1",
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journal = "Plant Ecology",
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TY - JOUR

T1 - Effects of root endophytic fungi on response of Chenopodium quinoa to drought stress

AU - González-Teuber, M.

AU - Urzúa, A.

AU - Plaza, P.

AU - Bascuñán-Godoy, L.

N1 - Export Date: 11 April 2018 CODEN: PLECF Correspondence Address: González-Teuber, M.; Max Planck Partner Group, Facultad de Química y Biología, Universidad de Santiago de ChileChile; email: marcia.gonzalez.t@usach.cl Funding details: Usach, Universidad de Santiago de Chile Funding details: MPG, Max-Planck-Gesellschaft Funding text: Acknowledgements We thank Carolina Murciano and Andrea Morales for their valuable help in the laboratory. MGT is also very grateful to Convenio de Desempeño Proyecto Basal, Universidad de Santiago de Chile. This work was supported by the Max Planck Society through the Max Planck Partner Group. References: Adams, A.E., Kazenel, M.R., Rudgers, J.A., Does a foliar endophyte improve plant fitness under flooding? (2017) Plant Ecol, 218, pp. 711-723; Alvarez-Flores, R., Winkel, T., Nguyen-Thi-Truc, A., Joffre, R., Root foraging capacity depends on root system architecture and ontogeny in seedlings of three Andean Chenopodium species (2014) Plant Soil, 380, pp. 415-428. , COI: 1:CAS:528:DC%2BC2cXmtlWhtLg%3D; Armas, C., Ordiales, R., Pugnaire, F.I., Measuring plant interactions: a new comparative index (2004) Ecology, 85, pp. 2682-2686; Arnold, A.E., Engelbrecht, B.M.J., Fungal endophytes double minimum leaf conductance in seedlings of a tropical tree (2007) J Trop Ecol, 23, pp. 369-372; Arnold, A.E., Maynard, Z., Gilbert, G.S., Coley, P.D., Kursar, T.A., Are tropical fungal endophytes hyperdiverse? (2000) Ecol Lett, 3, pp. 267-274; Bascuñán-Godoy, L., Sanhueza, C., Cuba, M., Zuñiga, G.E., Corcuera, L.J., Bravo, L., Cold-acclimation limits low temperature induced photoinhibition by promoting a higher photochemical quantum yield and a more effective PSII restoration in darkness in the Antarctic rather than the Andean ecotype of Colobanthus quitensis Kunt Bartl (Cariophyllaceae) (2012) BMC Plant Biol, 12, p. 114. , PID: 22827966; Bascuñán-Godoy, L., Reguera, M., Blumwald, Y.M., Blumwald, E., Water deficit stress-induced changes in carbon and nitrogen partitioning in Chenopodium quinoa willd (2016) Planta, 243, pp. 591-603. , PID: 26560134; Bertero, H.D., Ruiz, R.A., Reproductive partitioning in sea level quinoa (Chenopodium quinoa Willd.) cultivars (2010) Field Crops Res, 118, pp. 94-101; Bhargava, A., Shukla, S., Ohri, D., Chenopodium quinoa—an Indian perspective (2006) Ind Crops Prod, 23, pp. 73-87. , COI: 1:CAS:528:DC%2BD28XotVChtw%3D%3D; Bray, E.A., Plant responses to water deficit (2007) Trends Plant Sci, 2, pp. 48-54; Chaves, M.M., Oliveira, M.M., Mechanisms underlying plant resilience to water deficits—prospects for water-saving agriculture (2004) J Exp Bot, 55, pp. 2365-2384. , COI: 1:CAS:528:DC%2BD2cXovVOisr0%3D, PID: 15475377; Chaves, M.M., Maroco, J.P., Pereira, J.S., Understanding plant responses to drought—from genes to the whole plant (2003) Funct Plant Biol, 30, pp. 239-264. , COI: 1:CAS:528:DC%2BD3sXjtVKlt7o%3D; Cheplick, G.P., Conceptual model for the analysis of plant-endophyte symbiosis in relation to abiotic stress (2009) Defensive mutualism in microbial symbiosis, pp. 322-323. , White JF, Torres MS, (eds), CRC Press, Boca Raton; Cheplick, G.P., Faeth, S.H., (2009) Ecology and evolution of the grass-endophyte symbiosis, , Oxford University Press, Oxford; Clay, K., Schardl, C., Evolutionary origins and ecological consequences of endophyte symbiosis with grasses (2002) Am Nat, 160, pp. 99-127; Contreras-Cornejo, H.A., Macías-Rodriguez, L., Cortés-Penagos, C., López-Bucio, J., Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxindependent mechanism in (2009) Plant Physiol, 149, pp. 1579-1592. , COI: 1:CAS:528:DC%2BD1MXlsFCiu7w%3D, PID: 19176721; Cusack, D., Quinoa: grain of the Incas (1984) Ecologist, 14, pp. 21-31; Dai, C.-C., Yu, B.-Y., Li, X., Screening of endophytic fungi that promote the growth of Euphorbia pekinensis (2008) Afr J Biotechnol, 7, pp. 3505-3510. , COI: 1:CAS:528:DC%2BD1cXhtlygsL3J; Davitt, A.J., Chen, C., Rudgers, J.A., Understanding context-dependency in plant–microbe symbiosis: the influence of abiotic and biotic contexts on host fitness and the rate of symbiont transmission (2011) Environ Exp Bot, 71, pp. 137-145. , COI: 1:CAS:528:DC%2BC3MXhvFWitr8%3D; De Micco, V., Aronne, G., Morpho-anatomical traits for plant adaptation to drought (2012) Plant responses to drought stress: from morphological to molecular features, pp. 37-61. , Aroca R, (ed), Springer, Heidelberg; Elmi, A.A., West, C.P., Endophyte effects on tall fescue stomatal response, osmotic adjustment and tiller survival (1995) New Phytol, 131, pp. 61-67; Fuentes, F., Bhargava, A., Morphological analysis of quinoa germplasm grown under lowland desert conditions (2011) J Agron Crop Sci, 197, pp. 124-134; González-Teuber, M., Vilo, C., Bascuñán-Godoy, L., Molecular characterization of endophytic fungi associated with the roots of Chenopodium quinoa inhabiting the Atacama Desert, Chile (2017) Genom Data, 11, pp. 109-112. , PID: 28116242; Houston, J., Hartley, A.J., The central andean west-slope rainshadow and its potential contribution to the origin of hyperaridity in the Atacama Desert (2003) Int J Climatol, 23, pp. 1453-1464; Hubbard, M., Germida, J., Vujanovic, V., Fungal endophytes enhance wheat heat and drought tolerance in terms of grain yield and second generation seed viability (2013) J Appl Microbiol, 116, pp. 109-122. , PID: 23889706; (2014) Boletín nacional de análisis de riesgos agroclimáticos para las principales especies frutales y cultivos, y la ganadería, , http://newsflash.asoex.cl/userfiles/file/269; Jankovic, S., Popovic, V., Ikanovic, J., Rakic, S., Kuzevski, J., Gavrilovic, M., Productivity traits of rye (Secale cereale), khorasan wheat (Triticum turgidum. ssp. 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PY - 2018

Y1 - 2018

N2 - Symbiotic associations with microbes can help plants to respond to environmental changes. In this study, we investigated how colonization by root endophytic fungi enhances performance of Chenopodium quinoa and its ability to cope with extended periods of drought. The fungus Penicillium minioluteum, which was isolated from quinoa naturally occurring in the Atacama Desert, was used for endophyte colonization. We developed a greenhouse experiment, subjecting endophyte-infected (E+) and endophyte-free (E−) plants to two treatments: water deficit and abundant water availability. Differences in plant performance, photosynthesis, water-use efficiency and photochemical efficiency between E+ and E− plants under both water treatments were examined. We assessed the nature of the plant–symbiont interaction (parasitic or mutualistic) under both treatment conditions. We found that P. minioluteum initially affected radicle growth, subsequently triggering improvements in root formation, with the latter particularly evident under drought conditions. Under low water, E+ plants demonstrated a 40% improvement in root formation relative to E− plants; however, physiological responses to drought were not demonstrably enhanced by the presence of endophytic fungi. The nature of the interaction appeared to be positive, but only under conditions of water stress. Our study demonstrates that, in C. quinoa, P. minioluteum assists in coping with water stress primarily by affecting substantial root biomass adjustments, and that host benefits in this relationship are conferred in conditions of stress only. © 2017, Springer Science+Business Media B.V., part of Springer Nature.

AB - Symbiotic associations with microbes can help plants to respond to environmental changes. In this study, we investigated how colonization by root endophytic fungi enhances performance of Chenopodium quinoa and its ability to cope with extended periods of drought. The fungus Penicillium minioluteum, which was isolated from quinoa naturally occurring in the Atacama Desert, was used for endophyte colonization. We developed a greenhouse experiment, subjecting endophyte-infected (E+) and endophyte-free (E−) plants to two treatments: water deficit and abundant water availability. Differences in plant performance, photosynthesis, water-use efficiency and photochemical efficiency between E+ and E− plants under both water treatments were examined. We assessed the nature of the plant–symbiont interaction (parasitic or mutualistic) under both treatment conditions. We found that P. minioluteum initially affected radicle growth, subsequently triggering improvements in root formation, with the latter particularly evident under drought conditions. Under low water, E+ plants demonstrated a 40% improvement in root formation relative to E− plants; however, physiological responses to drought were not demonstrably enhanced by the presence of endophytic fungi. The nature of the interaction appeared to be positive, but only under conditions of water stress. Our study demonstrates that, in C. quinoa, P. minioluteum assists in coping with water stress primarily by affecting substantial root biomass adjustments, and that host benefits in this relationship are conferred in conditions of stress only. © 2017, Springer Science+Business Media B.V., part of Springer Nature.

KW - Plant tolerance

KW - Quinoa

KW - Root formation

KW - Root-associated fungi

KW - Water deficit

KW - biomass

KW - colonization

KW - drought stress

KW - endophyte

KW - fungus

KW - herb

KW - physiological response

KW - root system

KW - water availability

KW - water stress

KW - Atacama Desert

KW - Chile

KW - Chenopodium quinoa

KW - Fungi

KW - Penicillium minioluteum

U2 - 10.1007/s11258-017-0791-1

DO - 10.1007/s11258-017-0791-1

M3 - Article

VL - 219

SP - 231

EP - 240

JO - Plant Ecology

T2 - Plant Ecology

JF - Plant Ecology

SN - 1385-0237

IS - 3

ER -