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Plant function and evolutionary biology
RESEARCH ARTICLE

Impact of an arbuscular mycorrhizal fungus on the growth and nutrition of fifteen crop and pasture plant species

Binh T. T. Tran A B , Stephanie J. Watts-Williams A C and Timothy R. Cavagnaro https://orcid.org/0000-0002-9922-5677 A D
+ Author Affiliations
- Author Affiliations

A The Waite Research Institute and The School of Agriculture, Food and Wine, The University of Adelaide, Waite Campus, PMB1 Glen Osmond, SA 5064, Australia.

B Faculty of Agriculture and Forestry, Tay Nguyen University, Buon Ma Thuot city, Daklak Province, 63131, Vietnam.

C Australian Research Council Centre of Excellence in Plant Energy Biology, University of Adelaide, Waite Campus, PMB1 Glen Osmond, SA 5064, Australia.

D Corresponding author. Email: timothy.cavagnaro@adelaide.edu.au

Functional Plant Biology 46(8) 732-742 https://doi.org/10.1071/FP18327
Submitted: 13 July 2018  Accepted: 21 March 2019   Published: 16 May 2019

Abstract

The formation of arbuscular mycorrhizas (AM) can result in positive, neutral or negative responses in the growth and mineral nutrition of host plants, particularly that of P, Zn and other micronutrients. This study examined the growth and nutritional responses of 15 agriculturally important plant species, including cereals, legumes and vegetables, with and without inoculation with the AM fungus (AMF) Rhizophagus irregularis. Furthermore, we explored whether the responses differed between different functional groups of plants such as monocots and dicots, C3 and C4 plants, and N-fixing and non-N-fixing plants. We found that that mycorrhizal colonisation of roots, plant growth and plant nutrient responses differed between plant species. Among the species analysed, leek (Allium ampeloprasum L. var. porrum) was the most mycorrhiza-responsive, displaying the highest mycorrhizal colonisation and biomass response, and the greatest increases in most mineral nutrients. In other plant species, the concentration of P, Cu, Zn and S were generally enhanced by inoculation with AMF. Furthermore, ionomes differed more greatly between plant species than in response to inoculation with AMF. This research further improves our understanding of the responses of different and diverse plant species to the formation of AM in terms of growth and ionomics under standardised growth conditions. The results of this study may be used in further studies and to inform agricultural practices.

Additional keywords: food crops, growth response, ionomics, plant nutrition, Rhizophagus irregularis, yield.


References

Agte VV, Tarwadi KV, Mengale S, Chiplonkar SA (2000) Potential of traditionally cooked green leafy vegetables as natural sources for supplementation of eight micronutrients in vegetarian diets. Journal of Food Composition and Analysis 13, 885–891.
Potential of traditionally cooked green leafy vegetables as natural sources for supplementation of eight micronutrients in vegetarian diets.Crossref | GoogleScholarGoogle Scholar |

Ashwin R, Bagyaraj D, Mohan Raju B (2018) Evaluation of different arbuscular mycorrhizal fungi for selecting the best for inoculating soybean cultivars MAUS 2 and MAUS 212. Pertanika. Journal of Tropical Agricultural Science 41, 1587–1598.

Augé RM (2000) Stomatal behavior of arbuscular mycorrhizal plants. In ‘Arbuscular mycorrhizas: physiology and function’. (Eds Y Kapulnik, DD Douds) pp. 201–237. (Springer: Dordrecht).

Balog A, Loxdale H, Bálint J, Benedek K, Szabó K-A, Jánosi-Rancz KT, Erzsébet D (2017) The arbuscular mycorrhizal fungus Rhizophagus irregularis affects arthropod colonization on sweet pepper in both the field and greenhouse. Journal of Pest Science 90, 935–946.
The arbuscular mycorrhizal fungus Rhizophagus irregularis affects arthropod colonization on sweet pepper in both the field and greenhouse.Crossref | GoogleScholarGoogle Scholar |

Baum C, El-Tohamy W, Gruda N (2015) Increasing the productivity and product quality of vegetable crops using arbuscular mycorrhizal fungi: a review. Scientia Horticulturae 187, 131–141.
Increasing the productivity and product quality of vegetable crops using arbuscular mycorrhizal fungi: a review.Crossref | GoogleScholarGoogle Scholar |

Bender SF, Conen F, van der Heijden MGA (2015) Mycorrhizal effects on nutrient cycling, nutrient leaching and N2O production in experimental grassland. Soil Biology & Biochemistry 80, 283–292.
Mycorrhizal effects on nutrient cycling, nutrient leaching and N2O production in experimental grassland.Crossref | GoogleScholarGoogle Scholar |

Bender SF, Schlaeppi K, Held A, van der Heijden MGA (2019) Establishment success and crop growth effects of an arbuscular mycorrhizal fungus inoculated into Swiss corn fields. Agriculture, Ecosystems & Environment 273, 13–24.
Establishment success and crop growth effects of an arbuscular mycorrhizal fungus inoculated into Swiss corn fields.Crossref | GoogleScholarGoogle Scholar |

Bowles TM, Jackson LE, Loeher M, Cavagnaro TR (2017) Ecological intensification and arbuscular mycorrhizas: a meta-analysis of tillage and cover crop effects. Journal of Applied Ecology 54, 1785–1793.
Ecological intensification and arbuscular mycorrhizas: a meta-analysis of tillage and cover crop effects.Crossref | GoogleScholarGoogle Scholar |

Brundrett MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant and Soil 320, 37–77.
Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis.Crossref | GoogleScholarGoogle Scholar |

Cavagnaro TR (2015) Chapter 5: Biologically regulated nutrient supply systems: compost and arbuscular mycorrhizas – a review’. In ‘Advances in Agronomy. Vol. 129’. pp. 293–322. (Ed. DL Sparks) (Academic Press, San Diego, CA)

Cavagnaro TR, Smith FA, Lorimer MF, Haskard KA, Ayling SM, Smith SE (2001) Quantitative development of Paris-type arbuscular mycorrhizas formed between Asphodelus fistulosus and Glomus coronatum. New Phytologist 149, 105–113.
Quantitative development of Paris-type arbuscular mycorrhizas formed between Asphodelus fistulosus and Glomus coronatum.Crossref | GoogleScholarGoogle Scholar |

Feddermann N, Boller T, Salzer P, Elfstrand S, Wiemken A, Elfstrand M (2008) Medicago truncatula shows distinct patterns of mycorrhiza-related gene expression after inoculation with three different arbuscular mycorrhizal fungi. Planta 227, 671–680.
Medicago truncatula shows distinct patterns of mycorrhiza-related gene expression after inoculation with three different arbuscular mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar | 17965878PubMed |

Garg N, Chandel S (2011) Effect of mycorrhizal inoculation on growth, nitrogen fixation, and nutrient uptake in Cicer arietinum (L.) under salt stress. Turkish Journal of Agriculture and Forestry 35, 205–214.

Giovannetti M, Avio L (2002) Biotechnology of arbuscular mycorrhizas. In ‘Applied mycology and biotechnology Vol. 2: Agricultural and food production’. (Eds GG Khachatourians, DK Arora) pp. 275–310. (Elsevier: Amsterdam).

Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytologist 84, 489–500.
An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots.Crossref | GoogleScholarGoogle Scholar |

Hart MM, Forsythe JA (2012) Using arbuscular mycorrhizal fungi to improve the nutrient quality of crops; nutritional benefits in addition to phosphorus. Scientia Horticulturae 148, 206–214.
Using arbuscular mycorrhizal fungi to improve the nutrient quality of crops; nutritional benefits in addition to phosphorus.Crossref | GoogleScholarGoogle Scholar |

Hart MM, Antunes PM, Chaudhary VB, Abbott LK (2018) Fungal inoculants in the field: is the reward greater than the risk? Functional Ecology 32, 126–135.
Fungal inoculants in the field: is the reward greater than the risk?Crossref | GoogleScholarGoogle Scholar |

Hindumathi A, Reddy BN (2011) Dependency of sorghum on arbuscular mycorrhizal colonization for growth and development. Indian Journal of Mycology and Plant Pathology 41, 537–542.

Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC, Karst J, Koide RT, Pringle A, Zabinski C, Bever JD, Moore JC, Wilson GWT, Klironomos JN, Umbanhowar J (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecology Letters 13, 394–407.
A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar | 20100237PubMed |

Ibrikci H, Knewtson SJ, Grusak MA (2003) Chickpea leaves as a vegetable green for humans: evaluation of mineral composition. Journal of the Science of Food and Agriculture 83, 945–950.
Chickpea leaves as a vegetable green for humans: evaluation of mineral composition.Crossref | GoogleScholarGoogle Scholar |

IJdo M, Cranenbrouck S, Declerck S (2011) Methods for large-scale production of AM fungi: past, present, and future. Mycorrhiza 21, 1–16.
Methods for large-scale production of AM fungi: past, present, and future.Crossref | GoogleScholarGoogle Scholar | 20803040PubMed |

Kaeppler SM, Parke JL, Mueller SM, Senior L, Stuber C, Tracy WF (2000) Variation among maize inbred lines and detection of quantitative trait loci for growth at low phosphorus and responsiveness to arbuscular mycorrhizal fungi. Crop Science 40, 358–364.
Variation among maize inbred lines and detection of quantitative trait loci for growth at low phosphorus and responsiveness to arbuscular mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar |

Kahiluoto H, Vestberg M (1998) The effect of arbuscular mycorrhiza on biomass production and phosphorus uptake from sparingly soluble sources by leek (Allium porrum L.) in Finnish field soils. Biological Agriculture and Horticulture 16, 65–85.
The effect of arbuscular mycorrhiza on biomass production and phosphorus uptake from sparingly soluble sources by leek (Allium porrum L.) in Finnish field soils.Crossref | GoogleScholarGoogle Scholar |

Kim SJ, Eo JK, Lee EH, Park H, Eom AH (2017) Effects of arbuscular mycorrhizal fungi and soil conditions on crop plant growth. Mycobiology 45, 20–24.
Effects of arbuscular mycorrhizal fungi and soil conditions on crop plant growth.Crossref | GoogleScholarGoogle Scholar | 28435350PubMed |

Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84, 2292–2301.
Variation in plant response to native and exotic arbuscular mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar |

Kučová L, Kopta T, Sękara A, Pokluda R (2018) Controlling nitrate and heavy metals content in leeks (Allium porrum L.) using arbuscular mycorrhizal fungi inoculation. Polish Journal of Environmental Studies 27, 137–143.
Controlling nitrate and heavy metals content in leeks (Allium porrum L.) using arbuscular mycorrhizal fungi inoculation.Crossref | GoogleScholarGoogle Scholar |

Lehmann A, Veresoglou SD, Leifheit EF, Rillig MC (2014) Arbuscular mycorrhizal influence on zinc nutrition in crop plants – a meta-analysis. Soil Biology & Biochemistry 69, 123–131.
Arbuscular mycorrhizal influence on zinc nutrition in crop plants – a meta-analysis.Crossref | GoogleScholarGoogle Scholar |

Leigh J, Hodge A, Fitter AH (2009) Arbuscular mycorrhizal fungi can transfer substantial amounts of nitrogen to their host plant from organic material. New Phytologist 181, 199–207.
Arbuscular mycorrhizal fungi can transfer substantial amounts of nitrogen to their host plant from organic material.Crossref | GoogleScholarGoogle Scholar | 18811615PubMed |

Li H, Smith SE, Holloway RE, Zhu Y, Smith FA (2006) Arbuscular mycorrhizal fungi contribute to phosphorus uptake by wheat grown in a phosphorus-fixing soil even in the absence of positive growth responses. New Phytologist 172, 536–543.
Arbuscular mycorrhizal fungi contribute to phosphorus uptake by wheat grown in a phosphorus-fixing soil even in the absence of positive growth responses.Crossref | GoogleScholarGoogle Scholar | 17083683PubMed |

Miller RO (1998) Microwave digestion of plant tissue in a closed vessel. In ‘Handbook and reference methods for plant analysis’. (Ed. YP Kalra) pp. 53–56. (CRC Press: New York)

Miller RE, Gleadow RM, Cavagnaro TR (2014) Age versus stage: does ontogeny modify the effect of phosphorus and arbuscular mycorrhizas on above- and below-ground defence in forage sorghum? Plant, Cell & Environment 37, 929–942.
Age versus stage: does ontogeny modify the effect of phosphorus and arbuscular mycorrhizas on above- and below-ground defence in forage sorghum?Crossref | GoogleScholarGoogle Scholar |

Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nature Reviews. Microbiology 6, 763–775.
Arbuscular mycorrhiza: the mother of plant root endosymbioses.Crossref | GoogleScholarGoogle Scholar | 18794914PubMed |

Pellegrino E, Öpik M, Bonari E, Ercoli L (2015) Responses of wheat to arbuscular mycorrhizal fungi: a meta-analysis of field studies from 1975 to 2013. Soil Biology & Biochemistry 84, 210–217.
Responses of wheat to arbuscular mycorrhizal fungi: a meta-analysis of field studies from 1975 to 2013.Crossref | GoogleScholarGoogle Scholar |

Plenchette C, Fortin JA, Furlan V (1983) Growth responses of several plant species to mycorrhizae in a soil of moderate P-fertility. Plant and Soil 70, 199–209.
Growth responses of several plant species to mycorrhizae in a soil of moderate P-fertility.Crossref | GoogleScholarGoogle Scholar |

Porcel R, Aroca R, Ruiz-Lozano JM (2012) Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. Agronomy for Sustainable Development 32, 181–200.
Salinity stress alleviation using arbuscular mycorrhizal fungi. A review.Crossref | GoogleScholarGoogle Scholar |

Reinhart KO, Wilson GW, Rinella MJ (2012) Predicting plant responses to mycorrhizae: integrating evolutionary history and plant traits. Ecology Letters 15, 689–695.
Predicting plant responses to mycorrhizae: integrating evolutionary history and plant traits.Crossref | GoogleScholarGoogle Scholar | 22507627PubMed |

Rillig MC, Aguilar-Trigueros CA, Camenzind T, Cavagnaro TR, Degrune F, Hohmann P, Lammel DR, Mansour I, Roy J, van der Heijden MGA, Yang G (2019) Why farmers should manage the arbuscular mycorrhizal symbiosis: a response to Ryan & Graham (2018) ‘Little evidence that farmers should consider abundance or diversity of arbuscular mycorrhizal fungi when managing crops’. New Phytologist 222, 1171–1175.
Why farmers should manage the arbuscular mycorrhizal symbiosis: a response to Ryan & Graham (2018) ‘Little evidence that farmers should consider abundance or diversity of arbuscular mycorrhizal fungi when managing crops’.Crossref | GoogleScholarGoogle Scholar | 30657593PubMed |

Rouphael Y, Cardarelli M, Di Mattia E, Tullio M, Rea E, Colla G (2010) Enhancement of alkalinity tolerance in two cucumber genotypes inoculated with an arbuscular mycorrhizal biofertilizer containing Glomus intraradices. Biology and Fertility of Soils 46, 499–509.
Enhancement of alkalinity tolerance in two cucumber genotypes inoculated with an arbuscular mycorrhizal biofertilizer containing Glomus intraradices.Crossref | GoogleScholarGoogle Scholar |

Ryan MH, Angus JF (2003) Arbuscular mycorrhizae in wheat and field pea crops on a low P soil: increased Zn-uptake but no increase in P-uptake or yield. Plant and Soil 250, 225–239.
Arbuscular mycorrhizae in wheat and field pea crops on a low P soil: increased Zn-uptake but no increase in P-uptake or yield.Crossref | GoogleScholarGoogle Scholar |

Ryan MH, Graham JH (2018) Little evidence that farmers should consider abundance or diversity of arbuscular mycorrhizal fungi when managing crops. New Phytologist 220, 1092–1107.
Little evidence that farmers should consider abundance or diversity of arbuscular mycorrhizal fungi when managing crops.Crossref | GoogleScholarGoogle Scholar | 29987890PubMed |

Sasa M, Zahka G, Jakobsen I (1987) The effect of pretransplant inoculation with VA mycorrhizal fungi on the subsequent growth of leeks in the field. Plant and Soil 97, 279–283.
The effect of pretransplant inoculation with VA mycorrhizal fungi on the subsequent growth of leeks in the field.Crossref | GoogleScholarGoogle Scholar |

Smith SE, Read D (2008) Mycorrhizas in agriculture, horticulture and forestry. In ‘Mycorrhizal symbiosis’. (Eds SE Smith, D Read) pp. 144–187. (Academic Press: Oxford, UK)

Smith FA, Smith SE (2011) What is the significance of the arbuscular mycorrhizal colonisation of many economically important crop plants? Plant and Soil 348, 63
What is the significance of the arbuscular mycorrhizal colonisation of many economically important crop plants?Crossref | GoogleScholarGoogle Scholar |

Smith SE, Smith FA, Jakobsen I (2004) Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake. New Phytologist 162, 511–524.
Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake.Crossref | GoogleScholarGoogle Scholar |

Sorensen J, Larsen J, Jakobsen I, Tremblay N (Eds) (2002) ‘Management strategies for capturing the benefits of mycorrhizas in the production of field-grown vegetables, XXVI International Horticultural Congress: Toward ecologically sound fertilization strategies for field vegetable production 627.’ 11 August 2002, Toronto, Canada. (International Society for Horticultural Science)

Tang J, Chen J, Chen X (2006) Response of 12 weedy species to elevated CO2 in low-phosphorus-availability soil. Ecological Research 21, 664–670.
Response of 12 weedy species to elevated CO2 in low-phosphorus-availability soil.Crossref | GoogleScholarGoogle Scholar |

Tawaraya K (2003) Arbuscular mycorrhizal dependency of different plant species and cultivars. Soil Science and Plant Nutrition 49, 655–668.
Arbuscular mycorrhizal dependency of different plant species and cultivars.Crossref | GoogleScholarGoogle Scholar |

Thirkell TJ, Charters MD, Elliott AJ, Sait SM, Field KJ (2017) Are mycorrhizal fungi our sustainable saviours? Considerations for achieving food security. Journal of Ecology 105, 921–929.
Are mycorrhizal fungi our sustainable saviours? Considerations for achieving food security.Crossref | GoogleScholarGoogle Scholar |

van der Heijden MGA (2003) Arbuscular mycorrhizal fungi as a determinant of plant diversity: in search of underlying mechanisms and general principles. In ‘Mycorrhizal ecology’. (Eds MGA van der Heijden, IR Sanders) pp. 243–265. (Springer: Berlin, Heidelberg)

van der Heijden MGA, Streitwolf-Engel R, Riedl R, Siegrist S, Neudecker A, Ineichen K, Boller T, Wiemken A, Sanders IR (2006) The mycorrhizal contribution to plant productivity, plant nutrition and soil structure in experimental grassland. New Phytologist 172, 739–752.
The mycorrhizal contribution to plant productivity, plant nutrition and soil structure in experimental grassland.Crossref | GoogleScholarGoogle Scholar |

Vierheilig H, Coughlan AP, Wyss U, Piche Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Applied and Environmental Microbiology 64, 5004–5007.

Walker C, Vestberg M (1994) A simple and inexpensive method for producing and maintaining closed pot cultures of arbuscular mycorrhizal fungi. Agricultural and Food Science in Finland 3, 233–240.
A simple and inexpensive method for producing and maintaining closed pot cultures of arbuscular mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar |

Watts-Williams SJ, Patti AF, Cavagnaro TR (2013) Arbuscular mycorrhizas are beneficial under both deficient and toxic soil zinc conditions. Plant and Soil 371, 299–312.
Arbuscular mycorrhizas are beneficial under both deficient and toxic soil zinc conditions.Crossref | GoogleScholarGoogle Scholar |

Watts-Williams SJ, Tyerman SD, Cavagnaro TR (2017) The dual benefit of arbuscular mycorrhizal fungi under soil zinc deficiency and toxicity: linking plant physiology and gene expression. Plant and Soil 420, 375–388.
The dual benefit of arbuscular mycorrhizal fungi under soil zinc deficiency and toxicity: linking plant physiology and gene expression.Crossref | GoogleScholarGoogle Scholar |

Watts-Williams SJ, Emmett BD, Levesque-Tremblay V, MacLean AM, Sun X, Satterlee JW, Fei Z, Harrison MJ (2019a) Diverse Sorghum bicolor accessions show marked variation in growth and transcriptional responses to arbuscular mycorrhizal fungi. Plant, Cell & Environment
Diverse Sorghum bicolor accessions show marked variation in growth and transcriptional responses to arbuscular mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar |

Watts-Williams SJ, Cavagnaro TR, Tyerman SD (2019b) Variable effects of arbuscular mycorrhizal fungal inoculation on physiological and molecular measures of root and stomatal conductance of diverse Medicago truncatula accessions. Plant, Cell & Environment 42, 285–294.
Variable effects of arbuscular mycorrhizal fungal inoculation on physiological and molecular measures of root and stomatal conductance of diverse Medicago truncatula accessions.Crossref | GoogleScholarGoogle Scholar |

Zangaro W, Nishidate FR, Vandresen J, Andrade G, Nogueira MA (2007) Root mycorrhizal colonization and plant responsiveness are related to root plasticity, soil fertility and successional status of native woody species in southern Brazil. Journal of Tropical Ecology 23, 53–62.
Root mycorrhizal colonization and plant responsiveness are related to root plasticity, soil fertility and successional status of native woody species in southern Brazil.Crossref | GoogleScholarGoogle Scholar |

Zhang X, Wang L, Ma F, Yang JX, Su M (2017) Effects of arbuscular mycorrhizal fungi inoculation on carbon and nitrogen distribution and grain yield and nutritional quality in rice (Oryza sativa L.). Journal of the Science of Food and Agriculture 97, 2919–2925.
Effects of arbuscular mycorrhizal fungi inoculation on carbon and nitrogen distribution and grain yield and nutritional quality in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 27935053PubMed |

Zhang S, Lehmann A, Zheng W, You Z, Rillig MC (2019) Arbuscular mycorrhizal fungi increase grain yields: a meta-analysis. New Phytologist 222, 543–555.
Arbuscular mycorrhizal fungi increase grain yields: a meta-analysis.Crossref | GoogleScholarGoogle Scholar | 30372522PubMed |