Abstract
Increasing water use efficiency (WUE) in crops is critical to maintaining agricultural production under climate change-exacerbated drought. One of these approaches may consist of leveraging on the beneficial interactions between crops and arbuscular mycorrhizal fungi (AMF). In this study, we investigated how inoculation with AMF from three different taxa (Claroideoglomus etunicatum (T1), Gigaspora margarita (T2), and Rhizophagus irregularis (T3)) and their combination (T123) and a non-inoculated “control” treatment in a greenhouse could achieve increased biomass production and water use efficiency in cassava under three levels of water availability (100% PC, 60%—moderate stress, and 30%—severe stress). Whereas T1 and T2 resulted in a lower growth rate for the plants than the control, T123 enhanced cassava height and the number of petioles and leaves. T123 and T3 increased the total plant dry biomass in comparison with uninoculated plants by 30% and 26%, respectively. The T123 and plants inoculated with T3 significantly increased cassava above-ground biomass by 19% as compared to T1 (8.68 ± 2.44 g) and T2 (8.68 ± 2.44 g) inoculated plants. T123 resulted in higher WUE, which was validated by the leaf carbon (δ13C) isotopic signature, significantly outperforming cassava with T1 and T2, yet there was no difference between the control and T3. Overall, this study demonstrated that the use of multiple AMF from different taxa can increase cassava growth and WUE under greenhouse conditions.
Graphical Abstract
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Data and codes are available upon request.
References
Ali S, Xu Y, Jia Q et al (2018) Cultivation techniques combined with deficit irrigation improves winter wheat photosynthetic characteristics, dry matter translocation and water use efficiency under simulated rainfall conditions. Agric Water Manag 201:207–218. https://doi.org/10.1016/j.agwat.2018.01.017
Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42. https://doi.org/10.1007/s005720100097
Boyer LR, Brain P, Xu XM, Jeffries P (2015) Inoculation of drought-stressed strawberry with a mixed inoculum of two arbuscular mycorrhizal fungi: effects on population dynamics of fungal species in roots and consequential plant tolerance to water deficiency. Mycorrhiza 25:215–227. https://doi.org/10.1007/s00572-014-0603-6
Carluccio AV, David LC, Claußen J, Sulley M, Adeoti SR, Abdulsalam T, Gerth S, Zeeman SC, Gisel A, Stavolone L (2022) Set up from the beginning: the origin and early development of cassava storage roots. Plant Cell Environ 45(6):1779–1795. https://doi.org/10.1111/pce.14300
Chen YJ, Yu JJ, Huang B (2015) Effects of elevated CO2 concentration on water relations and photosynthetic responses to drought stress and recovery during rewatering in tall fescue. J Am Soc Hortic Sci 140:19–26. https://doi.org/10.21273/jashs.140.1.19
Chen S, Zhao H, Zou C et al (2017) Combined inoculation with multiple arbuscular mycorrhizal fungi improves growth, nutrient uptake and photosynthesis in cucumber seedlings. Front Microbiol 8:1–11. https://doi.org/10.3389/fmicb.2017.02516
Coelho IR, Pedone-Bonfim MV, Silva FS, Maia LC (2014) Optimization of the production of mycorrhizal inoculum on substrate with organic fertilizer. Braz J Microbiol 5:11738. https://doi.org/10.1590/S1517-83822014000400007
Daniels BA, Skipper HA (1982) Methods for the recovery and quantitative estimation of propagules from soil. In: Schenck NC (ed) Methods & Principles of Mycorrhizal Research. American Phytopathological Society, St. Paul, pp 29–35
Drapal M, Barros De Carvalho E, Ovalle Rivera TM et al (2019) Capturing biochemical diversity in cassava (Manihot esculenta Crantz) through the application of metabolite profiling. J Agric Food Chem 67:986–993. https://doi.org/10.1021/acs.jafc.8b04769
Du B, Zheng J, Ji H et al (2021) Stable carbon isotope used to estimate water use efficiency can effectively indicate seasonal variation in leaf stoichiometry. Ecol Indic 121:107250. https://doi.org/10.1016/j.ecolind.2020.107250
Eleki K, Cruse RM, Albrecht KA (2005) Root segregation of C3 and C4 species using carbon isotope composition. Crop Sci 45:879–882. https://doi.org/10.2135/cropsci2004.0170
Evelin H, Devi TS, Gupta S, Kapoor R (2019) Mitigation of salinity stress in plants by arbuscular mycorrhizal symbiosis: current understanding and new challenges. Front Plant Sci 2019:470. https://doi.org/10.3389/fpls.2019.00470
Farquhar GD, Richards RA (1984) Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes. Aust J Plant Physiol 11:539–552. https://doi.org/10.1071/PP9840539
Fitter AH (2005) Darkness visible: reflections on underground ecology. J Ecol 93:231–243. https://doi.org/10.1111/j.0022-0477.2005.00990.x
Hart MM, Reader RJ (2002) Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytol 153:335–344. https://doi.org/10.1046/j.0028-646X.2001.00312.x
Hart MM, Reader RJ, Klironomos JN (2001) Life-history strategies of arbuscular mycorrhizal fungi in relation to their successional dynamics. Mycologia 93:1186–1194. https://doi.org/10.1080/00275514.2001.12063251
Hu S, Hu B, Chen Z, Vosatka M, Vymazal J (2020) Antioxidant response in arbuscular mycorrhizal fungi inoculated wetland plant under Cr stress. Environ Res 1(191):110203. https://doi.org/10.1016/j.envres.2020.110203
Imakumbili MLE (2019) Making water stress treatments in pot experiments: an illustrated step-by-step guide. ProtocolsIo 7:1–20. https://doi.org/10.17504/protocols.io.2xdgfi6
Imakumbili MLE, Semu E, Semoka JMR et al (2021) Managing cassava growth on nutrient poor soils under different water stress conditions. Heliyon 7:e07331. https://doi.org/10.1016/j.heliyon.2021.e07331
IPCC (2018) Summary for policymakers. In: Masson-Delmotte V, Zhai P, Pörtner H-O, Roberts D, Skea J, Shukla PR, Pirani A, Moufouma-Okia W, Péan C, Pidcock R, Connors S, Matthews JBR, Chen Y, Zhou X, Gomis MI, Lonnoy E, Maycock T, Tignor M, Waterfield T (eds) Global warming of 1.5°C. An IPCC special report on the impacts of global warming of 1.5 °C above pre-industrial levels and related global greenhouse gas emission pathways, in the context of strengthening the global response to the threat of climate change, sustainable development, and efforts to eradicate poverty. World Meteorological Organization, Geneva, Switzerland. Retrieved February 20, 2019, from https://www.ipcc.ch/sr15/chapter/summary-for-policy-makers/
Jangra S, Mishra A, Kamboj D, Yadav NR, Yadav RC (2017) Engineering abiotic stress tolerance traits for mitigating climate change . In: Gahlawat SK (ed) Plant biotechnology: recent advancements and developments. Springer Nature Singapore Pte Ltd, pp 59–73. https://doi.org/10.1007/978-981-10-4732-9_3
Jansa J, Smith FA, Smith SE (2008) Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi? New Phytol 177:779–789. https://doi.org/10.1111/j.1469-8137.2007.02294.x
Kakouridis A, Hagen JA, Kan MP et al (2022) Routes to roots: direct evidence of water transport by arbuscular mycorrhizal fungi to host plants. New Phytol. https://doi.org/10.1111/nph.18281
Klironomos JN, Hart MM (2002) Colonization of roots by arbuscular mycorrhizal fungi using different sources of inoculum. Mycorrhiza 12:181–184. https://doi.org/10.1007/s00572-002-0169-6
Koide RT (2000) Functional complementarity in the arbuscular mycorrhizal symbiosis. New Phytol 147:233–235. https://doi.org/10.1046/j.1469-8137.2000.00710.x
Kong J, Pei Z, Du M et al (2014) Effects of arbuscular mycorrhizal fungi on the drought resistance of the mining area repair plant sainfoin. Int J Min Sci Technol 24:485–489. https://doi.org/10.1016/j.ijmst.2014.05.011
Kostaki KI, Coupel-Ledru A, Bonnell VC et al (2020) Guard cells integrate light and temperature signals to control stomatal aperture. Plant Physiol 182:1404–1419. https://doi.org/10.1104/PP.19.01528
Lawson T, Matthews J (2020) Guard cell metabolism and stomatal function. Annu Rev Plant Biol 71:273–302. https://doi.org/10.1146/annurev-arplant-050718-100251
Marshall JD, Zhang J (2014) Rockies and water-use. Carbon isotope discrimination and water-use efficiency in native plants of the North-Central rockies. Ecology 75(7):1887–1895. https://doi.org/10.2307/1941593
McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytologist 115(3):495–501
Monokrousos N, Papatheodorou EM, Orfanoudakis M et al (2020) The effects of plant type, AMF inoculation and water regime on rhizosphere microbial communities. Eur J Soil Sci 71:265–278. https://doi.org/10.1111/ejss.12882
Oliveira TC, Cabral JSR, Santana LR et al (2022) The arbuscular mycorrhizal fungus Rhizophagus clarus improves physiological tolerance to drought stress in soybean plants. Sci Rep 12:1–15. https://doi.org/10.1038/s41598-022-13059-7
Ortas I, Sari N, Akpinar C, Yetisir H (2013) Selection of arbuscular mycorrhizal fungi speciesfor tomato seedling growth, mycorrhizal dependency and nutrient uptake. Eur J Hortic Sci 78(5):209–218
Oyetunji OJ, Ekanayake IJ, Osonubi O (2007) Chlorophyll fluorescence analysis for assessing water deficit and arbuscular mycorrhizal fungi (AMF) inoculation in cassava (Manihot esculenta Crantz). Adv Biol Res 1(3–4):108–17
Pellegrino E, Bedini S (2014) Enhancing ecosystem services in sustainable agriculture: biofertilization and biofortification of chickpea (Cicer arietinum L.) by arbuscular mycorrhizal fungi. Soil Biol Biochem 68:429–439. https://doi.org/10.1016/j.soilbio.2013.09.030
Peña-Venegas CP, Kuyper TW, Davison J, Jairus T, Vasar M, Stomph TJ, Öpik M (2019) Distinct arbuscular mycorrhizal fungal communities associate with different manioc landraces and Amazonian soils. Mycorrhiza 29:263–275. https://doi.org/10.1007/s00572-019-00891-5
Pirasteh-Anosheh H, Saed-Moucheshi A, Pakniyat H, Pessarakli M (2016) Stomatal responses to drought stress. Water Stress Crop Plants A Sustain Approach 1–2:24–40. https://doi.org/10.1002/9781119054450.ch3
Powell JR, Rillig MC (2018) Biodiversity of arbuscular mycorrhizal fungi and ecosystem function. New Phytol 220:1059–1075
Rauf S, Al-Khayri JM, Zaharieva M et al (2016) Breeding strategies to enhance drought tolerance in crops. Adv Plant Breed Strateg Agron Abiotic Biot Stress Trait 2:397–445. https://doi.org/10.1007/978-3-319-22518-0_11
Samarah NH (2005) Effects of drought stress on growth and yield of barley. Agron Sustain Dev 25:145–149. https://doi.org/10.1051/agro
Sánchez-Díaz M, Honrubia M (1994) Water relations and alleviation of drought stress in mycorrhizal plants. Impact Arbuscular Mycorrhizas Sustain Agric Nat Ecosyst 167–178. https://doi.org/10.1007/978-3-0348-8504-1_13
Schmidt G, Gebauer G, Widmann K, Ziegler H (1993) Influence of nitrogen supply and temperature on stable carbon isotope ratios in plants of different photosynthetic pathways (C 3, C 4, CAM). Isot Isot Environ Heal Stud 29:9–13. https://doi.org/10.1080/10256019308046129
Seibt U, Rajabi A, Griffiths H, Berry JA (2008) Carbon isotopes and water use efficiency: sense and sensitivity. Oecologia 155:441–54. https://doi.org/10.1007/s00442-007-0932-7
Serdeczny O, Adams S, Baarsch F et al (2017) Climate change impacts in Sub-Saharan Africa: from physical changes to their social repercussions. Reg Environ Chang 17:1585–1600. https://doi.org/10.1007/s10113-015-0910-2
Silva FSB, Yano-Melo AM, Brandão JAC, Maia LC(2005) Sporulation of arbuscular mycorrhizal fungi using Tris-HCl buffer in addition to nutrient solutions. Brazillian J Microbiol 327–332. https://www.scielo.br/j/bjm/a/hZf9DjfWTJbfjhY75RzJggN/?lang=en
Smith SE, Read D (2008) Mineral nutrition, toxic element accumulation and water relations of arbuscular mycorrhizal plants. Mycorrhizal Symbiosis 145–VI. https://doi.org/10.1016/b978-012370526-6.50007-6
Stanhill G (1986) Water use efficiency. Adv Agron 39:53–85
Straker CJ, Hilditch AJ, Rey ME (2010) Arbuscular mycorrhizal fungi associated with cassava (Manihot esculenta Crantz) in South Africa. S Afr J Bot 76(1):102–111. https://doi.org/10.1016/j.sajb.2009.09.005
Sun ZJ, Livingston NJ, Guy RD, Ethier GJ (1996) Stable carbon isotopes as indicators of increased water use efficiency and productivity in white spruce (Picea glauca (Moench) Voss) seedlings. Plant, Cell Environ 19:887–894. https://doi.org/10.1111/j.1365-3040.1996.tb00425.x
Sylvia DM (1994) Vesicular-arbuscular mycorrhizal (VAM) fungi. In: Weaver RW, Angle JS, Bottomley PJ, Bezdicek D, Smith S, Tabatabai A, Wollum AG (eds) Methods of Soil Analysis, part 2. Microbiological and Biochemical Properties. Soil Science Society of America, Madison, Wis, pp 351–378
Tallec T, Béziat P, Jarosz N et al (2013) Crops’ water use efficiencies in temperate climate: comparison of stand, ecosystem and agronomical approaches. Agric for Meteorol 168:69–81. https://doi.org/10.1016/j.agrformet.2012.07.008
Thanni B, Merckx R, De Bauw P et al (2022) Spatial variability and environmental drivers of cassava—arbuscular mycorrhiza fungi (AMF) associations across Southern Nigeria. Mycorrhiza 32:1–13. https://doi.org/10.1007/s00572-021-01058-x
Tilman D (1997) Community invasibility, recruitment limitation, and grassland biodiversity. Ecology 78(1):81–92
Turner NC (2019) Imposing and maintaining soil water deficits in drought studies in pots. Plant and Soil 45–55. https://doi.org/10.1007/s11104-018-3893-1
UN (2022) Department of Economic and Social Affairs, Population Division. World Population Prospects: The 2022 Revision. United Nations, New York. https://www.un.org/en/desa/world-population-reach-8-billion-15-november-2022
Van der Heijden MGA, Boller T, Wiemken A, Sanders IR (1998) Different arbuscular mycorrhizal fungal species are potential determinants of plant community structure. Ecology 79:2082–2091. https://doi.org/10.1890/0012-9658(1998)079[2082:DAMFSA]2.0.CO;2
Van Geel M, De Beenhouwer M, Lievens B, Honnay O (2016) Crop-specific and single-species mycorrhizal inoculation is the best approach to improve crop growth in controlled environments. Agron Sustain Dev 36:1–10
Wang FY, Lin XG, Yin R (2007) Effect of arbuscular mycorrhizal fungal inoculation on heavy metal accumulation of maize grown in a naturally contaminated soil. Int J Phytoremediation 9:345–353. https://doi.org/10.1080/15226510701476214
Wickham H (2016) ggplot2: Elegant graphics for data analysis. Springer-Verlag, New York
World Resources Institute (WRI) (2018) World Resources Institute FLW value calculator. Retrieved from http://www.flwprotocol.org/why-measure/food-loss-and-waste-value-calculator/
Acknowledgements
B.T. acknowledges Kasper Van Acker for his unrelenting support throughout the experiment. We also thank The International Institute of Tropical Agriculture, Ibadan (IITA) for the supply of cassava stakes.
Funding
B.T. benefits from a PhD grant of the Research Council of KU Leuven, from 2020 to 2024. Research costs were also provided by a Bill and Melinda Gate Foundation grant (INV-023484) African Cassava Agronomy Initiative to IITA.
Author information
Authors and Affiliations
Contributions
The research was designed by B.T., R.M., and O.H.; samples were collected by B.T.; laboratory analysis was done by B.T.; data were analyzed by B.T.; and the manuscript draft was written by B.T. with substantial contributions from O.H., R.M., S.H., and A.S. All authors reviewed and edited the final manuscript, and supervision of the research was done by R.M. and O.H.
Corresponding author
Ethics declarations
Ethics approval
Approval of the research program was obtained by the Ethics and Privacy Committee of KU Leuven preceding grant approval.
Competing interests
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Thanni, B., Merckx, R., Hauser, S. et al. Multiple taxa inoculants of arbuscular mycorrhizal fungi enhanced colonization frequency, biomass production, and water use efficiency of cassava (Manihot esculenta). Int Microbiol (2023). https://doi.org/10.1007/s10123-023-00466-7
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10123-023-00466-7