Abstract
Arbuscular mycorrhizal fungi (AMF) are obligate plant symbionts of most land plants. In these organisms, thousands of nuclei that are either genetically similar (homokaryotic) or derived from two distinct parents (dikaryotic) co-exist in a large syncytium. Here, we investigated the impact of these two nuclear organizations on the mycorrhizal response of potatoes (Solanum tuberosum) by inoculating four potato cultivars with eight Rhizophagus irregularis strains individually (four homokaryotic and four dikaryotic). By evaluating plant and fungal fitness-related traits four months post inoculation, we found that AMF genetic organization significantly affects the mycorrhizal response of host plants. Specifically, homokaryotic strains lead to higher total, shoot, and tuber biomass and a higher number of tubers, compared to dikaryotic strains. However, fungal fitness-related traits showed no clear differences between homokaryotic and dikaryotic strains. Nucleotype content analysis of single spores confirmed that the nucleotype ratio of AMF heterokaryon spores can shift depending on host identity. Together, these findings continue to highlight significant ecological differences derived from the two distinct genetic organizations in AMF.
Similar content being viewed by others
Availability of data and materials
Data are available as a supplemental excel file and metadata file.
References
Bago B, Azcón-Aguilar C, Piché Y (1997) Architecture and developmental dynamics of the external mycelium of the arbuscular mycorrhizal fungus Glomus intraradices grown under monoxenic conditions. Mycologia 90:52–62. https://doi.org/10.1080/00275514.1998.12026878
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):1–48. https://doi.org/10.18637/jss.v067.i01
Baon JB, Smith SE, Alston AM (1993) Mycorrhizal responses of barley cultivars differing in P efficiency. Plant Soil 157:97–105. https://doi.org/10.1007/BF02390231
Bécard G, Fortin JA (1988) Early events of vesicular–arbuscular mycorrhiza formation on Ri T-DNA transformed roots. New Phytol 108:211–218. https://doi.org/10.1111/j.1469-8137.1988.tb03698.x
Black RLB, Tinker PB (1977) Interaction between effects of vesicular- arbuscular mycorrhiza and fertilizer phosphorus on yields of potatoes in field. Nature 267:510–511. https://doi.org/10.1038/267510a0
Bonfante P, Genre A (2010) Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis. Nat Commun 1:1–11. https://doi.org/10.1038/ncomms1046
Ceballos I, Mateus ID, Peña R, Peña-Quemba DC, Robbins C, Ordoñez YM, Rosikiewicz P, Rojas EC, Thuita M, Mlay DP, Masso C, Vanlauwe B, Rodriguez A, Sanders IR (2019) Using variation in arbuscular mycorrhizal fungi to drive the productivity of the food security crop cassava. bioRxiv 1–21. https://doi.org/10.1101/830547
Chen ECH, Mathieu S, Hoffrichter A, Sedzielewska-Toro K, Peart M, Pelin A, Ndikumana S, Ropars J, Dreissig S, Fuchs J, Brachmann A, Corradi N (2018a) Single nucleus sequencing reveals evidence of inter-nucleus recombination in arbuscular mycorrhizal fungi. Elife 7:1–17. https://doi.org/10.7554/eLife.39813
Chen ECH, Morin E, Beaudet D, Noel J, Yildirir G, Ndikumana S, Charron P, St-Onge C, Giorgi J, Krüger M, Marton T, Ropars J, Grigoriev IV, Hainaut M, Henrissat B, Roux C, Martin F, Corradi N (2018b) High intraspecific genome diversity in the model arbuscular mycorrhizal symbiont Rhizophagus irregularis. New Phytol 220:1161–1171. https://doi.org/10.1111/NPH.14989
Chen M, Arato M, Borghi L, Nouri E, Reinhardt D (2018c) Beneficial services of arbuscular mycorrhizal fungi – from ecology to application. Front Plant Sci 9:1–14. https://doi.org/10.3389/fpls.2018.01270
Cornell C, Kokkoris V, Turcu B, Dettman J, Stefani F, Corradi N (2022) The arbuscular mycorrhizal fungus Rhizophagus irregularis harmonizes nuclear dynamics in the presence of distinct abiotic factors. Fungal Genet Biol 158:103639. https://doi.org/10.1016/J.FGB.2021.103639
Dai M, Hamel C, Bainard LD, Arnaud MS, Grant CA, Lupwayi NZ, Malhi SS, Lemke R (2014) Negative and positive contributions of arbuscular mycorrhizal fungal taxa to wheat production and nutrient uptake efficiency in organic and conventional systems in the Canadian prairie. Soil Biol Biochem 74:156–166. https://doi.org/10.1016/j.soilbio.2014.03.016
Davies FT, Calderón CM, Huaman Z (2005) Influence of arbuscular mycorrhizae indigenous to Peru and a flavonoid on growth, yield, and leaf elemental concentration of “Yungay” potatoes. HortScience 40:381–385. https://doi.org/10.21273/hortsci.40.2.381
Doner LW, Bécard G (1991) Solubilization of gellan gels by chelation of cations. Biotechnol Tech 5:25–28. https://doi.org/10.1007/BF00152749
Duffy EM, Cassells AC (2000) The effect of inoculation of potato (Solanum tuberosum L.) microplants with arbuscular mycorrhizal fungi on tuber yield and tuber size distribution. Appl Soil Ecol 15:137–144. https://doi.org/10.1016/S0929-1393(00)00089-5
Ehinger M, Koch AM, Sanders IR (2009) Changes in arbuscular mycorrhizal fungal phenotypes and genotypes in response to plant species identity and phosphorus concentration. New Phytol 184:412–423. https://doi.org/10.1111/j.1469-8137.2009.02983.x
Feng Z, Liu X, Feng G, Zhu H, Yao Q (2020) Linking lipid transfer with reduced arbuscule formation in tomato roots colonized by arbuscular mycorrhizal fungus under low pH stress. Environ Microbiol 22:1036–1051. https://doi.org/10.1111/1462-2920.14810
Gerdemann JW, Nicolson TH (1963) Spores of mycorrhizal Endogone species extracted from soil by wet sieving and decanting. Trans Br Mycol Soc 46:235–244. https://doi.org/10.1016/s0007-1536(63)80079-0
Hammer EC, Pallon J, Wallander H, Olsson PA (2011) Tit for tat? A mycorrhizal fungus accumulates phosphorus under low plant carbon availability. FEMS Microbiol Ecol 76:236–244. https://doi.org/10.1111/J.1574-6941.2011.01043.X
Hijri M (2016) Analysis of a large dataset of mycorrhiza inoculation field trials on potato shows highly significant increases in yield. Mycorrhiza 26:209–214. https://doi.org/10.1007/s00572-015-0661-4
Janos DP (2007) Plant responsiveness to mycorrhizas differs from dependence upon mycorrhizas. Mycorrhiza 17:75–91. https://doi.org/10.1007/S00572-006-0094-1/FIGURES/5
Jin H, Germida JJ, Walley FL (2013) Impact of arbuscular mycorrhizal fungal inoculants on subsequent arbuscular mycorrhizal fungi colonization in pot-cultured field pea (Pisum sativum L.). Mycorrhiza 23:45–59. https://doi.org/10.1007/s00572-012-0448-9
Jung SC, Martinez-Medina A, Lopez-Raez JA, Pozo MJ (2012) Mycorrhiza-induced resistance and priming of plant defences. J Chem Ecol 38:651–664. https://doi.org/10.1007/S10886-012-0134-6
Keymer A, Pimprikar P, Wewer V, Huber C, Brands M, Bucerius SL, Delaux PM, Klingl V, von Röpenack-Lahaye E, Wang TL, Eisenreich W, Dörmann P, Parniske M, Gutjahr C (2017) Lipid transfer from plants to arbuscular mycorrhiza fungi. Elife 6. https://doi.org/10.7554/ELIFE.29107
Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301. https://doi.org/10.1890/02-0413
Klironomos JN, McCune J, Moutoglis P (2004) Species of arbuscular mycorrhizal fungi affect mycorrhizal responses to simulated herbivory. Appl Soil Ecol 26:133–141. https://doi.org/10.1016/j.apsoil.2003.11.001
Klironomos JN, McCune J, Hart M, Neville J, (2000) The influence of arbuscular mycorrhizae on the relationship between plant diversity and productivity. Ecol Lett 3:137–141. https://doi.org/10.1046/j.1461-0248.2000.00131.x
Koch AM, Antunes PM, Maherali H, Hart MM, Klironomos JN (2017) Evolutionary asymmetry in the arbuscular mycorrhizal symbiosis: conservatism in fungal morphology does not predict host plant growth. New Phytol 214:1330–1337. https://doi.org/10.1111/NPH.14465
Kokkoris V, Chagnon P-L, Yildirir G, Clarke K, Goh D, MacLean AM, Dettman J, Stefani F, Corradi N (2021a) Host identity influences nuclear dynamics in arbuscular mycorrhizal fungi. Curr Biol 31:1531–1538.e6. https://doi.org/10.1016/j.cub.2021.01.035
Kokkoris V, Hamel C, Hart MM (2019a) Mycorrhizal response in crop versus wild plants. PLoS ONE 14:1–16. https://doi.org/10.1371/journal.pone.0221037
Kokkoris V, Hart MM (2019) The role of in vitro cultivation on symbiotic trait and function variation in a single species of arbuscular mycorrhizal fungus. Fungal Biol 123:732–744. https://doi.org/10.1016/j.funbio.2019.06.009
Kokkoris V, Pogiatzis A, Hart MM (2019b) Contrasting common measures of arbuscular mycorrhizal fungal root colonization. J Microbiol Methods 167. https://doi.org/10.1016/j.mimet.2019.105727
Kokkoris V, Stefani F, Dalpé Y, Dettman J, Corradi N (2020) Nuclear dynamics in the arbuscular mycorrhizal fungi. Trends Plant Sci 25:765–778. https://doi.org/10.1016/j.tplants.2020.05.002
Kokkoris V, Vukicevich E, Richards A, Thomsen C, Hart MM (2021b) Challenges using droplet digital PCR for environmental samples. Appl Microbiol 1:74–88. https://doi.org/10.3390/applmicrobiol1010007
Liu C, Ravnskov S, Liu F, Rubæk GH, Andersen MN (2018) Arbuscular mycorrhizal fungi alleviate abiotic stresses in potato plants caused by low phosphorus and deficit irrigation/partial root-zone drying. J Agric Sci 156:46–58. https://doi.org/10.1017/S0021859618000023
Martignoni MM, Garnier J, Zhang X, Rosa D, Kokkoris V, Tyson RC, Hart MM (2021) Co-inoculation with arbuscular mycorrhizal fungi differing in carbon sink strength induces a synergistic effect in plant growth. J Theor Biol 531:110859. https://doi.org/10.1016/J.JTBI.2021.110859
Mathieu S, Cusant L, Roux C, Corradi N (2018) Arbuscular mycorrhizal fungi: intraspecific diversity and pangenomes. New Phytol 220:1129–1134. https://doi.org/10.1111/NPH.15275
McArthur DAJ, Knowles NR (1993) Influence of species of vesicular-arbuscular mycorrhizal fungi and phosphorus nutrition on growth, development, and mineral nutrition of potato (Solanum tuberosum L.). Plant Physiol 102:771–782. https://doi.org/10.1104/pp.102.3.771
McGonigle TP, Miller MH, Evans DG, Fairchild GL, SWAN, J.A., (1990) A new method which gives an objective measure of colonization of roots by vesicular- arbuscular mycorrhizal fungi. New Phytol 115:495–501. https://doi.org/10.1111/j.1469-8137.1990.tb00476.x
Mitra D, Saritha B, Janeeshma E, Gusain P, Khoshru B, Abo Nouh FA, Rani A, Olatunbosun AN, Ruparelia J, Rabari A, Mosquera-Sánchez LP, Mondal R, Verma D, Panneerselvam P, Das Mohapatra PK, Guerra Sierra BE (2022) Arbuscular mycorrhizal fungal association boosted the arsenic resistance in crops with special responsiveness to rice plant. Environ Exp Bot 193. https://doi.org/10.1016/j.envexpbot.2021.104681
Nelson DW, Sommers LE (1973) Determination of total nitrogen in plant material. Agron J 65:109–112. https://doi.org/10.2134/agronj1973.00021962006500010033x
Oksanen J, Blanchet G, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Henry M, Stevens H, Szoecs E, and Wagner H (2020) vegan: Community Ecology Package. R package version 2.5-7. https://CRAN.R-project.org/package=vegan
Peterson RA (2021) Finding optimal normalizing transformations via bestNormalize. The R Journal 13(1):310–329. https://doi.org/10.32614/RJ-2021-041
Püschel D, Bitterlich M, Rydlová J, Jansa J (2020) Facilitation of plant water uptake by an arbuscular mycorrhizal fungus: a Gordian knot of roots and hyphae. Mycorrhiza 30:299–313. https://doi.org/10.1007/s00572-020-00949-9
R Core Team (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Ropars J, Toro KS, Noel J, Pelin A, Charron P, Farinelli L, Marton T, Krüger M, Fuchs J, Brachmann A, Corradi N (2016) Evidence for the sexual origin of heterokaryosis in arbuscular mycorrhizal fungi. Nat Microbiol 1:1–9. https://doi.org/10.1038/nmicrobiol.2016.33
Ryan MH, Kirkegaard JA (2012) The agronomic relevance of arbuscular mycorrhizas in the fertility of Australian extensive cropping systems. Agric Ecosyst Environ 163:37–53. https://doi.org/10.1016/j.agee.2012.03.011
Ryan MH, van Herwaarden AF, Angus JF, Kirkegaard JA (2005) Reduced growth of autumn-sown wheat in a low-P soil is associated with high colonisation by arbuscular mycorrhizal fungi. Plant Soil. https://doi.org/10.1007/s11104-004-1611-7
Sawers RJH, Gutjahr C, Paszkowski U (2008) Cereal mycorrhiza: an ancient symbiosis in modern agriculture. Trends Plant Sci 13:93–97. https://doi.org/10.1016/j.tplants.2007.11.006
Serghi EU, Kokkoris V, Cornell C, Dettman J, Stefani F, Corradi N (2021) Homo- and dikaryons of the arbuscular mycorrhizal fungus Rhizophagus irregularis differ in life history strategy. Front Plant Sci 12. https://doi.org/10.3389/fpls.2021.715377
Smith S, Read D (2008) Mycorrhizal symbiosis, mycorrhizal symbiosis. Academic Press. https://doi.org/10.1016/B978-0-12-370526-6.X5001-6
Sperschneider J, Yildirir G, Rizzi Y, Malar CM, Sorwar E, Chen EC, Iwasaki W, Brauer EK, Bosnich W, Gutjahr C, Corradi N (2023) Resolving the haplotypes of arbuscular mycorrhizal fungi highlights the role of two nuclear populations in host interactions. bioRxiv 2023.01.15.524138. https://doi.org/10.1101/2023.01.15.524138
Stahlhut KN, Conway M, Mason CM, Bauer JT (2023) Intraspecific variation in mycorrhizal response is much larger than ecological literature suggests. Ecology 104:5. https://doi.org/10.1002/ecy.4015
Tedersoo L, Bahram M, Zobel M (2020) How mycorrhizal associations drive plant population and community biology. Science 367. https://doi.org/10.1126/science.aba1223
Trouvelot A (1986) Estimation of vesicular arbuscular mycorrhizal infection levels: Research for methods having a functional significance. Physiol Genet Asp Mycorrhizae 217–221
van’t Padje A, Bonfante P, Ciampi LT, Kiers ET (2021a) Quantifying nutrient trade in the arbuscular mycorrhizal symbiosis under extreme weather events using quantum-dot tagged phosphorus. Front Ecol Evol 9. https://doi.org/10.3389/fevo.2021.613119
van’t Padje A, Werner GDA, Kiers ET (2021b) Mycorrhizal fungi control phosphorus value in trade symbiosis with host roots when exposed to abrupt ‘crashes’ and ‘booms’ of resource availability. New Phytol 229:2933–2944. https://doi.org/10.1111/NPH.17055
Vierheilig H, Coughlan AP, Wyss U, Piché Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microbiol 64:5004–5007. https://doi.org/10.1128/AEM.64.12.5004-5007.1998
Wickham H (2016) ggplot2: Elegant Graphics for Data Analysis. https://ggplot2.tidyverse.org
Yamaguchi J (2002) Measurement of root diameter in field-grown crops under a microscope without washing. Soil Sci Plant Nutr 48:625–629. https://doi.org/10.1080/00380768.2002.10409248
Yildirir G, Sperschneider J, Malar C M, Chen ECH, Iwasaki W, Cornell C, Corradi N (2022) Long reads and Hi-C sequencing illuminate the two-compartment genome of the model arbuscular mycorrhizal symbiont Rhizophagus irregularis. New Phytol 233:1097–1107. https://doi.org/10.1111/NPH.17842
Acknowledgements
We thank Andrew Vigars and Savannah Pilgrim for their assistance in lab.
Funding
Our research was funded by the Discovery Program of the Natural Sciences and Engineering Research Council (RGPIN2020-05643), a Discovery Accelerator Supplements Program (RGPAS-2020–00033). NC is a University of Ottawa Research Chair and VK was supported by the MITACS Industrial PDF program (IT16902) and by the Agriculture and Agri-Food Canada (AAFC) through the project J-002272.
Author information
Authors and Affiliations
Contributions
N.C. and V.K. conceived and designed the experiments. V.K. maintained and propagated the potato in-vitro plantlets. V.T. maintained and propagated the AMF strains. V.T., V.K., and B.T. established the greenhouse experiment. V.T. monitored the greenhouse experiment for its duration and V.T., V.K., B.T., M.V.L., and C.C. harvested the experiment. Z.Z. performed the plant tissue nutrient analysis, K.C. quantified the spores, V.T. and M.V.L. quantified the mycorrhizal colonization and the plant biomass, V.T. performed the ddPCR analysis for nucleotype abundance. V.T. and V.K. performed the statistical analysis. V.T., N.C., and V.K. drafted the manuscript, and all co-authors discussed the results and contributed to the final version of the manuscript.
Corresponding author
Ethics declarations
Ethics approval
Not applicable.
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
Terry, V., Kokkoris, V., Villeneuve-Laroche, M. et al. Mycorrhizal response of Solanum tuberosum to homokaryotic versus dikaryotic arbuscular mycorrhizal fungi. Mycorrhiza 33, 333–344 (2023). https://doi.org/10.1007/s00572-023-01123-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00572-023-01123-7