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Exogenous abscisic acid and root volatiles increase sporulation of Rhizophagus irregularis DAOM 197198 in asymbiotic and pre-symbiotic status

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Abstract

Several studies have demonstrated asymbiotic growth and development of arbuscular mycorrhizal (AM) fungi, although AM fungi are regarded as obligately symbiotic root-inhabiting fungi. Phytohormones, root exudates, and volatiles are important factors regulating the host-AM fungi interaction. However, the effects of phytohormones, root exudates, and volatiles on asymbiotic (without roots present) or pre-symbiotic (with roots present but no colonization) sporulation of AM fungi are unexplored. In this study, we tested the asymbiotic sporulation of Rhizophagus irregularis DAOM 197198 and further investigated the influences of abscisic acid (ABA), the exudates, and volatiles of tomato hairy roots on asymbiotic or pre-symbiotic sporulation in vitro. Results indicated that mother spores asymbiotically and pre-symbiotically produced daughter spores singly or in pairs. Compared with symbiotically produced spores, pre-symbiotically produced spores were significantly smaller (43.1 μm vs. 89.2 μm in diameter). Exogenous ABA applied to mother spores significantly increased the number of daughter spores, and root volatiles also significantly promoted pre-symbiotic sporulation. Our results provide the first evidence that exogenous ABA can promote AM fungal asymbiotic and pre-symbiotic sporulation, which highlights the potential role of phytohormones in AM fungal propagation.

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References

  • Akiyama K, Matsuzaki KI, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827

    CAS  PubMed  Google Scholar 

  • Al-Babili S, Bouwmeester HJ (2015) Strigolactones, a novel carotenoid-derived plant hormone. Ann Rev Plant Biol 66:161–186

    CAS  Google Scholar 

  • Bécard G, Piché Y (1992) Establishment of vesicular-arbuscular mycorrhiza in root organ culture: review and proposed methodology. In: Norris JR, Read DJ, Varma AK (eds) Methods in microbiology, vol 24. Academic Press, Cambridge, pp 89–108

    Google Scholar 

  • Bécard G, Douds DD, Pfeffer PE (1992) Extensive in vitro hyphal growth of vesicular-arbuscular mycorrhizal fungi in the presence of CO2 and flavonols. Appl Environ Microbiol 58:821–825

    PubMed  PubMed Central  Google Scholar 

  • Besserer A, Bécard G, Jauneau A, Roux C, Séjalon-Delmas N (2008) GR24, a synthetic analog of strigolactones, stimulates the mitosis and growth of the arbuscular mycorrhizal fungus Gigaspora rosea by boosting its energy metabolism. Plant Physiol 148:402–413

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cao FY, DeFalco TA, Moeder W, Li B, Gong Y, Liu XM, Taniguchi M, Lumba S, Toh S, Shan L, Ellis B, Desveaux D, Yoshioka K (2018) Arabidopsis ETHYLENE RESPONSE FACTOR 8 (ERF8) has dual functions in ABA signaling and immunity. BMC Plant Biol 18:211

    CAS  PubMed  PubMed Central  Google Scholar 

  • Charpentier M, Sun J, Wen J, Mysore KS, Oldroyd GE (2014) Abscisic acid promotion of arbuscular mycorrhizal colonization requires a component of the PROTEIN PHOSPHATASE 2A complex. Plant Physiol 166:2077–2090

    PubMed  PubMed Central  Google Scholar 

  • Chen W, Li J, Zhu H, Xu P, Chen J, Yao Q (2017) The differential and interactive effects of arbuscular mycorrhizalfungus and phosphorus on the lateral root formation in Poncirus trifoliata (L.). Sci Hortic 217:258–265

    CAS  Google Scholar 

  • Coelho L, Mignoni DS, Silva FS, Braga MR (2019) Seed exudates of Sesbania virgata (Cav.) Pers. stimulate the asymbiotic phase of the arbuscular mycorrhizal fungus Gigaspora albida Becker Hall. Hoehnea 46:e272018

    Google Scholar 

  • Declerck S, Strullu DG, Plenchette C (1998) Monoxenic culture of the intraradical forms of Glomus sp. isolated from a tropical ecosystem: a proposed methodology for germplasm collection. Mycologia 90:579–585

    Google Scholar 

  • Dijksterhuis J (2018) Fungal spores: highly variable and stress-resistant vehicles for distribution and spoilage. Food Microbiol 81:2–11

    PubMed  Google Scholar 

  • Egamberdieva D, Wirth SJ, Alqarawi AA, Abd_Allah EF, Hashem A (2017) Phytohormones and beneficial microbes: essential components for plants to balance stress and fitness. Front Microbiol 8:2104

    PubMed  PubMed Central  Google Scholar 

  • Etemadi M, Gutjahr C, Couzigou JM, Zouine M, Lauressergues D, Timmers A, Audran C, Bouzayen M, Bécard G, Combier JP (2014) Auxin perception is required for arbuscule development in arbuscular mycorrhizal symbiosis. Plant Physiol 166:281–292

    PubMed  PubMed Central  Google Scholar 

  • Fousia S, Tsafouros A, Roussos PA, Tjamos SE (2018) Increased resistance to Verticillium dahliae in Arabidopsis plants defective in auxin signalling. Plant Pathol 67:1749–1757

    CAS  Google Scholar 

  • Gemma JN, Koske RE (1988) Pre-infection interactions between roots and the mycorrhizal fungus Gigaspora gigantea: chemotropism of germ-tubes and root growth response. Trans Bri Mycol Soc 91:123–132

    Google Scholar 

  • Graham JH (1982) Effect of citrus root exudates on germination of chlamydospores of the vesicular-arbuscular mycorrhizal fungus, Glomus epigaeum. Mycologia 74:831–835

    Google Scholar 

  • Groot SP, Karssen CM (1992) Dormancy and germination of abscisic acid-deficient tomato seeds: studies with the sitiens mutant. Plant Physiol 99:952–958

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hartung W (2010) The evolution of abscisic acid (ABA) and ABA function in lower plants, fungi and lichen. Funct Plant Biol 37:806–812

    CAS  Google Scholar 

  • Hartung W, Sauter A, Turner NC, Fillery I, Heilmeier H (1996) Abscisic acid in soils: what is its function and which factors and mechanisms influence its concentration? Plant Soil 184:105–110

    CAS  Google Scholar 

  • Herrera-Medina MJ, Steinkellner S, Vierheilig H, Ocampo Bote JA, García Garrido JM (2007) Abscisic acid determines arbuscule development and functionality in the tomato arbuscular mycorrhiza. New Phytol 175:554–564

    CAS  PubMed  Google Scholar 

  • Hildebrandt U, Janetta K, Bothe H (2002) Towards growth of arbuscular mycorrhizal fungi independent of a plant host. Appl Environ Microbiol 68:1919–1924

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hildebrandt U, Ouziad F, Marner FJ, Bothe H (2005) The bacterium Paenibacillus validus stimulates growth of the arbuscular mycorrhizal fungus Glomus intraradices up to the formation of fertile spores. FEMS Microbiol Lett 254:258–267

    Google Scholar 

  • Hong C, Michailides TJ (1999) Mycelial growth, sporulation, and survival of Monilinia fructicola in relation to osmotic potential and temperature. Mycologia 91:871–876

    Google Scholar 

  • Ishii T, Shrestha YH, Matsumoto I, Kadoya K (1996) Effect of ethylene on the growth of vesicular-arbuscular mycorrhizal fungi and on the mycorrhizal formation of trifoliate orange roots. J Jap Soc Hort Sci 65:525–529

    CAS  Google Scholar 

  • Kokkoris V, Miles T, Hart MM (2019) The role of in vitro cultivation on asymbiotic trait variation in a single species of arbuscular mycorrhizal fungus. Fungal Biol 123:307–317

    PubMed  Google Scholar 

  • Kuromori T, Seo M, Shinozaki K (2018) ABA transport and plant water stress responses. Trend Plant Sci 23:513–522

    CAS  Google Scholar 

  • Leal PL, Varón-López M, de Oliveira Prado IG, dos Santos JV, Soares CRFS, Siqueira JO, de Souza Moreira FM (2016) Enrichment of arbuscular mycorrhizal fungi in a contaminated soil after rehabilitation. Braz J Microbiol 47:853–862

    CAS  Google Scholar 

  • Liao D, Wang S, Cui M, Liu J, Chen A, Xu G (2018) Phytohormones regulate the development of arbuscular mycorrhizal symbiosis. Int J Mol Sci 19:3146

    PubMed Central  Google Scholar 

  • Louis I, Chew A, Lim G (1988) Influence of spore density and extracellular conidial matrix on spore germination in Colletotrichum capsici. Trans Bri Mycol Soc 91:694–697

    Google Scholar 

  • Martín-Rodríguez JÁ, León-Morcillo R, Vierheilig H, Ocampo JA, Ludwig-Müller J, García-Garrido JM (2011) Ethylene-dependent/ethylene-independent ABA regulation of tomato plants colonized by arbuscular mycorrhiza fungi. New Phytol 190:193–205

    PubMed  Google Scholar 

  • Müller A, Ngwene B, Peiter E, George E (2017) Quantity and distribution of arbuscular mycorrhizal fungal storage organs within dead roots. Mycorrhiza 27:201–210

    PubMed  Google Scholar 

  • Nair MG, Safir GR, Siqueira JO (1991) Isolation and identification of vesicular-arbuscular mycorrhiza-stimulatory compounds from clover (Trifolium repens) roots. Appl Environ Microbiol 57:434–439

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nitsch L, Kohlen W, Oplaat C, Charnikhova T, Cristescu S, Michieli P, Rieu I (2012) ABA-deficiency results in reduced plant and fruit size in tomato. J Plant Physiol 169:878–883

    CAS  PubMed  Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PRO, Hara RB,Simpson GL, Solymos P, Stevens MHH, Wagner H (2016) Vegan: Community Ecology Package. R Package Vegan, Vers 2. 3–5, https://cran.r-project. org/web/packages/vegan/index.html

  • Page DE, Glen M, Ratkowsky DA, Beadle CL, Rimbawanto A, Mohammed CL (2017) Ganoderma basidiospore germination responses as affected by spore density, temperature and nutrient media. Trop Plant Pathol 42:328–338

    Google Scholar 

  • Peres-Neto PR, Legendre P, Dray S, Borcard D (2006) Variation partitioning of species data matrices: estimation and comparison of fractions. Ecology 87:2614–2625

    PubMed  Google Scholar 

  • Powell JR, Rillig MC (2018) Biodiversity of arbuscular mycorrhizal fungi and ecosystem function. New Phytol 220:1059–1075

    PubMed  Google Scholar 

  • Redecker D, Kodner R, Graham LE (2000) Glomalean fungi from the Ordovician. Science 289:1920–1921

    CAS  PubMed  Google Scholar 

  • Scervino JM, Ponce MA, Erra-Bassells R, Vierheilig H, Ocampo JA, Godeas A (2005) Arbuscular mycorrhizal colonization of tomato by Gigaspora and Glomus species in the presence of root flavonoids. J Plant Physiol 162:625–633

    CAS  PubMed  Google Scholar 

  • Scervino JM, Ponce MA, Erra-Bassells R, Bompadre MJ, Vierheilig H, Ocampo JA, Godeas A (2006) Glycosidation of apigenin results in a loss of its activity on different growth parameters of arbuscular mycorrhizal fungi from the genus Glomus and Gigaspora. Soil Biol Biochem 38:2919–2922

    CAS  Google Scholar 

  • Selvakumar G, Shagol CC, Kang Y, Chung BN, Han SG, Sa TM (2018) Arbuscular mycorrhizal fungi spore propagation using single spore as starter inoculum and a plant host. J Appl Microbiol 124:1556–1565

    CAS  PubMed  Google Scholar 

  • Silva-Flores P, Bueno CG, Neira J, Palfner G (2019) Factors affecting arbuscular mycorrhizal fungi spore density in the Chilean mediterranean-type ecosystem. J Soil Sci Plant Nutrit 19:42–50

    CAS  Google Scholar 

  • Spatafora JW, Chang Y, Benny GL, Lazarus K, Smith ME, Berbee ML, Bonito G, Corradi N, Grigoriev I, Gryganskyi A, James TY, O’Donnell K, Roberson RW, Taylor TN, Uehling J, Vilgalys R, White MM, Stajich JE (2016) A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108:1028–1046

    CAS  PubMed  PubMed Central  Google Scholar 

  • Spraker JE, Sanchez LM, Lowe TM, Dorrestein PC, Keller NP (2016) Ralstonia solanacearum lipopeptide induces chlamydospore development in fungi and facilitates bacterial entry into fungal tissues. ISME J 10:2317–2330

    CAS  PubMed  PubMed Central  Google Scholar 

  • Suriyapperuma SP, Koske RE (1995) Attraction of germ tubes and germination of spores of the arbuscular mycorrhizal fungus Gigaspora gigantea in the presence of roots of maize exposed to different concentrations of phosphorus. Mycologia 87:772–778

    Google Scholar 

  • Takeda N, Handa Y, Tsuzuki S, Kojima M, Sakakibara H, Kawaguchi M (2015) Gibberellins interfere with symbiosis signaling and gene expression and alter colonization by arbuscular mycorrhizal fungi in Lotus japonicus. Plant Physiol 167:545–557

    CAS  PubMed  Google Scholar 

  • Tisserant E, Malbreil M, Kuo A, Kohler A, Symeonidi A, Balestrini R, Charron P, Duensing N, dit Frey NF, Gianinazzi-Pearson V, Gilbert LB, Handa Y, Herr JR, Hijri M, Koul R, Kawaguchi M, Krajinski F, Lammers PJ, Masclaux FG, Murat C, Morin E, Ndikumana S, Pagni M, Petitpierre D, Requena N, Rosikiewicz P, Riley R, Saito K, San Clemente H, Shapiro H, van Tuinen D, Bécard G, Bonfante P, Paszkowski U, Shachar-Hill YY, Tuskan GA, Young JPW, Sanders IR, Henrissat B, Rensing SA, Grigoriev IV, Corradi N, Roux C, Martin F (2013) Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. PNAS 110:20117–20122

    CAS  PubMed  PubMed Central  Google Scholar 

  • Twanabasu BR, Stevens KJ, Venables BJ (2013) The effects of triclosan on spore germination and hyphal growth of the arbuscular mycorrhizal fungus Glomus intraradices. Sci Total Environ 454:51–60

    PubMed  Google Scholar 

  • Vives-Peris V, Gómez-Cadenas A, Pérez-Clemente RM (2017) Citrus plants exude proline and phytohormones under abiotic stress conditions. Plant Cell Rep 36(12):1971–1984

    CAS  PubMed  Google Scholar 

  • Zhang W, Sun K, Shi RH, Yuan J, Wang XJ, Dai CC (2018) Auxin signalling of Arachis hypogaea activated by colonization of mutualistic fungus Phomopsis liquidambari enhances nodulation and N2-fixation. Plant Cell Environ 41:2093–2108

    CAS  PubMed  Google Scholar 

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Funding

This study was financially supported by the Guangdong Province Science and Technology Innovation Strategy Special Fund (No. 2018B020205001) and the National Natural Science Foundation of China (31570395).

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Correspondence to Honghui Zhu or Qing Yao.

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Liu, X., Feng, Z., Zhu, H. et al. Exogenous abscisic acid and root volatiles increase sporulation of Rhizophagus irregularis DAOM 197198 in asymbiotic and pre-symbiotic status. Mycorrhiza 29, 581–589 (2019). https://doi.org/10.1007/s00572-019-00916-z

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