ARBUSCULAR MYCORRHIZA – PARTNER IN COMMUNICATION
Anna Konieczny
Unit of Plant Nutrition, Institute of Plant Biology and Biotechnology, Faculty of Biotechnology and Horticulture, University of Agriculture in Kraków, 29 Listopada 54, 31-425 Krakow, PolandIwona Kowalska
Unit of Plant Nutrition, Institute of Plant Biology and Biotechnology, Faculty of Biotechnology and Horticulture, University of Agriculture in Kraków, 29 Listopada 54, 31-425 Krakow, PolandAbstract
Arbuscular mycorrhiza is one of the most common type of mycorrhiza in plant kingdom. Process of plant root colonization by arbuscular mycorrhizal fungi is consisted of four phases: presymbiotic phase, phase of contact and hyphae penetration to the roots, growth phase of hyphae inside the roots and phase of mycorrhizal intracellular structure development. The formation of symbiosis between fungi and host plant requires the exchange of molecular signals between these organisms. Plant signal molecules are described as strigolactones and cutin monomers whereas fungal signal molecules are lipo-chito-oligo-saccharides and
short chito-oligosaccharides. During the contact with plant roots fungal hyphae form appresorium on the surface of epidermis. After appresorium creation, the pre-penetration apparatus (PPA) is formed in plant cell, which is a structure defining a route of the hyphae overgrowing across the plant cell. Afterwards the fungus penetrates the epidermal cell and the cell of root cortex, where hyphae leave the cell and enter into appoplast, growing and branching along the root axis.
Keywords:
arbuscular mycorrhizal fungi, root colonization, strigolactones, signalingReferences
Akiyama, K., Matsuzaki, K., Hayashi, H. (2005). Plant sesquiterpens induce a hyphal branching in arbuscular mycorrhizal fungi. Nature, 435(9), 824–827.
Alexander, T., Meier, R., Toth, R., Weber, Ch. (1988). Dynamics of arbuscule development and degeneration in mycorrhizas of Triticum asetivum L. and Avena sativa L. with reference to Zea mays L. New Phytol., 110(3), 363–370.
Aroca, R., Porcel, R., Ruiz-Lozano, J.M. (2007). How does arbuscular mycorrhizal symbiosis regulate root hydraulic properites and plasma membrane aquaporins in Phaseolus vulgaris under drought, cold or salinity stresses? New Phytol., 173, 808–816.
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.
Besserer, A., Puech-Pagès, V., Keifer, P., Gomez-Roldan, V., Jauneau, A., Roy, S., Portais, J.-C., Roux, C., Bécard, G., Séjalon-Delmas, N. (2006). Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol., 4(7), 1239–1247.
Bécard, G., Kosuta, S., Tamasloukht, M., Séjalon-Delmas, N., Roux, C. (2004). Partner communication in the arbuscular mycorrhizal interaction. Can. J. Bot., 82, 1186–1197.
Bonfante, P., Genre, A. (2015). Arbuscular mycorrhizal dialogues: do you speak ‘plantish’ or ‘fungish’? Trend. Plant Sci., 20(3), 150–154.
Buee, M., Rossignol, M., Jauneau, A., Ranjeva, R., Bécard, G. (2000). The presymbiotic growth of arbuscular mycorrhizal fungi is induced by a branching factor partially purified from plant root exudates. Mol. Plant Microbe Interact., 13(6), 693–698.
Cavagnaro, T.R., Smith, F.A., Ayling, S.M., Smith, S.E. (2001a). Growth and phosphorus nutrition of a Paris-type arbuscular mycorrhizal symbiosis. New Phytol., 157, 127–134.
Cavagnaro, T.R., Smith, F.A., Lorimer, M.F., Haskard, K.A., Ayling, S.M., Smith, S.E. (2001b). Quantitive development of Paris-type arbuscular mycorrhizas formed between Asphodelus fistulosus and Glomus coronatum. New Phytol., 149, 105–113.
Drissner, D., Kunze, G., Callewaert, N., Gehrig, P., Ta-masloukht, M.B., Boller, T., Felix, G., Amrhein, N., Bucher, M. (2007). Lyso-phosphatidylocholine is a signal in the arbuscular mycorrhizal symbiosis. Science, 318, 265–268.
Fitter, A.H. (2005). Darkness visible: reflections or underground ecology. J. Ecol., 93, 231–243.
Genre, A., Chabaud, M., Balzergue, C., Puech-Pagès, V., Novero, M., Rey, T., Founrier, J., Rochange, S., Bécard, G., Bonfante, P., Barker, D.G. (2013). Shortchain chitin oligomers from arbuscular mycorrhizal fungi tigger nuclear Ca2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone. New Phytol., 198, 179–189.
Giovannetti, M., Sbrana, C., Avio, L., Citernesi, A.S., Logi, C. (1993). Differential hyphal morphogenesis in arbuscular mycorrhizal fungi during preinfection stages. New Phytol., 125, 587–593.
Javot, H., Penmetsa, R.V., Terzaghi, N., Cook, D.R., Har-rison, M.J. (2007). A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. PNAS, 104(5), 1720–1725.
Karagiannidis, N., Nikolaou, N., Ipsilantis, I., Zioziou, E. (2007). Effects of different N fertilizers on the activity of Glomus mosseae and on grapewine nutrition and berry composition. Mycorrhiza, 18, 43–50.
Li, X., Christie, P. (2001). Changes in soil solution Zn and pH and uptake of Zn by arbuscular mycorrhizal red clover in Zn-contaminated soil. Chemosphere, 42, 20–207.
Logi, C., Sbrana, C., Giovannetti. M. (1998). Cellular events involved in survival of individual arbuscular mycorrhizal symbionts growing in the absence of the host. Appl. Environ. Microbiol., 64(9), 3473–3479.
Maillet, F., Poinsot, V., André, O., Puech-Pagès, V., Haouy, A., Gueunier, M., Cromer, L., Giraudet, D., Formey, D., Niebel, A., Martinez, E.A., Driguez, H., Bécard, G., Dénarié, J. (2011). Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhizal fungi. Nature, 469, 58–64.
Marzec, M., Muszyńska, A. (2012). Strigolaktony – nowi kandydaci na hormony roślinne. Postępy Biol. Komórki, 39(1), 63–86.
Murray, J.D., Cousins, D.R., Jackson, K.J., Liu, C. (2013). Signaling at the root surface: The role of cutin monomers in mycorrhization. Mol. Plant, 6(5), 1381–1383.
Parniske, M. (2008). Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat. Rev. Microbiol., 6, 763–775.
Porcel, R., Aroca, R., Azcón, R., Ruiz-Lozano, J.M. (2006). PIP aquaporin gene expression in arbuscular mycorrhizal Glycine max and Lactuca sativa plants in relation to drought stress tolerance. Plant Mol. Biol., 60, 389–404.
Ruiz-Lozano, J.M., Aroca, R., Zamarreño, Á.M., Molina, S., Andreo-Jiménez, B., Porcel, R., García-Mina, J.M., Ruyter-Spira, C., López-Ráez, J.A. (2016). Arbuscular mycorrhizal symbiosis induces strigolactone biosynthesis under drought and improves drought tolerance in lettuce and tomato. Plant Cell Environ., 39(2), 441–452.
Sedas, P., Gianinazi-Pearson, V., Schoefs, B., Kuster, H., Wipf, D. (2009). Communications and signaling in the plant-fungus symbiosis. In: Plant-Environment Interac-tions, Baluška, F. (ed.). Springer-Verlag, Berlin-Heidelberg, 45–72.
Smith, S.E., Read, D.J. (2008). Mycorrhizal symbiosis. Elsevier Academic Press, Amsterdam.
Sun, J., Miller, B., Granqvist, E., Wiley-Kalil, A., Gobbato, E., Maillet, F., Cottaz, S., Samain, E., Venkateshwaran, M., Fort, S., Morris, J., Ané, J-M., Dénarié, J., Oldroyd, G.E.D. (2015). Activation of symbiosis signaling by arbuscular mycorrhizal fungi in legumes and rice. The Plant Cell., 27, 823–838.
Timonen, S., Peterson, R.L. (2002). Cytoskeleton in mycorrhizal symbiosis. Plant Soil, 244, 199–210.
Toussaint, J.P., Smith, F.A., Smith, S.E. (2007). Arbuscular mycorrhizal fungi can induce the production of phytochemicals in sweet basil irrespective of phosphorus nutrition. Mycorrhiza, 17(4), 291–297.
Wang, E., Schornack, S., Marsh, J.F., Gobbato, E., Schwessinger, B., Eastmond, P., Schultze, M., Kamoun, S., Oldroyd, G.E.D. (2012). A common signal-ing process that promotes mycorrhizal and oomycete colonization of plants. Curr. Biol., 4, 2242–2246.
Wang, B., Qiu, Y.L. (2006). Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza, 16, 299–363.
Vierheilig, H., Alt, M., Mäder, P., Boller, T., Wiemken, A. (1995). Spreading of Glomus mosseae, a vesicular-arbuscular mycorrhizal fungus, across the rhizosphere of host and non-host plants. Soil Biol. Biochem., 27, 1113–1115.
Vierheilig, H., Bago, B., Albrecht, C., Poulin, M.J., Piché, Y. (1998). Flavonoids and arbuscular mycorrhizal fun-gi. Adv. Exp. Med. Biol., 439, 9–33.
Vincente-Sánches, J., Nicolás, E., Pedrero, F., Alarcón, J.J., Maestre-Valero, J.F., Fernández, F. (2014). Arbuscular mycorrhizal symbiosis alleviates detrimental effects of saline reclaimed water in lettuce plants. Mycorrhiza, 24, 339–348.
Yoneyama, K., Xie, X., Kim, H.I., Kisugi, T., Nomura, T., Sekimoto, H., Yokota, T. Yoneyama, K. (2012). How do nitrogen and phosphorus deficiencies affect strigolactone production and exudation? Planta, 235, 1197–1207.
Zhu, X.Q., Wang, C.Y., Chen, H., Tang, M. (2014). Effects of arbuscular mycorrhizal fungi on photosynthesis, carbon content and calorific value of black locust seedlings. Photosynthetica, 52, 247–252.
Alexander, T., Meier, R., Toth, R., Weber, Ch. (1988). Dynamics of arbuscule development and degeneration in mycorrhizas of Triticum asetivum L. and Avena sativa L. with reference to Zea mays L. New Phytol., 110(3), 363–370.
Aroca, R., Porcel, R., Ruiz-Lozano, J.M. (2007). How does arbuscular mycorrhizal symbiosis regulate root hydraulic properites and plasma membrane aquaporins in Phaseolus vulgaris under drought, cold or salinity stresses? New Phytol., 173, 808–816.
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.
Besserer, A., Puech-Pagès, V., Keifer, P., Gomez-Roldan, V., Jauneau, A., Roy, S., Portais, J.-C., Roux, C., Bécard, G., Séjalon-Delmas, N. (2006). Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol., 4(7), 1239–1247.
Bécard, G., Kosuta, S., Tamasloukht, M., Séjalon-Delmas, N., Roux, C. (2004). Partner communication in the arbuscular mycorrhizal interaction. Can. J. Bot., 82, 1186–1197.
Bonfante, P., Genre, A. (2015). Arbuscular mycorrhizal dialogues: do you speak ‘plantish’ or ‘fungish’? Trend. Plant Sci., 20(3), 150–154.
Buee, M., Rossignol, M., Jauneau, A., Ranjeva, R., Bécard, G. (2000). The presymbiotic growth of arbuscular mycorrhizal fungi is induced by a branching factor partially purified from plant root exudates. Mol. Plant Microbe Interact., 13(6), 693–698.
Cavagnaro, T.R., Smith, F.A., Ayling, S.M., Smith, S.E. (2001a). Growth and phosphorus nutrition of a Paris-type arbuscular mycorrhizal symbiosis. New Phytol., 157, 127–134.
Cavagnaro, T.R., Smith, F.A., Lorimer, M.F., Haskard, K.A., Ayling, S.M., Smith, S.E. (2001b). Quantitive development of Paris-type arbuscular mycorrhizas formed between Asphodelus fistulosus and Glomus coronatum. New Phytol., 149, 105–113.
Drissner, D., Kunze, G., Callewaert, N., Gehrig, P., Ta-masloukht, M.B., Boller, T., Felix, G., Amrhein, N., Bucher, M. (2007). Lyso-phosphatidylocholine is a signal in the arbuscular mycorrhizal symbiosis. Science, 318, 265–268.
Fitter, A.H. (2005). Darkness visible: reflections or underground ecology. J. Ecol., 93, 231–243.
Genre, A., Chabaud, M., Balzergue, C., Puech-Pagès, V., Novero, M., Rey, T., Founrier, J., Rochange, S., Bécard, G., Bonfante, P., Barker, D.G. (2013). Shortchain chitin oligomers from arbuscular mycorrhizal fungi tigger nuclear Ca2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone. New Phytol., 198, 179–189.
Giovannetti, M., Sbrana, C., Avio, L., Citernesi, A.S., Logi, C. (1993). Differential hyphal morphogenesis in arbuscular mycorrhizal fungi during preinfection stages. New Phytol., 125, 587–593.
Javot, H., Penmetsa, R.V., Terzaghi, N., Cook, D.R., Har-rison, M.J. (2007). A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. PNAS, 104(5), 1720–1725.
Karagiannidis, N., Nikolaou, N., Ipsilantis, I., Zioziou, E. (2007). Effects of different N fertilizers on the activity of Glomus mosseae and on grapewine nutrition and berry composition. Mycorrhiza, 18, 43–50.
Li, X., Christie, P. (2001). Changes in soil solution Zn and pH and uptake of Zn by arbuscular mycorrhizal red clover in Zn-contaminated soil. Chemosphere, 42, 20–207.
Logi, C., Sbrana, C., Giovannetti. M. (1998). Cellular events involved in survival of individual arbuscular mycorrhizal symbionts growing in the absence of the host. Appl. Environ. Microbiol., 64(9), 3473–3479.
Maillet, F., Poinsot, V., André, O., Puech-Pagès, V., Haouy, A., Gueunier, M., Cromer, L., Giraudet, D., Formey, D., Niebel, A., Martinez, E.A., Driguez, H., Bécard, G., Dénarié, J. (2011). Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhizal fungi. Nature, 469, 58–64.
Marzec, M., Muszyńska, A. (2012). Strigolaktony – nowi kandydaci na hormony roślinne. Postępy Biol. Komórki, 39(1), 63–86.
Murray, J.D., Cousins, D.R., Jackson, K.J., Liu, C. (2013). Signaling at the root surface: The role of cutin monomers in mycorrhization. Mol. Plant, 6(5), 1381–1383.
Parniske, M. (2008). Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat. Rev. Microbiol., 6, 763–775.
Porcel, R., Aroca, R., Azcón, R., Ruiz-Lozano, J.M. (2006). PIP aquaporin gene expression in arbuscular mycorrhizal Glycine max and Lactuca sativa plants in relation to drought stress tolerance. Plant Mol. Biol., 60, 389–404.
Ruiz-Lozano, J.M., Aroca, R., Zamarreño, Á.M., Molina, S., Andreo-Jiménez, B., Porcel, R., García-Mina, J.M., Ruyter-Spira, C., López-Ráez, J.A. (2016). Arbuscular mycorrhizal symbiosis induces strigolactone biosynthesis under drought and improves drought tolerance in lettuce and tomato. Plant Cell Environ., 39(2), 441–452.
Sedas, P., Gianinazi-Pearson, V., Schoefs, B., Kuster, H., Wipf, D. (2009). Communications and signaling in the plant-fungus symbiosis. In: Plant-Environment Interac-tions, Baluška, F. (ed.). Springer-Verlag, Berlin-Heidelberg, 45–72.
Smith, S.E., Read, D.J. (2008). Mycorrhizal symbiosis. Elsevier Academic Press, Amsterdam.
Sun, J., Miller, B., Granqvist, E., Wiley-Kalil, A., Gobbato, E., Maillet, F., Cottaz, S., Samain, E., Venkateshwaran, M., Fort, S., Morris, J., Ané, J-M., Dénarié, J., Oldroyd, G.E.D. (2015). Activation of symbiosis signaling by arbuscular mycorrhizal fungi in legumes and rice. The Plant Cell., 27, 823–838.
Timonen, S., Peterson, R.L. (2002). Cytoskeleton in mycorrhizal symbiosis. Plant Soil, 244, 199–210.
Toussaint, J.P., Smith, F.A., Smith, S.E. (2007). Arbuscular mycorrhizal fungi can induce the production of phytochemicals in sweet basil irrespective of phosphorus nutrition. Mycorrhiza, 17(4), 291–297.
Wang, E., Schornack, S., Marsh, J.F., Gobbato, E., Schwessinger, B., Eastmond, P., Schultze, M., Kamoun, S., Oldroyd, G.E.D. (2012). A common signal-ing process that promotes mycorrhizal and oomycete colonization of plants. Curr. Biol., 4, 2242–2246.
Wang, B., Qiu, Y.L. (2006). Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza, 16, 299–363.
Vierheilig, H., Alt, M., Mäder, P., Boller, T., Wiemken, A. (1995). Spreading of Glomus mosseae, a vesicular-arbuscular mycorrhizal fungus, across the rhizosphere of host and non-host plants. Soil Biol. Biochem., 27, 1113–1115.
Vierheilig, H., Bago, B., Albrecht, C., Poulin, M.J., Piché, Y. (1998). Flavonoids and arbuscular mycorrhizal fun-gi. Adv. Exp. Med. Biol., 439, 9–33.
Vincente-Sánches, J., Nicolás, E., Pedrero, F., Alarcón, J.J., Maestre-Valero, J.F., Fernández, F. (2014). Arbuscular mycorrhizal symbiosis alleviates detrimental effects of saline reclaimed water in lettuce plants. Mycorrhiza, 24, 339–348.
Yoneyama, K., Xie, X., Kim, H.I., Kisugi, T., Nomura, T., Sekimoto, H., Yokota, T. Yoneyama, K. (2012). How do nitrogen and phosphorus deficiencies affect strigolactone production and exudation? Planta, 235, 1197–1207.
Zhu, X.Q., Wang, C.Y., Chen, H., Tang, M. (2014). Effects of arbuscular mycorrhizal fungi on photosynthesis, carbon content and calorific value of black locust seedlings. Photosynthetica, 52, 247–252.
Anna Konieczny
Unit of Plant Nutrition, Institute of Plant Biology and Biotechnology, Faculty of Biotechnology and Horticulture, University of Agriculture in Kraków, 29 Listopada 54, 31-425 Krakow, Poland
Unit of Plant Nutrition, Institute of Plant Biology and Biotechnology, Faculty of Biotechnology and Horticulture, University of Agriculture in Kraków, 29 Listopada 54, 31-425 Krakow, Poland
Iwona Kowalska
Unit of Plant Nutrition, Institute of Plant Biology and Biotechnology, Faculty of Biotechnology and Horticulture, University of Agriculture in Kraków, 29 Listopada 54, 31-425 Krakow, Poland
Unit of Plant Nutrition, Institute of Plant Biology and Biotechnology, Faculty of Biotechnology and Horticulture, University of Agriculture in Kraków, 29 Listopada 54, 31-425 Krakow, Poland
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