Arbuscular mycorrhizal fungi communities associated with wild plants in a coastal ecosystem

Abstract

Arbuscular mycorrhizal fungi (AMF) form a near-ubiquitous mutualistic association with roots to help plants withstand harsh environments, and play a key role in the establishment of coastal beach plant communities. Yet little is known about the structure and composition of AMF communities on coastal beaches of eastern China. In this study, we investigated the occurrence, community composition and diversity of AMF associated with common wild plants on a coastal beach of North Jiangsu, China. Almost all of the local wild species were colonized by AMF except for Chenopodium album L. Thirty-seven AMF species were isolated from the rhizosphere belonging to 12 genera in seven families. Glomus was the dominant genus and Funneliformis mosseae the dominant species. The colonization, spore composition and diversity of AMF were strongly related to edaphic factors. Sodium (Na⁺) ions in the soil significantly and negatively affected the colonization rate by AMF and both soil Na⁺ levels and pH had a significant negative effect on AMF spore density and evenness. However, there was a significant positive correlation between species richness and total organic carbon. The results provide insights into soil factors affecting native AMF communities in coastal beach habitats which could benefit vegetation recovery and soil reclamation efforts.

Keywords

AMF diversity / Coastal beach / Edaphic factors / Mycorrhizal composition / Wild hosts

References

[1] Alguacil MM, Lumini E, Roldán A, Sakinas-Garcia JR, Bonfante P, Bianciotto V. The impact of tillage practices on arbuscular mycorrhizal fungal diversity in subtropical crops. Ecol Appl, 2008, 18(2): 527-536.

[2] Allen MF, Allen EB, Friese CF. Responses of the non-mycotrophic plant Salsola kali to invasion by vesicular-arbuscular mycorrhizal fungi. New Phytol, 1989, 111(1): 45-49.

[3] Álvarez-Sánchez J, Johnson NC, Antoninka A, Chaudhary VB, Lau MK, Owen SM, Guadarrama P, Castillo S. Pagano M. Large-scale diversity patterns in spore communities of arbuscular mycorrhizal fungi. Mycorrhiza: occurrence in natural and restored environments, 2012, New York: Nova Science Publishers Inc. 29 47

[4] Atul-Nayyar A, Hamel C, Hanson K, Germida J. The arbuscular mycorrhizal symbiosis links N mineralization to plant demand. Mycorrhiza, 2009, 19(4): 239-246.

[5] Bencherif K, Boutekrabt A, Dalpé Y, Sahraoui AH. Soil and seasons affect arbuscular mycorrhizal fungi associated with Tamarix rhizosphere in arid and semi-arid steppes. Appl Soil Ecol, 2016, 107: 182-190.

[6] Blaszkowski J, Czerniawska B. Arbuscular mycorrhizal fungi (Glomeromycota) associated with roots of Ammophila arenaria growing in maritime dunes of Bornholm (Denmark). Acta Soc Bot Pol, 2011, 80(1): 63-76.

[7] Brundrett MC. Mycorrhizas in natural ecosystems. Adv Ecol Res, 1991, 21: 171-313.

[8] Brundrett MC, Tedersoo L. Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol, 2018, 220(4): 1108-1115.

[9] Cai XB, Peng YL, Gai JP. Ecological distribution of arbuscular mycorrhizal fungi in alpine grasslands of Tibet Plateau. Chin J Appl Ecol, 2010, 21(10): 2635-2644. (in Chinese)

[10] Camprubí A, Calvet C, Cabot P, Pitet M, Estaún V. Arbuscular mycorrhizal fungi associated with psammophilic vegetation in Mediterranean coastal sand dunes. Span J Agric Res, 2010, 8(1): 96-102.

[11] Cardoso IM, Boddington C, Janssen BH, Oenema O, Kuyper TW. Distribution of mycorrhizal fungal spores in soils under agroforestry and monocultural coffee systems in Brazil. Agrofor Syst, 2003, 58(1): 33-43.

[12] Cardoso EJBN, Bini D, Vasconcellos RLF, Bini D, Miyauchi MYH, dos Santos CA, Alves PRL, de Paula AM, Nakatani AS, Pereira JM, Nogueira MA. Soil health: looking for suitable indicators. What should be considered to assess the effects of use and management on soil health?. Sci Agric, 2013, 70(4): 274-289.

[13] Carvalho F, de Souza FA, Carrenho R, de Souza Moreira FM, da Conçeição Jesus E, Fernandes GW. The mosaic of habitats in the high-altitude Brazilian rupestrian fields is a hotspot for arbuscular mycorrhizal fungi. Appl Soil Ecol, 2012, 52: 9-19.

[14] Chen Z, He XL, Guo HJ, Yao XQ, Chen C. Diversity of arbuscular mycorrhizal fungi in the rhizosphere of three host plants in the farming-pastoral zone, north China. Symbiosis, 2012, 57(3): 149-160.

[15] Clapp JP, Young JPW, Merryweather JW, Fitter AH. Diversity of fungal symbionts in arbuscular mycorrhizas from a natural community. New Phytol, 2010, 130(2): 259-265.

[16] da Silva IR, de Mello CMA, Alves Ferreira Neto R, Alves da Silva DK, de Melo AL, Oehl F, Maia LC. Diversity of arbuscular mycorrhizal fungi along an environmental gradient in the Brazilian semiarid. Appl Soil Ecol, 2014, 84: 166-175.

[17] da Silva IR, de Souza FA, Alves da Silva DK, Oehl F, Maia LC. Patterns of arbuscular mycorrhizal fungal distribution on mainland and island sandy coastal plain ecosystems in Brazil. Microb Ecol, 2017, 74(3): 654-669.

[18] Daniell TJ, Husband R, Fitter AH, Yong JPW. Molecular diversity of arbuscular mycorrhizal fungi colonising arable crops. FEMS Microbiol Ecol, 2001, 36(2–3): 203-209.

[19] de Oliveira Freitas R, Buscardo E, Nagy L, dos Santos Maciel AB, Carrenbo R, Luizão RC. Arbuscular mycorrhizal fungal communities along a pedo-hydrological gradient in a Central Amazonian terra firme forest. Mycorrhiza, 2014, 24(1): 21-32.

[20] del Mar Alguacil M, Torres MP, Montesinos-Navarro A, Roldán A. Soil characteristics driving arbuscular mycorrhizal fungal communities in semiarid Mediterranean soils. Appl Environ Microb, 2016, 82(11): 3348-3356.

[21] Ding NN, Wang BS, Liang ZH, Liu DH. Effects of different amelioration measures on coastal saline soil in the David’s deer reserve of Dafeng county of Jiangsu province. Soils, 2011, 43(3): 487-492. (in Chinese)

[22] Dufrêne M, Legendre P. Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr, 1997, 67(3): 345-366.

[23] Estrada B, Aroca R, Azón-Aguilar C, Barea JM, Ruiz-Lozano JM. Importance of native arbuscular mycorrhizal inoculation in the halophyte Asteriscus maritimua for successful establishment and growth under saline condition. Plant Soil, 2013, 370: 175-185.

[24] Estrada B, Beltrán-Hermoso M, Palenzuela J, Iwase K, Ruiz-Lozano JM, Barea JM, Oehl F. Diversity of arbuscular mycorrhizal fungi in the rhizosphere of Asteriscus maritimus (L.) Less., a representative plant species in arid and saline Mediterranean ecosystems. J Arid Environ, 2013, 97: 170-175.

[25] Evelin H, Kapoor R, Giri B. Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot, 2009, 104(7): 1263-1280.

[26] Friese CF, Koske RE. The spatial dispersion of spores of vesicular-arbuscular mycorrhizal fungi in a sand dune: microscale patterns associated with the root architecture of American beach grass. Mycol Res, 1991, 95(8): 952-957.

[27] Gerdemann JW, Nicolson TH. Spores of mycorrhizal endogone species extracted from soil by wet sieving and decanting. Trans Br Mycol Soc, 1963, 46(2): 235-244.

[28] Giovannetti M, Mosse B. An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol, 1980, 84(3): 489-500.

[29] Goto BT, Jardim JG, da Silva GA, Furrazola E, Torres-Arias Y, Oehl F. Glomus trufemii (Glomeromycetes), a new sporocarpic species from Brazilian sand dunes. Mycotaxon, 2012, 120(1): 1-9.

[30] Hart MM, Reader RJ. Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytol, 2002, 153(2): 335-344.

[31] Hashem A, Alqarawi AA, Radhakrishnan R, Al-Arjani AF, Aldehaish HA, Egamberdieva D, Abd-Allah EF. Arbuscular mycorrhizal fungi regulate the oxidative system, hormones and ionic equilibrium to trigger salt stress tolerance in Cucumis sativus L.. Saudi J Biol Sci, 2018, 25(6): 1102-1114.

[32] Hildebrandt U, Janetta K, Ouziad F, Renne B, Nawrath K, Bothe H. Arbuscular mycorrhizal colonization of halophytes in Central European salt marshes. Mycorrhiza, 2001, 10(4): 175-183.

[33] Ievinsh G. Biological basis of biological diversity: physiological adaptations of plants to heterogeneous habitats along a sea coast. Acta Univ Latv, 2006, 710: 53-79.

[34] Jefwa JM, Sinclair R, Maghembe JA. Diversity of glomale mycorrhizal fungi in maize/sesbania intercrops and maize monocrop systems in Southern Malawi. Agrofor Syst, 2006, 67(2): 107-114.

[35] Jenkins WR. A rapid centrifugal-flotation technique for separating nematodes from soil. Plant Dis Rep, 1964 48 9 692

[36] Juniper S, Abbott LK. Soil salinity delays germination and limits growth of hyphae from propagules of arbuscular mycorrhizal fungi. Mycorrhiza, 2006, 16(5): 371-379.

[37] Kahiluoto H, Ketoja E, Vestberg M, Saarela I. Promotion of AM utilization through reduced P fertilization 2. Field studies. Plant Soil, 2001, 231(1): 65-79.

[38] Kamble VR. Status of AM fungi in some medicinal plants from panambur beach mangalore India. J Pharm Biol Sci, 2012, 3(4): 1-4.

[39] Kamble VR, Agre DG, Dixit GB. Incidence of arbuscular mycorrhizal fungi in indian squill: drimia indica from coastal sand dunes of Konkan, India. J Pharm Biol Sci, 2012, 4(3): 31-36.

[40] Koske RE. Distribution of VA mycorrhizal fungi along a latitudinal temperature gradient. Mycologia, 1987, 79(1): 55-68.

[41] Koske RE, Gemma JN. Arbuscular mycorrhizal fungi in Hawaiian sand dunes: Island of Kauai. Pac Sci, 1996, 50(1): 36-45.

[42] Krüger M, Krüger C, Walker C, Stockinger H, Schüssler A. Phylogenetic reference data for systematic and phylotaxonomy of arbuscular mycorrhizal fungi from phylum to species level. New Phytol, 2012, 193(4): 970-984.

[43] Kulkarni SS, Raviraja NS, Sridhar KR. Arbuscular mycorrhizal fungi of tropical sand dunes of west coast of India. J Coast Res, 1997, 13(3): 931-936.

[44] Leifheit EF, Veresoglou SD, Lehmann A, Morris EK, Rillig MC. Multiple factors influence the role of arbuscular mycorrhizal fungi in soil aggregation—a meta-analysis. Plant Soil, 2014, 374: 523-537.

[45] Lekberg Y, Koide RT, Rohr JR, Aldrich-Wolfe L, Morton JB. Role of niche restrictions and dispersal in the composition of arbuscular mycorrhizal fungal communities. J Ecol, 2007, 95(1): 95-105.

[46] Li JL, Sun YQ, Jiang XL, Chen BD, Zhang X. Arbuscular mycorrhizal fungi alleviate arsenic toxicity to Medicago sativa by influencing arsenic speciation and partitioning. Ecotoxicol Environ Saf, 2018, 157: 235-243.

[47] Liu RJ, Wang FY. Selection of appropriate host plants used in trap culture of arbuscular mycorrhizal fungi. Mycorrhiza, 2003, 13(3): 123-127.

[48] Liu S, Guo XL, Feng G, Maimaitiaili B, Fan JL, He XH. Indigenous arbuscular mycorrhizal fungi can alleviate salt stress and promote growth of cotton and maize in saline fields. Plant Soil, 2016, 398(1–2): 195-206.

[49] Miransari M. Interactions between arbuscular mycorrhizal fungi and soil bacteria. Appl Microbiol Biot, 2011, 89(4): 917-930.

[50] Morton JB. Taxonomy of VA mycorrhizal fungi: classification, nomenclature, and identification. Mycotaxon, 1988, 32: 267-324.

[51] Muleta D, Assefa F, Nemomissa S, Granhall U. Composition of coffee shade tree species and density of indigenous arbuscular mycorrhizal fungi (AMF) spores in Bonga natural coffee forest, southwestern Ethiopia. For Ecol Manag, 2007, 241(1–3): 145-154.

[52] Nagahashi G, Douds DD. Rapid and sensitive bioassay to study signals between root exudates and arbuscular mycorrhizal fungi. Biotechnol Tech, 1999, 13(12): 893-897.

[53] Ocampo JA, Martin J, Hayman DS. Influence of plant interactions on vesicular-arbuscular mycorrhizal infections. I. Host and non-host plants grown together. New Phytol, 1980, 84(1): 27-35.

[54] Oehl F, Sieverding E, Palenzuela J, Ineichen K, da Silva GA. Advances in Glomeromycota taxonomy and classification. IMA Fungus, 2011, 2(2): 191-199.

[55] Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. USDA Circular No 939, US Gov Print Office, Washington

[56] Pereira CMR, Alves da Silva DK, de Almeida Ferreira AC, Goto BT, Maia LC. Diversity of arbuscular mycorrhizal fungi in Atlantic forest areas under different land uses. Agric Ecosyst Environ, 2014, 185(3): 245-252.

[57] Phillips JM, Hayman DS. Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc, 1970, 55(1): 158-161.

[58] Pontes JS, Oehl F, Pereira CD, Machado CT, Coyne D, da Silva DK, Maia LC. Diversity of arbuscular mycorrhizal fungi in the Brazilian’s Cerrado and in soybean under conservation and conventional tillage. Appl Soil Ecol, 2017, 117–118: 178-189.

[59] Purin S, Rillig MC. The arbuscular mycorrhizal fungal protein glomalin: limitations, progress, and a new hypothesis for its function. Pedobiologia, 2008, 51(2): 123-130.

[60] Qin F, Shinozaki K, Yamaguchi-Shinozaki K. Achievements and challenges in understanding plant abiotic stress responses and tolerance. Plant Cell Physiol, 2011, 52(9): 1569-1582.

[61] Rodríguez-Echeverría S, Hol WHG, Freitas H, Eason WR, Cool R. Arbuscular mycorrhizal fungi of Ammophila arenaria (L.) link: spore abundance and root colonisation in six locations of the European coast. Eur J Soil Biol, 2008, 44(1): 30-36.

[62] Sarkar A, Asaeda T, Wang QY, Kaneko Y, Rashid MH. Response of Miscanthus sacchariflorus to zinc stress mediated by arbuscular mycorrhizal fungi. Flora, 2017, 234: 60-68.

[63] Schenck NC, Perez Y. Manual for the identification of VA mycorrhizal fungi, 1990 3 Corvallis: Synergistic Publications.

[64] Schüßler A, Walker C (2010) The Glomeromycota: a species list with new families and genera. Libraries at the royal botanical garden Edinburgh, the royal botanic garden Kew, botanische staatssammlung Munich, and Oregon State University

[65] Shannon CE, Weaver W, Wiener N. The mathematical theory of communication, 1949, Urbana: The University of Illinois Press.

[66] Sheng M, Tang M, Zhang FF, Huang YH. Effect of soil factors on arbuscular mycorrhizal fungi in saline alkaline soils of Gansu, Inner Mongolia and Ningxia. Biodivers Sci, 2011, 19(1): 85-92.

[67] Soka GE, Ritchie ME. Arbuscular mycorrhizal spore composition and diversity associated with different land uses in a tropical savanna landscape, Tanzania. Appl Soil Ecol, 2018, 125: 222-232.

[68] Stürmer SL, Bellei MM. Composition and seasonal variation of spore populations of arbuscular mycorrhizal fungi in dune soils on the island of Santa Catarina, Brazil. Can J Bot, 1994, 72(3): 359-363.

[69] Stürmer SL, Stürmer R, Pasqualini D. Taxonomic diversity and community structure of arbuscular mycorrhizal fungi (Phylum Glomeromycota) in three maritime sand dunes in Santa Catarina state, south Brazil. Fungal Ecol, 2013, 6(1): 27-36.

[70] Sun L, Zhu ZS, Liu Y, Zhang JL. Evaluation of service values of the intertidal land eco-system of Dafeng city. Rural Eco-environ, 2004, 20(3): 10-14. (in Chinese)

[71] Sylvia DM, Will ME. Establishment of vesicular-arbuscular mycorrhizal fungi and other microorganisms on a beach replenishment site in Florida. Appl Environ Microbiol, 1988, 54(2): 348-352.

[72] Talaat NB, Shawky BT. Protective effects of arbuscular mycorrhizal fungi on wheat (Triticum aestivum L.) plants exposed to salinity. Environ Exp Bot, 2014, 98: 20-31.

[73] Tang M. Diversity and distribution of arbuscular mycorrhizal fungi in saline alkaline soil, Inner Mongolia. Acta Pedol Sin, 2007, 44(6): 1105-1110. (in Chinese)

[74] Tedersoo L, Bahram M, Pölme S, Köijalg U, Yorou NS, Wijesundera R, Ruiz LV, Vasco-Palacios AM, Thu PQ, Suija A, Smith ME, Sharp C, Saluveer E, Saitta A, Rosas M, Riit T, Ratkowsky D, Pritsch K, Pöldmaa K, Piepenbring M, Phosri C, Peterson M, Parts K, Pӓrtel K, Otsing E, Nouhra E, Njouonkou AL, Nilsson NRH, Morgado LN, Mayor J, May TW, Majuakim L, Lodge DJ, Lee SS, Larsson K, Kohout P, Hosaka K, Hiiesalu I, Henkel TW, Harend H, Guo LD, Greslebin A, Grelet G, Geml J, Gates G, Dunstan W, Dunk C, Drenkhan R, Dearnaley J, Kesel AD, Dang T, Chen X, Buegger F, Brearley FQ, Bonito G, Anslan S, Abell S, Abarenkov K. Global diversity and geography of soil fungi. Science, 2014, 346(6213): 1-10.

[75] Tian H, Gaia JP, Christie P, Li XL. Arbuscular mycorrhizal fungi associated with wild forage plants in typical steppe of eastern Inner Mongolia. Eur J Soil Biol, 2009, 45(4): 321-327.

[76] Trufem SFB. Aspectos ecológicos de fungos micorrízicos vesículo-arbusculares da mata tropical úmida da Ilha do Cardoso, SP, Brasil. Acta Bot Bras, 1990, 4(2): 31-45.

[77] Turrini A, Agnolucci M, Palla M, Tomé E, Tagliavini M, Scandellari F, Giovannetti M. Species diversity and community composition of native arbuscular mycorrhizal fungi in apple roots are affected by site and orchard management. Appl Soil Ecol, 2017, 116: 42-54.

[78] van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Strietwolf-Engel R, Boller T, Wiemken A, Sanders IR. Mycorrhizal fungi diversity determines the plant diversity, ecosystem variability and productivity. Nature, 1998, 396: 69-72.

[79] Vierheilig H, Ocampo JA. Role of root extract and volatile substances of non-host plants on vesicular-arbuscular mycorrhizal spore germination. Symbiosis, 1990, 9: 199-202.

[80] Vierheilig H, Iseli B, Alt M, Raikhel N, Wiemken A, Boller T. Resistance of Urtica dioica to mycorrhizal colonization: a possible involment of Urtica dioica agglutinin. Plant Soil, 1996, 183: 131-136.

[81] Wang YS, Liu RJ. A checklist of arbuscular mycorrhizal fungi in the recent taxonomic system of Glomeromycota. Mycosystema, 2017, 36(7): 820-850. (in Chinese)

[82] Wang S, Lin X, Shi YQ. Effects of arbuscular mycorrhiza on resistance of plants to environmental stress. Chin J Ecol, 2001, 20(3): 27-30. (in Chinese)

[83] Wang FY, Liu RJ, Lin XG, Zhou JM. Arbuscular mycorrhizal status of wild plants in saline-alkaline soils of the Yellow River Delta. Mycorrhiza, 2004, 14(2): 133-137.

[84] Wang JJ, Qiang W, Liu HY, Ge JL, Zuo YL, He XL. Effects of plants pecies on diversity of arbuscular mycorrhizal fungi in extremely arid desert environment. Mycosystema, 2017, 36(7): 861-869. (in Chinese)

[85] Wang JP, Wang GG, Zhang B, Yuan ZM, Fu ZY, Yuan YD, Zhu LJ, Shilin Ma, Zhang JC. Arbuscular mycorrhizal fungi associated with tree species in a planted forest of eastern China. Forests, 2019 10 5 424

[86] Wicaksono WA, Sansom CE, Jones EE, Perry NB, Monk J, Ridgway HJ. Arbuscular mycorrhizal fungi associated with Leptospermum scoparium (mānuka): effects on plant growth and essential oil content. Symbiosis, 2017, 75: 39-50.

[87] Wilson B, Sykes MT. Is zonation on coastal sand dunes determined primarily by sand burial or by salt spray? A test in New Zealand dunes. Ecol Lett, 1999, 2(4): 233-236.

[88] Yamato M, Ikeda S, Iwase K. Community of arbuscular mycorrhizal fungi in drought-resistant plants, Moringa spp., in semiarid regions in Madagascar and Uganda. Mycoscience, 2009, 50(2): 100-105.

[89] Zhang Y, Guo LD, Liu RJ. Survey of arbuscular mycorrhizal fungi in deforested and natural forest land in the subtropical region of Dujiangyan, southwest China. Plant Soil, 2004, 261: 257-263.

[90] Zhang YF, Qi BI, Yang YF, Zhang ZH, Hu CJ, Zhao SS, Wang XG. Arbuscular mycorrhizal fungi diversity in saline-alkaline Leymus chinensis grasslands on the Songnen Plain. Acta Prataculturae Sin, 2015, 24(9): 80-88. (in Chinese)

[91] Zhang T, Hu YJ, Zhang K, Tian CY, Guo JX. Arbuscular mycorrhizal fungi improve plant growth of Ricinus communis by altering photosynthetic properties and increasing pigments under drought and salt stress. Ind Crop Prod, 2018, 117: 13-19.

[92] Zhao XF, Yang JS, Yao RJ. Relationship between soil salt dynamics and factors of water balance in the typical coastal area of Northern Jiangsu Province. Trans CSAE, 2010, 26(3): 52-57. (in Chinese)

[93] Zhao H, Li XZ, Zhang ZM, Zhao Y, Yang JT, Zhu YW. Species diversity and drivers of arbuscular mycorrhizal fungal communities in a semi-arid mountain in China. Peer J, 2017 5 12 e4155