Abstract
A new arbuscular mycorrhizal fungus was found in an agricultural plantation of Plukenetia volubilis, the inka nut (also called “sacha inchi” or “inka peanut”) in the Amazonia region of San Martín State in Peru. In this site, the inka nut was grown in mixed cultures together with Zea mays and Phaseolus vulgaris. The fungus was propagated in bait and single-species cultures on Sorghum vulgare, Brachiaria brizantha, Medicago sativa, and Plukenetia volubilis as host plants. The fungus differentiates hyaline spores terminally or intercalary on cylindrical to slightly funnel-shaped hyphae, singly or in spore clusters with up to ca. 90 spores per cluster. The spores are bi-layered, (20–)25–36(–45) μm in diameter and show regularly a visible septum at the spore base, despite the small spore and tiny hyphae sizes. Phylogenetically, the new fungus represents a new genus in a separated clade, near to the already known Dominikia clades. It can be distinguished from other species by the small spore size, the characteristics of the spore wall layers, and the clearly visible septum at the spore base, which in Kamienskia and Microkamienskia species has rarely to never been reported, while Dominikia species usually have a higher variability of spore sizes and spore wall characteristics. The fungus is here described under the epithet Nanoglomus plukenetiae, serving as type species of the new genus Nanoglomus. The revision of the species and environmental sequences in the Dominikia clades, based on both morphological and molecular phylogenetic analyses, revealed at least two other new genera: Microdominikia gen. nov., based on D. litorea, and Orientoglomus gen. nov., based on D. emiratia. Finally, in the present study, a key for all small-spored species in the Glomeraceae is included comprising all known Dominikia, Kamienskia, Microdominikia, Microkamienskia, Nanoglomus, Orientoglomus spp., and all small-spored Rhizoglomus spp.
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References
Alguacil MM, Torrecillas E, Torres P, García-Orenes F, Roldán A (2012) Long-term effects of irrigation with waste water on soil AM fungi diversity and microbial activities: the implications for agro-ecosystem resilience. PLoS One 7:e47680
Al-Yahya’ei MN, Mullath SK, AlDhaheri LA, Kozłowska A, Błaszkowski J (2017) Dominikia emiratia and Rhizoglomus dunense, two new species in the Glomeromycota. Botany 95:629–639
An GH, Miyakawa S, Kawahara A, Osaki M, Ezawa T (2008) Community structures of arbuscular mycorrhizal fungi associated with pioneer grass species Miscanthus sinensis in acid sulfate soils: habitat segregation along pH gradients. Soil Sci Plant Nutr 54:517–528
Avio L, Castaldini M, Fabiani A, Bedini S, Sbrana et al (2013) Impact of nitrogen fertilization and soil tillage on arbuscular mycorrhizal fungal communities in a Mediterranean agroecosystem. Soil Biol Biochem 67:285–294
Baltruschat H, Santos VM, Silva DKA, Schellenberg I, Deubel A, Sieverding E, Oehl F (2019) Unexpectedly high diversity of arbuscular mycorrhizal fungi in fertile Chernozem croplands in Central Europe. Catena 182:104135. https://doi.org/10.1016/j.catena.2019.104135
Błaszkowski J (2012) Glomeromycota. W. Szafer Institute of Botany, Polish Academy of Sciences, Kraków
Błaszkowski J, Tadych M, Madej T (2000) Glomus minutum, a new species in Glomales (Zygomycetes) from Poland. Mycotaxon 76:187–195
Błaszkowski J, Ryszka P, Oehl F, Koegel S, Wiemken A et al (2009) Glomus achrum and G. bistratum, two new species of arbuscular mycorrhizal fungi (Glomeromycota) found in maritime sand dunes. Botany 87:260–271
Błaszkowski J, Wubet T, Harikumar VS, Ryszka P, Buscot F (2010) Glomus indicum, a new arbuscular mycorrhizal fungus. Botany 88:132–143
Błaszkowski J, Chwat G, Góralska A, Ryszka P, Kovács GM (2015a) Two new genera, Dominikia and Kamienskia, and D. disticha sp. nov. in Glomeromycota. Nova Hedwigia 100:225–238
Błaszkowski J, Chwat G, Symanczik S, Góralska A (2015b) Dominikia duoreactiva sp. nov. and Dominikia difficilevidera sp. nov., two new species in the Glomeromycota. Botany 93:389–396
Błaszkowski J, Chwat G, Góralska A (2016) Dominikia lithuanica and Kamienskia divaricata: new species in the Glomeromycota. Botany 94:1075–1085
Błaszkowski J, Kozłowska A, Niezgoda P, Goto BT, Dalpé Y (2018a) A new genus, Oehlia with Oehlia diaphana comb. nov. and an emended description of Rhizoglomus vesiculiferum comb. nov. in the Glomeromycotina. Nova Hedwigia 107:501–518
Błaszkowski J, Ryszka P, Kozłowska A (2018b) Dominikia litorea, a new species in the Glomeromycotina, and biogeographic distribution of Dominikia. Phytotaxa 338:241–254
Brundrett M, Melville L, Peterson L (1994) Practical methods in mycorrhizal research. Mycologue Publications, University of Guelph, Guelph
Cheng Y, Ishimoto K, Kuriyama Y, Osaki M, Ezawa T (2013) Ninety-year-, but not single, application of phosphorus fertilizer has a major impact on arbuscular mycorrhizal fungal communities. Plant Soil 365:397–407
Corazon-Guivin MA, Mendoza AC, Guerrero-Abad JC, Vallejos-Tapullima A, Carballar-Hernández S, Silva GA, Oehl F (2019a) Funneliglomus, gen. nov., and Funneliglomus sanmartinensis, a new arbuscular mycorrhizal fungus from the Amazonia region in Peru. Sydowia 71:17–24
Corazon-Guivin MA, Mendoza AC, Guerrero-Abad JC, Vallejos-Tapullima A, Carballar-Hernández S, Silva GA, Oehl F (2019b) Microkamienskia gen. nov. and Microkamienskia peruviana, a new arbuscular mycorrhizal fungus from Western Amazonia. Nova Hedwigia 109:355–368..
Declerck S, Cranenbrouck S, Dalpé Y, Séguin S, Grandmougin-Ferjani A, Fontaine J, Sancholle M (2000) Glomus proliferum sp. nov.: a description based on morphological, biochemical, molecular and monoxenic cultivation data. Mycologia 92:1178–1187
Garcés-Ruiz M, Senés-Guerrero C, Declerck S, Cranenbrouck S (2019) Community composition of arbuscular mycorrhizal fungi associated with native plants growing in a petroleum-polluted soil of the Amazon region of Ecuador. Microbiologyopen 8:e00703
Gerdemann JW, Trappe JM (1974) The Endogonaceae in the Pacific northwest. Mycol Memoirs 5:1–76
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704
Hall IR (1977) Species and mycorrhizal infections of New Zealand Endogonaceae. Trans Brit Mycol Soc 68:341–356
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41:95–98.
Hewitt EJ (1966) Sand and water culture methods used in the study of plant nutrition. Farnhan Royal, Commonwealth Agricultural Bureau, Farnham
Jobim K, Błaszkowski J, Niezgoda P, Kozłowska A, Zubek S et al (2019) New sporocarpic taxa in the phylum Glomeromycota: Sclerocarpum amazonicum gen. Et sp. nov. in the family Glomeraceae (Glomerales) and Diversispora sporocarpia sp. nov. in the Diversisporaceae (Diversisporales). Mycol Progress 18:369–384
Koske RE, Tessier B (1983) A convenient, permanent slide mounting medium. Mycol Soc Am Newsl 34:59
Koske RE, Gemma JN, Olexia PD (1986) Glomus microaggregatum, a new species in the Endogonaceae. Mycotaxon 26:125–132
Krüger M, Stockinger H, Krüger C, Schüßler A (2009) DNA-based species level detection of Glomeromycota: one PCR primer set for all arbuscular mycorrhizal fungi. New Phytol 183:212–223
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948
Li LF, Li T, Zhang Y, Zhao ZW (2010) Molecular diversity of arbuscular mycorrhizal fungi and their distribution patterns related to host-plants and habitats in a hot and arid ecosystem, Southwest China. FEMS Microbiol Ecol 71:418–427
Lin TC, Silva GA, Oehl F (2019) Acaulospora tsugae, a new species in the Glomeromycetes from Taiwan, and a key to species in Acaulosporaceae. Nova Hedwigia 108:475–488
López-García A, Azcón-Aguilar C, Barea JM (2014) The interactions between plant life form and fungal traits of arbuscular mycorrhizal fungi determine the symbiotic community. Oecologia 176:1075–1086
Magurno F, Sasvári Z, Barchi L, Posta K (2014) From monoculture to Norfolk system: how the number of crops in rotation can influence the biodiversity of arbuscular mycorrhiza assemblages in the soil. Open J Ecol 4:1080–1088
Marinho F, Silva IR, Oehl F, Maia LC (2018) Checklist of arbuscular mycorrhizal fungi in tropical forests. Sydowia 70:107–127
Marinho F, Oehl F, Silva IR, Coyne D, Veras JS, Maia LC (2019) High diversity of arbuscular mycorrhizal fungi in natural and anthropized sites of a Brazilian tropical dry forest (Caatinga). Fungal Ecol 40:82–91
Milne I, Wright F, Rowe G, Marshal DF, Husmeier D et al (2004) TOPALi: software for automatic identification of recombinant sequences within DNA multiple alignments. Bioinformatics 20:1806–1807
Mosse B (1962) Establishment of vesicular-arbuscular mycorrhiza under aseptic conditions. J Genetic Microbiol 27:509–520
Oehl F, Wiemken A, Sieverding E (2003) Glomus aureum, a new sporocarpic species in the Glomales from European grasslands. J Appl Bot 77:111–115
Oehl F, Redecker D, Sieverding E (2005) Glomus badium, a new sporocarpic arbuscular mycorrhizal fungal species from European grasslands of higher soil pH. J Appl Bot Food Qual 79:38–43
Oehl F, Silva GA, Goto BT, Sieverding E (2011) Glomeromycota: three new genera, and glomoid species reorganized. Mycotaxon 116:75–120
Oehl F, Sánchez-Castro I, Sousa NMF, Silva GA, Palenzuela J (2015) Dominikia bernensis, a new arbuscular mycorrhizal fungus from a Swiss no-till farming site, and D. aurea, D. compressa, and D. indica, three new combinations in Dominikia. Nova Hedwigia 101:65–76
Oehl F, Laczko E, Oberholzer H-R, Jansa J, Egli S (2017) Diversity and biogeography of arbuscular mycorrhizal fungi in agricultural soils. Biol Fertil Soils 53:777–797
Oehl F, Sánchez-Castro I, Silva DKA, Santos VM, Palenzuela J, Silva GA (2019) Septoglomus nigrum, a new arbuscular mycorrhizal fungus from France, Germany and Switzerland. Nova Hedwigia 109:121–134.
Palenzuela J, Azcón-Aguilar C, Barea JM, Silva GA, Oehl F (2013) Septoglomus altomontanum, a new arbuscular mycorrhizal fungus from mountainous and alpine areas in Andalucía (southern Spain). IMA Fungus 4:243–249
Pirozynski KA, Dalpé Y (1989) Geological history of the Glomaceae with particular reference to mycorrhizal symbiosis. Symbiosis 7:1–36
Procter AC, Ellis JC, Fay PA, Polley HW, Jackson RB (2014) Fungal community responses to past and future atmospheric CO2 differ by soil type. Appl Environ Microbiol 80:7364–7377
Rojas-Mego KC, Elizarbe-Melgar C, Gárate-Díaz MH, Ayala-Montejo D, Ruíz-Cubillas P, Sieverding E (2014) Hongos de micorriza arbuscular en tres agroecosistemas de cacao (Theobroma cacao L.) en la amazonía peruana. Folia Amazónica 23:149–156
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Ruíz P, Rojas KC, Sieverding E (2011) La distribución geográfica de los hongos de micorriza arbuscular: una prioridad de investigación en la Amazonía peruana. Espacio y Desarrollo 23:47–63
Schnoor TK, Lekberg Y, Rosendahl S, Olsson PA (2011) Mechanical soil disturbance as a determinant of arbuscular mycorrhizal fungal communities in semi-natural grassland. Mycorrhiza 21:211–220
Schüßler A, Walker C (2010) The Glomeromycota: a species list with new families and new genera. The Royal Botanic Garden Kew, Botanische Staatssammlung Munich, and Oregon State University, effectively published 16 December 2010 in Gloucester (England)
Sieverding E (1991) Vesicular-Arbuscular Mycorrhiza Management in Tropical Agrosystems. Deutsche Gesellschaft für Technische Zusammenarbeit Nr. 224. Hartmut Bremer Verlag, Friedland
Sieverding E, Silva GA, Berndt R, Oehl F (2014) Rhizoglomus, a new genus in the Glomeraceae. Mycotaxon 129:373–386
Spain JL (1990) Arguments for diagnoses based on unaltered wall structures. Mycotaxon 38:71–76
Srichamnong W, Ting P, Pitchakarn P, Nuchuchua O, Temviriyanukul P (2018) Safety assessment of Plukenetia volubilis (Inca peanut) seeds, leaves, and their products. Food Sci Nutr 6:962–969
Symanczik S, Al-Yahya’ei MN, Kozłowska A, Ryszka P, Błaszkowski J (2018) A new genus, Desertispora, and a new species, Diversispora sabulosa, in the family Diversisporaceae (order Diversisporales, subphylum Glomeromycotina). Mycol Progress 17:437–449
Tulasne LR, Tulasne C (1845) Fungi nonnulli hypogaei, novi minus cogniti act. Giorn Bot Ital 2:35–63
Turrini A, Saran M, Giovannetti M, Oehl F (2018) Rhizoglomus venetianum, a new arbuscular mycorrhizal fungal species from a heavy metal contaminated site, downtown Venice in Italy. Mycol Progress 17:1213–1224
Vieira LC, Silva DKA, Silva IR, Gonçalves CM, Assis DMA, Oehl F, Silva GA (2019) Ecological aspects of arbuscular mycorrhizal fungal communities in different habitat-types of a Brazilian mountain. Ecol Res 34:182–192
Vierheilig H, Coughlan AP, Wyss U, Piché Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microbiol 4:5004–5007
Vu D, Groenewald M, de Vries M, Gehrmann T, Stielow B et al (2019) Large-scale generation and analysis of filamentous fungal DNA barcodes boosts coverage for kingdom fungi and reveals thresholds for fungal species and higher taxon delimitation. Stud Mycol 92:135–154
Wang Y, Huang Y, Qiu Q, Xin G, Yang Z, Shi S (2011) Flooding greatly affects the diversity of arbuscular mycorrhizal fungi communities in the roots of wetland plants. PLoS One 6:e24512
Wang Y, Li T, Li Y, Qiu Q, Li S, Xin G (2015) Distribution of arbuscular mycorrhizal fungi in four semi-mangrove plant communities. Ann Microbiol 65:603–610
Wang S, Zhu F, Kakuda Y (2018) Sacha inchi (Plukenetia volubilis L.): nutritional composition, biological activity, and uses. Food Chem 265:316–328
Yamato M, Yagame T, Yoshimura Y, Iwase K (2012) Effect of environmental gradient in coastal vegetation on communities of arbuscular mycorrhizal fungi associated with Ixeris repens (Asteraceae). Mycorrhiza 22:623–630
Yang W, Zheng Y, Gao C, He X, Ding Q et al (2013) The arbuscular mycorrhizal fungal community response to warming and grazing differs between soil and roots on the Qinghai-Tibetan plateau. PLoS One 8:e76447
Acknowledgments
The authors thank all the members of the Laboratorio de Biología y Genética Molecular for collaborating in the publication of this article and to the farmers of the towns of Palmiche and Paucarpata (Lamas) for providing us with the facilities for the collection of soil samples.
Funding
The study was financially supported by the Programa Nacional de Innovación Agraria (PNIA) and the Universidad Nacional de San Martín-Tarapoto (UNSM-T) through the contract N° 037-2015-INIA-PNIA-IE; through the loan agreement N° 8331-PE, signed between the government of Peru and the International Bank for Reconstruction and Development –BIRF. Likewise, at Consejo Nacional de Ciencia y Tecnología, CIENCIACTIVA (CONCYTEC, Peru) for the financing granted within the framework of the project with SUBVENTION AGREEMENT N° 187-2015-FONDECYT. Gladstone Alves da Silva thanks to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the Fellowship granted (Proc. 312186/2016-9).
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Corazon-Guivin, M.A., Cerna-Mendoza, A., Guerrero-Abad, J.C. et al. Nanoglomus plukenetiae, a new fungus from Peru, and a key to small-spored Glomeraceae species, including three new genera in the “Dominikia complex/clades”. Mycol Progress 18, 1395–1409 (2019). https://doi.org/10.1007/s11557-019-01522-1
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DOI: https://doi.org/10.1007/s11557-019-01522-1