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Acaulospora Aspera, a New Fungal Species in the Glomeromycetes from Rhizosphere Soils of the Inka Nut (Plukenetia Volubilis

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Acaulospora Aspera, a New Fungal Species in the Glomeromycetes from Rhizosphere Soils of the Inka Nut (Plukenetia Volubilis Journal of Applied Botany and Food Quality 92, 250 - 257 (2019), DOI:10.5073/JABFQ.2019.092.035 1Laboratorio de Biología y Genética Molecular, Universidad Nacional de San Martín, Morales, Peru 2Instituto Nacional de Innovación Agraria (INIA), Dirección General de Recursos Genéticos y Biotecnología, La Molina - Lima, Peru 3Departamento de Micologia, CB, Universidade Federal de Pernambuco, Cidade Universitária, Recife, Brazil 4Agroscope, Competence Division for Plants and Plant Products, Ecotoxicology, Wädenswil, Switzerland Acaulospora aspera, a new fungal species in the Glomeromycetes from rhizosphere soils of the inka nut (Plukenetia volubilis L.) in Peru Mike Anderson Corazon-Guivin1*, Agustin Cerna-Mendoza1, Juan Carlos Guerrero-Abad1,2, Adela Vallejos-Tapullima1, Gladstone Alves da Silva3, Fritz Oehl4* (Submitted: July 1, 2019; Accepted: September 8, 2019) Summary In San Martín State, located in the transition of the last mountain A new fungal species of the Glomeromycetes, Acaulospora aspera, ridges in the Peruvian Andes towards the Amazonian lowlands, a was isolated from the rhizosphere of the inka nut (Plukenetia volubi- few new AM fungal species have been detected recently, such as two lis) in San Martín State of Peru (Western Amazonia) and propagated new species of the Glomeraceae, Funneliglomus sanmartinensis and in bait cultures on Sorghum spp., Brachiaria brizantha, Medicago Microkamienskia peruviana (Corazon-Guivin et al., 2019a, b). Re- sativa and P. volubilis as host plants. The fungus forms brownish markably, these were isolated in rhizosphere soils of the inka nut yellow to yellow brown spores, (120-)135-195 × (120-)130-187 μm in (Plukenetia volubilis L.) that usually is grown there in mixed cul- diameter. The surface of the structural spore wall layer is crowded ture systems together with several annual crops, such as Zea mays, with small depressions, 0.4-0.7 μm in diameter, up to 0.8 μm deep, Phaseolus vulgaris, Arachis hypogaea, seeded between the rows of and only 1.1-1.8 apart, giving the spore surface a rough, washboard- the main crop inka nut. The inka nut is native to the Peruvian Ama- like appearance, especially when the outermost, evanescent wall lay- zon and has gained increasing agronomic and economic attention er has disappeared. Phylogenetically, the new species is close to A. in Peru and other tropical countries due to its elevated contents of spinosissima, A. excavata and to other morphologically more similar unsaturated fatty acids (omega 3, 6, and 9; CHIRINOS et al., 2013; species such as A. spinosa and A. tuberculata, which form spiny or SRICHAMNONG et al., 2018; wanG et al., 2018). The inka nut plant, tuberculate projections on the outermost, semi-persistent spore wall its cultivation and the fruits/nuts are presented in the Figs. 1-12. layer, or A. herrerae, A. kentinensis, A. scrobiculata and A. minuta, During diversity studies in inka nut plantations of the Peruvian which on the structural spore wall layer all have more pronunced pits Amazonian lowlands and adjacent low level mountain ranges of San than A. aspera. In this study, also the name of A. spinosissima was Martin State in Peru, a further new glomeromycotean fungus was validated, as it had been preliminary declared invalid because of a detected morphologically resembling to Acaulospora laevis, Acau- typing error in the diagnosis section of its original description. lospora spinosissima and Acaulospora herrerae in spore color and sizes (GERDEMANN and TRAPPE, 1974; Furrazola et al., 2013; oehl et al., 2014). The objective of the present study was to analyze Key words: Acaulospora spinosissima, Acaulosporaceae, arbuscu- thoroughly the spores of the new fungus both morphologically and lar mycorrhizal fungi, biodiversity, Glomeromycetes, phylogeny. phylogenetically and to describe it under the new epithet Acaulo- spora aspera. Finally, we validated the name of the fungus Acau- lospora spinosissima, for which in the original description a typing Introduction error in the accession number of the holotype slide had been made in the diagnosis section (oehl et al., 2014). Arbuscular mycorrhizal (AM) fungi are beneficial soil fungi that deliver a couple of important ecosystem services, such plant growth promotion and improved water infiltration and soil aggregation (SIEVERDING, 1991). During the last decades, the knowledge about Material and methods the taxonomy, diversity and biogeography of arbuscular mycorrhizal Study sites and Soil sampling (AM) fungi has considerably been increased (e.g. JANOS and TRAPPE, Soil samples (0-30 cm depth) were repeatedly taken in agricultural 1982; SCHENCK et al., 1984; SIEVERDING et al., 2014; Błaszkowski field site with inka nut at Palmiche (06°20´02.40´´S, 076°36´00.00´´W; et al., 2015; PONTES et al., 2017; TURRINI et al., 2018). This is in 858 m a.s.l.) in the Peruvian Amazonia lowlands and adjacent An- particular true for species of the family Acaulosporaceae (Furrazola dean low mountain ranges in the Department San Martín of the et al., 2013; Palenzuela et al., 2013, 2014, 2015; PEREIRA et al., province Lamas. The site is a traditional agroforestry site, where the 2015). While in 1974 only two Acaulospora species were known inka nut is grown in a mixed culture with maize, beans, peanuts and (GERDEMANN and TRAPPE, 1974) that raised to 15 species in 1990 other annual field crops without addition of chemical fertilizers and (SCHENCK and Pérez, 1990), an increasing number of Acaulospora pesticides. Mean annual temperatures in the study area are about spp. could be included in the continuously developing morphological 25-27 °C, with variation between 18 and 32 °C throughout the year. identification keys o( ehl et al., 2006, 2012; lin et al., 2019). At time, Mean annual precipitation is approximately 1300 mm. already > 50 species are attributed to the Acaulosporaceae (lin et al., 2019). Especially some tropical areas are considered as hot-spots for Acau- AM fungal pot cultures losporaceae (SIEVERDING, 1991; PAGANO et al., 2013; PEREIRA et al., Bait cultures were established in the greenhouse under ambient tem- 2015; BONFIM et al., 2016; JOBIM et al., 2018; MARINHO et al., 2018). perature conditions, in cylindrical 3 L pots with 3 kg of substrate. The substrate consisted of a 1:1 mixture of collected field soil sam- * Corresponding author ples and coarse river sand. The substrate mixtures were autoclaved A new fungal species from rhizosphere soils of the inka nut in Peru 251 Figs. 1-12 Plukenetia volubilis: 1. Inka nut plantation at the type location in Palmiche (province Lamas, San Martín, Peru). The annual agricultural crops maize, peanuts and beans planted in the inter-rows had already been harvested at sampling time. 2-3. Inka nut plants grown at the University of San Martín in Tarapoto. The inka nut plantations in San Martín State last for 4-5 years in the same field and can be replaced by new plantations or other field crops. 4-6. Inka nut capsule fruits in different ripening stages. 7-9. Inka nut plants in different development stages, grown in the greenhouse of the University San Martín in Tarapoto. Inka nut is a semi-woody, climbing plant and need support for vertical growth at early stages, either abiotically or by living plants. 10. Decapsulation of a seed. 11. Dark brown, field collected seeds, each 1-2 cm in diam. 12. Toasted almonds of the inka nut, photographed at a local market in Lamas. at 121 °C for 60 min, three weeks before establishment of the bait the seeds were covered with the remaining 25% of the autoclaved cultures. At bait culture establishment, the pots were first filled to substrate. The cultures were maintained in the greenhouse of the 75% with the autoclaved substrate. Thereafter 100 g of rhizospheric Facultad de Ciencias Agrárias, Universidad Nacional de San Martín- soils were added to the substrate surface, and five seeds either of Tarapoto for eight months, with 21.4 °C, 29 °C and 38.2 ºC as mini- Sorghum vulgaris L., alfalfa (Medicago sativa L.), bread grass (Bra- mum, mean and maximum temperatures, respectively. The relative chiaria brizantha (Hochst. ex A. Rich.) R.Webster) and inka nut humidity was from 48 to 74% between April and November 2018. (Plukenetia volubilis L.) were seeded in order to establish the mycor- The pots were irrigated every other day and fertilized with a Long rhizal association and reproduce spores of the new fungal species Anston nutrient solution with reduced P contents (60% reduction; together with the native AMF communities. The seeds were surface hewitt, 1966) every two weeks. So far, the new fungal species has sterilized before seeding, using sodium hypochlorite (0.5%). Finally, not reproduced spores in single species cultures. 252 M. Anderson Corazon-Guivin, A. Cerna-Mendoza, J.C. Guerrero-Abad, A. Vallejos-Tapullima, G. Alves da Silva, F. Oehl Morphological analyses sporoid spore formation. Photographs (Figs. 13-17) were taken with AM fungal spores were obtained from the field soil and bait cul- a Leica DFC 290 digital camera on a Leitz Laborlux S compound ture samples by a wet sieving, density-gradient, centrifugation and microscope using the Leica Application Suite Version V 2.5.0 R1 decanting process as described by SIEVERDING (1991). The spore software. Specimens mounted in PVLG and PVLG+Melzer’s reagent morphological characteristics and their subcellular structures were were deposited at Z+ZT (ETH Zurich, Switzerland). described from specimens mounted in: (i) polyvinyl alcohol-lactic acid-glycerol (PVLG); (ii) a mixture (1:1) of PVLG and Melzer’s reagent; (iii) a mixture of lactic acid and water (1:1); (iv) Melzer’s Molecular analyses reagent; and (v) water. The spore structure terminology follows oehl Intact, healthy spores were isolated from field soil and bait culture et al. (2012) and Furrazola et al. (2013) for species with acaulo- samples, and superficially cleaned of soil particles by friction on Figs.
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