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Sacculospora Felinovii, a Novel Arbuscular Mycorrhizal Fungal Species (Glomeromycota) from Dunes on the West Coast of India

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Sacculospora Felinovii, a Novel Arbuscular Mycorrhizal Fungal Species (Glomeromycota) from Dunes on the West Coast of India Mycol Progress (2016) 15:791–798 DOI 10.1007/s11557-016-1208-6 ORIGINAL ARTICLE Sacculospora felinovii, a novel arbuscular mycorrhizal fungal species (Glomeromycota) from dunes on the west coast of India Andy Willis1,2 & Janusz Błaszkowski3 & Tanvi Prabhu 1 & Gerard Chwat3 & Anna Góralska3 & Burla Sashidhar 4 & Phil Harris2 & James D’Souza1 & Jyoti Vaingankar1 & Alok Adholeya4 Received: 12 January 2016 /Revised: 11 June 2016 /Accepted: 14 June 2016 /Published online: 27 June 2016 # German Mycological Society and Springer-Verlag Berlin Heidelberg 2016 Abstract During an arbuscular mycorrhiza fungal spore Keywords Entrophosporoid spore . Molecular phylogeny . survey on a primary coastal sand-dune system in Goa Morphology . Tropical coastal dunes on the west coast of India, entrophosporoid spores tight- ly covered with a dense hyphal mantle were recovered. When intact, the spores, at first sight, seemed to be Introduction identical in morphology to those of Sacculospora baltica (originally described as Entrophospora baltica) Of the ca. 280 described arbuscular mycorrhizal fungal extracted from Polish maritime sand dunes and, to date, (AMF) species of the phylum Glomeromycota C. Walker & the sole member of the recently described genus A. Schüßler, only five form spores inside the neck of a Sacculospora in the new family Sacculosporaceae, phy- sporiferous saccule (Błaszkowski 2012). From one side, the lum Glomeromycota. Later detailed morphological stud- neck is continuous with a mycorrhizal extraradical hypha and ies indicated that both fungi produce two-walled spores from the other side, the neck passes into a globose to ellipsoi- but the structure and phenotypic features of components dal saccule. Contents from both structures are used in spore of the outer spore wall in the novel fungus differ con- genesis. In fully developed specimens, the saccule is usually siderably from those of S. baltica. Differences between empty and frequently detached from spores and the neck wall the fungi were subsequently confirmed in the phyloge- is continuous with the outermost spore wall layer, forming the netic analysis of SSU–ITS–LSU nrDNA sequences. spore surface (Błaszkowski 2012). This mode of spore syn- Consequently, we describe the novel species as thesis was first described by Ames and Schneider (1979)ina Sacculospora felinovii sp. nov. species originally named Glomus infrequens I.R. Hall (Hall 1977). Ames and Schneider (1979) subsequently transferred G. infrequens to a newly erected genus Entrophospora R.N. Section Editor: Marco Thines Ames & R.W. Schneid., with E. infrequens (I.R. Hall) R.N. Ames & R.W. Schneid. as type species. The other four species * Andy Willis accommodated in Entrophospora were E. baltica Błaszk., [email protected] Madej & Tadych, E. colombiana Spain & N.C. Schenck, E. kentinensis C.G. Wu & Y.S. Liu and E. schenckii Sieverd. 1 Department of Botany, Goa University, Taleigao Plateau, Goa 403 &S.Toro(Schencketal.1984; Sieverding and Toro 1987; 206, India Wu et al. 1995;Błaszkowski et al. 1998). Such a mode of 2 Centre for Agroecology, Water and Resilience, Coventry University, spore formation and the spores themselves have been named Priory St., Coventry CV1 5FB, UK entrophosporoid (Goto and Maia 2006). 3 Department of Ecology, Protection and Shaping of Environment, From observed differences in the subcellular structure of West Pomeranian University of Technology in Szczecin, spores and the phenotypic and histochemical characters of Słowackiego 17, 71434 Szczecin, Poland components of spore walls of Entrophospora species, 4 The Energy and Resources Institute (TERI), Darbari Seth Block, Sieverding and Oehl (2006) transferred three of the species India Habitat Centre, New Delhi 110 003, India to two newly erected genera, Intraspora Oehl & Sieverd., with 792 Mycol Progress (2016) 15:791–798 I. schenckii (Sieverd. & S. Toro) Oehl & Sieverd. (formerly specimens, indicated that traits in the outer spore wall differed. E. schenckii) in the family Archaeosporaceae J.B. Morton & Unsure if the differences represented intraspecific variability D. Redecker, and Kuklospora Oehl & Sieverd., with of one organism, a comparison was made using molecular K. colombiana (Spain & N.C. Schenck) Oehl & Sieverd. (for- methods. The molecular analyses confirmed the previous con- merly E. colombiana)andK. kentinensis (C.G. Wu & Y.S. clusions resulting from morphological observations that the Liu) Oehl & Sieverd. (formerly E. kentinensis) in the family novel fungal species differs considerably from S. baltica. Acaulosporaceae J.B. Morton & Benny. Kaonongbua et al. Consequently, the fungus is described as Sacculospora (2010) and Schüßler and Walker (2010) rejected Kuklospora felinovii sp. nov. and Intraspora, respectively, later substantiated by the phylo- genetic analyses of Krüger et al. (2012). Oehl et al. (2011) concluded from phylogenetic analyses of nrDNA sequences Materials and methods that E. infrequens and E. baltica differ at the family level and, therefore, erected Sacculosporaceae Oehl et al. fam. nov., Extraction of spores, establishment and growth of trap with Sacculospora Oehl et al. gen. nov. and S. baltica and single-species cultures (Błaszk., Madej & Tadych) Oehl et al. comb. nov. To date, the genus Sacculospora has been represented by Spores were extracted by the wet-sieving and decanting meth- S. baltica alone. Morphologically, S. baltica differs clearly od (Gerdemann and Nicolson 1963) from field-collected sam- from all other known species forming entrophosporoid spores. ples of rhizosphere soil of the perennial C4 Zoysia matrella The most conspicuous structure is the hyphal mantle tightly (L.) Merr. (Poaceae) and incorporated into pot trap cultures, covering spores. The spore subcellular structure, which is 12 cm diam., 9 cm high (1018 cm3). The pots were maintained complex and difficult to define, further distinguishes the spe- outdoors at temperatures of 18–30 °C for 10 months at Goa cies. According to Błaszkowski et al. (1998), S. baltica spores University. Host plants were Z. matrella, rhizomes transferred contain two spore walls: an outer wall with four layers and an from the dunes, along with stem cuttings of Solenostemon inner three-layered wall. Oehl et al. (2011) stated that layer 1 scutellarioides (L.) R.Br. (Lamiaceae), cultured in unsterilised of the inner wall sensu Błaszkowski et al. (1998) clearly sep- Z. matrella rhizosphere soil. Plants were watered 2–3 times a arates from the other layers of the wall and, therefore, week. No nutrients were applied during the growing period. redefined the subcellular structure of S. baltica spores as Subsequently, spores (ca. 200) extracted from the trap culture three-walled. However, neither Błaszkowski et al. (1998)nor were placed in pots at the base of holes into which stem cut- Oehl et al. (2011) performed ontogenetic studies of the spe- tings of S. scutellarioides were inserted. The medium was cies, characterising the subcellular structure of S. baltica sterilised (180 °C for 12 h × 3) dune sand. The plants were spores based only on the spatial grouping of its components raised in a ‘closed’ greenhouse (i.e. no ventilation, reducing in crushed specimens. Importantly, the spatial arrangement of risk of outside contamination) at Goa University. Hoaglands spore subcellular components in AMF may be influenced by solution minus P was applied fortnightly. After 8 months, the vigour of spore crushing (Błaszkowski, pers. observ.). single-species spore cultures were achieved and harvested. Study of the ontogeny of S. baltica spores is severely hindered This two-stage method follows that of Dr. B. F. Rodrigues, for two reasons. First, the fungus is difficult to grow in culture. Goa University (unpublished), demonstrating successful In the literature, there is no report that the species has been single-species culture where, all too often, novel species cul- grown in single-species cultures and numerous efforts to ob- ture fails. Nevertheless, only one of two initial cultures spor- tain such cultures by J. Błaszkowski failed (Błaszkowski et al. ulated and only one of two subsequent cultures has sporulated 1998;Błaszkowski 2012). The ontogeny of any AMF may be but in less abundance. The morphological and histochemical known with certainty only by the examination of specimens features of mycorrhizal structures revealed following staining originating from single-species cultures. Second, the disclo- in Trypan blue (Phillips and Hayman 1970) testified that they sure of sequences of differentiation and organisation of the represent one species of AMF. In addition, in the cultures, no spore subcellular components may be difficult, or impossible, other spore morphotypes were found among the characteristic because of the obscuring influence of the dense and coloured spores of the new species. hyphal mantle. Whilst investigating AMF spore density and diversity on Microscopy and nomenclature an interrupted belt transect across a primary dune system on the coast of Goa, India (73°40′33″ E, 14°53′54″ N), AMF The morphological features of spores and the phenotypic and spore specimens were found that seemed identical to those histochemical characters of spore wall layers were determined of S. baltica. Detailed morphological studies of the spore sub- after examination of at least 100 spores mounted in water, cellular structure, however, and the phenotypic and histo- lactic acid, polyvinyl alcohol/lactic acid/glycerol (PVLG; chemical characters of components of spore walls of the Omar
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