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Glomeromycotean associations in liverworts: a molecular, cellular, and taxonomic analysis¹

Dipartimento di Scienze ambientali, Seconda Università di Napoli, via A. Vivaldi 43, I-81100 Caserta, Italy; Dipartimento di Biologia vegetale, Università degli Studi di Torino, and Consiglio Nazionale delle Ricerche (CNR), Istituto per la Protezione delle Piante, Sezione di Torino, Viale P. A. Mattioli 25, I-10125, Torino, Italy; School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London E1 4NS, UK

ABSTRACT

Liverworts form endophytic associations with fungi that mirror mycorrhizal associations in tracheophytes. Here we report a worldwide survey of liverwort associations with glomeromycotean fungi (GAs), together with a comparative molecular and cellular analysis in representative species. Liverwort GAs are circumscribed by a basal assemblage embracing the Haplomitriopsida, the Marchantiopsida (except a few mostly derived clades), and part of the Metzgeriidae. Fungal endophytes from Haplomitrium, Conocephalum, Fossombronia, and Pellia were related to Glomus Group A, while the endophyte from Monoclea was related to Acaulospora. An isolate of G. mosseae colonized axenic thalli of Conocephalum, producing an association similar to that in the wild. Fungal colonization in marchantialean liverworts suppressed cell wall autofluorescence and elicited the deposition of a new wall layer that specifically bound the monoclonal antibody CCRC-M1 against fucosylated side groups associated with xyloglucan and rhamnogalacturonan I. The interfacial material covering the intracellular fungus contained the same epitopes present in host cell walls. The taxonomic distribution and cytology of liverwort GAs suggest an ancient origin and multiple more recent losses, but the occurence in widely separated liverwort taxa of fungi related to glomeromycotean lineages that form arbuscular mycorrhizas in tracheophytes, notably the Glomus Group A, is better explained by host shifting from tracheophytes to liverworts.

Key Words: arbuscular mycorrhizas • cell walls • DNA sequencing • Glomeromycota • immunocytochemistry • liverworts • symbiosis • ultrastructure

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