Cryptic diversity and significant cophylogenetic signal detected by DNA barcoding the rust fungi (Pucciniaceae) of Cyperaceae–Juncaceae

Abstract

Plants play important roles as habitat and food for a tremendous diversity of specialist animals and fungi. The disappearance of any plant species can lead to extinction cascades of its associated biota. In consequence, documenting the diversity and specificity of plant-associated organisms is of high practical relevance in biodiversity conservation. Here, we present the first large-scale molecular investigation into the diversity, host specificity, and cophylogenetic congruence of an especially rich plant-fungal association, the rust fungi (Pucciniaceae) of Cyperaceae and Juncaceae. Using the largest rust fungi DNA barcoding dataset published to date (252 sequences, 82 taxa), we reject the presence of a global ITS2-28S barcode gap, but find a local gap in Cyperaceae-Juncaceae rusts, and suggest the existence of many cryptic species in North America, with some broadly circumscribed species possibly corresponding to >10 cryptic species. We test previous hypotheses of correlations between the phylogenies of rust fungi and their Cyperaceae-Juncaceae hosts using a combination of global-fit and event-based cophylogenetic methods. A significant cophylogenetic signal is detected between rusts and their hosts, but the small number of cospeciations argues for preferential host jumps as the driving process behind these correlations. In addition, temporal congruence between the origin of major Carex clades and their rusts suggests that host diversification may have promoted parasite diversification. Finally, we discuss the relevance of rust infection patterns to the systematics of Cyperaceae, highlight some taxonomic problems uncovered by the analyses, and call attention to the promise of DNA barcoding for bridging knowledge gaps in poorly studied plant-associated microorganisms.

Targeted sequencing supports morphology and embryo features in resolving the classification of Cyperaceae tribe Fuireneae s.l.

“…forms a grade of successive sisters terminating with tribe Cypereae. Moreover, morphology, anatomy, embryo features (Goetghebeur & Simpson, 1991;Tatanov, 2007), and even fungal parasites (Savile, 1972;Léveillé-Bourret et al, 2021) suggest a distant relationship between Bolboschoenus and Schoenoplectus s.s. Likewise, the genus Fuirena is monophyletic and very strongly supported as in previous molecular analyses (e.g., Hinchliff et al, 2010;Spalink et al, 2016;Glon et al, 2017).…”

Genetic time traveling: sequencing old herbarium specimens, including the oldest herbarium specimen sequenced from kingdom Fungi, reveals the population structure of an agriculturally significant rust

“…DNA extractions were accomplished using the Chelex method in the United States laboratory (Walsh et al ., 1991; ER and WTU) or as described by Léveillé‐Bourret et al . (2021; DAOM) in the Canadian laboratory. Briefly, rust fruiting bodies were incised from the herbarium specimen and placed in a 2‐ml tube containing 50 μl of Chelex InstaGene Matrix (BioRad).…”

Rtapas: An R package to assess cophylogenetic signal between two evolutionary histories

“…Random Tapas is especially helpful in aiding the biological interpretation of large tanglegrams (e.g. Dupeyron et al 2021; Léveillé-Bourret et al 2021) and provides a way to incorporate phylogenetic uncertainty into estimation of cophylogenetic signal (e.g. Hayward et al 2021).…”