Early evolutionary colocalization of the nuclear ribosomal 5S and 45S gene families in seed plants: evidence from the living fossil gymnosperm Ginkgo biloba

Abstract

In seed plants, the colocalization of the 5S loci within the intergenic spacer (IGS) of the nuclear 45S tandem units is restricted to the phylogenetically derived Asteraceae family. However, fluorescent in situ hybridization (FISH) colocalization of both multigene families has also been observed in other unrelated seed plant lineages. Previous work has identified colocalization of 45S and 5S loci in Ginkgo biloba using FISH, but these observations have not been confirmed recently by sequencing a 1.8 kb IGS. In this work, we report the presence of the 45S-5S linkage in G. biloba, suggesting that in seed plants the molecular events leading to the restructuring of the ribosomal loci are much older than estimated previously. We obtained a 6.0 kb IGS fragment showing structural features of functional sequences, and a single copy of the 5S gene was inserted in the same direction of transcription as the ribosomal RNA genes. We also obtained a 1.8 kb IGS that was a truncate variant of the 6.0 kb IGS lacking the 5S gene. Several lines of evidence strongly suggest that the 1.8 kb variants are pseudogenes that are present exclusively on the satellite chromosomes bearing the 45S-5S genes. The presence of ribosomal IGS pseudogenes best reconciles contradictory results concerning the presence or absence of the 45S-5S linkage in Ginkgo. Our finding that both ribosomal gene families have been unified to a single 45S-5S unit in Ginkgo indicates that an accurate reassessment of the organization of rDNA genes in basal seed plants is necessary.

Dancing together and separate again: gymnosperms exhibit frequent changes of fundamental 5S and 35S rRNA gene (rDNA) organisation

“…The A 1 subregion located 85–330-bp downstream from the 26S gene was composed of short 39-bp long units. The second subregion (A 2 ) corresponding to the A subregion reported by Galián et al (2012) was located within 671–1228 bp and contained 2.3 copies of a 240 bp repeat. The A 2 monomeric unit was internally repetitive composed of several subrepeats of 39–57 bp in size.…”

“…On the basis of these numerous studies, it has been proposed that in gymnosperms the 5S repeats also hold the separated configuration typical for vascular plants (Wicke et al , 2011). Conversely, Galián et al (2012) undertaking a PCR-based strategy promptly isolated clones from G. biloba with 5S genes integrated in the 26S–18S spacer. The potentially functional 5S gene was located ∼2 kb downstream of the 26S gene.…”

Linked 5S and 45S rDNA Sites Are Highly Conserved through the Subfamily Aurantioideae (Rutaceae)

“…In most species, the loci for 5S and 45S rRNA genes are located in different chromosomes, whereas in other species the 2 loci are found in the same chromosome pair, sometimes closely linked to each other, as observed for example in different species of Brassica [Hasterok et al, 2006], Aristolochia [Berjano et al, 2009] and Rhynchospora [Sousa et al, 2011]. A completely different kind of association, where a single repeat unit contains both rDNA families, first reported in some members of the daisy family Asteraceae [García et al, 2009;Mazzella et al, 2010] and in the gymnosperm Ginkgo biloba [Galián et al, 2012], may be more common than initially thought.…”

Non-Random Distribution of 5S rDNA Sites and Its Association with 45S rDNA in Plant Chromosomes

“…In these cases, the 5S rRNA gene can be encoded on the same strand as the other rRNA genes, as in Marchantia polymorpha [Sone et al, 1999] and Ginkgo biloba [Galián et al, 2012], or in the opposite strand, as in species of Asteraceae [Garcia et al, 2009] and Podocarpus [Garcia and Kovařík, 2013]. In addition, 5S rRNA genes can also be linked to other repeated sequences in tandem, either coding or non-coding [Drouin and Moniz de Sá, 1995;Elder and Turner, 1995;Cabral-deMello et al, 2011].…”