Genomic Organization of Repetitive DNA in Woodpeckers (Aves, Piciformes): Implications for Karyotype and ZW Sex Chromosome Differentiation

Thays Duarte De Oliveira,Marcelo De Bello Cioffi,Edivaldo Herculano Corrêa De Oliveira,Rafael Kretschmer,Natasha Avila Bertocchi,Tiago Marafiga Degrandi,Analía Del Valle Garnero,Ricardo José Gunski,Arthur J Lustig

doi:10.1371/journal.pone.0169987

Abstract

Birds are characterized by a low proportion of repetitive DNA in their genome when compared to other vertebrates. Among birds, species belonging to Piciformes order, such as woodpeckers, show a relatively higher amount of these sequences. The aim of this study was to analyze the distribution of different classes of repetitive DNA—including microsatellites, telomere sequences and 18S rDNA—in the karyotype of three Picidae species (Aves, Piciformes)—Colaptes melanochloros (2n = 84), Colaptes campestris (2n = 84) and Melanerpes candidus (2n = 64)–by means of fluorescence in situ hybridization. Clusters of 18S rDNA were found in one microchromosome pair in each of the three species, coinciding to a region of (CGG)10 sequence accumulation. Interstitial telomeric sequences were found in some macrochromosomes pairs, indicating possible regions of fusions, which can be related to variation of diploid number in the family. Only one, from the 11 different microsatellite sequences used, did not produce any signals. Both species of genus Colaptes showed a similar distribution of microsatellite sequences, with some difference when compared to M. candidus. Microsatellites were found preferentially in the centromeric and telomeric regions of micro and macrochromosomes. However, some sequences produced patterns of interstitial bands in the Z chromosome, which corresponds to the largest element of the karyotype in all three species. This was not observed in the W chromosome of Colaptes melanochloros, which is heterochromatic in most of its length, but was not hybridized by any of the sequences used. These results highlight the importance of microsatellite sequences in differentiation of sex chromosomes, and the accumulation of these sequences is probably responsible for the enlargement of the Z chromosome.

Highlights

It is known that the avian genome is extremely compact, corresponding to approximately one third of the typical mammalian DNA content [1]
Karyotype analyses showed that woodpeckers have some distinctive features, such as high diploid numbers (2n), with some species possessing more than 100 chromosomes, and a large Z chromosome, the largest element of the karyotype [10,11,12,13,14,15]
Birds belonging to the Picidae family showed an interesting chromosomal variation, with 2n ranging from 64 to 108 (Table 4)

Summary

Introduction

It is known that the avian genome is extremely compact, corresponding to approximately one third of the typical mammalian DNA content [1]. This decrease occurred due to the loss of many genes and, in a higher proportion, DNA repetitive sequences [2]. The Picidae family (woodpeckers) shows the highest proportion of repetitive sequences in genomes among birds, reaching up to 22% of total DNA amount in the species Picoides pubescens, where the transposable element CR1 is one of the most important components [3]. Karyotype analyses showed that woodpeckers have some distinctive features, such as high diploid numbers (2n), with some species possessing more than 100 chromosomes, and a large Z chromosome, the largest element of the karyotype [10,11,12,13,14,15]

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Results

Conclusion