Cytogenetic and genomic organization analyses of chloroplast DNA invasions in the nuclear genome of Asparagus officinalis L. provides signatures of evolutionary complexity and informativity in sex chromosome evolution

Shu-Fen Li,Chuan-Liang Deng,Ke-Li Jia,Jin Wang,Jin-Hong Yuan,Ran Dong,Ning Li,Wu-Jun Gao,Jia-Rong Li,Hong-Wei Zhu

doi:10.1186/s12870-019-1975-8

Shu-Fen Li, Chuan-Liang Deng + Show 8 more

Open Access

https://doi.org/10.1186/s12870-019-1975-8

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Abstract

BackgroundThe transfer of chloroplast DNA into nuclear genome is a common process in plants. These transfers form nuclear integrants of plastid DNAs (NUPTs), which are thought to be driving forces in genome evolution, including sex chromosome evolution. In this study, NUPTs in the genome of a dioecious plant Asparagus officinalis L. were systematically analyzed, in order to investigate the characteristics of NUPTs in the nuclear genome and the relationship between NUPTs and sex chromosome evolution in this species.ResultsA total of 3155 NUPT insertions were detected, and they represented approximated 0.06% of the nuclear genome. About 45% of the NUPTs were organized in clusters. These clusters were derived from various evolutionary events. The Y chromosome contained the highest number and largest proportion of NUPTs, suggesting more accumulation of NUPTs on sex chromosomes. NUPTs were distributed widely in all of the chromosomes, and some regions preferred these insertions. The highest density of NUPTs was found in a 47 kb region in the Y chromosome; more than 75% of this region was occupied by NUPTs. Further cytogenetic and sequence alignment analysis revealed that this region was likely the centromeric region of the sex chromosomes. On the other hand, the male-specific region of the Y chromosome (MSY) and the adjacent regions did not have NUPT insertions.ConclusionsThese results indicated that NUPTs were involved in shaping the genome of A. officinalis through complicated process. NUPTs may play important roles in the centromere shaping of the sex chromosomes of A. officinalis, but were not implicated in MSY formation.

Highlights

The transfer of chloroplast DNA into nuclear genome is a common process in plants
Identification of nuclear integrants of plastid DNAs (NUPTs) in the nuclear genome of A. officinalis We analyzed the chloroplast DNA sequences integrated in the nuclear genome of A. officinalis
72.8% of the NUPTs had a size of 33–199 bp, where 1120 small NUPTs are shorter than 100 bp and 1176 NUPTs had a size ranging from 100 to 199 bp

Summary

Introduction

The transfer of chloroplast DNA into nuclear genome is a common process in plants. These transfers form nuclear integrants of plastid DNAs (NUPTs), which are thought to be driving forces in genome evolution, including sex chromosome evolution. In addition to nuclear genomes, two organellar genomes, namely, mitochondrial and plastid genomes, are found in plant cells These three genomes coexist within each individual cell, where DNA is horizontally transferred between these cell parts, especially from the organelles to the nucleus [1, 2]. The extensive sequence transfer of organellar DNA into the nucleus produces nuclear integrants of plastid DNA (NUPTs) or nuclear integrants of mitochondrial DNAs (NUMTs). NUMTs have been extensively studied [9, 10], but NUPTs are still under research even though they have been explored in a number of plants [11]

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