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

Abstract

Background 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 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. Results A 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. Conclusions These 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. Electronic supplementary material The online version of this article (10.1186/s12870-019-1975-8) contains supplementary material, which is available to authorized users.

Nuclear Integrants of Organellar DNA Contribute to Genome Structure and Evolution in Plants

“…NUPTs and NUMTs are frequently organized as clusters [21,38,39]. For example, we observed that approximately 45% of the 3155 NUPT insertions were organized in clusters in the genome of Asparagus officinalis [21].…”

“…NUPTs and NUMTs are frequently organized as clusters [21,38,39]. For example, we observed that approximately 45% of the 3155 NUPT insertions were organized in clusters in the genome of Asparagus officinalis [21]. In the model plant species Arabidopsis and rice, NUPTs and NUMTs are frequently nonrandomly arranged as loose clusters or tight clusters based on the physically linked degrees [39].…”

“…The nuclear integrants of organellar DNA were first discovered in a study in which a mitochondrial ATPase subunit gene was found in the nuclear genome, as well as in the mitochondrial genome of Neurospora crassa [25]. Since then, organelle-derived sequences were examined in the nuclear genome of a number of animals [26][27][28][29][30][31][32] and plants [15][16][17][18][19][20][21]. The availability of a large amount of plant organelle and nuclear genome data has made it possible to investigate the prevalence and characteristics of NUMTs and NUPTs in plants.…”

“…The presence of mosaic clusters containing NUPTs and NUMTs indicates that DNA fragments from different organelles might have concatemerized before insertion, or these nuclear regions are hotspots for integration [39,41]. Other organization patterns such as NUPTs/NUMTs with tandem duplications originating from one organelle fragment with the same orientation were occasionally observed [21]. These various organization patterns of NUPTs/NUMTs existing in plant genomes suggested that the origins and Correlation analysis between nuclear genome size and nuclear integrants of plastid DNA (NUPT)/nuclear integrants of mitochondrial DNA (NUMT) content or number in plants: (A) genome size versus cumulative length of NUPTs; (B) genome size versus total number of NUPTs; (C) genome size versus cumulative length of NUMTs; (D) genome size versus total number of NUMTs.…”

“…This makes the large-scale analysis of NUPTs and NUMTs in plants be possible. Currently, NUPTs and NUMTs in some plant genomes have been characterized [15][16][17][18][19][20][21]. The characterization of nuclear organellar DNAs in plants adds new insights into the role of NUPTs and NUMTs in genome structure and evolution.…”