A Panicum‐derived chromosomal segment captured by Hordeum a few million years ago preserves a set of stress‐related genes

Abstract

Intra-specific variability is a cornerstone of evolutionary success of species. Acquiring genetic material from distant sources is an important adaptive mechanism in bacteria, but it can also play a role in eukaryotes. In this paper, we investigate the nature and evolution of a chromosomal segment of panicoid (Poaceae, Panicoideae) origin occurring in the nuclear genomes of species of the barley genus Hordeum (Pooideae). The segment, spanning over 440 kb in the Asian Hordeum bogdanii and 219 kb in the South American Hordeum pubiflorum, resides on a pair of nucleolar organizer region (NOR)-bearing chromosomes. Conserved synteny and microcollinearity of the segment in both species indicate a common origin of the segment, which was acquired before the split of the respective barley lineages 5-1.7 million years ago. A major part of the foreign DNA consists of several approximately 68 kb long repeated blocks containing five stress-related protein-coding genes and transposable elements (TEs). Whereas outside these repeats, the locus was invaded by multiple TEs from the host genome, the repeated blocks are rather intact and appear to be preserved. The protein-coding genes remained partly functional, as indicated by conserved reading frames, a low amount of non-synonymous mutations, and expression of mRNA. A screen across Hordeum species targeting the panicoid protein-coding genes revealed the presence of the genes in all species of the section Stenostachys. In summary, our study shows that grass genomes can contain large genomic segments obtained from distantly related species. These segments usually remain undetected, but they may play an important role in the evolution and adaptation of species.

Horizontally Acquired nrDNAs Persist in Low Amounts in Host Hordeum Genomes and Evolve Independently of Native nrDNA

“…For these, several scenarios have been described, including maintenance of the different ribotypes within their original loci, formation of new recombinant ribotypes or gradual replacement of one ribotype by another due to interlocus recombination (reviewed in Álvarez and Wendel, 2003). We found only a small proportion of nrDNA is of foreign origin, supporting their presence solely in minor arrays, co-localised with other genetic material of foreign origin as expected under the HGT scenario (Mahelka et al, 2017(Mahelka et al, , 2021. Due to their localisation, out of reach of homogenisation mechanisms, such minor arrays may remain conserved in plant genomes in relatively stable amounts over millions of years (Mahelka et al, 2021).…”

“…We hypothesise that a minor proportion of foreign ribotypes in the total nrDNA, coupled with independent evolution of foreign and native ribotypes, suggest the persistence of foreign nrDNAs within minor nrDNA loci aside from the main and active nrDNA loci (NORs). Together with other lines of evidence, such as non-functionality of the foreign nrDNAs and their confirmed occurrences in chromosomal parts located outside the NORs (Mahelka et al, 2017(Mahelka et al, , 2021, the above scenario would constitute additional support for the status of foreign nrDNAs in Hordeum as dead-end by-products of HGT events.…”

“…The copy number of Panicum-like ribotypes as inferred from qPCR shows higher values (21 copies in H. bogdanii BCC2023 and 29 copies in H. pubiflorum BCC2028). This higher count can be explained by the presence of additional copies beyond the boundaries of the Panicum-derived segment, which would not have been detected by Mahelka et al (2021). Furthermore, we still cannot rule out the possibility that some of the foreign ribotypes reside within the native nrDNA loci.…”

“…The CNV of individual foreign ribotypes provides valuable information, as it may indicate potential functionality and thus evolutionary potential in Hordeum genomes through their quantity and inferred chromosomal localisation. In another study, Mahelka et al (2021) provide detailed characterisation of the Panicum-derived chromosomal segment in Hordeum species. The authors reconstructed the foreign DNA segment using sequencing of BAC clones in H. bogdanii (specimen BCC2063) and H. pubiflorum (BCC2028).…”

“…Based on substitution patterns within the ITS region and the absence of mRNA expression, the authors considered the foreign ribotypes as pseudogenes (Mahelka et al, 2017). In a follow-up study, Mahelka et al (2021) focused specifically on the transfer from a Panicum-like donor into Hordeum that is likely the oldest of the nine transfers between panicoid grasses and Hordeum. It predated the diversification of sect.…”