The Increase of Simple Sequence Repeats during Diversification of Marchantiidae, An Early Land Plant Lineage, Leads to the First Known Expansion of Inverted Repeats in the Evolutionarily-Stable Structure of Liverwort Plastomes

Abstract

The chloroplast genomes of liverworts, an early land plant lineage, exhibit stable structure and gene content, however the known resources are very limited. The newly sequenced plastomes of Conocephalum, Riccia and Sphaerocarpos species revealed an increase of simple sequence repeats during the diversification of complex thalloid liverwort lineage. The presence of long TA motifs forced applying the long-read nanopore sequencing method for proper and dependable plastome assembly, since the length of dinucleotide repeats overcome the length of Illumina short reads. The accumulation of SSRs (simple sequence repeats) enabled the expansion of inverted repeats by the incorporation of rps12 and rps7 genes, which were part of large single copy (LSC) regions in the previously sequenced plastomes. The expansion of inverted repeat (IR) at the genus level is reported for the first time for non-flowering plants. Moreover, comparative analyses with remaining liverwort lineages revealed that the presence of SSR in plastomes is specific for simple thalloid species. Phylogenomic analysis resulted in trees confirming monophyly of Marchantiidae and partially congruent with previous studies, due to dataset-dependent results of Dumortiera-Reboulia relationships. Despite the lower evolutionary rate of Marchantiales plastomes, significant barcoding gap was detected, even for recently divergent holarctic Conocephalum species. The sliding window analyses revealed the presence of 18 optimal (500 bp long) barcodes that enable the molecular identification of all studied species.

Sequencing of Organellar Genomes of Nowellia curvifolia (Cephaloziaceae Jungermanniales) Revealed the Smallest Plastome with Complete Gene Set and High Intraspecific Variation Suggesting Cryptic Speciation

“…The number of SNPs between closely related Calypogeia species (C. muelleriana and C. integristipula) detected for the whole genome was one third of the amount detected for CDS for Nowellia specimens, and the intraspecific differentiation was limited to few SNPs, however all the samples had European origin [5]. Lower genetic differentiation was also detected at interand intraspecific level of complex thalloid liverwort genera Marchantia and Conocephalum [9], but this lineage is known from low genetic differentiation and slow evolutionary rate of organellar genomes [35]. The level of CDS polymorphism found among remaining Asian specimens is similar to those found among cryptic lineages of A. pinguis complex [18,36,37].…”

“…The smallest plastome (108,007 bp) was found in mycoheterotrophic Aneura mirabilis [8], while the largest one (128,728 bp) in the early divergent Haplomitrium blumei [4]. The plastome of the latter species also shows the highest GC-content, with 44.4%, whereas the lowest GC-content (28.2%) was found in the plastid genome of the complex thalloid Conocephalum salebrosum [9].…”

“…The structural changes of plastomes are mainly limited to small rearrangements at borders of inverted repeats and single copy regions, which lead to IR expansion [4,7] or losing of six genes by a pseudogenization in mycoheterotrophic species [6]. The gene content of plastome units is conserved in almost all known liverworts, with exception of Conocephalum conicum where two genes, rps7 and rps12 were transferred from LSC to IR [9].…”

“…The well-developed morphological features are one of the reason of overlooked cryptic diversity, which often lead to description of new species [15][16][17]. Despite recent publication of several papers dealing with liverwort plastomes [4,5,9,10,18], the GenBank entries didn't include any representative of the Cephaloziaceae family.…”

Genome-Wide Characterization and Comparative Analyses of Simple Sequence Repeats among Four Miniature Pig Breeds

“…Simple sequence repeats (SSRs), also known as microsatellites or short tandem repeats (STRs), consist of 2 to 6 base-pair motifs repeated several times in tandem. As a consequence of their wide distribution and high mutation rate in eukaryotic genomes [ 1 ], SSRs have been used in genetic diversity and population structure studies [ 2 , 3 , 4 , 5 ], for discrimination among species or breeds [ 6 , 7 ], in marker-assisted selection [ 8 , 9 , 10 ] and in evolution analysis [ 11 ]. In humans, SSRs were predicted to be bound by protein-coding transcripts, long non-coding RNAs (lncRNAs) and circular RNAs (circRNAs) and affect competing endogenous RNA crosstalk [ 12 ].…”