Figure 6. Maximum likelihood tree of Primula species
based on chloroplast genomes. Bootstrap support values over 95% are
labeled with asterisks. Outgroups and P. poissonii complex are
highlighted with gray and purple shadings, respectively.
4. Discussion
4.1. The general characteristics of Primula chloroplast genomes
As with most angiosperms, the chloroplast genomes were conserved inPrimula species, with similar GC content and typical
quadripartite structures, including small and large single copy (SSC and
LSC) regions separated by two inverted repeats (IRs) regions [60].
However, gene loss was found here. The infA gene, which encodes
translation initiation factor 1 [61], was present in the chloroplast
genome of P. poissonii and P. wilsonii , but was not
present in the related Primula chloroplast genomes in our study.
Additionally, these findings are consistent with the results of somePrimula species and other groups in angiosperm chloroplast
genomes in previous studies [62, 63]. Remarkably, the ycf15gene was only missing in the chloroplast genomes of P. wilsonii .ycf15 was located in the IR region and was highly conserved. The
absence of ycf15 was also reported in many other plants, such asColchicum genus [64]. However, the function of theycf15 gene remains unclear and needs to be further investigated.
The patterns of gene loss we revealed here could be used for phylogeny
reconstruction and species identification. The loss of ycf15 gene
in colchicine plants successfully determined the infrageneric
relationship in the expanded Colchicum genus [64]. Thus, the
non-presence of ycf15 we found here might be a valuable molecular
marker to separate P. wilsonii from P. poissonii , which is
morphologically similar to P. wilsonii . Both of the two species
are perennial herbs with candelabra inflorescence and purple flowers, so
some scholars argue P. wilsonii should be merged into P.
poissonii or treated as a subspecies of P. poissonii . Here we
suggested that the missing ycf15 gene in the P. wilsoniichloroplast genome could be extremely useful for distinguishing the two
confusing species at the molecular level.
4.2. The evolution of the chloroplast genomes in Primula
IR regions are highly conserved in most angiosperm chloroplast genomes.
However, the contraction and expansion of IR regions are not rare
[65]. In this study, gene orders at the boundaries of SC/IR regions
were the same among the five chloroplast genomes of Primula .
However, the accurate positions of the genes at the SC/IR border were
slightly varied, such as the genes rps19 , ndhF ,ycf1 , rpl2 and trnH [63]. In addition, some
genes normally located in the SC region, such as ndhF , had moved
to IR region due to the expansion of the IR region. It was reported that
the chloroplast genomes’ size, the LSC/SSC length, the gene numbers and
pseudogene origination could vary among different species due to the
expansion and contraction of IR regions [66, 67]. Moreover, the loss
of IR regions has been occasionally detected in some taxa [68].
Thiscould be the reason that the chloroplast genome size of P.
miyabeana was the largest among the five Primula species with
the longest IR region, and the chloroplast genome size of P.
secundiflora was the smallest with the shortest IR region. Furthermore,
a large number of studies also confirmed that the length of IR region
greatly affected the chloroplast genome size [69, 70].
Species of Primula are famous for their ornamental value and
heterostyly phenomenon in Southwest China. More genomic resources are
needed to deeply investigate the phylogeny, biogeography, genetics and
heterostyly evolution of Primula species. In addition,
considering that P. wilsonii is a plant species with extremely
small populations (PSESP), we need more genetic information for the
conservation of germplasm resources. The numbers and distributions of
repeat sequences, especially large repeats that are longer than 20 bp
and 60 bp, may play important roles in the arrangement and recombination
of the plastid genome [71, 72]. A total of 123 repeats were detected
in the six Primula chloroplast genomes. All the repeat sequences
appeared to be shorter than 60 bp in length. These findings are
consistent with the results in other Primula species [63,
73], but not in agreement with the results of some other angiosperm
plants, such as herbaceous Alpinia species [74] or woodyAquilaria species [70]. Our study detected very high levels
of polymorphism in the large repeat sequences among the sixPrimula species in terms of both the types or numbers. Therefore,
these large repeats might be an informative source for developing
genetic markers for population genetics and phylogenetic constructions
of Primula [75]. SSRs markers are a valuable genetic resource
for phylogenetic investigations, population genetics assessment and
species discrimination due to their abundant polymorphism and codominant
inheritance [70, 76]. The SSRs markers detected here were mostly A/T
mono-nucleotide repeats (28/38), similar to the results of otherPrimula species [63] and some other angiosperm species [77,
78]. The vast majority of SSRs loci were in SC regions (78.95% in LSC
regions and 15.79% in SSC regions), yet few of them were present in IR
regions. Moderate sequence divergence with greater variability in the SC
region of Primula chloroplast genomes was displayed, which
corresponded with previous studies [79]. Since the hyper-variable
regions of the chloroplast genome are useful for phylogenetic
construction, population genetics and DNA barcoding, the 17 highly
polymorphic loci and the SSRs markers found in our study could serve as
potential genetic markers for further phylogenetic and biogeographic
analyses, population genetics and conservation analysis ofPrimula species.
4.3. Phylogenetic relationships of Chinese Primula
A total of 60 species representing 20 of 24 sections in ChinesePrimula were sampled in our phylogenetic construction using
chloroplast genome sequences based on ML method. Three major clades ofPrimula were detected with high internal support in this study,
which was in accordance with previous studies [25, 73, 80]. Several
sections did not exhibit monophyletic taxa, such as Sects.Monocarpicae , Crystallophlomis , Obconicolisteri ,Denticulata and Proliferae , which were partly or entirely
confirmed by the previous viewpoints [25, 73, 80]. A decision on the
monophyly of Sect. Proliferae requires additional consideration.
It has been treated as a monophyletic group based on the concatenation
of ITS, matK and rbcL sequences [25, 73]. However, the
chloroplast transcripts and protein coding sequences from chloroplast
genomes analyses strengthen the assumption that Sects.Amethyatina and Petiolares species are nested within Sect.Proliferae [80]. This assumption is additionally
supported by the results based on the whole chloroplast genome analysis
in our investigation. This is corroborated by morphological traits such
as an umbel with multiple flowers, campanulate calyx, and globose
capsule. On the one hand, the conflicting phylogenetic diagnoses of
nuclear and chloroplast sequences are common in plants [81]. On the
other hand, the adaptive radiation caused by heterostyly,
polyploidization and natural hybridization, or gene introgression might
complicate the phylogenetic relationships under Primula[20-24]. This would explain why quite a few sections inPrimula didn’t belong to monophyletic group according to
morphological characters.
P. wilsonii , together with P. poissonii , P.
anisodora, and P. miyabeana (endemic to Taiwan) form to P.
poissonii complex, which was one of the taxonomically challenging
groups in Sect. Proliferae . The close relationship of these
species has been revealed in studies, and P. wilsonii was closest
to P. miyabeana based on rbcL + matK + ITS
sequences, with low support [25]. However, the closest relative
species was P. anisodora with very high support based on
chloroplast genomic sequences in this study. Therefore, we suggest that
the phylogenetic relationships between Primula species need to be
further studied based on more genetic information, especially at the
genome level, and we may come to the conclusion that chloroplast genomes
sequences could provide a valuable resource for phylogenetic
constructing of Primula .
5. Conclusions
This study compared the basic characteristics of the chloroplast genomes
from several Chinese Primula species. We assessed the variation
and IR boundaries evolution among these species. Furthermore, we
constructed the phylogenetic relationships of the genus Primulacovering a wide range of samples based on their chloroplast genomic
sequences. In addition, we determined the conserved and variable regions
in the chloroplast genomes. The large repeat sequences, SSRs loci, and
17 hypervariable regions were detected here, which could be used for
population genetics and phylogenetic analysis in the future. Three major
clades in Primula were confirmed, yet the sections were not in
accordance with morphological traits, reflecting in the non-monophyletic
nature of several sections. Therefore, we suggest that chloroplast
genomes provide useful genetic and evolutionary information for studies
on the phylogeny, population genetics, and conservation ofPrimula species.
Funding: This research was funded by National Natural Science
Foundation of China (32100169) and Natural Science Foundation of Anhui
Province (2108085QC104), Natural Science Foundation from Educational
Commission of Anhui Province (KJ2020B25) to Y.P. Xie, the Henan Province
Youth Talent Lift Project of China (212102310242) and the Key Scientific
and Technological Project of Henan Province (2021HYTP042) to G.-G. Yang.
Institutional
Review Board Statement: Not applicable.
Data Availability Statement: The data presented in the study
are depositing in the NCBI repository, and the accession numbers are
shown in the article.
Acknowledgments: The authors wish to thank Jian-Li Zhao and Li
Li for help in collecting samples and operation of software; Heng-Yi
Shao and MPDI for their advices on the language organization and English
editing.
Conflicts of Interest: The authors declare no conflict of
interest.
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