bims-plasge 2025-04-13 papers

Issue of 2025–04–13
four papers selected by
Vera S. Bogdanova, ИЦиГ СО РАН

BMC Genomics. 2025 Apr 04. 26(1): 340

Substantial structural variation and repetitive DNA content contribute to intraspecific plastid genome evolution.

Alfredo López-Caamal, Tyler Gandee, Laura F Galloway, Karen B Barnard-Kubow.

BACKGROUND: Plastids have highly conserved genomes in most land plants. However, in several families, plastid genomes exhibit high rates of nucleotide substitution and structural rearrangements among species. This elevated rate of evolution has been posited to lead to increased rates of plastid-nuclear incompatibilities (PNI), potentially acting as a driver of speciation. However, the extent to which plastid structural variation exists within a species is unknown. This study investigates whether plastid structural variation, observed at the interspecific level in Campanulaceae, also occurs within Campanula americana, a species with strong intraspecific PNI. We assembled multiple plastid genomes from three lineages of C. americana that exhibit varying levels of PNI when crossed. We then investigated the structural variation and repetitive DNA content among these lineages and compared the repetitive DNA content with that of other species within the family.
RESULTS: We found significant variation in plastid genome size among the lineages of C. americana (188,309-201,788 bp). This variation was due in part to multiple gene duplications in the inverted repeat region. Lineages also varied in their repetitive DNA content, with the Appalachian lineage displaying the highest proportion of tandem repeats (~ 10%) compared to the Eastern and Western lineages (~ 6%). In addition, genes involved in transcription and protein transport showed elevated sequence divergence between lineages, and a strong correlation was observed between genome size and repetitive DNA content. Campanula americana was found to have one of the most repetitive plastid genomes within Campanulaceae.
CONCLUSIONS: These findings challenge the conventional view of plastid genome conservation within a species and suggest that structural variation, differences in repetitive DNA content, and divergence of key genes involved in transcription and protein transport may play a role in PNI. This study highlights the need for further research into the genetic mechanisms underlying PNI, a key process in the early stages of speciation.

Keywords: Campanulaceae; Chloroplast genome evolution; Comparative genomics; Cyto-nuclear incompatibility; Plastid-nuclear incompatibility; Repetitive DNA

DOI: https://doi.org/10.1186/s12864-025-11525-w

Mol Biol Evol. 2025 Apr 07. pii: msaf082. [Epub ahead of print]

Unequally Abundant Chromosomes and Unusual Collections of Transferred Sequences Characterize Mitochondrial Genomes of Gastrodia (Orchidaceae), One of the Largest Mycoheterotrophic Plant Genera.

Hanchen Wang, Deyi Wang, Bingyi Shao, Jingrui Li, Zhanghai Li, Mark W Chase, Jianwu Li, Yanlei Feng, Yingying Wen, Shiyu Qin, Binghua Chen, Zhiqiang Wu, Xiaohua Jin.

The mystery of genomic alternations in heterotrophic plants is among the most intriguing in evolutionary biology. Compared to plastid genomes (plastomes) with parallel size reduction and gene loss, mitochondrial genome (mitogenome) variation in heterotrophic plants remains underexplored in many aspects. To further unravel evolutionary outcomes of heterotrophy, we present a comparative mitogenomic study with 13 de novo assemblies of Gastrodia (Orchidaceae), one of the largest fully mycoheterotrophic plant genera, and its relatives. Analyzed Gastrodia mitogenomes range from 0.56 to 2.1 Mb, each consisting of numerous, unequally abundant chromosomes. Size variation might have evolved through chromosome rearrangements followed by stochastic loss of "dispensable" chromosomes, with deletion-biased mutations. The discovery of a hyper-abundant (∼15 times intragenomic average) chromosome in two assemblies represents the hitherto most extreme copy number variation in any mitogenomes, with similar architectures discovered in two metazoan lineages. Transferred sequence contents highlight asymmetric evolutionary consequences of heterotrophy: despite drastically reduced intracellular plastome transfers convergent across heterotrophic plants, their rarity of horizontally acquired sequences sharply contrasts parasitic plants, where massive transfers from their hosts prevail. Rates of sequence evolution are markedly elevated but not explained by copy number variation, extending prior findings of accelerated molecular evolution from parasitic to heterotrophic plants. Putative evolutionary scenarios for these mitogenomic convergence and divergence fit well with the common (e.g., plastome contraction) and specific (e.g., host identity) aspects of the two heterotrophic types. These idiosyncratic mycoheterotrophs expand known architectural variability of plant mitogenomes and provide mechanistic insights into their content and size variation.

Keywords: convergent evolution; horizontal gene transfer; mutation rate; organelle genome; plant-microbe interaction

DOI: https://doi.org/10.1093/molbev/msaf082

Sci Rep. 2025 Apr 11. 15(1): 12498

Differences in homologous and heterologous nucleocytoplasmic interactions of cytoplasmic male sterility lines in Gossypium barbadense.

Jingyi You, Min Li, Xiangjun Kong, Qingguang Hou, Hongwei Li, Bin Li, Qiong Zhou, Ruiyang Zhou.

The utilization of crop hybrids plays an important role in crop breeding and production, and the innovation of the male sterile germplasm is the basis for this utilization. Cotton has a very clear hybrid advantage, and the hybrid advantage in yield and quality has been widely utilized in cotton breeding. However, the exploitation of heterosis in cotton is currently dominated by cytoplasmic male sterility (CMS) lines. These CMS lines are found only in Harknessi cotton. They have a single cytoplasmic origin. Additionally, they exhibit a significant negative effect of cytoplasmic-nuclear interactions. To minimize this effect, it is necessary to select and breed CMS lines. In these CMS lines, both the cytoplasm and nucleus should originate from the same variety. However, no homologous cytoplasmic-nuclear CMS germplasm has been created, and its mechanism of occurrence has not been determined. In this study, two homologous cytoplasmic-nuclear CMS lines and two heterologous cytoplasmic-nuclear CMS lines were utilized, and the heterologous cytoplasmic-nuclear CMS lines were aborted at a relatively early stage. The physiological indexes related to reactive oxygen species ROS-mediated metabolic processes in the heterologous cytoplasmic-nuclear CMS lines were lower than those of the homologous cytoplasmic-nuclear CMS lines, including the enzyme activities of POD and CAT from tetrad to mature pollen grain, and the metabolite content of malondialdehyde (MDA) was inversely correlated with the enzyme activities of the heterologous cytoplasmic-nuclear CMS lines. Resequencing analysis of four cotton mitochondrial genomes (mt genomes) revealed that the heterologous cytoplasmic-nuclear CMS lines were more complex than the homologous cytoplasmic-nuclear CMS lines, and the homologous CMS lines showed a higher degree of collinearity with the maintainer lines. This indicates that heterologous cytoplasmic-nuclear interactions are more likely to lead to mtDNA structural variation. Taken together, the results showed that the cytoplasmic-nuclear homologous system was less affected by the cytoplasmic-nuclear interaction and was the best combination for the study of male sterility.

Keywords: CMS line with heterologous cytoplasm and its nucleus; CMS line with homologous cytoplasm and its nucleus; Cotton; Mitochondrial genome; Mitochondrial genome structural variation; Reactive oxygen species

DOI: https://doi.org/10.1038/s41598-025-95027-5

Nucleic Acids Res. 2025 Apr 10. pii: gkaf279. [Epub ahead of print]53(7):

De novo RNA base editing in plant organelles with engineered synthetic P-type PPR editing factors.

Sébastien Mathieu, Elena Lesch, Shahinez Garcia, Stéfanie Graindorge, Mareike Schallenberg-Rüdinger, Kamel Hammani.

In plant mitochondria and chloroplasts, cytidine-to-uridine RNA editing is necessary for the production of functional proteins. While natural PLS-type PPR proteins are specialized in this process, synthetic PPR proteins offer significant potential for targeted RNA editing. In this study, we engineered chimeric editing factors by fusing synthetic P-type PPR guides with the DYW cytidine deaminase domain of a moss mitochondrial editing factor, PPR56. These designer PPR editors (dPPRe) elicited efficient and precise de novo RNA editing in Escherichia coli as well as in the chloroplasts and mitochondria of Nicotiana benthamiana. Chloroplast transcriptome-wide analysis of the most efficient dPPRe revealed minimal off-target effects, with only three nontarget C sites edited due to sequence similarity with the intended target. This study introduces a novel and precise method for RNA base editing in plant organelles, paving the way for new approaches in gene regulation applicable to plants and potentially other organisms.

DOI: https://doi.org/10.1093/nar/gkaf279