The Somatic Inheritance of Plant Organelles

Heinhorst, Sabine; Chi-Ham, Cecilia L.; Adamson, Steven W.; Cannon, Gordon C.

doi:10.1007/978-1-4020-3166-3_3

Cited by 4 publications

(3 citation statements)

References 313 publications

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“…Interestingly, RecA1 could not be found in any whole-genome or RNA-seq data of different spikemoss species, suggesting the loss/fractionation of RecA1 in Selaginellaceae. The RecA family plays a key role in the accurate pairing of homologous sequences and mediates the strand-exchange reaction in all kinds of homologous recombinations (Cox et al, 2000;Heinhorst et al, 2004;Rowan et al, 2010). Increasing homologous recombination activities in organelle genomes with disruption of the RecA homologs have been reported (Shedge et al, 2007;Terasawa et al, 2007;Odahara et al, 2009).…”

Section: Subgenomic and Master Genomic Conformations Of The Multipartmentioning

confidence: 99%

Distinctive evolutionary pattern of organelle genomes linked to the nuclear genome in Selaginellaceae

et al. 2020

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Plastids and mitochondria are endosymbiotic organelles that store genetic information. The genomes of these organelles generally exhibit contrasting patterns regarding genome architecture and genetic content. However, they have similar genetic features in Selaginellaceae, and little is known about what causes parallel evolution. Here, we document the multipartite plastid genomes (plastomes) and the highly divergent mitochondrial genomes (mitogenomes) from spikemoss obtained by combining short-and long-reads. The 188-kb multipartite plastome has three ribosomal operon copies in the master genomic conformation, creating the alternative subgenomic conformation composed of 110-and 78-kb subgenomes. The long-read data indicated that the two different genomic conformations were present in almost equal proportions in the plastomes of Selaginella nipponica. The mitogenome of S. nipponica was assembled into 27 contigs with a total size of 110 kb. All contigs contained directly arranged repeats at both ends, which introduced multiple conformations. Our results showed that plastomes and mitogenomes share high tRNA losses, GC-biased nucleotides, elevated substitution rates and complicated organization. The exploration of nuclear-encoded organelle DNA replication, recombination and repair proteins indicated that, several single-targeted proteins, particularly plastid-targeted recombinase A1, have been lost in Selaginellaceae; conversely, the dualtargeted proteins remain intact. According to the reported function of recombinase A1, we propose that the plastomes of spikemoss often fail to pair homologous sequences during recombination, and the dual-targeted proteins play a key role in the convergent genetic features of plastomes and mitogenomes. Our results provide a distinctive evolutionary pattern of the organelle genomes in Selaginellaceae and evidence of their convergent evolution.

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Section: Subgenomic and Master Genomic Conformations Of The Multipartmentioning

confidence: 99%

Distinctive evolutionary pattern of organelle genomes linked to the nuclear genome in Selaginellaceae

et al. 2020

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“…There is little further change in chloroplast size or pigmentation during the extended period of photosynthetic activity in the fully expanded leaf. The number of copies of the plastid genome per plastid increases during the transition from proplastid to chloroplast early in leaf development (Kuroiwa 1991;Heinhorst and Cannon 1993;Heinhorst et al 2004), as might be expected to meet the increasing demand for photosynthesis, but the fate of the chloroplast DNA (cpDNA) in mature leaves is surprisingly variable among plant species. In early investigations, the level of DNA per plastid appeared to decrease by dilution, as chloroplasts continued to divide after cpDNA replication had ceased, and the level of cpDNA per cell in seedlings remained rather constant (Lamppa et al 1980;Scott and Possingham 1980).…”

Section: Introductionmentioning

confidence: 99%

Loss or retention of chloroplast DNA in maize seedlings is affected by both light and genotype

Oldenburg

Rowan

Жао

et al. 2006

Planta

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We examined the chloroplast DNA (cpDNA) from plastids obtained from wild type maize (Zea mays L.) seedlings grown under different light conditions and from photosynthetic mutants grown under white light. The cpDNA was evaluated by real-time quantitative PCR, quantitative DNA fluorescence, and blot-hybridization following pulsed-field gel electrophoresis. The amount of DNA per plastid in light-grown seedlings declines greatly from stalk to leaf blade during proplastid-to-chloroplast development, and this decline is due to cpDNA degradation. In contrast, during proplastid-to-etioplast development in the dark, the cpDNA levels increase from the stalk to the blade. Our results suggest that DNA replication continues in the etioplasts of the upper regions of the stalk and in the leaves. The cpDNA level decreases rapidly, however, after dark-grown seedlings are transferred to light and the etioplasts develop into photosynthetically active chloroplasts. Light, therefore, triggers the degradation of DNA in maize chloroplasts. The cpDNA is retained in the leaf blade of seedlings grown under red, but not blue light. We suggest that light signaling pathways are involved in mediating cpDNA levels, and that red light promotes replication and inhibits degradation and blue light promotes degradation. For five of nine photosynthetic mutants, cpDNA levels in expanded leaves are higher than in wild type, indicating that nuclear genotype can affect the loss or retention of cpDNA.

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“…For example, the plastid-targeted RecA1 and mitochondrion-targeted RecA3 are absent, and only dual-targeted RecA2 exists in the Selaginellaceae. The function of the RecA gene family was reported to play a key part in the accurate pairing of various types of homologous recombination, via suppressing the illegitimate recombination between short repeats (Cox et al, 2000;Heinhorst et al, 2004;Odahara et al, 2009Odahara et al, , 2015Rowan et al, 2010). The dual-targeted RecA2 in the Selaginellaceae was proposed to be responsible for the convergent evolution of the two compartments (Kang et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

The evolution of extremely diverged plastomes in Selaginellaceae (lycophyte) is driven by repeat patterns and the underlying DNA maintenance machinery

Xiang

Tang

et al. 2022

The Plant Journal

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Two factors are proposed to account for the unusual features of organellar genomes: the disruptions of organelle-targeted DNA replication, repair, and recombination (DNA-RRR) systems in the nuclear genome and repetitive elements in organellar genomes. Little is known about how these factors affect organellar genome evolution. The deep-branching vascular plant family Selaginellaceae is known to have a deficient DNA-RRR system and convergently evolved organellar genomes. However, we found that the plastid genome (plastome) of Selaginella sinensis has extremely accelerated substitution rates, a low GC content, pervasive repeat elements, a dynamic network structure, and it lacks direct or inverted repeats. Unexpectedly, its organelle DNA-RRR system is short of a plastid-targeted Recombinase A1 (RecA1) and a mitochondriontargeted RecA3, in line with other explored Selaginella species. The plastome contains a large collection of short-and medium-sized repeats. Given the absence of RecA1 surveillance, we propose that these repeats trigger illegitimate recombination, accelerated mutation rates, and structural instability. The correlations between repeat quantity and architectural complexity in the Selaginella plastomes support these conclusions. We, therefore, hypothesize that the interplay of the deficient DNA-RRR system and the high repeat content has led to the extraordinary divergence of the S. sinensis plastome. Our study not only sheds new light on the mechanism of plastome divergence by emphasizing the power of cytonuclear integration, but it also reconciles the longstanding contradiction on the effects of DNA-RRR system disruption on genome structure evolution.

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The Somatic Inheritance of Plant Organelles

Cited by 4 publications

References 313 publications

Distinctive evolutionary pattern of organelle genomes linked to the nuclear genome in Selaginellaceae

Distinctive evolutionary pattern of organelle genomes linked to the nuclear genome in Selaginellaceae

Loss or retention of chloroplast DNA in maize seedlings is affected by both light and genotype

The evolution of extremely diverged plastomes in Selaginellaceae (lycophyte) is driven by repeat patterns and the underlying DNA maintenance machinery

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