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

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Title: Distinctive evolutionary pattern of organelle genomes linked to the nuclear genome in Selaginellaceae.
Authors: Kang, Jong‐Soo1,2 (AUTHOR), Zhang, Hong‐Rui1 (AUTHOR), Wang, Ya‐Rong1 (AUTHOR), Liang, Si‐Qi1,2 (AUTHOR), Mao, Zhi‐Yuan2,3 (AUTHOR), Zhang, Xian‐Chun1 (AUTHOR), Xiang, Qiao‐Ping1 (AUTHOR) qpxiang@ibcas.ac.cn
Source: Plant Journal. Dec2020, Vol. 104 Issue 6, p1657-1672. 16p.
Subjects: Genomes, DNA replication, Genomics, Convergent evolution, Mitochondria, Organelles
Abstract: Summary: 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 dual‐targeted 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. Significance Statement: Plastid and mitochondrial genomes usually exhibit contrasting patterns of conserved plastid genomes and diverged mitochondrial genomes. Here, we document that both the organelle genomes in Selaginellaceae exhibit parallel genetic features. In addition, we explore which factor is likely responsible for the unconventional features of plastid genomes, and convergent evolution of the two organelle genomes. This study helps explain the distinctive evolutionary patterns of organelle genomes in Selaginellaceae, and advance our current understanding of organelle genomics. [ABSTRACT FROM AUTHOR]
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Abstract:Summary: 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 dual‐targeted 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. Significance Statement: Plastid and mitochondrial genomes usually exhibit contrasting patterns of conserved plastid genomes and diverged mitochondrial genomes. Here, we document that both the organelle genomes in Selaginellaceae exhibit parallel genetic features. In addition, we explore which factor is likely responsible for the unconventional features of plastid genomes, and convergent evolution of the two organelle genomes. This study helps explain the distinctive evolutionary patterns of organelle genomes in Selaginellaceae, and advance our current understanding of organelle genomics. [ABSTRACT FROM AUTHOR]
ISSN:09607412
DOI:10.1111/tpj.15028