Characterization and Dynamics of Intracellular Gene Transfer in Plastid Genomes of Viola (Violaceae) and Order Malpighiales
Functional gene transfer from organelles to the nucleus, known as intracellular gene transfer (IGT), is an ongoing process in flowering plants. The complete plastid genomes (plastomes) of two Ulleung island endemic violets, Viola ulleungdoensis and V. woosanensis, were characterized, revealing a lac...
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Frontiers Media S.A.
2021-08-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2021.678580/full |
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| author | JiYoung Yang Seongjun Park Hee-Young Gil Jae-Hong Pak Jae-Hong Pak Jae-Hong Pak Seung-Chul Kim |
| author_facet | JiYoung Yang Seongjun Park Hee-Young Gil Jae-Hong Pak Jae-Hong Pak Jae-Hong Pak Seung-Chul Kim |
| author_sort | JiYoung Yang |
| collection | DOAJ |
| description | Functional gene transfer from organelles to the nucleus, known as intracellular gene transfer (IGT), is an ongoing process in flowering plants. The complete plastid genomes (plastomes) of two Ulleung island endemic violets, Viola ulleungdoensis and V. woosanensis, were characterized, revealing a lack of the plastid-encoded infA, rpl32, and rps16 genes. In addition, functional replacement of the three plastid-encoded genes in the nucleus was confirmed within the genus Viola and the order Malpighiales. Three strategies for the acquisition of a novel transit peptide for successful IGT were identified in the genus Viola. Nuclear INFA acquired a novel transit peptide with very low identity between these proteins, whereas the nuclear RPL32 gene acquired an existing transit peptide via fusion with the nuclear-encoded plastid-targeted SOD gene (Cu-Zn superoxide dismutase superfamily) as one exon, and translated both proteins in the cytosol using alternative mRNA splicing. Nuclear RPS16 contains an internal transit peptide without an N-terminal extension. Gene loss or pseudogenization of the plastid-borne rpl32 and rps16 loci was inferred to occur in the common ancestor of the genus Viola based on an infrageneric phylogenetic framework in Korea. Although infA was lost in the common ancestor of the order Malpighiales, the rpl32 and rps16 genes were lost multiple times independently within the order. Our current study sheds additional light on plastid genome composition and IGT mechanisms in the violet genus and in the order Malpighiales. |
| first_indexed | 2024-12-22T10:38:55Z |
| format | Article |
| id | doaj.art-5648fd677c7b4795887a56bb417f0454 |
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| issn | 1664-462X |
| language | English |
| last_indexed | 2024-12-22T10:38:55Z |
| publishDate | 2021-08-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-5648fd677c7b4795887a56bb417f04542022-12-21T18:29:05ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-08-011210.3389/fpls.2021.678580678580Characterization and Dynamics of Intracellular Gene Transfer in Plastid Genomes of Viola (Violaceae) and Order MalpighialesJiYoung Yang0Seongjun Park1Hee-Young Gil2Jae-Hong Pak3Jae-Hong Pak4Jae-Hong Pak5Seung-Chul Kim6Research Institute for Dok-do and Ulleung-do Island, Kyungpook National University, Daegu, South KoreaInstitute of Natural Science, Yeungnam University, Gyeongsan, South KoreaDMZ Botanic Garden, Korea National Arboretum, Yanggu, South KoreaResearch Institute for Dok-do and Ulleung-do Island, Kyungpook National University, Daegu, South KoreaDepartment of Biology, School of Life Science, BK21 FOUR KNU Creative BioResearch Group, Kyungpook National University, Daegu, South KoreaDepartment of Integrative Natural Sciences for the East Sea Rim, Kyungpook National University, Daegu, South KoreaDepartment of Biological Sciences, Sungkyunkwan University, Suwon, South KoreaFunctional gene transfer from organelles to the nucleus, known as intracellular gene transfer (IGT), is an ongoing process in flowering plants. The complete plastid genomes (plastomes) of two Ulleung island endemic violets, Viola ulleungdoensis and V. woosanensis, were characterized, revealing a lack of the plastid-encoded infA, rpl32, and rps16 genes. In addition, functional replacement of the three plastid-encoded genes in the nucleus was confirmed within the genus Viola and the order Malpighiales. Three strategies for the acquisition of a novel transit peptide for successful IGT were identified in the genus Viola. Nuclear INFA acquired a novel transit peptide with very low identity between these proteins, whereas the nuclear RPL32 gene acquired an existing transit peptide via fusion with the nuclear-encoded plastid-targeted SOD gene (Cu-Zn superoxide dismutase superfamily) as one exon, and translated both proteins in the cytosol using alternative mRNA splicing. Nuclear RPS16 contains an internal transit peptide without an N-terminal extension. Gene loss or pseudogenization of the plastid-borne rpl32 and rps16 loci was inferred to occur in the common ancestor of the genus Viola based on an infrageneric phylogenetic framework in Korea. Although infA was lost in the common ancestor of the order Malpighiales, the rpl32 and rps16 genes were lost multiple times independently within the order. Our current study sheds additional light on plastid genome composition and IGT mechanisms in the violet genus and in the order Malpighiales.https://www.frontiersin.org/articles/10.3389/fpls.2021.678580/fullintracellular gene transferViolainfArpl32rps16Malpighiales |
| spellingShingle | JiYoung Yang Seongjun Park Hee-Young Gil Jae-Hong Pak Jae-Hong Pak Jae-Hong Pak Seung-Chul Kim Characterization and Dynamics of Intracellular Gene Transfer in Plastid Genomes of Viola (Violaceae) and Order Malpighiales Frontiers in Plant Science intracellular gene transfer Viola infA rpl32 rps16 Malpighiales |
| title | Characterization and Dynamics of Intracellular Gene Transfer in Plastid Genomes of Viola (Violaceae) and Order Malpighiales |
| title_full | Characterization and Dynamics of Intracellular Gene Transfer in Plastid Genomes of Viola (Violaceae) and Order Malpighiales |
| title_fullStr | Characterization and Dynamics of Intracellular Gene Transfer in Plastid Genomes of Viola (Violaceae) and Order Malpighiales |
| title_full_unstemmed | Characterization and Dynamics of Intracellular Gene Transfer in Plastid Genomes of Viola (Violaceae) and Order Malpighiales |
| title_short | Characterization and Dynamics of Intracellular Gene Transfer in Plastid Genomes of Viola (Violaceae) and Order Malpighiales |
| title_sort | characterization and dynamics of intracellular gene transfer in plastid genomes of viola violaceae and order malpighiales |
| topic | intracellular gene transfer Viola infA rpl32 rps16 Malpighiales |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2021.678580/full |
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