TY - JOUR
T1 - Two Independent Plastid accD Transfers to the Nuclear Genome of Gnetum and Other Insights on Acetyl-CoA Carboxylase Evolution in Gymnosperms
AU - Sudianto, Edi
AU - Chaw, Shu Miaw
AU - Renner, Susanne
N1 - Funding Information:
We thank the Plant Tech Core Facility and Advanced Optical Microscope Core Facility of Agricultural Biotechnology Research Center, Academia Sinica, for supplying Arabidopsis plants and assisting with the laser confocal scanning microscope, respectively. We also thank oneKP for making the data publicly available. We are grateful to Dr Chung-Shien Wu and Dr William Martin for their critical reading and comments on our draft. We would like to thank the two anonymous reviewers and Dr Susanne S. Renner for their suggestions and valuable comments, which greatly improve the first version of manuscript. We are indebted to Dr Celicia Koo Botanic Garden for providing fresh leaves of several rare gymnso-perms. This work was supported by research grants from the Ministry of Science and Technology Taiwan (MOST 103- 2621-B-001-007-MY3 to S.-M.C.); Biodiversity Research Center’s PI grant (from 2016 to 2018 to S.-M.C.); Central Academic Advisory Committee of Academia Sinica (to S.-M.C.); and the Taiwan International Graduate Program Student Fellowship (to E.S.).
Publisher Copyright:
© 2019 The Author(s). Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
PY - 2019/6/1
Y1 - 2019/6/1
N2 - Acetyl-CoA carboxylase (ACCase) is the key regulator of fatty acid biosynthesis. In most plants, ACCase exists in two locations (cytosol and plastids) and in two forms (homomeric and heteromeric). Heteromeric ACCase comprises four subunits, three of them (ACCA-C) are nuclear encoded (nr) and the fourth (ACCD) is usually plastid encoded. Homomeric ACCase is encoded by a single nr-gene (ACC). We investigated the ACCase gene evolution in gymnosperms by examining the transcriptomes of newly sequenced Gnetum ula, combined with 75 transcriptomes and 110 plastomes of other gymnosperms. AccD-coding sequences are elongated through the insertion of repetitive DNA in four out of five cupressophyte families (except Sciadopityaceae) and were functionally transferred to the nucleus of gnetophytes and Sciadopitys. We discovered that, among the three genera of gnetophytes, only Gnetum has two copies of nr-accD. Furthermore, using protoplast transient expression assays, we experimentally verified that the nr-accD precursor proteins in Gnetum and Sciadopitys can be delivered to the plastids. Of the two nr-accD copies of Gnetum, one dually targets plastids and mitochondria, whereas the other potentially targets plastoglobuli. The distinct transit peptides, gene architectures, and flanking sequences between the two Gnetum accDs suggest that they have independent origins. Our findings are the first account of two distinctly targeted nr-accDs of any green plants and the most comprehensive analyses of ACCase evolution in gymnosperms to date.
AB - Acetyl-CoA carboxylase (ACCase) is the key regulator of fatty acid biosynthesis. In most plants, ACCase exists in two locations (cytosol and plastids) and in two forms (homomeric and heteromeric). Heteromeric ACCase comprises four subunits, three of them (ACCA-C) are nuclear encoded (nr) and the fourth (ACCD) is usually plastid encoded. Homomeric ACCase is encoded by a single nr-gene (ACC). We investigated the ACCase gene evolution in gymnosperms by examining the transcriptomes of newly sequenced Gnetum ula, combined with 75 transcriptomes and 110 plastomes of other gymnosperms. AccD-coding sequences are elongated through the insertion of repetitive DNA in four out of five cupressophyte families (except Sciadopityaceae) and were functionally transferred to the nucleus of gnetophytes and Sciadopitys. We discovered that, among the three genera of gnetophytes, only Gnetum has two copies of nr-accD. Furthermore, using protoplast transient expression assays, we experimentally verified that the nr-accD precursor proteins in Gnetum and Sciadopitys can be delivered to the plastids. Of the two nr-accD copies of Gnetum, one dually targets plastids and mitochondria, whereas the other potentially targets plastoglobuli. The distinct transit peptides, gene architectures, and flanking sequences between the two Gnetum accDs suggest that they have independent origins. Our findings are the first account of two distinctly targeted nr-accDs of any green plants and the most comprehensive analyses of ACCase evolution in gymnosperms to date.
KW - accD
KW - acetyl-CoA carboxylase (ACCase)
KW - evolution
KW - fatty acid biosynthesis
KW - plastid localization
KW - plastid-to-nucleus gene transfer
UR - http://www.scopus.com/inward/record.url?scp=85068886771&partnerID=8YFLogxK
U2 - 10.1093/gbe/evz059
DO - 10.1093/gbe/evz059
M3 - Article
C2 - 30924880
AN - SCOPUS:85068886771
SN - 1759-6653
VL - 11
SP - 1691
EP - 1705
JO - Genome Biology and Evolution
JF - Genome Biology and Evolution
IS - 6
ER -