Abstract
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.
Highlights
Fatty acid biosynthesis in plants begins with the conversion of acetyl-CoA into malonyl-CoA, catalyzed by acetyl-CoA carboxylase (ACCase)
Transcripts encoding heteromeric and homomeric ACCases were identified in most gymnosperms
A single copy of homomeric ACCase (ACC) transcripts was present in all examined gymnosperms, Genome Biol
Summary
Fatty acid biosynthesis in plants begins with the conversion of acetyl-CoA into malonyl-CoA, catalyzed by acetyl-CoA carboxylase (ACCase). There are generally two types of ACCases in plants: the multisubunit heteromeric ACCase (ACCA–D) in plastids and the singlepolypeptide homomeric ACCase (ACC) in the cytosol (Sasaki and Nagano 2004). Heteromeric ACCase consists of four subunits: 1) the alpha-subunit of carboxyltransferase (a-CT; encoded by accA), 2) biotin-carboxyl carrier protein (BCCP; encoded by accB), 3) biotin-carboxylase (BC; encoded by accC), and 4) the beta-subunit of carboxyltransferase (b-CT; encoded by accD). Genes encoding the former three reside in the nuclei, whereas accD resides in the plastids of most plant species. Loss of plastid accD has been reported in some seed plants, including monocots: Poaceae (Konishi and Sasaki 1994) and Acorus (Goremykin et al 2005); eudicots: Trifolium (Magee et al 2010), some Silene species (Sloan et al 2012), Campanulaceae (Rousseau-Gueutin et al 2013), and a few species of Pelargonium (Roschenbleck et al 2017);
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