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Proc Natl Acad Sci U S A. 2019 Mar 19;116(12):5665-5674. doi: 10.1073/pnas.1811661116. Epub 2019 Mar 4.

Chloroplast competition is controlled by lipid biosynthesis in evening primroses.

Author information

1
Department Organelle Biology, Biotechnology and Molecular Ecophysiology, Max Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany.
2
Department Molecular Physiology, Max Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany.
3
Department Metabolic Networks, Max Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany.
4
Department of Ecology & Evolutionary Biology, University of Toronto, ON M5S 3B2, Canada.
5
Department of Molecular Biology, Institute of Biotechnology, John Paul II Catholic University of Lublin, Konstantynów 1I, 20-708, Poland.
6
Center for Plant Science Innovation and Department of Biochemistry, University of Nebraska-Lincoln, Lincoln, NE 68588.
7
Department of Plant Biology, Michigan State University, East Lansing, MI 48824-1312.
8
Department Organelle Biology, Biotechnology and Molecular Ecophysiology, Max Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany; greiner@mpimp-golm.mpg.de.

Abstract

In most eukaryotes, organellar genomes are transmitted preferentially by the mother, but molecular mechanisms and evolutionary forces underlying this fundamental biological principle are far from understood. It is believed that biparental inheritance promotes competition between the cytoplasmic organelles and allows the spread of so-called selfish cytoplasmic elements. Those can be, for example, fast-replicating or aggressive chloroplasts (plastids) that are incompatible with the hybrid nuclear genome and therefore maladaptive. Here we show that the ability of plastids to compete against each other is a metabolic phenotype determined by extremely rapidly evolving genes in the plastid genome of the evening primrose Oenothera Repeats in the regulatory region of accD (the plastid-encoded subunit of the acetyl-CoA carboxylase, which catalyzes the first and rate-limiting step of lipid biosynthesis), as well as in ycf2 (a giant reading frame of still unknown function), are responsible for the differences in competitive behavior of plastid genotypes. Polymorphisms in these genes influence lipid synthesis and most likely profiles of the plastid envelope membrane. These in turn determine plastid division and/or turnover rates and hence competitiveness. This work uncovers cytoplasmic drive loci controlling the outcome of biparental chloroplast transmission. Here, they define the mode of chloroplast inheritance, as plastid competitiveness can result in uniparental inheritance (through elimination of the "weak" plastid) or biparental inheritance (when two similarly "strong" plastids are transmitted).

KEYWORDS:

acetyl-CoA carboxylase; biparental inheritance; correlation mapping; selfish cytoplasmic elements; ycf2

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