Beyond conservation: the landscape of chloroplast genome rearrangements in angiosperms

Abstract

Chloroplast genomes (plastomes) have long been considered structurally conserved, but recent sequencing efforts have uncovered pervasive rearrangements that challenge this assumption. This review catalogues the main types of plastome modifications: large and small inversions; insertions and deletions (indels); gene and intron losses; horizontal gene transfers; shifts in inverted repeat boundaries; and gene duplications. It then explains the molecular processes that generate these changes, from repeat-mediated recombination and slipped-strand mispairing to rare foreign-DNA integration events. These structural variants serve as informative phylogenetic markers, enabling resolution of both ancient divergences and recent radiations within angiosperms. Beyond their value for systematics, plastome rearrangements can reshape gene order and copy number, with measurable effects on gene expression, metabolic pathways, and photosynthetic efficiency. Evidence shows that, in certain lineages, plastid genes have been transferred to the nucleus to compensate for gene loss and preserve essential cellular functions. Looking ahead, three emerging approaches promise to deepen our understanding of plastome dynamics: comprehensive pan-plastome surveys coupled with long-read sequencing of under-sampled lineages; targeted plastid transformation to engineer specific rearrangements; and advanced genome editing to test their adaptive significance. Together, these strategies will illuminate how plastid structural change impacts plant evolution and adaptation.

Keywords: IR boundary shifts; angiosperms; chloroplast genome; gene loss; inversions; plant adaptation; plastome rearrangements; structural variants.

Fig. 1

Overview of chloroplast genome structure and comparative synteny among angiosperms. (a) A circular map of the Nicotiana tabacum chloroplast genome (GenBank accession NC_001879) illustrates the canonical quadripartite structure found in most angiosperm plastomes, comprising a large single copy (LSC) region, a small single copy (SSC) region, and two inverted repeats (IRs). Genes are color‐coded by functional category and their orientations are indicated. (b) Comparative synteny between N. tabacum (NC_001879) and four other angiosperms: Arabidopsis thaliana (NC_000932), Cicer arietinum (NC_011163), Passiflora edulis (NC_034285), and Pelargonium transvaalense (NC_031206). Notably, C. arietinum serves as the representative of the IR‐lacking clade (IRLC), exemplifying the loss of the typical inverted‐repeat structure. Structural rearrangements, such as inversions, are indicated by dashed connecting blocks, and the inverted‐repeat region is shaded in blue. Figure was partially created in BioRender (https://biorender.com/sghsas8).

Fig. 2

Schematic overview of chloroplast genome rearrangement types. This schema illustrates a representative chloroplast genome in its reference state (Ref) and summarizes key structural modifications. Deletions are represented as missing segments relative to the reference, while duplications appear as repeated sequence blocks. Gene loss is indicated by the absence of specific genes that are normally present in the reference genome. Horizontal gene transfer events are shown by arrows indicating the movement of sequences from the mitochondrial genome to the plastome. Inversions are depicted as segments that have been excised and reinserted in reverse orientation, thereby altering gene order. Insertions are illustrated as additional sequence blocks that disrupt the typical organization. Finally, inverted repeat (IR) boundary shifts are indicated by arrows outside the boxes, reflecting the sequence expansion at the IR large single‐copy (LSC)/small single‐copy (SSC) junctions. The figure was created in BioRender (https://biorender.com/hh2dsow) and is inspired by the conceptual schema from Alkan et al. (2011).