Transposon insertions regulate genome-wide allele-specific expression and underpin flower colour variations in apple (Malus spp.)

Plant Biotechnol J. 2022 Jul;20(7):1285-1297. doi: 10.1111/pbi.13806. Epub 2022 Apr 1.

Abstract

Allele-specific expression (ASE) can lead to phenotypic diversity and evolution. However, the mechanisms regulating ASE are not well understood, particularly in woody perennial plants. In this study, we investigated ASE genes in the apple cultivar 'Royal Gala' (RG). A high quality chromosome-level genome was assembled using a homozygous tetra-haploid RG plant, derived from anther cultures. Using RNA-sequencing (RNA-seq) data from RG flower and fruit tissues, we identified 2091 ASE genes. Compared with the haploid genome of 'Golden Delicious' (GD), a parent of RG, we distinguished the genomic sequences between the two alleles of 817 ASE genes, and further identified allele-specific presence of a transposable element (TE) in the upstream region of 354 ASE genes. These included MYB110a that encodes a transcription factor regulating anthocyanin biosynthesis. Interestingly, another ASE gene, MYB10 also showed an allele-specific TE insertion and was identified using genome data of other apple cultivars. The presence of the TE insertion in both MYB genes was positively associated with ASE and anthocyanin accumulation in apple petals through analysis of 231 apple accessions, and thus underpins apple flower colour evolution. Our study demonstrated the importance of TEs in regulating ASE on a genome-wide scale and presents a novel method for rapid identification of ASE genes and their regulatory elements in plants.

Keywords: Malus; Hi-C; allele-specific expression; anthocyanin; comparative genomics; genome assembly; genome sequencing; proximity-guided assembly; transposable element.

MeSH terms

  • Alleles
  • Anthocyanins
  • Color
  • DNA Transposable Elements
  • Flowers / genetics
  • Flowers / metabolism
  • Fruit / metabolism
  • Gene Expression Regulation, Plant / genetics
  • Genome, Plant
  • Malus* / metabolism
  • Plant Proteins / genetics

Substances

  • Anthocyanins
  • DNA Transposable Elements
  • Plant Proteins