Genome-scale investigation and identification of variations associated with early flowering based on whole genome resequencing and transcriptome integrated analysis in tree peony

•Early-flowering mutant of Paeonia ostii ‘Fengdan’ was observed. Flowering phenotype of early-flowering mutant of Paeonia ostii ‘Fengdan’, Paeonia ostii ‘Fengdan’ and Paeonia suffruticosa ‘Lianhe’ were investigated and characterized.•SNP and InDel Variants associated with early-flowering phenotype using early- and late-flowering tree peony genotypes were conducted by Whole genome re-sequencing and transcriptome integrated analysis.•DEGs harboring SNPs and Indels variants mainly enriched in phenylpropanoid biosynthesis, flavonoid biosynthesis, plant hormone signal transduction, RNA degradation, and MAPK signaling pathways were identified and validated. Tree peony, a traditional ornamental flower and candidate national flower of China, has thousands of varieties with different flower colors and types after a long history of natural selection and artificial breeding. However, the short and concentrated florescence period and a shortage of early- and late-flowering varieties limit the enhancement of ornamental values. Single nucleotide polymorphisms (SNPs) and insertion/deletion mutations (InDels) are important factors for mutant genotypes generation. Whole genome resequencing and transcriptome integrated analysis was conducted using early-flowering genotype Paeonia ostii ‘Fengdan’ (FD), early-flowering mutant of Paeonia ostii ‘Fengdan’ (MU), and late-flowering genotype Paeonia suffruticosa ‘Lianhe’ (LH) to identify variants related to the early-flowering phenotype. Comparison of FD vs LH, MU vs LH, and MU vs FD revealed 1,488 SNPs, 1,261 InDels, and 1,912 differential expressed genes (DEGs) specific to early-flowering genotype FD and MU, respectively. Additionally, 329 DEGs affected by SNPs and InDels variants were differentially expressed in three tree peony genotypes at the full-blooming stage. Furthermore, 37 DEGs affected by SNP variants and 44 DEGs affected by InDel variants were identified in the early-flowering genotype FD and its corresponding MU at the full-blooming stage. Most of these genes were related to phenylpropanoid biosynthesis, flavonoid biosynthesis, plant hormone signal transduction, RNA degradation, and MAPK signaling pathway. Additionally, four SNPs were validated in FD, MU, and LH by Sanger sequencing. Expression profiles of 25 DEGs containing SNP/Indels associated with the early-flowering trait were verified by RT-qPCR. The abundant genetic variations identified in this study offer valuable genomic resources for ongoing functional and