Multi-omics analysis reveals the genetic basis of rice fragrance mediated by betaine aldehyde dehydrogenase 2

Abstract

Introduction: Fragrance is an important economic and quality trait in rice. The trait is controlled by the recessive gene betaine aldehyde dehydrogenase 2 (BADH2) via the production of 2-acetyl-1-pyrroline (2AP).

Objectives: Variation in BADH2 was evaluated at the population, genetic, transcriptional, and metabolic levels to obtain insights into fragrance regulation in rice.

Methods: Whole-genome resequencing of the Korean World Rice Collection of 475 rice accessions, including 421 breeding lines and 54 wild accessions, was performed. Transcriptome analyses of a subset of 279 accessions, proteome analyses of 64 accessions, and volatile profiling of 421 breeding lines were also performed.

Results: We identified over 3.1 million high-quality single nucleotide polymorphisms (SNPs) in Korean rice collection. Most SNPs were present in intergenic regions (79%), and 190,148 SNPs (6%) were located in the coding sequence, of which 53% were nonsynonymous. In total, 38 haplotypes were identified in the BADH2 coding region, including four novel haplotypes (one in cultivated and three in wild accessions). Tajima's D values suggested that BADH2 was under balancing selection in japonica rice. Furthermore, we identified 316 expression quantitative trait loci (eQTL), including 185 cis-eQTLs and 131 trans-eQTLs, involved in BADH2 regulation. A protein quantitative trait loci (pQTL) analysis revealed the presence of trans-pQTLs; 13 pQTLs were mapped 1 Mbp from the BADH2 region. Based on variable importance in projection (VIP) scores, 15 volatile compounds, including 2AP, discriminated haplotypes and were potential biomarkers for rice fragrance.

Conclusion: We generated a catalog of haplotypes based on a resequencing analysis of a large number of rice accessions. eQTLs and pQTLs associated with BADH2 gene expression and protein accumulation are likely involved in the regulation of 2AP variation in fragrant rice. These data improve our understanding of fragrance and provide valuable information for rice breeding.

Keywords: Betaine aldehyde dehydrogenase 2; Expression quantitative trait loci; Fragrant rice; Haplotype; Protein quantitative trait loci; Volatiles.