Loss-of-function variants of CYP706A3 in two natural accessions of Arabidopsis thaliana increase floral sesquiterpene emission.

Abstract

Background: The major floral scent compounds of Arabidopsis thaliana flowers are terpenes. Although A. thaliana is generally considered to be a self-pollinating plant, there are natural variation in terpene volatile emission from flowers. However, the genetic mechanisms underlying the natural variation in Arabidopsis floral scents remain limited.

Results: Here, we screened 116 natural accessions of A. thaliana and observed a substantial variability in the levels of terpene emission across these accessions. A genome-wide association study (GWAS) uncovered a genomic region associated with the observed variability in myrcene, one of monoterpene compounds. We then performed high-throughput genetic mapping using two representative accessions: Col-0 and Fr-2, which emit low and large amounts of floral terpenes, respectively. Next-generation mapping and RNA sequencing analyses revealed that the natural premature stop codon of CYP706A3 of Fr-2, located at the 98th codon, confers high emission of sesquiterpene from flowers. We also found an independent mutation of CYP706A3 of Np-0 in different position, leading to increased sesquiterpene emission. Interestingly, the expression levels of defense-related genes in Fr-2 were lower than those in Col-0 flowers, which suggests that terpene volatiles are potentially linked to floral defense.

Conclusions: The natural variation in Arabidopsis floral scent emission was partially explained by one natural allele of CYP706A3. Since some natural accessions harboring a functional allele of CYP706A3 still emit the large amount of floral sesquiterpene, it is possible that rare variants located on other loci increase scent emission.