Duplication and Specialization of NUDX1 in Rosaceae Led to Geraniol Production in Rose Petals

Abstract

Nudix hydrolases are conserved enzymes ubiquitously present in all kingdoms of life. Recent research revealed that several Nudix hydrolases are involved in terpenoid metabolism in plants. In modern roses, RhNUDX1 is responsible for formation of geraniol, a major compound of rose scent. Nevertheless, this compound is produced by monoterpene synthases in many geraniol-producing plants. As a consequence, this raised the question about the origin of RhNUDX1 function and the NUDX1 gene evolution in Rosaceae, in wild roses or/and during the domestication process. Here, we showed that three distinct clades of NUDX1 emerged in the Rosoidae subfamily (Nudx1-1 to Nudx1-3 clades), and two subclades evolved in the Rosa genus (Nudx1-1a and Nudx1-1b subclades). We also showed that the Nudx1-1b subclade was more ancient than the Nudx1-1a subclade, and that the NUDX1-1a gene emerged by a trans-duplication of the more ancient NUDX1-1b gene. After the transposition, NUDX1-1a was cis-duplicated, leading to a gene dosage effect on the production of geraniol in different species. Furthermore, the NUDX1-1a appearance was accompanied by the evolution of its promoter, most likely from a Copia retrotransposon origin, leading to its petal-specific expression. Thus, our data strongly suggest that the unique function of NUDX1-1a in geraniol formation was evolved naturally in the genus Rosa before domestication.

Identification and Characterization of Transcription Factors Involved in Geraniol Biosynthesis in Rosa chinensis

“…Interestingly, only 5 out of these 30 genes were significantly upregulated in OB petals compared to OBL: RcHMGCR (encoding hydroxymethylglutaryl-CoA reductase), RcGGPPS (encoding geranylgeranyl diphosphate synthase), RcNUDX1 (encoding a geranyl diphosphate phosphohydrolase), RcG8H (encoding geraniol 8-hydroxylase), and RcCYP82D47 . We hypothesized that RcNUDX1 exerts the same function as RhNUDX1 (GenBank accession number JQ820249), which leads to geraniol production [ 23 ]. RcNUDX1 was present as four tandem copies on chromosome 2 of R. chinensis (RchiOBHmChr2g0142071, RchiOBHmChr2g0142081, RchiOBHmChr2g0142111, and RchiOBHmChr2g0142121).…”

BOX38, a DNA Marker for Selection of Essential Oil Yield of Rosa × rugosa

“…B38 repeats originated from 3′ long-terminal repeat (LTR) of Copia R24558 and the repeat number in promotor should tend to neutral evolution in wild species [ 24 ]. Seven repeats were also found in the wild Rugosa, which is the common ancestor of cultivars of Rugosa pedigree.…”

“…While modern roses rely on a specific cytosolic pathway [ 22 , 23 ] which dephosphorylates GPP to geranyl phosphate (GP) by Nudix hydrolase ( NUDX1 ), then to geraniol by one uncharacterized phosphatase. The NUDX1 family includes 4 sub-family, i.e., Nudx1-1(a/b), −2, −3, −4, while only NUDX1-1a gene clusters are specific to geraniol producing rose species whose NUDX1-1a copy number is more than non-geraniol-producing species [ 24 , 25 ]. The NUDX1-1a copy number positively correlated with the NUDX1-1a expression, and it could be a candidate marker for high geraniol level cultivars or mutations [ 24 ].…”

“…The NUDX1 family includes 4 sub-family, i.e., Nudx1-1(a/b), −2, −3, −4, while only NUDX1-1a gene clusters are specific to geraniol producing rose species whose NUDX1-1a copy number is more than non-geraniol-producing species [ 24 , 25 ]. The NUDX1-1a copy number positively correlated with the NUDX1-1a expression, and it could be a candidate marker for high geraniol level cultivars or mutations [ 24 ]. Besides the NUDX1-1a gene, transposon elements (TEs) in promotors could also be candidate markers for scented-rose breeding [ 21 , 24 ].…”

“…The NUDX1-1a copy number positively correlated with the NUDX1-1a expression, and it could be a candidate marker for high geraniol level cultivars or mutations [ 24 ]. Besides the NUDX1-1a gene, transposon elements (TEs) in promotors could also be candidate markers for scented-rose breeding [ 21 , 24 ]. Here, based on the analysis of the conservation and variation of transposon fragments relevant motifs in R. × rugosa , a rose-specific motif, Box38, was selected as a robust marker for the early selection of high-oil-yield cultivars.…”