Evolution of a Novel and Adaptive Floral Scent in Wild Tobacco

Abstract

Many plants emit diverse floral scents that mediate plant–environment interactions and attain reproductive success. However, how plants evolve novel and adaptive biosynthetic pathways for floral volatiles remains unclear. Here, we show that in the wild tobacco, Nicotiana attenuata, a dominant species-specific floral volatile (benzyl acetone, BA) that attracts pollinators and deters florivore is synthesized by phenylalanine ammonia-lyase 4 (NaPAL4), isoflavone reductase 3 (NaIFR3), and chalcone synthase 3 (NaCHAL3). Transient expression of NaFIR3 alone in N. attenuata leaves is sufficient and necessary for ectopic foliar BA emissions, and coexpressing NaIFR3 with NaPAL4 and NaCHAL3 increased the BA emission levels. Independent changes in transcription of NaPAL4 and NaCHAL3 contributed to intraspecific variations of floral BA emission. However, among species, the gain of expression of NaIFR3 resulted in the biosynthesis of BA, which was only found in N. attenuata. This study suggests that novel metabolic pathways associated with adaptation can arise via reconfigurations of gene expression.

Allelic differences of clustered terpene synthases contribute to correlated intraspecific variation of floral and herbivory‐induced volatiles in a wild tobacco

“…The quantitative trait locus (QTL) mapping was described in detail in our previous study (Zhou et al ., 2017) and was conducted with the R package qtlrel (Cheng et al ., 2011) following the tutorial. In brief, the genotype information of AI‐RIL plants and the linkage map were obtained from a dataset reported earlier (Zhou et al ., 2017; Guo et al ., 2020). In total, we obtained 25 469 single nucleotide polymorphism (SNP) markers among 248 individuals.…”

Allelic differences of clustered terpene synthases contribute to correlated intra-specific variation of floral and herbivory-induced volatiles in a wild tobacco

“…In addition to a flower-specific volatile, benzoyl acetone (Guo et al ., 2020), the three terpenoids in HIPVs, ( E )-β-ocimene, linalool, and ( E )-α-bergamotene were also found in N. attenuata floral volatiles (Kessler et al ., 2007). We reasoned that if the same compound in HIPVs and floral volatiles was regulated by the same genetic mechanism, its abundance would show correlated changes in HIPVs and floral volatiles amounts among different genotypes.…”

“…The QTL mapping was described in detail in our previous study (Zhou et al ., 2017) and was conducted with the R package QTLRel (Cheng et al ., 2011) following the tutorial. In brief, the genotype information of AI-RIL plants and the linkage map were obtained from a dataset reported earlier (Guo et al ., 2020, Zhou et al ., 2017). In total, we obtained 25,469 SNP markers among 248 individuals.…”

Single-cell RNA-sequencing of Nicotiana attenuata petal cells reveals the entire biosynthetic pathway of a floral scent

“…By analyzing differential gene expression among the rose cultivars that vary widely in floral scent emission, researchers identified a sesquiterpene synthase (Guterman et al, 2002) and a nudix hydrolase (Magnard et al, 2015), a new type of monoterpene synthase. In addition, when a biosynthetic gene in a multi-step pathway is available, this gene can be used as "bait" to calculate its degree of association to the entire transcriptome (gene co-expression network analysis) (Wisecaver et al, 2017) and to construct a gene cluster that would regulate the production of metabolites, including volatiles (Li et al, 2020). For instance, TPS11 enzymes in Arabidopsis thaliana flowers synthesize (+)--barbatene and (+)thujopsene.…”

“…Most BA is produced from corolla limbs (Kessler and Baldwin, 2007;Euler and Baldwin, 1996), which is regulated by the circadian clock (Yon et al, 2016). Lphenylalanine (Phe) is a precursor of BA, and phenylalanine ammonia-lyase 4 (PAL4) is known to be the first enzyme in the BA biosynthetic pathway (Guo et al, 2020). In the plant kingdom, the major Phe-derived floral volatiles are phenylpropanoid (a phenyl ring with a three-carbon side chain, C6-C3) and benzenoid (C6-C1) (Widhalm and Dudareva, 2015).…”