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.2023 Nov 6;10(12):uhad237.
doi: 10.1093/hr/uhad237. eCollection 2023 Dec.

DiverseO-methyltransferases catalyze the biosynthesis of floral benzenoids that repel aphids from the flowers of waterlilyNymphaea prolifera

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DiverseO-methyltransferases catalyze the biosynthesis of floral benzenoids that repel aphids from the flowers of waterlilyNymphaea prolifera

Guanhua Liu et al. Hortic Res..

Abstract

Nymphaea is a key genus of the ANA grade (Amborellales, Nymphaeales, and Austrobaileyales) of basal flowering plants, which serve as a key model to study the early evolution of floral traits. In this study, we comprehensively investigated the emission, biosynthesis, and biological function of the floral scent in a night-blossoming waterlilyNymphaea prolifera. The headspace volatile collection combined with GC-MS analysis showed that the floral scent ofN. prolifera is predominately comprised by methylated benzenoids including anisole, veratrole, guaiacol, and methoxyanisole. Moreover, the emission of these floral benzenoids inN. prolifera exhibited temporal and spatial pattern with circadian rhythm and tissue specificity. By creating and mining transcriptomes ofN. prolifera flowers, 12 oxygen methyltransferases (NpOMTs) were functionally identified. Byin vitro enzymatic assay, NpOMT3, 6, and 7 could produce anisole and NpOMT5, 7, 9, produce guaiacol, whereas NpOMT3, 6, 9, 11 catalyzed the formation of veratrole. Methoxyanisole was identified as the universal product of all NpOMTs. Expression patterns ofNpOMTs provided implication for their roles in the production of the respective benzenoids. Phylogenetic analysis of OMTs suggested aNymphaea-specific expansion of the OMT family, indicating the evolution of lineage-specific functions. In bioassays, anisole, veratrole, and guaiacol in the floral benzenoids were revealed to play the critical role in repelling waterlily aphids. Overall, this study indicates that the basal flowering plantN. prolifera has evolved a diversity and complexity of OMT genes for the biosynthesis of methylated benzenoids that can repel insects from feeding the flowers. These findings provide new insights into the evolutional mechanism and ecological significance of the floral scent from early-diverged flowering plants.

© The Author(s) 2023. Published by Oxford University Press on behalf of Nanjing Agricultural University.

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Conflict of interest statement

The authors declare no competing financial interest.

Figures

Figure 1
Figure 1
The floral volatile compound (FVOC) emission from different types of flowers inNymphaea prolifera.A Different types of flowers based on the blooming time and growth characteristic inN. prolifera. M = mother flowers; D = daughter flowers; and GD = granddaughter flowers.B The chromatogram profile of FVOCs of the mother/daughter/granddaughter flowers ofN. prolifera during the first blossom. Six detectable volatile compounds were marked in the first blossoming mother flowers. 1, anisole; 2, guaiacol; 3, veratrole; 4, methoxyanisole; 5, α-terpineol; and 6, pentadecane. The IS means the1-octanol as the internal standard.C The emission rate of four benzenoids of mother/daughter/granddaughter flowers during the first blossom.D The ratio of four major benzenoids in the total emission rate of FVOCs from mother−/daughter−/granddaughter flowers ofN. prolifera.
Figure 2
Figure 2
The NMDS (non-metric multidimensional scaling) analysis of FVOCs fromNymphaea prolifera mother flower with the other 20 species in Nymphaeaceae by R with vegan and ggplot2 packages. The detailed information of FVOCs in these Nymphaeaceae species was profiled in Table S5 (see online supplementary material).
Figure 3
Figure 3
The rhythmic emission pattern of major volatile compounds of mother/daughter/granddaughter flowers during 48 h observation.A The emission pattern of total volatile compounds, anisole, and veratrole of mother flowers.B The emission pattern of total volatile compounds, anisole, and veratrole of daughter flowers.C The emission pattern of total volatile compounds and veratrole of granddaughter flowers. The black and gray bars indicate the nighttime and daytime, respectively. Different letters denote statistically significant differences among the mean values according to the analysis of variance (P < 0.05). The statistical test was conducted by Tukey-HSD by using SPSS (version 26).
Figure 4
Figure 4
Emission rates of floral volatiles from different floral organs inNymphaea prolifera. Intact fully opened mother flowers for the first time were separated into sepals, petals, stamens, and pistils and were subjected to dynamic headspace collection and GC–MS analysis, respectively.A The emission rate of total floral volatile compounds (FVOCs).B The total benzenoids in the four organs ofN. prolifera mother flowers, respectively.C–F The emission rate of anisole, veratrole, methoxyanisole, and guaiacol in four floral organs (sepals, petals, stamens, and pistils).G The emission ratio of anisole, veratrole, methoxyanisole, and guaiacol from the four organs of mother flowers, respectively. The total VOCs and total benzenoids means that sum of all the compounds emission rate or all the benzenoids in each organ based on Table S4 (see online supplementary material), respectively. Bar widths correspond to the relative percentage of VOCs. The bipartite graph was constructed by R with bipartite package.
Figure 5
Figure 5
In vitro products catalyzed byNymphaea prolifera oxygen methyltransferases (NpOMTs) with gas chromatography–mass spectrometry analysis.A The production of NpOMT3, NpOMT6, and NpOMT7 using phenol and S-adenosyl-L-methionine (SAM) as substrates.B The production of NpOMT3, NpOMT4, NpOMT11 using mequinol and SAM as substrates.C The production of NpOMT5, NpOMT7, NpOMT9, and NpOMT11 using catechol and SAM as substrates.D The production of NpOMT3, NpOMT8, NpOMT11, and NpOM13 using mequinol and SAM as substrates. The CK means the empty pET32a(+) as negative control. 1, anisole; 2, phenol; 3, methoxyaisole; 4, mequinol; 5, guaiacol; 6, catechol; 7, veratrole. All these seven compounds were confirmed by comparing the retention time and mass spectrum with their chemical standards.
Figure 6
Figure 6
The relative expression analysis ofNpOMTs inNymphaea prolifera flowers, foliage, and stalk and correlation analysis of four major benzenoids withNpOMTs expression patterns.A The expression patterns ofNpOMTs in foliage, mother/daughter/granddaughter flowers.B The expression patterns ofNpOMTs in blooming floral organs of mother flowers.C The correlation analysis ofNpOMTs expression patterns with four major benzenoids emission from mother−/daughter−/granddaughter flowers.D The correlation analysis ofNpOMTs expression patterns with four major benzenoids emission from different organs in mother flowers. The gene transcript levels were measured using qRT-PCR withNpActin as the internal control, which was dug out from the transcriptome ofN. prolifera mother flowers. The relative expression was evaluated using the 2-ΔΔCT method. The correlation analysis was conducted by R studio with ggplot2 package. The numbers in the correlation map mean the relative coefficient.
Figure 7
Figure 7
The phylogenetic analysis of NpOMTs with the putative OMTs identified from the genomes ofAmborella trichopoda,Nymphaea colorata,Arabidopsis thaliana,Sorghum bicolor,Euryale ferox,Selaginella moellendorffii, and fiveChlorophyta species, as well as functionally characterized OMTs from other plant species. Protein sequence alignments were produced by MEGA X, and the phylogenetic tree was constructed using the maximum likelihood method with 1000 bootstrap repetitions. The phylogeny was visualized by iTOL [49]. The putative OMTs ofN. colorata,E. ferox,S. bicolor,A. thaliana, andS. moellendorffii were retrieved from NCBI by BlastP. The putative OMTs of the five Chlorophyta species were obtained from the UniProt TrEMBL protein database by referring to previous reports [50]. The functionally characterized OMTs represent that their catalyzed activities have been evaluated in previous reports and the detailed information is presented in Table S7 (see online supplementary material). “*” depicts OMTs involved in the biosynthesis of volatile hydroxy-methyl benzenoids/phenylpropanoids. Group I a, Group I b, and Group II c were distinguished based on substrates and sequence features. The detailed information on the functionally characterized OMTs is presented in Table S7 (see online supplementary material), and the detailed group information on the phylogenetic analysis is presented in Fig. S4 (see online supplementary material).
Figure 8
Figure 8
The preferences of aphids (Rhopalosiphum nymphaeas) to different odor resources.A The Y-tube assay for determining the preference of waterlily aphids to granddaughter/daughter flowers and foliage (GD + D + Foliage), mother flowers (first blossoming), and first closed mother flowers.B The preference assay of chemical standard (GC) anisole, veratrole, and guaiacol with respect to water lily aphids. The concentrations of anisole, veratrole, and guaiacol were selected based on the rhythmic emission ratio of mother flowers during the 24 h observation period. Control (air) was set with a solvent (paroline). Numbers refer to the percentage of the water lily aphids choosing an odor source.N is >54 per test. The total number of respondents involved in the selection was set as 100%. Significant differences were analysed using the chi-square test and are marked with asterisks (**P < 0.01; *P < 0.05).
Figure 9
Figure 9
Proposed scheme for the biosynthesis of benzenoids in mother/daughter/granddaughter flowers ofNymphaea prolifera.
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