Functional diversification in the Nudix hydrolase gene family drives sesquiterpene biosynthesis in Rosa × wichurana

Sun, Pulu; Dégut, Clément; Réty, S.; Caissard, Jean‐Claude; Oyant, Laurence Hibrand‐Saint; Bony, Aurélie; Paramita, Saretta N.; Conart, Corentin; Magnard, Jean‐Louis; Jeauffre, Julien; Abd-El-Haliem, Ahmed; Marie-Magdelaine, Jordan; Thouroude, Tatiana; Baltenweck, Raymonde; Tisné, Carine; Foucher, Fabrice; Haring, Michel A.; Hugueney, Philippe; Schuurink, Robert C.; Baudino, Sylvie

doi:10.1111/tpj.14916

Cited by 23 publications

(34 citation statements)

References 71 publications

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“…The reduced release of (E)-β-caryophyllene observed at 48 hpi with five aphids is likely the result of aphid effectors that may modify several plant defense tools including the emission of VOCs, as also shown for other plant-aphid interaction (Schwartzberg et al, 2011). Coherently with this observation we registered at 48 hpi the down-regulation of a NUDX1 (CUCPE_TC20679), a gene associated with the biosynthesis of sesquiterpenoids (Sun et al, 2020) and of a gene associated with isopentenyl diphosphate biosynthesis (CUCPE_TC9431), a compound associated with terpenoid biosynthesis (McCaskill and Croteau, 1999), that might explain the reduced release of (E)-β-caryophyllene observed at this time point. In addition, a strong down-regulation of a gene encoding for a terpene synthase was observed at 96 hpi suggesting a possible further reduction of (E)-β-caryophyllene, or other terpenes, at a low aphid density.…”

Section: Aphid Density and Time Of Plant Infestation Modify (E)-β-carsupporting

confidence: 74%

Zucchini Plants Alter Gene Expression and Emission of (E)-β-Caryophyllene Following Aphis gossypii Infestation

et al. 2021

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Zucchini (Cucurbita pepo L.) is widely cultivated in temperate regions. One of the major production challenges is the damage caused by Aphis gossypii (Homoptera: Aphididae), a polyphagous aphid, which can negatively affect its host plant, both directly by feeding and indirectly by vectoring viruses. To gain insights into the transcriptome events that occur during the zucchini–aphid interaction and to understand the early-to-late defense response through gene expression profiles, we performed RNA-sequencing (RNA-Seq) on zucchini leaves challenged by A. gossypii (24, 48, and 96 h post-infestation; hpi). Data analysis indicated a complex and dynamic pattern of gene expression and a transient transcriptional reconfiguration that involved more than 700 differentially expressed genes (DEGs), including a large number of defense-related genes. The down-regulation of key genes of plant immunity, such as leucine-rich repeat (LRR) protein kinases, transcription factors, and genes associated with direct (i.e., protease inhibitors, cysteine peptidases, etc.) and indirect (i.e., terpene synthase) defense responses, suggests the aphid ability to manipulate plant immune responses. We also investigated the emission of volatile organic compounds (VOCs) from infested plants and observed a reduced emission of (E)-β-caryophyllene at 48 hpi, likely the result of aphid effectors, which reflects the down-regulation of two genes involved in the biosynthesis of terpenoids. We showed that (E)-β-caryophyllene emission was modified by the duration of plant infestation and by aphid density and that this molecule highly attracts Aphidius colemani, a parasitic wasp of A. gossypii. With our results we contributed to the identification of genes involved in cucurbit plant interactions with phloem feeders. Our findings may also help pave the way toward developing tolerant zucchini varieties and to identify molecules for sustainable management of harmful insect populations.

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Section: Aphid Density and Time Of Plant Infestation Modify (E)-β-carsupporting

confidence: 74%

Zucchini Plants Alter Gene Expression and Emission of (E)-β-Caryophyllene Following Aphis gossypii Infestation

et al. 2021

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“…We found tricyclene (E)-beta-ocimene synthase (EBOS) at 63.49 Mbp. Monoterpene (E)-ß-ocimene is one of the major components in several plant families [ 55 , 56 , 57 ] and is also described in roses [ 9 , 58 ].…”

Section: Discussionmentioning

confidence: 99%

“…Flower traits, e.g., the number and color of petals, were among the first traits investigated in genetic studies [ 2 , 3 ]. In addition, a large number of studies have also addressed the basic aspects of unique features of the rose flower, e.g., the unique composition of scent metabolites that make up the rose fragrance [ 4 , 5 , 6 , 7 , 8 , 9 , 10 ].…”

Section: Introductionmentioning

confidence: 99%

Detection of Reproducible Major Effect QTL for Petal Traits in Garden Roses

Schulz

Linde

Debener

2021

Plants

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The detection of QTL by association genetics depends on the genetic architecture of the trait under study, the size and structure of the investigated population and the availability of phenotypic and marker data of sufficient quality and quantity. In roses, we previously demonstrated that major QTL could already be detected in small association panels. In this study, we analyzed petal number, petal size and fragrance in a small panel of 95 mostly tetraploid garden rose genotypes. After genotyping the panel with the 68 K Axiom WagRhSNP chip we detected major QTL for all three traits. Each trait was significantly influenced by several genomic regions. Some of the QTL span genomic regions that comprise several candidate genes. Selected markers from some of these regions were converted into KASP markers and were validated in independent populations of up to 282 garden rose genotypes. These markers demonstrate the robustness of the detected effects independent of the set of genotypes analyzed. Furthermore, the markers can serve as tools for marker-assisted breeding in garden roses. Over an extended timeframe, they may be used as a starting point for the isolation of the genes underlying the QTL.

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“…This stands in contrast to a highly similar enzyme, RwNUDIX1–2, recently isolated from Rosa wichurana , which converts FDP to E , E ‐farnesol in the cytosol (Sun et al. , 2020).…”

Section: Discussionmentioning

confidence: 59%

“…This subclade includes PgNdx1, rose Nudix hydrolases involved in sesquiterpene volatiles (Sun et al. , 2020), and a Tanacetum cinerariifolium Nudix sequence involved in pyrethrin biosynthesis (Li et al. , 2020).…”

Section: Resultsmentioning

confidence: 99%

Cytosolic geraniol and citronellol biosynthesis require a Nudix hydrolase in rose‐scented geranium (Pelargonium graveolens)

2021

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Summary Geraniol, citronellol and their esters are high‐value acyclic monoterpenes used in food technology, perfumery and cosmetics. A major source of these compounds is the essential oil of rose‐scented geraniums of the genus Pelargonium. We provide evidence that their biosynthesis mainly takes place in the cytosol of glandular trichomes via geranyl monophosphate (GP) through the action of a Nudix hydrolase. Protein preparations could convert geranyl diphosphate (GDP) to geraniol in in vitro assays, a process which could be blocked by inorganic phosphatase inhibitors, suggesting a two‐step conversion of GDP to geraniol. Pelargonium graveolens chemotypes enriched in either geraniol or (−)‐citronellol accumulate GP or citronellyl monophosphate (CP), respectively, the presumed precursors to their monoterpenoid end products. Geranyl monophosphate was highly enriched in isolated glandular trichomes of lines producing high amounts of geraniol. In contrast, (−)‐isomenthone‐rich lines are depleted in these prenyl monophosphates and monoterpene alcohols and instead feature high levels of GDP, the precursor to plastidic p‐menthane biosynthesis. A Nudix hydrolase cDNA from Pelargonium glandular trichomes, dubbed PgNdx1, encoded a cytosolic protein capable of hydrolyzing GDP to GP with a KM of about 750 nm but is only weakly active towards farnesyl diphosphate. In citronellol‐rich lines, GDP, GP and CP were detected in nearly equimolar amounts, while citronellyl diphosphate was absent, suggesting that citronellol biosynthesis may proceed by reduction of GP to CP in this species. These findings highlight the cytosol as a compartment that supports monoterpene biosynthesis and expands the roles of Nudix hydrolases in the biosynthesis of plant volatiles.

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Functional diversification in the Nudix hydrolase gene family drives sesquiterpene biosynthesis in Rosa × wichurana

Cited by 23 publications

References 71 publications

Zucchini Plants Alter Gene Expression and Emission of (E)-β-Caryophyllene Following Aphis gossypii Infestation

Zucchini Plants Alter Gene Expression and Emission of (E)-β-Caryophyllene Following Aphis gossypii Infestation

Detection of Reproducible Major Effect QTL for Petal Traits in Garden Roses

Cytosolic geraniol and citronellol biosynthesis require a Nudix hydrolase in rose‐scented geranium (Pelargonium graveolens)

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