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1.
Mol Biol Evol ; 39(2)2022 02 03.
Article in English | MEDLINE | ID: mdl-35022771

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.


Subject(s)
Rosa , Rosaceae , Acyclic Monoterpenes , Domestication , Rosa/genetics , Rosa/metabolism
2.
Hortic Res ; 8(1): 76, 2021 Apr 01.
Article in English | MEDLINE | ID: mdl-33790245

ABSTRACT

Blooming seasonality is an important trait in ornamental plants and was selected by humans. Wild roses flower only in spring whereas most cultivated modern roses can flower continuously. This trait is explained by a mutation of a floral repressor gene, RoKSN, a TFL1 homologue. In this work, we studied the origin, the diversity and the selection of the RoKSN gene. We analyzed 270 accessions, including wild and old cultivated Asian and European roses as well as modern roses. By sequencing the RoKSN gene, we proposed that the allele responsible for continuous-flowering, RoKSNcopia, originated from Chinese wild roses (Indicae section), with a recent insertion of the copia element. Old cultivated Asian roses with the RoKSNcopia allele were introduced in Europe, and the RoKSNcopia allele was progressively selected during the 19th and 20th centuries, leading to continuous-flowering modern roses. Furthermore, we detected a new allele, RoKSNA181, leading to a weak reblooming. This allele encodes a functional floral repressor and is responsible for a moderate accumulation of RoKSN transcripts. A transient selection of this RoKSNA181 allele was observed during the 19th century. Our work highlights the selection of different alleles at the RoKSN locus for recurrent blooming in rose.

3.
Plant J ; 104(1): 185-199, 2020 09.
Article in English | MEDLINE | ID: mdl-32639596

ABSTRACT

Roses use a non-canonical pathway involving a Nudix hydrolase, RhNUDX1, to synthesize their monoterpenes, especially geraniol. Here we report the characterization of another expressed NUDX1 gene from the rose cultivar Rosa x wichurana, RwNUDX1-2. In order to study the function of the RwNUDX1-2 protein, we analyzed the volatile profiles of an F1 progeny generated by crossing R. chinensis cv. 'Old Blush' with R. x wichurana. A correlation test of the volatilomes with gene expression data revealed that RwNUDX1-2 is involved in the biosynthesis of a group of sesquiterpenoids, especially E,E-farnesol, in addition to other sesquiterpenes. In vitro enzyme assays and heterologous in planta functional characterization of the RwNUDX1-2 gene corroborated this result. A quantitative trait locus (QTL) analysis was performed using the data of E,E-farnesol contents in the progeny and a genetic map was constructed based on gene markers. The RwNUDX1-2 gene co-localized with the QTL for E,E-farnesol content, thereby confirming its function in sesquiterpenoid biosynthesis in R. x wichurana. Finally, in order to understand the structural bases for the substrate specificity of rose NUDX proteins, the RhNUDX1 protein was crystallized, and its structure was refined to 1.7 Å. By molecular modeling of different rose NUDX1 protein complexes with their respective substrates, a structural basis for substrate discrimination by rose NUDX1 proteins is proposed.


Subject(s)
Plant Proteins/metabolism , Pyrophosphatases/metabolism , Rosa/metabolism , Sesquiterpenes/metabolism , Farnesol/metabolism , Genes, Plant/genetics , Genes, Plant/physiology , Phylogeny , Plant Proteins/genetics , Plant Proteins/physiology , Pyrophosphatases/genetics , Pyrophosphatases/physiology , Quantitative Trait Loci/genetics , Rosa/genetics , Sequence Alignment , Nudix Hydrolases
4.
Int J Mol Sci ; 20(15)2019 Aug 04.
Article in English | MEDLINE | ID: mdl-31382685

ABSTRACT

The shoot branching pattern is a determining phenotypic trait throughout plant development. During shoot branching, BRANCHED1 (BRC1) plays a master regulator role in bud outgrowth, and its transcript levels are regulated by various exogenous and endogenous factors. RhBRC1 (the homologous gene of BRC1 in Rosa hybrida) is a main branching regulator whose posttranscriptional regulation in response to sugar was investigated through its 3'UTR. Transformed Rosa calluses containing a construction composed of the CaMV35S promoter, the green fluorescent protein (GFP) reporter gene, and the 3'UTR of RhBRC1 (P35S:GFP::3'UTRRhBRC1) were obtained and treated with various combinations of sugars and with sugar metabolism effectors. The results showed a major role of the 3'UTR of RhBRC1 in response to sugars, involving glycolysis/the tricarboxylic acid cycle (TCA) and the oxidative pentose phosphate pathway (OPPP). In Rosa vegetative buds, sequence analysis of the RhBRC1 3'UTR identified six binding motifs specific to the Pumilio/FBF RNA-binding protein family (PUF) and probably involved in posttranscriptional regulation. RhPUF4 was highly expressed in the buds of decapitated plants and in response to sugar availability in in-vitro-cultured buds. RhPUF4 was found to be close to AtPUM2, which encodes an Arabidopsis PUF protein. In addition, sugar-dependent upregulation of RhPUF4 was also found in Rosa calluses. RhPUF4 expression was especially dependent on the OPPP, supporting its role in OPPP-dependent posttranscriptional regulation of RhBRC1. These findings indicate that the 3'UTR sequence could be an important target in the molecular regulatory network of RhBRC1 and pave the way for investigating new aspects of RhBRC1 regulation.


Subject(s)
Arabidopsis Proteins/genetics , Arabidopsis/genetics , RNA-Binding Proteins/genetics , Rosa/genetics , Transcription Factors/genetics , 3' Untranslated Regions/genetics , Arabidopsis/metabolism , Gene Expression Regulation, Plant/genetics , Phenotype , Plant Proteins/genetics , Rosa/metabolism , Signal Transduction/genetics , Sugars/metabolism
5.
Plant Physiol ; 179(3): 1064-1079, 2019 03.
Article in English | MEDLINE | ID: mdl-30622153

ABSTRACT

Floral scent is one of the most important characters in horticultural plants. Roses (Rosa spp.) have been cultivated for their scent since antiquity. However, probably by selecting for cultivars with long vase life, breeders have lost the fragrant character in many modern roses, especially the ones bred for the cut flower market. The genetic inheritance of scent characters has remained elusive so far. In-depth knowledge of this quantitative trait is thus very much needed to breed more fragrant commercial cultivars. Furthermore, rose hybrids harbor a composite genomic structure, which complexifies quantitative trait studies. To understand rose scent inheritance, we characterized a segregating population from two diploid cultivars, Rosa × hybrida cv H190 and Rosa wichurana, which have contrasting scent profiles. Several quantitative trait loci for the major volatile compounds in this progeny were identified. One among these loci contributing to the production of 2-phenylethanol, responsible for the characteristic odor of rose, was found to be colocalized with a candidate gene belonging to the 2-phenylethanol biosynthesis pathway: the PHENYLACETALDEHYDE SYNTHASE gene RhPAAS An in-depth allele-specific expression analysis in the progeny demonstrated that only one allele was highly expressed and was responsible for the production of 2-phenylethanol. Unexpectedly, its expression was found to start early during flower development, before the production of the volatile 2-phenylethanol, leading to the accumulation of glycosylated compounds in petals.


Subject(s)
Phenylethyl Alcohol/metabolism , Plant Proteins/physiology , Rosa/metabolism , Alleles , Biosynthetic Pathways , Flowers/genetics , Flowers/metabolism , Odorants , Phenylethyl Alcohol/chemistry , Plant Proteins/genetics , Plant Proteins/metabolism , Quantitative Trait Loci , Rosa/genetics
6.
Science ; 349(6243): 81-3, 2015 Jul 03.
Article in English | MEDLINE | ID: mdl-26138978

ABSTRACT

The scent of roses (Rosa x hybrida) is composed of hundreds of volatile molecules. Monoterpenes represent up to 70% percent of the scent content in some cultivars, such as the Papa Meilland rose. Monoterpene biosynthesis in plants relies on plastid-localized terpene synthases. Combining transcriptomic and genetic approaches, we show that the Nudix hydrolase RhNUDX1, localized in the cytoplasm, is part of a pathway for the biosynthesis of free monoterpene alcohols that contribute to fragrance in roses. The RhNUDX1 protein shows geranyl diphosphate diphosphohydrolase activity in vitro and supports geraniol biosynthesis in planta.


Subject(s)
Monoterpenes/metabolism , Odorants , Plastids/enzymology , Pyrophosphatases/biosynthesis , Rosa/enzymology , Terpenes/metabolism , Volatile Organic Compounds/metabolism , Acyclic Monoterpenes , Molecular Sequence Data , Pyrophosphatases/genetics , Rosa/genetics , Transcriptome , Nudix Hydrolases
7.
New Phytol ; 202(1): 161-173, 2014 Apr.
Article in English | MEDLINE | ID: mdl-24308826

ABSTRACT

FT/TFL1 family members have been known to be involved in the development and flowering in plants. In rose, RoKSN, a TFL1 homologue, is a key regulator of flowering, whose absence causes continuous flowering. Our objectives are to functionally validate RoKSN and to explore its mode of action in rose. We complemented Arabidopsis tfl1 mutants and ectopically expressed RoKSN in a continuous-flowering (CF) rose. Using different protein interaction techniques, we studied RoKSN interactions with RoFD and RoFT and possible competition. In Arabidopsis, RoKSN complemented the tfl1 mutant by rescuing late flowering and indeterminate growth. In CF roses, the ectopic expression of RoKSN led to the absence of flowering. Different branching patterns were observed and some transgenic plants had an increased number of leaflets per leaf. In these transgenic roses, floral activator transcripts decreased. Furthermore, RoKSN was able to interact both with RoFD and the floral activator, RoFT. Protein interaction experiments revealed that RoKSN and RoFT could compete with RoFD for repression and activation of blooming, respectively. We conclude that RoKSN is a floral repressor and is also involved in the vegetative development of rose. RoKSN forms a complex with RoFD and could compete with RoFT for repression of flowering.


Subject(s)
Flowers/growth & development , Plant Proteins/metabolism , Repressor Proteins/metabolism , Rosa/growth & development , Arabidopsis/genetics , Arabidopsis Proteins/genetics , Flowers/physiology , Gene Expression Regulation, Developmental , Gene Expression Regulation, Plant , Genes, Plant/genetics , Genetic Complementation Test , Inflorescence/genetics , Inflorescence/growth & development , Mutation/genetics , Plant Proteins/genetics , Plants, Genetically Modified , RNA, Messenger/genetics , RNA, Messenger/metabolism , Repressor Proteins/genetics , Reproduction , Rosa/genetics
8.
J Exp Bot ; 63(18): 6543-54, 2012 Nov.
Article in English | MEDLINE | ID: mdl-23175671

ABSTRACT

The role of gibberellins (GAs) during floral induction has been widely studied in the annual plant Arabidopsis thaliana. Less is known about this control in perennials. It is thought that GA is a major regulator of flowering in rose. In spring, low GA content may be necessary for floral initiation. GA inhibited flowering in once-flowering roses, whereas GA did not block blooming in continuous-flowering roses. Recently, RoKSN, a homologue of TFL1, was shown to control continuous flowering. The loss of RoKSN function led to continuous flowering behaviour. The objective of this study was to understand the molecular control of flowering by GA and the involvement of RoKSN in this inhibition. In once-flowering rose, the exogenous application of GA(3) in spring inhibited floral initiation. Application of GA(3) during a short period of 1 month, corresponding to the floral transition, was sufficient to inhibit flowering. At the molecular level, RoKSN transcripts were accumulated after GA(3) treatment. In spring, this accumulation is correlated with floral inhibition. Other floral genes such as RoFT, RoSOC1, and RoAP1 were repressed in a RoKSN-dependent pathway, whereas RoLFY and RoFD repression was RoKSN independent. The RoKSN promoter contained GA-responsive cis-elements, whose deletion suppressed the response to GA in a heterologous system. In summer, once-flowering roses did not flower even after exogenous application of a GA synthesis inhibitor that failed to repress RoKSN. A model is presented for the GA inhibition of flowering in spring mediated by the induction of RoKSN. In summer, factors other than GA may control RoKSN.


Subject(s)
Florigen/metabolism , Flowers/genetics , Gene Expression Regulation, Plant/drug effects , Gibberellins/genetics , Rosa/genetics , Agrobacterium tumefaciens/genetics , Florigen/pharmacology , Flowers/growth & development , Flowers/metabolism , Gene Expression Regulation, Developmental/drug effects , Genes, Plant/drug effects , Gibberellins/metabolism , Gibberellins/pharmacology , Green Fluorescent Proteins/metabolism , Microscopy, Confocal , Plants, Genetically Modified/genetics , Plants, Genetically Modified/growth & development , Plants, Genetically Modified/metabolism , Promoter Regions, Genetic/drug effects , RNA, Plant/genetics , RNA, Plant/metabolism , Rosa/growth & development , Rosa/metabolism , Seasons , Sequence Alignment , Sequence Analysis, DNA , Nicotiana/genetics , Up-Regulation
9.
Plant J ; 69(1): 116-25, 2012 Jan.
Article in English | MEDLINE | ID: mdl-21895811

ABSTRACT

Flowering is a key event in plant life, and is finely tuned by environmental and endogenous signals to adapt to different environments. In horticulture, continuous flowering (CF) is a popular trait introduced in a wide range of cultivated varieties. It played an essential role in the tremendous success of modern roses and woodland strawberries in gardens. CF genotypes flower during all favourable seasons, whereas once-flowering (OF) genotypes only flower in spring. Here we show that in rose and strawberry continuous flowering is controlled by orthologous genes of the TERMINAL FLOWER 1 (TFL1) family. In rose, six independent pairs of CF/OF mutants differ in the presence of a retrotransposon in the second intron of the TFL1 homologue. Because of an insertion of the retrotransposon, transcription of the gene is blocked in CF roses and the absence of the floral repressor provokes continuous blooming. In OF-climbing mutants, the retrotransposon has recombined to give an allele bearing only the long terminal repeat element, thus restoring a functional allele. In OF roses, seasonal regulation of the TFL1 homologue may explain the seasonal flowering, with low expression in spring to allow the first bloom. In woodland strawberry, Fragaria vesca, a 2-bp deletion in the coding region of the TFL1 homologue introduces a frame shift and is responsible for CF behaviour. A diversity analysis has revealed that this deletion is always associated with the CF phenotype. Our results demonstrate a new role of TFL1 in perennial plants in maintaining vegetative growth and modifying flowering seasonality.


Subject(s)
Flowers/physiology , Fragaria/physiology , Plant Proteins/genetics , Plant Proteins/metabolism , Rosa/physiology , Arabidopsis Proteins , Gene Expression Regulation, Plant , Genetic Loci , Molecular Sequence Data , Mutation , Phylogeny , RNA, Messenger/metabolism , Retroelements , Seasons
10.
PLoS One ; 6(12): e28455, 2011.
Article in English | MEDLINE | ID: mdl-22194838

ABSTRACT

Cultivated for centuries, the varieties of rose have been selected based on a number of flower traits. Understanding the genetic and molecular basis that contributes to these traits will impact on future improvements for this economically important ornamental plant. In this study, we used scanning electron microscopy and sections of meristems and flowers to establish a precise morphological calendar from early rose flower development stages to senescing flowers. Global gene expression was investigated from floral meristem initiation up to flower senescence in three rose genotypes exhibiting contrasted floral traits including continuous versus once flowering and simple versus double flower architecture, using a newly developed Affymetrix microarray (Rosa1_Affyarray) tool containing sequences representing 4765 unigenes expressed during flower development. Data analyses permitted the identification of genes associated with floral transition, floral organs initiation up to flower senescence. Quantitative real time PCR analyses validated the mRNA accumulation changes observed in microarray hybridizations for a selection of 24 genes expressed at either high or low levels. Our data describe the early flower development stages in Rosa sp, the production of a rose microarray and demonstrate its usefulness and reliability to study gene expression during extensive development phases, from the vegetative meristem to the senescent flower.


Subject(s)
Flowers/growth & development , Flowers/genetics , Genes, Developmental/genetics , Genes, Plant/genetics , Genomics/methods , Rosa/growth & development , Rosa/genetics , Databases, Genetic , Expressed Sequence Tags , Flowers/ultrastructure , Gene Expression Regulation, Developmental , Gene Expression Regulation, Plant , Meristem/genetics , Meristem/growth & development , Meristem/ultrastructure , Molecular Sequence Annotation , Oligonucleotide Array Sequence Analysis , Real-Time Polymerase Chain Reaction , Transcriptome/genetics
11.
Plant Physiol Biochem ; 49(1): 2-8, 2011 Jan.
Article in English | MEDLINE | ID: mdl-20980156

ABSTRACT

Genes induced by a progressive 3 week salt stress (final NaCl concentration 300 mM) were identified in the phloem of celery (Apium graveolens L., cv Vert d'Elne). A subtractive library was constructed and screened for salt-induced, phloem-specific genes. Work was focused on phloem due to its central role in inter-organ exchanges. Three genes were studied in more details, 2 coding for metallothioneins (AgMT2 and AgMT3) and one for a new mannitol transporter (AgMaT3). Expression of a reporter gene in transgenic Arabidopsis under control of promoter of each gene was located in the phloem. pAgMT2 has a typical phloem pattern with slight induction by salt stress. pAgMT3 and pAgMaT3 expression was induced by salt stress, except in minor veins. pAgMaT3 was highly active in stressed roots. The promoters described here could be regarded as new tools for engineering salt-resistant plants.


Subject(s)
Apium/genetics , Gene Expression Regulation, Plant , Genes, Plant , Phloem/genetics , Promoter Regions, Genetic , Salt Tolerance/genetics , Salt-Tolerant Plants/genetics , Apium/metabolism , Arabidopsis/genetics , Arabidopsis/metabolism , Carrier Proteins/genetics , Carrier Proteins/metabolism , Gene Expression , Genes, Reporter , Membrane Proteins/genetics , Membrane Proteins/metabolism , Membrane Transport Proteins , Metallothionein/genetics , Metallothionein/metabolism , Phloem/metabolism , Plant Proteins/genetics , Plant Proteins/metabolism , Plant Roots , Plants, Genetically Modified/metabolism , Salt-Tolerant Plants/metabolism
12.
BMC Plant Biol ; 10: 245, 2010 Nov 12.
Article in English | MEDLINE | ID: mdl-21073695

ABSTRACT

BACKGROUND: In higher plants, sugars are not only nutrients but also important signal molecules. They are distributed through the plant via sugar transporters, which are involved not only in sugar long-distance transport via the loading and the unloading of the conducting complex, but also in sugar allocation into source and sink cells. The availability of the recently released grapevine genome sequence offers the opportunity to identify sucrose and monosaccharide transporter gene families in a woody species and to compare them with those of the herbaceous Arabidopsis thaliana using a phylogenetic analysis. RESULTS: In grapevine, one of the most economically important fruit crop in the world, it appeared that sucrose and monosaccharide transporter genes are present in 4 and 59 loci, respectively and that the monosaccharide transporter family can be divided into 7 subfamilies. Phylogenetic analysis of protein sequences has indicated that orthologs exist between Vitis and Arabidospis. A search for cis-regulatory elements in the promoter sequences of the most characterized transporter gene families (sucrose, hexoses and polyols transporters), has revealed that some of them might probably be regulated by sugars. To profile several genes simultaneously, we created a macroarray bearing cDNA fragments specific to 20 sugar transporter genes. This macroarray analysis has revealed that two hexose (VvHT1, VvHT3), one polyol (VvPMT5) and one sucrose (VvSUC27) transporter genes, are highly expressed in most vegetative organs. The expression of one hexose transporter (VvHT2) and two tonoplastic monosaccharide transporter (VvTMT1, VvTMT2) genes are regulated during berry development. Finally, three putative hexose transporter genes show a preferential organ specificity being highly expressed in seeds (VvHT3, VvHT5), in roots (VvHT2) or in mature leaves (VvHT5). CONCLUSIONS: This study provides an exhaustive survey of sugar transporter genes in Vitis vinifera and revealed that sugar transporter gene families in this woody plant are strongly comparable to those of herbaceous species. Dedicated macroarrays have provided a Vitis sugar transporter genes expression profiling, which will likely contribute to understand their physiological functions in plant and berry development. The present results might also have a significant impact on our knowledge on plant sugar transporters.


Subject(s)
Membrane Transport Proteins/genetics , Monosaccharide Transport Proteins/genetics , Plant Proteins/genetics , Vitis/genetics , Arabidopsis Proteins/classification , Arabidopsis Proteins/genetics , Arabidopsis Proteins/metabolism , Blotting, Northern , Carbohydrates/pharmacology , Gene Expression Profiling , Gene Expression Regulation, Plant/drug effects , Membrane Transport Proteins/classification , Membrane Transport Proteins/metabolism , Monosaccharide Transport Proteins/classification , Monosaccharide Transport Proteins/metabolism , Multigene Family , Oligonucleotide Array Sequence Analysis , Phylogeny , Plant Proteins/classification , Plant Proteins/metabolism , Polymers/metabolism , Promoter Regions, Genetic/genetics , Vitis/metabolism
13.
Plant Physiol ; 145(1): 62-74, 2007 Sep.
Article in English | MEDLINE | ID: mdl-17631523

ABSTRACT

A second mannitol transporter, AgMaT2, was identified in celery (Apium graveolens L. var. dulce), a species that synthesizes and transports mannitol. This transporter was successfully expressed in two different heterologous expression systems: baker's yeast (Saccharomyces cerevisiae) cells and tobacco (Nicotiana tabacum) plants (a non-mannitol-producing species). Data indicated that AgMaT2 works as an H(+)/mannitol cotransporter with a weak selectivity toward other polyol molecules. When expressed in tobacco, AgMaT2 decreased the sensitivity to the mannitol-secreting pathogenic fungi Alternaria longipes, suggesting a role for polyol transporters in defense mechanisms. In celery, in situ hybridization showed that AgMaT2 was expressed in the phloem of leaflets, petioles from young and mature leaves, floral stems, and roots. In the phloem of petioles and leaflets, AgMaT2, as localized with specific antibodies, was present in the plasma membrane of three ontologically related cell types: sieve elements, companion cells, and phloem parenchyma cells. These new data are discussed in relation to the physiological role of AgMaT2 in regulating mannitol fluxes in celery petioles.


Subject(s)
Apium/metabolism , Mannitol/metabolism , Membrane Transport Proteins/metabolism , Phloem/metabolism , Plant Proteins/metabolism , Alternaria/physiology , Apium/cytology , Apium/genetics , Cloning, Molecular , Gene Expression , Membrane Transport Proteins/genetics , Molecular Sequence Data , Phloem/cytology , Plant Diseases , Plant Proteins/genetics , Plants, Genetically Modified/metabolism , Plants, Genetically Modified/microbiology , Saccharomyces cerevisiae/genetics , Saccharomyces cerevisiae/metabolism , Nicotiana/genetics , Nicotiana/metabolism , Nicotiana/microbiology
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