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First published online July 9, 2004; 10.1104/pp.104.040832 Plant Physiology 135:1491-1501 (2004) © 2004 American Society of Plant Biologists Floral Meristem Identity Genes Are Expressed during Tendril Development in Grapevine1Departamento de Biotecnología, Escuela Técnica Superior Ingenieros Agrónomos, Universidad Politécnica de Madrid, 28040 Madrid, Spain (M.C., M.J.C.); Departamento de Genética Molecular de Plantas, Centro Nacional de Biotecnología, Consejo Superior de Investigaciones Científicas, Campus de la Universidad Autónoma de Madrid, Cantoblanco, 28049 Madrid, Spain (P.C., J.M.M.-Z.); and Departamento de Biotecnología, Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria, 28040 Madrid, Spain (J.M.M.-Z.)
To study the early steps of flower initiation and development in grapevine (Vitis vinifera), we have isolated two MADS-box genes, VFUL-L and VAP1, the putative FUL-like and AP1 grapevine orthologs, and analyzed their expression patterns during vegetative and reproductive development. Both genes are expressed in lateral meristems that, in grapevine, can give rise to either inflorescences or tendrils. They are also coexpressed in inflorescence and flower meristems. During flower development, VFUL-L transcripts are restricted to the central part of young flower meristems and, later, to the prospective carpel-forming region, which is consistent with a role of this gene in floral transition and carpel and fruit development. Expression pattern of VAP1 suggests that it may play a role in flowering transition and flower development. However, its lack of expression in sepal primordia, does not support its role as an A-function gene in grapevine. Neither VFUL-L nor VAP1 expression was detected in vegetative organs such as leaves or roots. In contrast, they are expressed throughout tendril development. Transcription of both genes in tendrils of very young plants that have not undergone flowering transition indicates that this expression is independent of the flowering process. These unique expression patterns of genes typically involved in reproductive development have implications on our understanding of flower induction and initiation in grapevine, on the origin of grapevine tendrils and on the functional roles of AP1-and FUL-like genes in plant development. These results also provide molecular support to the hypothesis that Vitis tendrils are modified reproductive organs adapted to climb.
The early phases of reproductive development and flower formation have been well characterized in the herbaceous model plants Arabidopsis and Antirrhinum majus (Egea-Cortines and Davies, 2000  ; Theissen, 2001; Mouradov et al., 2002; Simpson and Dean, 2002). In Arabidopsis, transition to flowering is dependent on the activity of floral meristem identity genes such as LEAFY (LFY), FRUITFULL (FUL), APETALA1 (AP1), and CAULIFLOWER (CAL; for review, see Pidkowich et al., 1999; Simpson et al., 1999; Kieffer and Davies, 2001; Zik and Irish, 2003). LFY expression in lateral meristems seems to be responsible for their acquisition of flower meristem identity (Blázquez et al., 1997). FUL, CAL, and AP1 are closely related MADS-box genes that belong to the SQUAMOSA (SQUA) gene subfamily, also called AP1/FUL gene lineage (Theissen et al., 2000; Becker and Theissen, 2003; Litt and Irish, 2003). Together with LFY, they play functionally redundant roles in the control of flower meristem identity (Mandel et al., 1992; Weigel et al., 1992; Mandel and Yanofsky, 1995; Liljegren et al., 1999; Ratcliffe et al. 1999; Ferrándiz et al., 2000). In Arabidopsis, the patterns of expression of these genes relate well with their proposed function. FUL is up-regulated in the shoot apical meristem (SAM) around the transition to flowering and before the initiation of flower meristems. LFY and AP1 are expressed in emerging flower meristems, while FUL is soon excluded from this region (Weigel et al., 1992; Mandel and Yanofsky, 1995). Apart from their function as floral meristem identity genes, AP1 and FUL also seem to play roles as organ identity genes at later stages of flower development. AP1 was initially defined as a class A gene involved in sepal and petal identity (Irish and Sussex, 1990; Coen and Meyerowitz, 1991; Theissen, 2001). FUL has been shown to play a role in carpel and fruit development that affects valve, replum, and style morphology (Gu et al., 1998; Ferrándiz et al., 2000).
Genetic and molecular characterization of the flowering process in different species reveals a conservation of the basic genetic mechanisms controlling the early stages of flower formation (Theissen and Saedler, 1999
We are studying the reproductive biology of grapevine (Vitis vinifera), a woody perennial vine with a pattern of organ formation and development quite distinct to those previously described for annual herbaceous plants (Mullins et al., 1992
In temperate regions, grapevine requires two consecutive growing seasons to flower. A rise in light intensity and temperature seems to be required to promote flowering (Butrosse, 1974
Because of its particular developmental features, we are interested in the process of flower initiation in grapevine. Furthermore, grapevine belongs to the Vitaceae, a basal family of core eudicots (Judd et al. 1999
Isolation of Grapevine FUL- and AP1-Like Genes
Genes belonging to the SQUA subfamily of MADS-box transcription factors were isolated using a 3'/5'RACE strategy. Two different cDNA types were identified. One of them (GenBank accession no. AY538747) contained an ORF of 741 bp preceded by a 5'-untranslated region of 83 bp. The 3'-untranslated region showed length heterogeneity, with four polyadenylation sites at positions 910, 997, 1012, and 1029 bp. The other cDNA type (GenBank accession no. AY538746) contained an ORF of 723 bp and the 5'-untranslated region was 166 bp in length. Two polyadenylation sites at positions 1058 and 1075 were detected in its 3'-untranslated region. The encoded MADS-box proteins (247 and 241 amino acids, respectively) aligned well with those from the SQUA subfamily (Fig. 1, A and B) based on sequence conservation in the I-region, which is typical for each MADS-box subfamily (Fig. 1, A and B, continuous line; Elo et al., 2001
Recent phylogenetic analyses have identified two clades of FUL-like genes in core eudicots, euFUL and FUL-like (Litt and Irish, 2003 ). To determine the evolutionary relationships between proteins encoded by the isolated grapevine genes and other core eudicots MADS-box proteins of the SQUA subfamily, a phylogenetic tree was constructed using the complete predicted protein sequences (Fig. 1C). This analysis grouped the grapevine genes within the FUL-like and the euAP1 clades, respectively (Fig. 1C), for what we refer to as VFUL-L and VAP1, respectively. The existence of a putative euFUL gene cannot be ruled out with our experimental approach.
The temporal and spatial expression patterns of VFUL-L and VAP1 were analyzed in buds collected during two consecutive years and in developing and mature reproductive structures (Figs. 2 and 3, see "Materials and Methods" and Carmona et al., 2002
In buds, the RNA levels of VFUL-L and VAP1 were analyzed by RNA-blot hybridization experiments (Fig. 2A). Transcripts of VFUL-L and VAP1 were barely detected in buds of the first season (Fig. 2A, latent buds) and in dormant buds (Fig. 2A, dormancy). During the first season, the SAM produces lateral meristems that generate inflorescence meristems. During the second season, expression of VFUL-L and VAP1 was already detectable in winter buds (end of stage A). The expression of the two transcripts increased significantly in swelling buds (stage B) and decreased in sprouting buds when shoots were beginning to grow out (stage C, Fig. 2A, second season). During stages A, B, and C of the second season, inflorescence meristems divide to generate additional branch inflorescence meristems, which give rise to flower meristems and flowers. Expression of both genes was also analyzed in developing inflorescences, berries, and seeds of the growing shoots (Fig. 2B). During inflorescence development, the expression patterns of VFUL-L and VAP1 were very similar, but the levels of VFUL-L transcripts were higher than those of VAP1. Transcripts were detected during flower development (Fig. 2B, stages E-H40). VFUL-L levels were particularly high during stage H when carpel development takes place (Fig. 2B, H25 and H40). The expression of the two genes decreased in mature flowers (Fig. 2B, stages H50 and I). VAP1 expression was not detected during fruit formation and maturation (Fig. 2B, berries and seeds). However, VFUL-L transcripts were detected during stage I of berry development. This expression decreased at stage II and disappeared as the ripening of the berry progressed (stage III). VFUL-L transcripts were not detected in seeds. To determine the spatial distribution of VAP1 and VFUL-L transcripts at different stages of reproductive development, we carried out in situ hybridization experiments (Fig. 3). The expression patterns of both genes were very similar during the first season when inflorescence meristems are forming (VAP1, Fig. 3, A–C, VFUL-L, not shown), but they diverged during the second season when flower initiation and development takes place (Fig. 3, D–I). In the first season, VAP1 and VFUL-L were detected from the earliest stages of inflorescence development (Fig. 3, A and B). At later stages, VAP1 and VFUL-L were strongly expressed in the inflorescence branch meristems but not in their subtending bracts (Fig. 3C). In the second season, when flower meristems were initiated, VAP1 and VFUL-L expression patterns diverged. VAP1 was broadly expressed in the newly formed flower meristems (Fig. 3D). As soon as sepal primordia began to grow, VAP1 was excluded from the sepal-forming region and became restricted to the inner part of the meristem that forms the petals, stamens, and carpels (Fig. 3D). Later, when petals and stamen primordia were visible, VAP1 mRNA preferentially accumulated at the tips of these growing primordia (Fig. 3, E and F) and then became mainly restricted to the carpel-forming region (Fig. 3F). On the other hand, VFUL-L was expressed in a small area of the central part of the meristem already in very young floral meristems, (Fig. 3G). During floral organ formation, VFUL-L was not detected in sepal, petal, or stamen primordia but was confined to the prospective carpel-forming region (Fig. 3, H and I).
Gene expression was also analyzed during vegetative development by RNA-blot hybridization. VFUL-L and VAP1 transcripts were not detected in the vegetative apices, leaves, or shoots at different stages of cane development (E, G, H50, and I) nor in roots of in vitro grown plants (data not shown). However, high levels of both transcripts were observed in tendrils. To further investigate this expression, three regions were distinguished in tendrils: the hypoclade (h) or basal zone, the branching zone (b) where the hypoclade splits in two arms, and the inner and outer arms (a). First, we analyzed the transcription of both genes in the arms of five consecutive developing tendrils nearest to the shoot apex (Fig. 4, T1–T5a). VFUL-L and VAP1 mRNAs were detected in all five tendrils with highest levels of expression in the most developed one (T5a). Then, we studied the spatial expression of VFUL-L and VAP1 in the three regions of tendril 5 (T5): arms (T5a), branching zone (T5b), and hypoclade (T5h). Expression of VFUL-L was high in the three tendril zones, while that of VAP1 was high in the arms, low in the branching zone, and undetectable in the hypoclade.
In situ hybridization experiments confirmed the results obtained by RNA-blot hybridizations. VFUL-L and VAP1 genes were expressed all along tendril development (Fig. 5). VFUL-L and VAP1 were expressed in the lateral meristem as soon as it became distinguishable in the periphery of the SAM (Fig. 5A for VFUL-L, VAP1 not shown). Both genes continued to be expressed throughout tendril development in different spatial patterns. VFUL-L was detected in all the regions of the developing tendrils (Fig. 5, B and C), whereas VAP1 expression was restricted to the tendril arms (Fig. 5, E and F). Transcripts accumulated in the parenchyma but not in the vascular tissues.
In Arabidopsis and in other herbaceous and woody species, expression of AP1-and FUL-like genes has been associated with developing reproductive structures. Detection of their grapevine homologs in tendrils, considered to be vegetative climbing structures, raised the question of whether this was a consequence of the maintenance, in tendrils, of an expression induced in inflorescences upon flowering. This could reflect the homology between tendrils and inflorescences, but it might not have a functional relevance. Alternatively, this expression could be independent of the flowering process and have a role on its own. To test whether VFUL-L and VAP1 expression in tendrils was related to the reproductive state of the plant, we analyzed their expression in the earliest formed tendrils of young plants that had not undergone flowering induction. Expression of both genes was already detected in the first formed tendril of plants grown from seeds that would still grow vegetatively for 2 to 5 more years before initiating flowering (Fig. 4, TJ). This indicates that this expression is not dependent on flowering induction but is specifically associated to tendril development. Other genes involved in the flowering process such as VFL (Carmona et al., 2002 ) or VSOC1, the putative ortholog of SOC1 (Samach et al., 2000), were not expressed at this early stage (data not shown), indicating that these expression patterns were not common to all genes involved in flowering initiation but typical of VFUL-L and VAP1.
We have isolated and characterized two grapevine MADS-box genes belonging to the SQUA subfamily or AP1/FUL gene lineage (Theissen et al., 2000 ; Becker and Theissen, 2003; Litt and Irish, 2003). Conservation of typical protein motifs in the deduced proteins grouped them as members of the FUL-like and AP1/SQUA (euAP1) gene clades, and consequently they were named as VFUL-L and VAP1. In spite of some peculiarities, their expression patterns also support that they are the putative orthologs of previously described FUL-like and AP1-like genes in other plant species.
VFUL-L and VAP1 expression in grapevine is related to reproductive development and spans two growing seasons as previously described for VFL (Carmona et al., 2002
VFUL-L and VAP1 are initially coexpressed in lateral meristems and are maintained at high levels in their derived structures. Coexpression of VFUL-L and VAP1 is in contrast to what has been found in herbaceous species like Arabidopsis and Antirrhinum where AP1-and FUL-like genes display mutually excluding spatial patterns of expression. AP1 and SQUA are specifically expressed in floral meristems (Huijser et al., 1992
During flower development, expression patterns of VFUL-L and VAP1 are not coincident. Very early, expression of VFUL-L becomes restricted to the carpel-forming region at the central part of the flower meristem and continues to be expressed at high levels through the early stages of fruit development. This expression pattern suggests that VFUL-L may play a role in carpel and fruit development in a similar way to what has been described for euFUL in Arabidopsis (Mandel and Yanofsky, 1995
The strong and distinctive expression of VFUL-L and VAP1 in developing tendrils and the fact that their expression is independent of the flowering induction suggest a relevant role of these genes in tendril development. This could represent a novel role for these genes that would have been recruited for the development of tendrils in Vitis. Examples of gene recruitment to carry out different developmental functions have been previously described. For instance, UNIFOLIATA (UNI) and PEA FIMBRIATA (PEAFIM), the pea orthologs of Arabidopsis LEAFY and UNUSUAL FLORAL ORGANS, do not only participate in flower initiation and development in pea but are also required for the development of its compound leaves (Gourlay et al., 2000
Transition from juvenile to adult phase in grapevine is marked by the initiation of lateral meristems at the flanks of the SAM. In vegetative growing plants, these structures differentiate as tendrils. However, upon flowering induction, several consecutive lateral meristems generate inflorescence meristems. Which are the genetic bases of this pattern of growth in which equivalent primordia give rise to either reproductive (inflorescence) or vegetative (tendril) structures? We have shown that VFUL-L and VAP1 as well as VFL (Carmona et al., 2002
Plant Material Grapevine (Vitis vinifera L. var Tempranillo) samples were collected in the fields of Instituto Madrileño de Investigaciones Agrarias (Alcalá de Henares, Madrid). RNA-blot and in situ hybridization analyses were performed on plant materials collected and fixed at different developmental stages during two growing seasons.
Cloning of VFUL-L and VAP1 was performed using a 3'/5'-RACE strategy (Frohman et al., 1988
To generate a phylogenetic tree, predicted proteins were aligned with ClustalW. Using this original data set, 100 data sets were generated by bootstrap resampling using SEQBOOT program. Distance matrices were made for each bootstrap data set using the PRODIST program-Dayhoff PAM matrix algorithm. The distance matrices obtained were used to construct 100 unrooted trees by the neighbor-joining method using the NEIGHBOR program. A consensus tree was obtained using CONSENSE. SEQBOOT, PROTDIST, NEIGHBOR, and CONSENSE programs belong to the PHYLIP program (Phylogeny Inference Package, version 3.57c, Department of Genetics, University of Washington, Seattle). Arabidopsis SEP1, SEP2, and SEP3 (Pélaz et al., 2000
Plant material was collected from organs and tissues at different developmental stages (phenological stages A–I; Baggiolini, 1952
In situ hybridizations were carried out on plant tissue collected and fixed during two growing seasons at the developmental stages described above. Late stages of flower and fruit development could not be analyzed by this method due to the high levels of background obtained in this plant material. Digoxigenin labeling of RNA probes, tissue preparation, and hybridization were performed as described by Coen et al. (1990) Sequence data from this article have been deposited with the EMBL/GenBank data libraries under accession numbers AY538747 and AY538746.
We thank Félix Cabello and the Instituto Madrileño de Investigaciones Agrarias (Alcalá de Henares, Madrid) for providing plant material for this research, Gemma Bravo and Elena González for excellent technical assistance, Leonor Ruíz-Garcia for providing material from young grapevine plants, and two anonymous reviewers for their suggestions and constructive criticism. Received February 13, 2004; returned for revision April 21, 2004; accepted April 26, 2004.
1 This work was supported by the Comunidad Autónoma de Madrid (grant no. 07G–0046–2000 and a postdoctoral fellowship to M.C.) and by Ministerio de Ciencia y Tecnología (grant no. BIO2001–3891–C02–02). Support to research activity at Centro Nacional de Biotecnología is provided through a specific agreement of Consejo Superior de Investigaciones Científicas-Instituto Nacional de Investigacion y Tecnologia Agraria y Alimentaria.  Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.104.040832. * Corresponding author; e-mail carmona{at}bit.etsia.upm.es; fax 34–913365757.
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