Berbel Tornero, Ana
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Berbel Tornero
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Ana
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- PublicationRegulation of Compound Leaf Development by PHANTASTICA in Medicago truncatula(American Society of Plant Biologists, 2014-01) Ge, Liangfa; Peng, Jianling; Berbel Tornero, Ana; Madueño Albi, Francisco; Chen, Ruijin; Instituto Universitario Mixto de Biología Molecular y Celular de Plantas; National Science Foundation, EEUU; Oklahoma Center for the Advancement of Science and Technology; Generalitat Valenciana[EN] Plant leaves, simple or compound, initiate as peg-like structures from the peripheral zone of the shoot apical meristem, which requires class I KNOTTED-LIKE HOMEOBOXI (KNOXI) transcription factors to maintain its activity. The MYB domain protein encoded by the ASYMMETRIC LEAVES1/ROUGH SHEATH2/PHANTASTICA (ARP) gene, together with other factors, excludes KNOXI gene expression from incipient leaf primordia to initiate leaves and specify leaf adaxial identity. However, the regulatory relationship between ARP and KNOXI is more complex in compound-leafed species. Here, we investigated the role of ARP and KNOXI genes in compound leaf development in Medicago truncatula. We show that the M. truncatula phantastica mutant exhibited severe compound leaf defects, including curling and deep serration of leaf margins, shortened petioles, increased rachises, petioles acquiring motor organ characteristics, and ectopic development of petiolules. On the other hand, the M. truncatula brevipedicellus mutant did not exhibit visible compound leaf defects. Our analyses show that the altered petiole development requires ectopic expression of ELONGATED PETIOLULE1, which encodes a lateral organ boundary domain protein, and that the distal margin serration requires the auxin efflux protein M. truncatula PIN-FORMED10 in the M. truncatula phantastica mutant.
- PublicationChanging the spatial pattern of TFL1 expression reveals its key role in the shoot meristem in controlling Arabidopsis flowering architecture(Oxford University Press (OUP), 2015-08) Baumann, Kim; Venail, Julien; Berbel Tornero, Ana; Domenech Mir, Mª José; Money, Tracy; Conti, Lucio; Hanzawa, Yoshie; Madueño Albi, Francisco; Bradley, Desmond; Instituto Universitario Mixto de Biología Molecular y Celular de Plantas; Ministerio de Ciencia e Innovación; Biotechnology and Biological Sciences Research Council, Reino UnidoModels for the control of above-ground plant architectures show how meristems can be programmed to be either shoots or flowers. Molecular, genetic, transgenic, and mathematical studies have greatly refined these models, suggesting that the phase of the shoot reflects different genes contributing to its repression of flowering, its vegetativeness (‘veg’), before activators promote flower development. Key elements of how the repressor of flowering and shoot meristem gene TFL1 acts have now been tested, by changing its spatiotemporal pattern. It is shown that TFL1 can act outside of its normal expression domain in leaf primordia or floral meristems to repress flower identity. These data show how the timing and spatial pattern of TFL1 expression affect overall plant architecture. This reveals that the underlying pattern of TFL1 interactors is complex and that they may be spatially more widespread than TFL1 itself, which is confined to shoots. However, the data show that while TFL1 and floral genes can both act and compete in the same meristem, it appears that the main shoot meristem is more sensitive to TFL1 rather than floral genes. This spatial analysis therefore reveals how a difference in response helps maintain the ‘veg’ state of the shoot meristem.
- PublicationArabidopsis thaliana SHOOT MERISTEMLESS Substitutes for Medicago truncatula SINGLE LEAFLET1 to Form Complex Leaves and Petals(MDPI AG, 2022-11) Pautot, Véronique; Berbel Tornero, Ana; Cayla, Thibaud; Eschstruth, Alexis; Adroher, Bernard; Ratet, Pascal; Madueño Albi, Francisco; Laufs, Patrick; Instituto Universitario Mixto de Biología Molecular y Celular de Plantas; Agencia Estatal de Investigación; European Regional Development Fund; Ministerio de Economía y Competitividad; Agence Nationale de la Recherche, Francia[EN] LEAFY plant-specific transcription factors, which are key regulators of flower meristem identity and floral patterning, also contribute to meristem activity. Notably, in some legumes, LFY orthologs such as Medicago truncatula SINGLE LEAFLET (SGL1) are essential in maintaining an undifferentiated and proliferating fate required for leaflet formation. This function contrasts with most other species, in which leaf dissection depends on the reactivation of KNOTTED-like class I homeobox genes (KNOXI). KNOXI and SGL1 genes appear to induce leaf complexity through conserved downstream genes such as the meristematic and boundary CUP-SHAPED COTYLEDON genes. Here, we compare in M. truncatula the function of SGL1 with that of the Arabidopsis thaliana KNOXI gene, SHOOT MERISTEMLESS (AtSTM). Our data show that AtSTM can substitute for SGL1 to form complex leaves when ectopically expressed in M. truncatula. The shared function between AtSTM and SGL1 extended to the major contribution of SGL1 during floral development as ectopic AtSTM expression could promote floral organ identity gene expression in sgl1 flowers and restore sepal shape and petal formation. Together, our work reveals a function for AtSTM in floral organ identity and a higher level of interchangeability between meristematic and floral identity functions for the AtSTM and SGL1 transcription factors than previously thought.
- PublicationAUXIN RESPONSE FACTOR3 Regulates Compound Leaf Patterning by Directly Repressing PALMATE-LIKE PENTAFOLIATA1 Expression in Medicago truncatula(Frontiers Media SA, 2017-09-20) Peng, Jianling; Berbel Tornero, Ana; Madueño Albi, Francisco; Chen, Rujin; Instituto Universitario Mixto de Biología Molecular y Celular de Plantas; Generalitat Valenciana; Samuel Roberts Noble Foundation; National Science Foundation, EEUU; European Regional Development Fund; Ministerio de Economía y Competitividad; Oklahoma Center for the Advancement of Science and Technology[EN] Diverse leaf forms can be seen in nature. In Medicago truncatula, PALM1 encoding a Cys(2) His(2) transcription factor is a key regulator of compound leaf patterning. PALM1 negatively regulates expression of SGL1, a key regulator of lateral leaflet initiation. However, how PALM1 itself is regulated is not yet known. To answer this question, we used promoter sequence analysis, yeast one-hybrid tests, quantitative transcription activity assays, ChIP-PCR analysis, and phenotypic analyses of overexpression lines and mutant plants. The results show that M. truncatula AUXIN RESPONSE FACTOR3 (MtARF3) functions as a direct transcriptional repressor of PALM1. MtARF3 physically binds to the PALM1 promoter sequence in yeast cells. MtARF3 selectively interacts with specific auxin response elements (AuxREs) in the PALM1 promoter to repress reporter gene expression in tobacco leaves and binds to specific sequences in the PALM1 promoter in vivo. Upregulation of MtARF3 or removal of both PHANTASTICA (PHAN) and ARGONAUTE7 (AGO7) pathways resulted in compound leaves with five narrow leaflets arranged in a palmate-like configuration. These results support that MtARF3, in addition as an adaxial-abaxial polarity regulator, functions to restrict spatiotemporal expression of PALM1, linking auxin signaling to compound leaf patterning in the legume plant M. truncatula.
- PublicationGenetic control of inflorescence architecture in legumes(Frontiers Media, 2015-07-21) Benlloch, Reyes; Berbel Tornero, Ana; Ali, Latifeh; Gohari, Gholamreza; Millán, Teresa; Madueño Albi, Francisco; Instituto Universitario Mixto de Biología Molecular y Celular de Plantas; European Commission; Ministerio de Economía y Competitividad; Generalitat Valenciana; European Regional Development Fund; Ministry of Higher Education, Siria[EN] The architecture of the inflorescence, the shoot system that bears the flowers, is a main component of the huge diversity of forms found in flowering plants. Inflorescence architecture has also a strong impact on the production of fruits and seeds, and on crop management, two highly relevant agronomical traits. Elucidating the genetic networks that control inflorescence development, and how they vary between different species, is essential to understanding the evolution of plant form and to being able to breed key architectural traits in crop species. Inflorescence architecture depends on the identity and activity of the meristems in the inflorescence apex, which determines when flowers are formed, how many are produced and their relative position in the inflorescence axis. Arabidopsis thaliana, where the genetic control of inflorescence development is best known, has a simple inflorescence, where the primary inflorescence meristem directly produces the flowers, which are thus borne in the main inflorescence axis. In contrast, legumes represent a more complex inflorescence type, the compound inflorescence, where flowers are not directly borne in the main inflorescence axis but, instead, they are formed by secondary or higher order inflorescence meristems. Studies in model legumes such as pea (Pisum sativum) or Medicago truncatula have led to a rather good knowledge of the genetic control of the development of the legume compound inflorescence. In addition, the increasing availability of genetic and genomic tools for legumes is allowing to rapidly extending this knowledge to other grain legume crops. This review aims to describe the current knowledge of the genetic network controlling inflorescence development in legumes. It also discusses how the combination of this knowledge with the use of emerging genomic tools and resources may allow rapid advances in the breeding of grain legume crops.
- PublicationPea VEGETATIVE2 Is an FD Homolog That Is Essential for Flowering and Compound Inflorescence Development(American Society of Plant Biologists, 2015-04) Sussmilch, FC; Berbel Tornero, Ana; Hecht, V; Vander, JK; Ferrandiz Maestre, Cristina; Madueño Albi, Francisco; Weller, JL; Instituto Universitario Mixto de Biología Molecular y Celular de Plantas; Australian Research Council; Ministerio de Ciencia e Innovación[EN] As knowledge of the gene networks regulating inflorescence development in Arabidopsis thaliana improves, the current challenge is to characterize this system in different groups of crop species with different inflorescence architecture. Pea (Pisum sativum) has served as a model for development of the compound raceme, characteristic of many legume species, and in this study, we characterize the pea VEGETATIVE2 (VEG2) locus, showing that it is critical for regulation of flowering and inflorescence development and identifying it as a homolog of the bZIP transcription factor FD. Through detailed phenotypic characterizations of veg2 mutants, expression analyses, and the use of protein-protein interaction assays, we find that VEG2 has important roles during each stage of development of the pea compound inflorescence. Our results suggest that VEG2 acts in conjunction with multiple FLOWERING LOCUS T (FT) proteins to regulate expression of downstream target genes, including TERMINAL FLOWER1, LEAFY, and MADS box homologs, and to facilitate cross-regulation within the FT gene family. These findings further extend our understanding of the mechanisms underlying compound inflorescence development in pea and may have wider implications for future manipulation of inflorescence architecture in related legume crop species.
- PublicationFunctional characterization of AGAMOUS-subfamily members from cotton during reproductive development and in response to plant hormones(Springer-Verlag, 2017) Menezes, S.; Artico, S.; Lima, C.; Muniz, S.; Berbel Tornero, Ana; Brilhante, O.; Grossi, M.F.; Ferrandiz Maestre, Cristina; Madueño Albi, Francisco; Alves, M.; Instituto Universitario Mixto de Biología Molecular y Celular de Plantas; European Commission[EN] Reproductive development in cotton, including the fruit and fiber formation, is a complex process; it involves the coordinated action of gene expression regulators, and it is highly influenced by plant hormones. Several studies have reported the identification and expression of the transcription factor family MADS-box members in cotton ovules and fibers; however, their roles are still elusive during the reproductive development in cotton. In this study, we evaluated the expression profiles of five MADS-box genes (GhMADS3, GhMADS4, GhMADS5, GhMADS6 and GhMADS7) belonging to the AGAMOUS-subfamily in Gossypium hirsutum. Phylogenetic and protein sequence analyses were performed using diploid (G. arboreum, G. raimondii) and tetraploid (G. barbadense, G. hirsutum) cotton genomes, as well as the AG-subfamily members from Arabidopsis thaliana, Petunia hybrida and Antirrhinum majus. qPCR analysis showed that the AG-subfamily genes had high expression during flower and fruit development in G. hirsutum. In situ hybridization analysis also substantiates the involvement of AG-subfamily members on reproductive tissues of G. hirsutum, including ovule and ovary. The effect of plant hormones on AG-subfamily genes expression was verified in cotton fruits treated with gibberellin, auxin and brassinosteroid. All the genes were significantly regulated in response to auxin, whereas only GhMADS3, GhMADS4 and GhMADS7 genes were also regulated by brassinosteroid treatment. In addition, we have investigated the GhMADS3 and GhMADS4 overexpression effects in Arabidopsis plants. Interestingly, the transgenic plants from both cotton AG-like genes in Arabidopsis significantly altered the fruit size compared to the control plants. This alteration suggests that cotton AG-like genes might act regulating fruit formation. Our results demonstrate that members of the AG-subfamily in G. hirsutum present a conserved expression profile during flower development, but also demonstrate their expression during fruit development and in response to phytohormones.
- PublicationLotus japonicus NOOT-BOP-COCH-LIKE1 is essential for nodule, nectary, leaf and flower development(Blackwell Publishing, 2018-06) Magne, K.; George, J.; Berbel Tornero, Ana; Broquet, B.; Madueño Albi, Francisco; Andersen, S.; Ratet, P.; Instituto Universitario Mixto de Biología Molecular y Celular de Plantas; Agence Nationale de la Recherche, Francia; Centre National de la Recherche Scientifique, Francia[EN] The NOOT-BOP-COCH-LIKE (NBCL) genes are orthologs of Arabidopsis thaliana BLADE-ON-PETIOLE1/2. The NBCLs are developmental regulators essential for plant shaping, mainly through the regulation of organ boundaries, the promotion of lateral organ differentiation and the acquisition of organ identity. In addition to their roles in leaf, stipule and flower development, NBCLs are required for maintaining the identity of indeterminate nitrogen-fixing nodules with persistent meristems in legumes. In legumes forming determinate nodules, without persistent meristem, the roles of NBCL genes are not known. We thus investigated the role of Lotus japonicus NOOT-BOP-COCH-LIKE1 (LjNBCL1) in determinate nodule identity and studied its functions in aerial organ development using LORE1 insertional mutants and RNA interference-mediated silencing approaches. In Lotus, LjNBCL1 is involved in leaf patterning and participates in the regulation of axillary outgrowth. Wild-type Lotus leaves are composed of five leaflets and possess a pair of nectaries at the leaf axil. Legumes such as pea and Medicago have a pair of stipules, rather than nectaries, at the base of their leaves. In Ljnbcl1, nectary development is abolished, demonstrating that nectaries and stipules share a common evolutionary origin. In addition, ectopic roots arising from nodule vascular meristems and reorganization of the nodule vascular bundle vessels were observed on Ljnbcl1 nodules. This demonstrates that NBCL functions are conserved in both indeterminate and determinate nodules through the maintenance of nodule vascular bundle identity. In contrast to its role in floral patterning described in other plants, LjNBCL1 appears essential for the development of both secondary inflorescence meristem and floral meristem.
- PublicationThe SINGLE FLOWER (SFL) gene encodes a MYB transcription factor that regulates the number of flowers produced by the inflorescence of chickpea(Blackwell Publishing, 2022-05) Caballo, Cristina; Berbel Tornero, Ana; Ortega, Raúl; Gil, Juan; Millán, Teresa; Rubio, Josefa; Madueño Albi, Francisco; Instituto Universitario Mixto de Biología Molecular y Celular de Plantas; Generalitat Valenciana; Agencia Estatal de Investigación; European Regional Development Fund; Ministerio de Economía y Competitividad; Instituto Nacional de Investigaciones Agrarias[EN] Legumes usually have compound inflorescences, where flowers/pods develop from secondary inflorescences (I2), formed laterally at the primary inflorescence (I1). Number of flowers per I2, characteristic of each legume species, has important ecological and evolutionary relevance as it determines diversity in inflorescence architecture; moreover, it is also agronomically important for its potential impact on yield. Nevertheless, the genetic network controlling the number of flowers per I2 is virtually unknown. Chickpea (Cicer arietinum) typically produces one flower per I2 but single flower (sfl) mutants produce two (double-pod phenotype). We isolated the SFL gene by mapping the sfl-d mutation and identifying and characterising a second mutant allele. We analysed the effect of sfl on chickpea inflorescence ontogeny with scanning electron microscopy and studied the expression of SFL and meristem identity genes by RNA in situ hybridisation. We show that SFL corresponds to CaRAX1/2a, which codes a MYB transcription factor specifically expressed in the I2 meristem. Our findings reveal SFL as a central factor controlling chickpea inflorescence architecture, acting in the I2 meristem to regulate the length of the period for which it remains active, and therefore determining the number of floral meristems that it can produce.
- PublicationVEGETATIVE1 is essential for development of the compound inflorescence in pea(Nature Publishing Group, 2012-04) Berbel Tornero, Ana; Ferrandiz Maestre, Cristina; Hecht, Valerie; Dalmais, Marion; Lund, Ole S.; Sussmilch, Frances C; Taylor, Scott A.; Bendahmane, Abdelhafid; Ellis, T. H. Noel; Beltran Porter, Jose Pio; Weller, James L.; Madueño Albi, Francisco; Instituto Universitario Mixto de Biología Molecular y Celular de Plantas; Ministerio de Ciencia e Innovación; Australian Research Council; European Commission; Generalitat Valenciana[EN] Unravelling the basis of variation in inflorescence architecture is important to understanding how the huge diversity in plant form has been generated. Inflorescences are divided between simple, as in Arabidopsis, with flowers directly formed at the main primary inflorescence axis, and compound, as in legumes, where they are formed at secondary or even higher order axes. The formation of secondary inflorescences predicts a novel genetic function in the development of the compound inflorescences. Here we show that in pea this function is controlled by VEGETATIVE1 (VEG1), whose mutation replaces secondary inflorescences by vegetative branches. We identify VEG1 as an AGL79-like MADS-box gene that specifies secondary inflorescence meristem identity. VEG1 misexpression in meristem identity mutants causes ectopic secondary inflorescence formation, suggesting a model for compound inflorescence development based on antagonistic interactions between VEG1 and genes conferring primary inflorescence and floral identity. Our study defines a novel mechanism to generate inflorescence complexity.