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Citrus Biotechnology

Citrus Biotechnology

Research line: Biotechnology and Plant Breeding of Cultivated Species

Citrus Biotechnology

Research line: Biotechnology and Plant Breeding of Cultivated Species

Citrus Biotechnology
  • Research
  • Staff
  • Publications
  • Projects
  • Other publications
  • Patent

Research

CITRUS BIOTECHNOLOGY

Our group’s research activity focuses on the use of biotechnology to address major challenges of interest to the citrus industry, such as the persistent demand from growers and the industry to obtain citrus varieties resistant to emerging diseases that are severely affecting citrus production worldwide, including Huanglongbing (HLB) and citrus black spot.

Another of the group’s research lines aims to increase the content of specific micronutrients or health-promoting phytochemicals in citrus fruits, with the goal of enhancing their nutraceutical properties. In doing so, we aim to develop new varieties that meet current demands in the citrus sector, while also serving as tools to expand our understanding of the roles played by volatile terpenes, flavonoids, and carotenoids in citrus fruit interactions with the biotic environment.

A more recent research line seeks to determine the role of terpenes present in orange peel in relation to frugivorous animals/fruit consumers, and how these interactions affect citrus seed dispersal in natural environments. The main research lines of the Citrus Biotechnology Group include:

• Development of citrus varieties that are repellent or resistant to major insect vectors and pathogens such as *Diaphorina citri* (vector of the bacterium causing HLB), *Phyllosticta citricarpa* (causal agent of citrus black spot), and *Xanthomonas citri* subsp. *citri* (causal agent of citrus canker), among others.

• Adding value to citrus fruits by increasing the accumulation of health-promoting compounds such as carotenoids and anthocyanins, as well as cloning and characterizing fruit-specific citrus promoters for biotechnological applications.

• Modulation of vegetative development for the generation of dwarfing rootstocks. Induction of early flowering/fruiting in juvenile plants as a biotechnological tool for the rapid analysis of flower and fruit improvement traits.

• Studies on fruit consumption by animals, seed dispersal, and the potential naturalization of transgenic citrus under field conditions.

Staff

Publications

  • Rodrigo, MJ; Lado, J., Alós, E., Alquézar, B., Dery, O., Hirschberg, J., Zacarías, L (2019)
    A mutant allele of ζ-carotene isomerase (ZISO) is associated with the yellow pigmentation of the “Pinalate” sweet orange mutant and reveals new insights into its role in fruit carotenogenesis

    BMC Plant Biology 19:465

  • Ruiz-Ruiz, S., Navarro, B., PEÑA, L., Navarro, L., Moreno, P., Di Serio, F., Flores, R (2019)
    Citrus Tristeza Virus: Host RNA Silencing and Virus Counteraction. Citrus Tristeza Virus: Methods and Protocols

    Methods in Molecular Biology 2015: 195-207

  • Soler, N., Plomer, M., Fagoaga, C., Moreno, P., Navarro, L., Flores, R. and PEÑA, L (2019)
    Methods for producing transgenic plants resistant to CTV. Citrus Tristeza Virus: Methods and Protocols

    Methods in Molecular Biology 2015: 229-243

  • Cifuentes-Arenas, J.C., Beattie, G.A.C., Peña, L., Lopes, S.A (2019)
    Murraya paniculata and Swinglea glutinosa as short-term transient hosts of ‘Candidatus Liberibacter asiaticus’ and implications for spread of Huanglongbing.

    Phytopathology

  • Caland, R.B.O., Cadavid, C.O.M., Carmona, L., PEÑA, L., Oliveira, R.P (2019)
    Pasteurized orange juice rich in carotenoids protects Caenorhabditis elegans against oxidative stress and β-amyloid toxicity through direct and indirect mechanisms

    Oxidative Medicine and Cellular Longevity. Article ID 5046280,

  • Carmona, L., Alquézar, B., Tárraga, S., PEÑA, L (2019)
    Protein analysis of Moro blood orange pulp during storage at low temperatures

    Food Chemistry 277: 75-83

  • Peris J.E., Malara T., Borges R., Falconi J.R., Peña, L., Fedriani, J.M. (2019)
    Reunion in the overseas: introduced wild boars and cultivated orange trees interact in the Mata Atlântica (Brazil).

    International Journal of Tropical Biology 67 (4): 901-912

  • Felisberto, P.A.C, Girardi, E.A., PEÑA, L. Felisberto, G., Beattie, G.A.C., Lopes (2019)
    Unsuitability of indigenous South American Rutaceae as potential hosts of Diaphorina citri

    Pest Management Science, DOI 10.1002/ps.5304

  • Wulff, Nelson A., Marques, Viviani V., Peris, Josep Enric., Pons, Elsa, Sanches, Andre L., Peña, Leandro (2018)
    Biossegurança de árvores frutíferas geneticamente modificadas no campo: o caso dos cítricos

    Biossegurança de árvores. Capítulo 12

  • Ruiz-Ruiz, S., Spàno, R., Navarro, L., Moreno, P., PEÑA, L. and Flores, R (2018)
Citrus tristeza virus co-opts glyceraldehyde 3-phosphate dehydrogenase for its infectious cycle by interacting with the viral-encoded protein p24

Plant Molecular Biology

  • Ruiz-Ruiz, S., Navarro, B., PEÑA, L., Navarro, L., Moreno, P., Di Serio, F. and Flores, R (2018)
    Citrus Tristeza Virus: Host RNA Silencing and Virus Counteraction.

    Methods in Molecular Biology.

  • Febres, Vicente J., Peña, Leandro, Folimonova, Svetlana, and Moore, Gloria A. (2018)
    Citrus. Biotechnology of Fruit and Nut Crops

    CABI Publishing, chapter 20.1, CAB International

  • Rodríguez, Ana; Kava, Vanessa; Latorre-García, Lorena; da Silva jr., Geraldo J.; Pereira, Rosana G.; Glienke, Chirlei; Ferreira-Maba, Lisandra S.; Vicent, Antonio; Shimada, Takehiko; Peña, Leandro. (2018)
    Engineering D-limonene synthase down-regulation in orange fruit induces resistance against the fungus Phyllosticta citricarpa through enhanced accumulation of monoterpene alcohols and activation of defence. Molecular

    Molecular Plant Pathology. 19 – 9, pp. 2077 – 2093

  • Soler, N., Plomer, M., Fagoaga, C., Moreno, P., Navarro, L., Flores, R. and PEÑA, L. (2018)
    Methods for producing transgenic plants resistant to CTV.

    Methods in Molecular Biology

  • Tomaseto, A.F., Marques, R.N., Fereres, A., Zanardi, O.Z., Volpe, H.X.L., Alquézar, B., PEÑA, L. and Miranda, M.P. (2018)
    Orange jasmine as a trap crop to control Diaphorina citri

    Scientific Reports 9: 2070

  • Carmona, Lourdes; Alquézar, Berta; Tárraga, Susana and Peña, Leandro. (2018)
    Protein analysis of Moro blood orange pulp during storage at low temperatures.

    Food Chemistry 277: 75-83

  • Carmona, Lourdes, Alquézar, Berta, Marques, Viviani V. and Peña, Leandro. (2017)
    Anthocyanin biosynthesis and accumulation in blood oranges during postharvest storage at different low temperatures

    Food Chemistry 237: 7-14

  • Shimada, Takehiko; Endo, Tomoko; Rodríguez, Ana; Fujii, Hiroshi; Goto, Shingo; Matsuura, Takakazu; Hojo, Yuko; Ikeda, Yoko; Mori, Izumi; Fujikawa, Takashi; Peña, Leandro; Omura, Mitsuo. (2017)
    Ectopic accumulation of linalool confers resistance to Xanthomonas citri subsp. citri in transgenic sweet orange plants.

    Tree Physiology. 37, pp. 654 – 664

  • Peris, Josep Enric; Rodríguez, Ana; Peña, Leandro; Fedriani, José María (2017)
    Fungal infestation boosts fruit aroma and fruit removal by mammals and birds

    Scientific Reports 7 – Article 5646, 2017

  • Alquézar, Berta; Rodríguez, Ana; de la Peña, Marcos; Peña, Leandro. (2017)
Genomic analysis of terpene synthase Family and functional characterization of seven sesquiterpene synthases from Citrus sinensis.

Frontiers in Plant Science 8 – Article 1481

  • Alquézar, Berta; Rodríguez, Ana; de la Peña, Marcos; Peña, Leandro. (2017)
    Genomic analysis of terpene synthase Family and functional characterization of seven sesquiterpene synthases from Citrus sinensis.

    Frontiers in Plant Science 8 – Article 1481

  • Rodríguez, Ana; Peris, Josep; Redondo, Ana; Shimada, Takehiko; Costell, Elvira; Carbonell, Inmaculada; Rojas, Cristina; Peña, Leandro (2017)
    Impact of d-limonene synthase up- or down-regulation on sweet orange fruit and juice odor perception.

    Food Chemistry. 217, pp. 139 – 150.

  • Pons, Elsa and Peña, Leandro (2017)
    Plant gene silencing: Mechanisms and applications. Chapter 8. CABI Biotechnology Series

    CABI Biotechnology Series, vol 5, pp. 147-165

  • Alquézar, Berta, Linhares Volpe, Haroldo X., Facchini Magnani, Rodrigo, Pedreira de Miranda, Marcelo, Almeida Santos, Mateus, Wulff, Nelson A., Bento, J. Mauricio S., Parra, Jose Roberto P., Bouwmeester, Harro and Peña, Leandro. (2017)
    β-caryophyllene emitted from a transgenic Arabidopsis or chemical dispenser repels Diaphorina citri, vector of Candidatus Liberibacters.

    Scientific Reports 7- Article 5639

  • Rodríguez, Ana; Peris, Josep; Redondo, Ana; Shimada, Takehiko; Peña, Leandro. (2016)
    Principal component analysis (PCA) of volatile terpene compounds dataset emitted by genetically modified sweet orange fruits and juices in which a D-limonene synthase was either up- or down-regulated vs. empty vector controls

    Data in Brief. 9, pp. 355 – 361. 2016.

Projects

INNEST: Mejora genética de mandarinos: Evaluación de una estrategia para la eliminación de los transgenes en plantas editadas de cítricos.
Entidades participantes: Generalitat Valenciana, Agencia Valenciana de la Innovavió y la Unión Europea a través del FEDER.
Fechas: 2023- 2025. 300.000,68 €
Entidad financiadora: INNEST S7065000 (2023 2 S7065 1 1)
Coordinador General (e IP de un WP): Leandro Peña
PRE-HLB: Preventing HLB epidemics for ensuring citrus survival in Europe
Entidades participantes: CSIC y otras 23 entidades de 9 países
Fechas: 2019- 2023. 8.001.690 € (6.639.815 € financiados por UE)
Entidad financiadora: EU H2020-SFS-2018-2
Coordinador General (e IP de un WP): Leandro Peña
FUND: Desarrollo de estrategias biotecnológicas en naranjo para generar (i) repelencia, resistencia o atracción al insecto Diaphorina citri, vector de las bacterias Candidatus Liberibacter spp., causantes del Huanglongbing (HLB), (ii) resistencia a Candidatus Liberibacter asiaticus (CLas),
principal bacteria causante del HLB.
Fecha: 01/12/2020-30/11/2022 (330.000 €)
Entidad financiadora: Fundo de Defesa da Citricultura (FUNDECITRUS)
IP: Leandro Peña
PID2019: Mejora genética de portainjertos cítricos para generar resistencia a viejas y nuevas enfermedades emergentes (PID2019-104569RB-I00)
Fechas: 01/01/2020-31/12/2022 (197.400 €)
Entidad financiadora: Proyecto PID2019-104569RB-I00 financiado por MCIN/ AEI /10.13039/501100011033
IP: Leandro Peña
GCM: Desarrollo de variedades de cítricos pigmentadas mediante biotecnología.
Fecha: 01/12/2021-30/11-20-24 (362.922 €)
Entidad financiadora: GCM Citrus S.L.
IP: Leandro Peña

Other publications

Tomaseto, A.F., Marques, R.N., Fereres, A., Zanardi, O.Z., Volpe, H.X.L., Alquézar, B., PEÑA, L. and Miranda, M.P. (2019)
Orange jasmine as a trap crop to control Diaphorina citri.
Scientific Reports 9: 2070 | https://doi.org/10.1038/s41598-019-38597-5, 2019
Soler, N., Plomer, M., Fagoaga, C., Moreno, P., Navarro, L., Flores, R. and PEÑA, L. (2019)
Methods for producing transgenic plants resistant to CTV.
Methods for producing transgenic plants resistant to CTV. Citrus Tristeza Virus: Methods and Protocols (Catara, A, Bar-Joseph, J and Licciardello, G., ed.) Methods in Molecular Biology, in press, 2019.
Felisberto, P.A.C, Girardi, E.A., PEÑA, L. Felisberto, G., Beattie, G.A.C. and Lopes, S.A. (2019)
Unsuitability of indigenous South American Rutaceae as potential hosts of Diaphorina citri.
Pest Management Science, DOI 10.1002/ps.5304, 2019.
Caland, R.B.O., Cadavid, C.O.M., Carmona, L., PEÑA, L. and Oliveira, R.P. (2019)
Pasteurized orange juice rich in carotenoids protects Caenorhabditis elegans against oxidative stress and β-amyloid toxicity through direct and indirect mechanisms
Oxidative Medicine and Cellular Longevity, in press, 2019.
Ruiz-Ruiz, S., Navarro, B., PEÑA, L., Navarro, L., Moreno, P., Di Serio, F. and Flores, R. (2019)
Citrus Tristeza Virus: Host RNA Silencing and Virus Counteraction
Citrus Tristeza Virus: Host RNA Silencing and Virus Counteraction. Citrus Tristeza Virus: Methods and Protocols (Catara, A, Bar-Joseph, J and Licciardello, G., ed.) Methods in Molecular Biology, in press, 2019.
Rodríguez, Ana; Kava, Vanessa; Latorre-García, Lorena; da Silva jr., Geraldo J.; Pereira, Rosana G.; Glienke, Chirlei; Ferreira-Maba, Lisandra S.; Vicent, Antonio; Shimada, Takehiko; Peña, Leandro (2018)
Engineering D-limonene synthase down-regulation in orange fruit induces resistance against the fungus Phyllosticta citricarpa through enhanced accumulation of monoterpene alcohols and activation of defence.
Molecular Plant Pathology. 19 – 9, pp. 2077 – 2093. 2018.
Ruiz-Ruiz, S., Spàno, R., Navarro, L., Moreno, P., PEÑA, L. and Flores, R. (2018)
Citrus tristeza virus co-opts glyceraldehyde 3-phosphate dehydrogenase for its infectious cycle by interacting with the viral-encoded protein p23.
Plant Molecular Biology 98: 363-373, 2018. DOI: 10.1007/s11103-018-0783-0.
Carmona, L., Alquézar, B., Tárraga, S. and PEÑA, L. (2018)
Protein analysis of Moro blood orange pulp during storage at low temperatures
Food Chemistry 277: 75-83, 2019. DOI: 10.1016/j.foodchem.2018.10.108
Soler, N., Plomer, M., Fagoaga, C., Moreno, P., Navarro, L., Flores, R. and PEÑA, L. Methods for producing transgenic plants resistant to CTV. Methods in Molecular Biology, in press, 2018. (2018)
Methods for producing transgenic plants resistant to CTV.
Methods in Molecular Biology, in press, 2018.
Wulff, Nelson A., Marques, Viviani V., Peris, Josep Enric., Pons, Elsa, Sanches, Andre L., Peña, Leandro (2018)
Biossegurança de árvores frutíferas geneticamente modificadas no campo: o caso dos cítricos.
Biossegurança de árvores. Capítulo 12. E-Book. (Pasquali, G., Ed.), in press, 2018.
Ruiz-Ruiz, S., Spàno, R., Navarro, L., Moreno, P., PEÑA, L. and Flores, R. (2018)
Citrus tristeza virus co-opts glyceraldehyde 3-phosphate dehydrogenase for its infectious cycle by interacting with the viral-encoded protein p23.
Plant Molecular Biology, in press, 2018.
Febres, Vicente J., Peña, Leandro, Folimonova, Svetlana, and Moore, Gloria A. Citrus. (2018)
Citrus. Biotechnology of Fruit and Nut Crops, 2nd edition.
Citrus. Biotechnology of Fruit and Nut Crops, 2nd edition. (Litz, R.E, Pliego-Alfaro, F and Hormaza, J.I., Ed.). CABI Publishing, chapter 20.1, CAB International, in press, 2018.
Shimada, Takehiko; Endo, Tomoko; Rodríguez, Ana; Fujii, Hiroshi; Goto, Shingo; Matsuura, Takakazu; Hojo, Yuko; Ikeda, Yoko; Mori, Izumi; Fujikawa, Takashi; Peña, Leandro; Omura, Mitsuo (2017)
Ectopic accumulation of linalool confers resistance to Xanthomonas citri subsp. citri in transgenic sweet orange plants.
Tree Physiology. 37, pp. 654 – 664. 2017
Rodríguez, Ana; Peris, Josep; Redondo, Ana; Shimada, Takehiko; Costell, Elvira; Carbonell, Inmaculada; Rojas, Cristina; Peña, Leandro (2017)
Impact of d-limonene synthase up- or down-regulation on sweet orange fruit and juice odor perception
Food Chemistry. 217, pp. 139 – 150. 2017.
Pons, Elsa and Peña, Leandro (2017)
Increasing nutritional value by RNA silencing
Increasing nutritional value by RNA silencing. In: Dalmay, T. (ed.) Plant gene silencing: Mechanisms and applications. Chapter 8. CABI Biotechnology Series, vol 5, pp. 147-165. 2017.
Alquézar, Berta; Rodríguez, Ana; de la Peña, Marcos; Peña, Leandro (2017)
Genomic analysis of terpene synthase Family and functional characterization of seven sesquiterpene synthases from Citrus sinensis
Frontiers in Plant Science 8 – Article 1481, 2017.
Carmona, Lourdes, Alquézar, Berta, Marques, Viviani V. and Peña, Leandro (2017)
Anthocyanin biosynthesis and accumulation in blood oranges during postharvest storage at different low temperatures
Food Chemistry 237: 7-14, 2017.
Peris, Josep Enric; Rodríguez, Ana; Peña, Leandro*; Fedriani, José María*. *: Two corresponding authors (2017)
Fungal infestation boosts fruit aroma and fruit removal by mammals and birds.
Scientific Reports 7 – Article 5646, 2017.
Alquézar, Berta, Linhares Volpe, Haroldo X., Facchini Magnani, Rodrigo, Pedreira de Miranda, Marcelo, Almeida Santos, Mateus, Wulff, Nelson A., Bento, J. Mauricio S., Parra, Jose Roberto P., Bouwmeester, Harro and Peña, Leandro (2017)
β-caryophyllene emitted from a transgenic Arabidopsis or chemical dispenser repels Diaphorina citri, vector of Candidatus Liberibacters
Scientific Reports 7- Article 5639, 2017.
Rodríguez, Ana; Peris, Josep; Redondo, Ana; Shimada, Takehiko; Peña, Leandro (2016)
Principal component analysis (PCA) of volatile terpene compounds dataset emitted by genetically modified sweet orange fruits and juices in which a D-limonene synthase was either up- or down-regulated vs. empty vector controls.
Data in Brief. 9, pp. 355 – 361. 2016.

Patent

Título: 
Repellent compositions and genetic approaches for controlling Huanglongbing.
Referencia ID: 
Application No. 14/733,439; Filed: June 8, 2015 Continuation-in-part of U.S. Application No. 13/501,739 filed April 12, 2012. Patent No. US 9,572,349 B2; Patent Date: February 21, 2017.
Autores: 
Alquézar, Berta, Rodríguez, Ana, Peris, Josep, Peña, Leandro, Henrique, Andreia, Pedreira, Marcelo, Yamamoto, Pedro T., Sposito, Marcelo B., Wulff, Nelson A., Teixeira, D.C., Ayres, A. Juliano, Cavalcanti, Newton, Simoes Bento, J. Mauricio, Parra, Jose Roberto P.
Título: 
Repellent compositions and genetic approaches for controlling Huanglongbing
Referencia ID: 
U.S.A. Patent No. 9,078,448, which is the US national phase of PCT application PCT/BR2010/000353. Date of patent: Oct. 28, 2009. PCT WO2011/050432 A1. Fundecitrus/IVIA. Patente aceptada (Enero de 2015) en China, Unión Europea, Sudáfrica y Chile
Autores: 
Alquézar, Berta, Rodríguez, Ana, Peris, Josep, Peña, Leandro, Henrique, Andreia, Pedreira, Marcelo, Yamamoto, Pedro T., Sposito, Marcelo B., Wulff, Nelson A., Teixeira, D.C., Ayres, A. Juliano, Cavalcanti, Newton, Simoes Bento, J. Mauricio, Parra, Jose Roberto P.
Título: 
Método para conseguir resistencia frente a enfermedades de los cítricos causadas por insectos, por hongos u omicetos o por bacterias o nematodos.
Referencia ID: 
2007. Solicitud Patente de Invención nº 200901283
Autores: 
Rodríguez, Ana; Cervera, Magdalena; Shimada, Takehiko; Redondo, Ana; Rodrigo, M. Jesús; San Andrés, Victoria; Palou, Lluís; Zacarías, Lorenzo; López, M. Milagros; Castañera, Pedro and Peña, Leandro.
Título: 
Method for generating resistance against citrus diseases caused by insects, fungi, oomycetes, bacteria or nematodes.
Referencia ID: 
2010. Patent number: 12/945,972
Autores: 
Rodríguez, Ana; Cervera, Magdalena; Shimada, Takehiko; Redondo, Ana; Rodrigo, M. Jesús; San Andrés, Victoria; Palou, Lluís; Zacarías, Lorenzo; López, M. Milagros; Castañera, Pedro and Peña, Leandro.

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