Skip to main content
Log in

The effect of drought conditions on sweet orange (Citrus sinensis) plants infected with citrus tristeza virus (CTV)

  • Original Article
  • Published:
Tropical Plant Pathology Aims and scope Submit manuscript

Abstract

Brazil is one of the world’s largest producers of citrus. However, production is challenged due to biotic and abiotic factors limiting crop health. The aim of this work was to evaluate the influence of water deficit in sweet orange (Citrus sinensis) cv. Pera Bianchi inoculated with citrus tristeza virus (CTV). Two isolates of CTV were used, one causing severe symptoms (Forte Rolândia) and the second causing mild symptoms (Pêra IAC), grafted on Rangpur lime (Citrus limonia) and Swingle citrumelo [Citrus paradisi x Poncirus trifoliata], and the indicator sweet orange Pêra Bianchi, free of virus, and healthy controls containing only the indicator budwood. The water regime for the plants was field capacity or 50% field capacity. After five months of controlled irrigation, biochemical variables were measured (protein, proline content and catalase activity), and real-time RT-PCR amplification of the virus was performed for detection and quantification of viral titer. Differences were observed in the total protein content and proline, with greater accumulation in plants maintained under water deficit. There was no effect of drought on the population of viral isolates, but the plants held at field capacity and inoculated with the severe isolate had a higher viral titer.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Aebi H (1974) Catalase. In: Bergmeyer HU (Ed.) Methods of enzymatic analysis. Academic Press, New York, pp 673–684

    Chapter  Google Scholar 

  • Bar-Joseph M, Garnsey SM, Gonçalves D (1979) The closteroviruses: a distinct group of elongated plant virus. Advanced in Virus Research 25:93–168

    Article  CAS  Google Scholar 

  • Bar-Joseph M, Marcus L, Lee RF (1989) The continuous challenge of citrus tristeza virus control. Annual Review of Phytopathology 27:291–316

    Article  Google Scholar 

  • Bastos DC, Ferreira EA, Passos OS, Sá JF, Ataíde EM, Calgaro M (2014) Cultivares copa e porta-enxertos para a citricultura brasileira. Informe Agropecuário 35:36–45

    Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant and Soil 39:205–207

    Article  CAS  Google Scholar 

  • Bennett CW, Costa AS (1949) Tristeza disease of citrus. Journal of Agricultural Research 78:207–237

    Google Scholar 

  • Bertolini E, Moreno A, Vidal E, Pérez-Panadés J, Cambra M (2008) Quantitative detection of citrus tristeza virus in plant tissues and single aphids by real-time RT-PCR. European Journal of Plant Pathology 120:177–188

    Article  CAS  Google Scholar 

  • Biswas KK (2008) Molecular diagnosis of citrus tristeza virus in mandarin (Citrus reticulata) orchards of Darjeeling hills of West Bengal. Indian Journal Virology 19:26–31

    Google Scholar 

  • Boyer JS (1995) Biochemical and biophysical aspects of water deficits and the predisposition to disease. Annual Review of Phytopathology 33:151–274

    Article  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72:246–254

    Article  Google Scholar 

  • Cambra M, Camarasa E, Gorris MT, Garnsey SM, Carbonell E (1991) Comparison of different immunosorbent assays for citrus tristeza virus (CTV) using CTV-specific monoclonal and polyclonal antibodies. In: Proceedings of the 11th Conference of the International Organization of Citrus Virologists. IOCV, Riverside. pp.38–45

  • Campos MKF, Carvalho K, Souza FS, Marur CJ, Pereira LFP, Bespalhok Filho JC, Vieira LGE (2011) Drought tolerance and antioxidant enzymatic activity in transgenic Swingle citrumelo plants over-accumulating proline. Environmental and Experimental Botany 72:242–250

    Article  CAS  Google Scholar 

  • Carillo P, Gibon Y (2011) Extraction and determination of proline. PrometheusWiki - protocols in ecological & environmental plant physiology. Available at: prometheuswiki.org/tiki-custom_home.php. Accessed on October 10, 2016

  • Carraro BP, Nunes WMC, Corazza-Nunes MJ, Machado MA, Stach-Machado DR (2003) Avaliação de complexos do citrus tristeza virus da região Norte do Paraná por meio de testes imunológicos e SSCP do gene da capa protéica. Acta Scientiarum (Agronomy) 25:269–227

    Google Scholar 

  • Carvalho LM, Carvalho HWL, Soares Filho WS, Martins CR, Passos OS (2016) Porta-enxertos promissores, alternativos ao limoeiro 'Cravo', nos Tabuleiros Costeiros de Sergipe. Pesquisa Agropecuária Brasileira 51:132–141

    Article  Google Scholar 

  • Claeys H, Inze D (2013) The agony of choice: how plants balance growth and survival under water-limiting conditions. Plant Physiology 162:1768–1779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Corazza MJ, Zanutto CA, Zanineli-Ré ML, Müller GW, Nunes WMC (2012) Comparison of citrus tristeza virus (CTV) isolates by RFLP analysis of the coat protein nucleotide sequences and by the severity of the symptoms. Tropical Plant Pathology 37:179–184

    Article  Google Scholar 

  • Costa AS, Müller GW (1980) Tristeza control by cross protection: a U.S.-Brazil cooperative success. Plant Disease 64:538–541

    Article  Google Scholar 

  • Davies FS, Albrigo LG (1994) Citrus. Wallingford, CAB International

  • Dória MS, Sousa AO, Barbosa C, Costa MG, Gesteira A, Souza RM, Freitas AC, Pirovani CP (2015) citrus tristeza virus (CTV) causing proteomic and enzymatic changes in sweet orange variety Westin. PLoS One 10:e0130950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferreira DF (2008) SISVAR: um programa para análises e ensino de estatística. Symposium 6:36–41

    Google Scholar 

  • Freitas-Astuá J, Bastianel M, Locali-Frabris EC, Novelli VM, Silva-Pinhati AC, Palmieri AC, Targon MLPN, Machado MA (2007) Differentially expressed stress-related genes in the compatible citrus-citrus leprosis virus interaction. Genetic and Molecular Biology 30:980–990

    Article  Google Scholar 

  • Gonçalves FP, Stuchi ES, Lourenço AS, Kriss AB, Gottwald TR, Amorim L (2014) The effect of irrigation on development of citrus variegated chlorosis symptoms. Crop Protection 57:8–14

    Article  Google Scholar 

  • Hančević K, Radić T, Pasković IU (2018) Biochemical and physiological responses to long-term citrus tristeza virus infection in Mexican lime plants. Plant Pathology 67:987–994

    Article  CAS  Google Scholar 

  • Hegedus A, Erdei S, Horváth G (2001) Comparative studies of H2O2 detoxifying enzymes in green and greening barley seedlings under cadmium stress. Plant Science 160:1085–1093

    Article  CAS  PubMed  Google Scholar 

  • Hu Z, Shen Y, Shen F, Su X (2009) Effects of feeding Clostera anachoreta on hydrogen peroxide accumulation and activities of peroxidase, catalase, and ascorbate peroxidase in Populos simonii x P. pyramidales ‘oOpera 8277’ leaves. Acta Physiologiae Plantarum 31:995–1002

    Article  CAS  Google Scholar 

  • Hussain S, Khalid MF, Saqib M, Ahmad S, Zafar W, Rao MJ, Morillon R, Anjum MA (2018) Drought tolerance in citrus rootstocks is associated with better antioxidant defense mechanism. Acta Physiologiae Plantarum 40:135

    Article  CAS  Google Scholar 

  • Karasev AV, Dawson WO, Hilf MEE, Garnsey SM (1998) Molecular biology of citrus tristeza virus: implications for disease diagnosis and control. Acta Horticulturae 472:333–337

  • Kitajima EW, Silva DM, Oliveira AR, Müller GW, Costa AS (1964) Thread-like particles associated with tristeza disease of citrus. Nature 201:1011–1012

    Article  CAS  PubMed  Google Scholar 

  • Kumar N, Ebel RC, Roberts PD (2011a) Antioxidant metabolism of grapefruit infected with Xanthomonas axonopodis pv. citri. Environmental and Experimental Botany 71:41–49

    Article  CAS  Google Scholar 

  • Kumar N, Ebel RC, Roberts PD (2011b) H2O2 metabolism during sweet orange (Citrus sinensis L. Osb.) ‘Hamlin’ Xanthomonas axonopodis pv. citri interaction. Scientia Horticulturae 128:465–472

    Article  CAS  Google Scholar 

  • Laborem EG, Wagner M, Reyes F (1991) Proline concentration as an indicator of water deficit in three citrus rootstocks. Fruits 46:259–264

    Google Scholar 

  • Laino P, Russo MP, Guardo M, Reforgiato-Recupero G, Vale G, Cattivelli L, Moliterni VMC (2016) Rootstock–scion interaction affecting citrus response to CTV infection: a proteomic view. Physiologia Plantarum 156:444–467

    Article  CAS  PubMed  Google Scholar 

  • Larcher W (2000) Ecofisiologia vegetal. RiMa, São Carlos

    Google Scholar 

  • Leite ML, Virgens Filho JSV, Rodrigues JD (2000) Variação de prolina em folhas de caupi (Vigna unguiculata (L.) Walp) submetido a diferentes déficits hídricos. Biotemas 12:21–33

    Google Scholar 

  • Li H, Sylvertsen JP, Stuart RJ, McCoy CW, Schumann A (2006) Water stress and root injury from simulated flooding and Diaprepes root weevil feeding in citrus. Soil Science 171:138–151

    Article  CAS  Google Scholar 

  • López C, Ayllón MA, Navas-Castillo J, Guerri J, Moreno P, Flores R (1998) Molecular variability of the 5′- and 3′- terminal regions of citrus tristeza virus RNA. Virology 88:685–691

    Google Scholar 

  • Machado EA, Oliveira RF, Ribeiro RV, Medina CL, Stuchi ES, Pavani LC (2007) Deficiência hídrica agrava os sintomas fisiológicos da clorose variegada dos citros em laranjeira 'Natal'. Bragantia 66:373–379

    Article  CAS  Google Scholar 

  • Marijuan MP, Bosch SM (2013) Ecophysiology of invasive plants: osmotic adjustment and antioxidants. Trends in Plant Science 18:660–666

    Article  CAS  Google Scholar 

  • Medina CL, Machado EC (1998) Trocas gasosas e relações hídricas em laranjeira 'Valência' enxertada sobre limoeiro 'Cravo' e trifoliata e submetida à deficiência hídrica. Bragantia 57:8–14

    Google Scholar 

  • Meneghini M (1946) Sobre la natureza y transmissibilidade de la doencia “Tristeza” de los citros. O Biológico 12:285–287

    Google Scholar 

  • Moreno P, Ambrós S, Albiach-Martí MR, Guerri J, Peña L (2008) Citrus tristeza virus: a pathogen that changed the course of the citrus industry. Molecular Plant Pathology 9:251–268

    Article  CAS  PubMed  Google Scholar 

  • Morgan JM (1984) Osmoregulation and water stress in higher plants. Annual Review of Plant Physiology 35:299–319

    Article  Google Scholar 

  • Müller GW, Costa AS (1977) Tristeza control in Brazil by preimmunization with mild strains. Proceedings of the International Society of Citriculture 3:868–872

    Google Scholar 

  • Müller GW, Targon MLP, Carvalho SA, Souza AA, Rodrigues JCV (2005) Doenças de citros causadas por vírus e viróides. In: Mattos-Junior D, De Negri JD, Pio RM, Pompeu-Junior J (Eds.) Citros. Instituto Agronômico/Fundag, Campinas. pp. 567–604

  • Nascimento JB, Barrigossi JAF (2014) O papel das enzimas antioxidantes na defesa das plantas contra insetos herbívoros e fitopatógenos. Agrarian Academy 1:234–250

    Article  Google Scholar 

  • Nolte KD, Hanson AD (1997) Proline accumulation and methylation to proline betaine in citrus: implications for genetic engineering of stress resistance. Journal of the American Society for Horticultural Science 22:8–13

    Article  Google Scholar 

  • Oliveira Neto CF, Lobato AKS, Costa RCL (2006) Teor de proteínas solúveis totais em folhas de duas cultivares de feijão-caupi sob estresse hídrico. Available at: www.cpamn.embrapa.br/anaisconac2006/resumos/FV03.pdf. Accessed on January 12, 2017

  • Ortuño MF, Nicolás AE, Torrecillas A (2004) Interpreting trunk diameter changes in young lemon trees under deficit irrigation. Plant Science 167:275–280

    Article  CAS  Google Scholar 

  • Pedroso FKJV, Prudente DA, Bueno ACR, Machado EC, Ribeiro RV (2014) Drought tolerance in citrus trees is enhanced by rootstock-dependent changes in root growth and carbohydrate availability. Environmental and Experimental Botany 101:26–35

    Article  CAS  Google Scholar 

  • Peixoto PHP, Cambraia J, Sant'anna R, Mosquim PR, Moreira MA (1999) Aluminum effects on lipid peroxidation and on the activities of enzymes of oxidative metabolism in sorghum. Revista Brasileira de Fisiologia Vegetal 11:137–143

    CAS  Google Scholar 

  • Pérez-Clemente RM, Montoliu A, Vives V, López CMF, Gómez-Cadenas A (2015) Photosynthetic and antioxidante responses of Mexican lime (Citrus aurantifolia) plants to citrus tristeza virus infection. Plant Pathology 64:16–24

    Article  CAS  Google Scholar 

  • Pompeu-Junior J (2005) Porta-enxertos. In: Mattos-Junior D, De Negri JD, Pio RM, Pompeu-Junior J (Eds.) Citros. Instituto Agronômico/Fundag, Campinas. pp. 61–104

  • Resende MLV, Salgado SML, Chaves ZM (2003) Espécies reativas de oxigênio na resposta de defesa de plantas a patógenos. Fitopatologia Brasileira 28:123–130

    Article  Google Scholar 

  • Ribeiro GD, Costa JNM, Vieira AH, Santos MRA (2005) Enxertia em fruteiras. Available at: www.infoteca.cnptia.embrapa.br/bitstream/doc/859550/1/rt92enxertiadefruteiras.pdf. Accessed on January 12, 2017

  • Ririe KM, Rasmussen RP, Witter CT (1997) Product differentiation by analysis of DNA melting curves during the polymerase chain reaction. Analytical Biochemistry 245:154–160

    Article  CAS  PubMed  Google Scholar 

  • Rubio L, Ayllón MA, Kong P, Fernández A, Polek M, Guerri J, Moreno P, Falk BW (2001) Genetic variation of citrus tristeza virus isolates from California and Spain: evidence for mixed infections and recombination. Journal of Virology 75:8054–8062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruiz-Ruiz S, Moreno P, Guerri J, Ambrós S (2006) The complete nucleotide sequence of a severe stem pitting isolate of citrus tristeza virus from Spain: comparison with isolates from different origins. Archives of Virology 151:387–398

    Article  CAS  PubMed  Google Scholar 

  • Ruiz-Ruiz S, Moreno P, Guerri J, Ambrós S (2007) A real-time RT-PCR assay for detection and absotute quantitation of citrus tristeza virus in different plant tissues. Journal of Virological Methods 145:96–105

    Article  CAS  PubMed  Google Scholar 

  • Salem-Fnayou AB, Belghith I, Lamine M, Mliki A, Ghorbel A (2016) Phisiological and ultrastructural responses of sour orange (Citrus aurantium L.) clones to water stress. Photosynthetica 54:532–541

    Article  CAS  Google Scholar 

  • Satyanarayana T, Gowda S, Boyko VP, Albiach-Marti MR, Mawassi M, Navas-Castillo J, Karasev AV, Dolja V, Hilf ME, Lewandowski DJ, Moreno P, Bar-Joseph M, Garnsey SM, Dawson WO (1999) An engineered closterovirus RNA replicon and analysis of heterologous terminal sequences for replication. Proceedings of the National Academy of Sciences, USA 96:7433–7438

    Article  CAS  Google Scholar 

  • Scandalios JG (1993) Oxygen stress and superoxide dismutase. Plant Physiology 101:7–12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Silva SEL, Souza AGC (2002) Produção de mudas de laranja. Avalaible at: ainfo.cnptia.embrapa.br/digital/bitstream/CPAA-2009-09/10248/1/circ_tec14.pdf. Accessed on January 12, 2017

  • Silva FAC, Santos RC, Azevedo Neto A, Granja MMC, Souza CCF, Melo Filho PA (2010) Descritores bioquímicos em cultivares de algodoeiro em resposta à inoculação com Colletotrichum gossypii var. cephalosporioides. Tropical Plant Pathology 35:114–118

    Article  Google Scholar 

  • Souza AA, Müller GW (2006) A premunização no controle da tristeza dos citros. Laranja 27:57–70

    Google Scholar 

  • Stenzel NMC, Neves CSVJ, Scholz MBS, Gomes JC (2005) Comportamento da laranjeira ‘folha murcha’ em sete porta-enxertos no noroeste do Paraná. Revista Brasileira de Fruticultura 27:408–411

    Article  Google Scholar 

  • Syvertsen JP, Hanlin EA (2008) Citrus tree stress: effects on growth and yield. Document HS1138. University of Florida, Gainesville

    Google Scholar 

  • Taylor CB (1996) Proline and water deficit: ups, downs, ins, and outs. Plant Cell 8:1221–1224

    Article  CAS  PubMed Central  Google Scholar 

  • Turner NC (1981) Techniques and experimental approaches for the measurement of plant water status. Plant and Soil 58:339–366

    Article  Google Scholar 

  • Van Breusegem F, Vranová E, Dat JF, Inzé D (2001) The role of active oxygen species in plant signal transduction. Plant Science 161:405–414

    Article  Google Scholar 

  • Vellosillo T, Vicente J, Kulasekaran S, Hamberg M, Castresana C (2010) Emerging complexity in reactive oxygen species production and signaling during the response of plants to pathogens. Plant Physiology 154:444–448

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wojtaszek P (1997) Oxidative burst: an early plant response to pathogen infection. Biochemical Journal 322:681–692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zandalinas SI, Rivero RM, Martínez V, Gómez-Cadenas A, Arbona V (2016) Tolerance of citrus plants to the combination of high temperatures and drought is associated to the increase in transpiration modulated by a reduction in abscisic acid levels. BMC Plant Biology 16:105–120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zanini JR, Pavani LC, Silva JAA (1998) Irrigação em citros. Funep, Jaboticabal

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rúbia O. Molina.

Additional information

Section Editor: F. Murilo Zerbini

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Silva, C.C., Molina, R.O., Back, L. et al. The effect of drought conditions on sweet orange (Citrus sinensis) plants infected with citrus tristeza virus (CTV). Trop. plant pathol. 44, 335–342 (2019). https://doi.org/10.1007/s40858-019-00291-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40858-019-00291-2

Keywords

Navigation