Skip to main content
Log in

Evaluation of susceptibility of commercial citrus rootstocks to white root rot incited by Rosellinia necatrix

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

Abstract

Spain reached the fifth position of citrus production and the first of fresh fruit exporter worldwide. Pre-harvest diseases caused by soil-borne pathogens can limit citrus crop production. Phytophthora spp. are considered the most serious soil-borne pathogens of citrus crops worldwide, but their management strategies are highly developed. Conversely, Rosellinia necatrix is another soil-borne pathogen with polyphagous behavior, including citrus trees, and without fully-effective control tools. In this sense, the aim of this study was to characterize the susceptibility of several commercial citrus rootstocks to R. necatrix disease. Potted plants from 10 different rootstocks were artificial inoculated with an isolate of R. necatrix. Plant physiological measurements of above-ground symptoms, chlorophyll content, biomass and leaf area were obtained. Flying Dragon and Forner-Alcaide 517 citrus rootstocks displayed the lowest disease incidence of SAUDPC, whereas Citrus macrophylla the highest symptoms rate. The highest chlorophyll content was found in Forner-Alcaide 517, and the lowest in Citrus macrophylla and Bitters C-22. Additionally, this last rootstock reached the highest reduction of biomass and the lowest leaf area rate. In conclusion, Forner-Alcaide 517 could be an interesting choice for those orchards with R. necatrix problems; contrarily, Citrus macrophylla and Bitters C-22 were the most sensitive candidates to this pathogen.

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.

Fig. 1
Fig. 2

Similar content being viewed by others

Data availability

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

References

  • Aleza P, Forner-Giner MA, Del-Pino Á (2020) El panorama varietal y los nuevos patrones. Análisis de la situación actual. In: García Álvarez-Coque JM, Moltó García E (eds) Una hoja de ruta para la citricultura española. Cajamar Caja Rural, Almería, Spain, pp 151–166

    Google Scholar 

  • Aparicio-Durán L, Arjona-López JM, Calero-Velázquez R, Hervalejo A, Arenas-Arenas FJ (2022) Respuesta de diferentes patrones de cítricos a podredumbre del cuello causada por Phytopthora. Levante Agrícola: Revista Internacional de Cítricos 460:33–37

    Google Scholar 

  • Arakawa M, Nakamura H, Uetake Y, Matsumoto N (2002) Presence and distribution of double-stranded RNA elements in the white root rot fungus Rosellinia necatrix. Mycoscience 43:21–26. https://doi.org/10.1007/s102670200004

    Article  CAS  Google Scholar 

  • Arjona-Girona I, López-Herrera CJ (2018a) First report of Rosellinia necatrix causing white root rot in mango trees in Spain. Plant Dis 102:2639. https://doi.org/10.1094/PDIS-01-18-0133-PDN

    Article  Google Scholar 

  • Arjona-Girona I, López-Herrera CJ (2018b) Study of a new biocontrol fungal agent for avocado white root rot. Biol Control 117:6–12. https://doi.org/10.1016/j.biocontrol.2017.08.018

    Article  Google Scholar 

  • Arjona-López JM, Capote N, López-Herrera CJ (2019a) Improved real-time PCR protocol for the accurate detection and quantification of Rosellinia necatrix in avocado orchards. Plant Soil 443:605–612. https://doi.org/10.1007/s11104-019-04215-6

    Article  CAS  Google Scholar 

  • Arjona-López JM, Capote N, Melero-Vara JM, López-Herrera CJ (2020) Control of avocado white root rot by chemical treatments with fluazinam in avocado orchards. Crop Prot 131:105100. https://doi.org/10.1016/j.cropro.2020.105100

    Article  CAS  Google Scholar 

  • Arjona-López JM, Gmitter FG, Romero-Rodríguez E, Grosser JW, Hervalejo A, López-Herrera CJ, Arenas-Arenas FJ (2022) Susceptibility of novel promising citrus rootstocks to white root rot. Plants 11:3388. https://doi.org/10.3390/plants11233388

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arjona-López JM, López-Herrera CJ (2021) Entoleuca sp. infected by mycoviruses as potential biocontrol agents of avocado white root rot. Eur J Plant Pathol 159:409–420. https://doi.org/10.1007/s10658-020-02171-x

    Article  CAS  Google Scholar 

  • Arjona-López JM, López-Herrera CJ (2020) Control of avocado white root rot using non-pathogenic Rosellinia necatrix isolates combined with low concentration of fluazinam. BioControl 65:247–255. https://doi.org/10.1007/s10526-019-09992-8

    Article  Google Scholar 

  • Arjona-López JM, Telengech P, Suzuki N, López-Herrera CJ (2021) A moderate level of hypovirulence conferred by a hypovirus in the avocado white root rot fungus, Rosellinia necatrix. Fungal Biol 125:69–76. https://doi.org/10.1016/j.funbio.2020.10.007

    Article  CAS  PubMed  Google Scholar 

  • Arjona-López JM, Tienda S, Arjona-Girona I, Cazorla FM, López-Herrera CJ (2019b) Combination of low concentrations of fluazinam and antagonistic rhizobacteria to control avocado white root rot. Biol Control 136:103996. https://doi.org/10.1016/j.biocontrol.2019.05.015

    Article  CAS  Google Scholar 

  • Armengol J, Vicent A, León M, Berbegal M, Abad-Campos P, García-Jiménez J (2010) Analysis of population structure of Rosellinia necatrix on Cyperus esculentus by mycelial compatibility and inter-simple sequence repeats (ISSR). Plant Pathol 59:179–185. https://doi.org/10.1111/j.1365-3059.2009.02150.x

    Article  CAS  Google Scholar 

  • Barceló-Muñoz A, Zea-Bonilla T, Jurado-Valle I, Imbroda-Solano I, Vidoy-Mercado I, Pliego-Alfaro F, López-Herrera CJ (2007) Programa de selección de portainjertos de aguacate tolerantes a la podredumbre blanca causada por Rosellinia necatrix en el sur de España (1995-2007). In: VI World Avocado Congress (Actas VI Congreso Mundial del Aguacate), Viña del Mar, Chile, 12–16 November 2007. pp 1–8

  • Behdad E (1976) The influence of several new systemic fungicides on Rosellinia necatrix (Hart.) Berl. Iran J Plant Pathol 12:40–41

    Google Scholar 

  • Bowman KD (2007) Notice to fruit growers and nurserymen relative to the naming and release of the US-897 citrus rootstock

  • Bowman KD (2010) Notice to fruit growers and nurserymen relative to the naming and release of the US-942 citrus rootstock

  • Bowman KD, Joubert J (2020) Citrus rootstocks. In: Talon M, Caruso M, Gmitter FG (eds) The genus citrus. Elsevier Inc., Amsterdam, The Netherlands, pp 105–127

    Chapter  Google Scholar 

  • Campbell CL, Madden LV (1990) Temporal analysis of epidemics I: descriptions and comparisons of disease progress curve. In: Campbell CL, Madden LV (eds) Introduction to plant disease epidemiology. Wiley, New York, pp 161–202

    Google Scholar 

  • Cazorla FM, Duckett SB, Bergström ET, Noreen S, Odijk R, Lugtenberg BJJ, Thomas-Oates JE, Bloember GV (2006) Biocontrol of avocado Dematophora root rot by antagonistic Pseudomonas fluorescens PCL1606 correlates with the production of 2-hexyl 5-propyl resorcinol. Mol Plant-Microbe Interact 19:418–428. https://doi.org/10.1094/MPMI-19-0418

    Article  CAS  PubMed  Google Scholar 

  • Chiba S, Salaipeth L, Lin Y-H, Sasaki A, Kanematsu S, Suzuki N (2009) A novel bipartite double-stranded RNA mycovirus from the white root rot fungus Rosellinia necatrix: molecular and biological characterization, taxonomic considerations, and potential for biological control. J Virol 83:12801–12812. https://doi.org/10.1128/JVI.01830-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choi B-H, Kim C-S, Jeong Y-J, Park I-H, Han S-G, Yoon T-M (2021) Resistance evaluation of G, CG, or M series apple rootstocks to soil-borne diseases (Phytophthora root rot, white root rot, and southern blight) and woolly apple aphid. Hortic Sci Tech 39:167–174. https://doi.org/10.7235/HORT.20210015

    Article  Google Scholar 

  • Citrus Variety Collection, 2023. University of California Riverside. https://citrusvariety.ucr.edu/. Accessed 16 March 2023

  • de Mendiburu F (2013) Statistical procedures for agricultural research. Package “Agricolae”, version 1.4-4. Comprehensive R archive network, Institute for statistics and mathematics, Vienna, Austria

  • Erwin DC, Ribeiro OK (1996) Phytophthora diseases worldwide. American Phytopathological Society (APS Press), St. Paul, MN, USA

    Google Scholar 

  • EU law - EUR-Lex, 2023. Access to European Union law. https://eur-lex.europa.eu/homepage.html. Accessed 8 March 2023

  • EU Pesticide Database, 2023. https://food.ec.europa.eu/plants/pesticides/eu-pesticides-database_en. Accessed 8 March 2023

  • FAOSTAT, 2023. Food and Agriculture Organization (FAO) of the United Nations. http://www.fao.org/faostat/es/#home. Accessed 26 Jan 2023

  • Farm to Fork strategy, 2023. European Commission. https://food.ec.europa.eu/horizontal-topics/farm-fork-strategy_en. Accessed 8 March 2023

  • Florida Citrus Rootstock Selection Guide, 4th Edition, 2023. https://crec.ifas.ufl.edu/extension/citrus_rootstock/tables.html. Accessed 20 March 2023

  • Forner-Giner MÁ (2020) Citrus tree named “CIVAC 19”. Patent Number: US 2020/028864 P1. United States Plant Patent Application Publication, 10 September 2020

  • Forner-Giner MA, Rodriguez-Gamir J, Martinez-Alcantara B, Quiñones A, Iglesias DJ, Primo-Millo E, Forner J (2014) Performance of Navel orange trees grafted onto two new dwarfing rootstocks (Forner-Alcaide 517 and Forner-Alcaide 418). Sci Hortic 179:376–387. https://doi.org/10.1016/j.scienta.2014.07.032

    Article  Google Scholar 

  • Forner JB, Forner-Giner MA, Alcaide A (2003) Forner-alcaide 5 and forner-alcaide 13: two new citrus rootstocks released in Spain. HortScience 38:629–630. https://doi.org/10.21273/HORTSCI.38.4.629

    Article  Google Scholar 

  • Fungal Databases (2022) U.S. National Fungus Collection, United States Department of Agriculture. https://nt.ars-grin.gov/fungaldatabases/. Accessed 5 Apr 2022

  • González-Domínguez E, Pérez-Sierra A, Álvarez LA, León M, Abad-Campos P, Armengol J, García-Jiménez J (2009) Agentes fúngicos presentes en plantaciones de nísperos (Eriobotrya japonica Lindl.) con síntomas de decaimiento en la provincia de Alicante. Boletín de Sanidad Vegetal -plagas 35:453–467

    Google Scholar 

  • Graham J, Feichtenberger E (2005) Citrus Phytophthora diseases: management challenges and successes. Rev General Psychol 9(2): 0–45

    CAS  Google Scholar 

  • Kanadani G, Date H, Nasu H (1998) Effect of fluazinam soil-drench on white root rot of grapevine. Jpn J Phytopathol 64:139–141. https://doi.org/10.3186/jjphytopath.64.139

    Article  CAS  Google Scholar 

  • Kanematsu S, Arakawa M, Oikawa Y, Onoue M, Osaki H, Nakamura H, Ikeda K, Kuga-Uetake Y, Nitta H, Sasaki K, Suzaki K, Yoshida K, Matsumoto N (2004) A Reovirus causes hypovirulence of Rosellinia necatrix. Phytopathology 94:561–568. https://doi.org/10.1094/PHYTO.2004.94.6.561

    Article  CAS  PubMed  Google Scholar 

  • Lee ATC, Joubert J, van Vuuren SP (2009) Rootstock choice. In: Joubert J, Van Vuuren SP (eds) Integrated production guidelines for export citrus: volume I. Citrus Research International Ltd, Nelspruit, South Africa, pp 29

    Google Scholar 

  • Lee SB, Ko K, Aldwinckle HS (2000) Resistance of selected Malus germplasm to Rosellinia necatrix. J Am Pomol Soc 54:219–228

    Google Scholar 

  • López-Herrera CJ (1989) Podredumbres radiculares del aguacate en la Costa del Sol. Años 1987-88. In: Moral J (ed) Estudios Fitopatología. SEFDGIEA, Badajoz, pp 172–176

    Google Scholar 

  • López-Herrera CJ, Pérez-Jiménez RM, Barceló-Muñoz A, Zea-Bonilla T (1999a) Evaluación de patrones de aguacate por su tolerancia a la podredumbre blanca. Revista Chapingo Serie Horticultura 5:267–270

    Google Scholar 

  • López-Herrera CJ, Pérez-Jiménez RM, Basallote-Ureba MJ, Zea-Bonilla T, Melero-Vara JM (1999b) Loss of viability of Dematophora necatrix in solarized soils. Eur J Plant Pathol 105:571–576. https://doi.org/10.1023/A:1008755017575

    Article  Google Scholar 

  • López-Herrera CJ, Pérez-Jiménez RM, Zea-Bonilla T, Basallote-Ureba MJ, Melero-Vara JM (1998) Soil solarization in established avocado trees for control of Dematophora necatrix. Plant Dis 82:1088–1092. https://doi.org/10.1094/PDIS.1998.82.10.1088

    Article  PubMed  Google Scholar 

  • López-Herrera CJ, Zea-Bonilla T (2007) Effects of benomyl, carbendazim, fluazinam and thiophanate methyl on white root rot of avocado. Crop Prot 26:1186–1192. https://doi.org/10.1016/j.cropro.2006.10.015

    Article  CAS  Google Scholar 

  • Mansoori B, Dorostkar M (2008) Reactions of some grape cultivars to Dematophora necatrix. Vitis 47:231–233

    Google Scholar 

  • Martínez-Ferri E, Moreno-Ortega G, van den Berg N, Pliego C (2019) Mild water stress-induced priming enhance tolerance to Rosellinia necatrix in susceptible avocado rootstocks. BMC Plant Biol 19:1–15. https://doi.org/10.21203/rs.2.11334/v1

    Article  Google Scholar 

  • Matheron ME (1988) Persistence of systemic activity for fungicides applied to citrus trunks to control Phytophthora gummosis. Plant Dis 72:170

    Article  Google Scholar 

  • McCarty CD, Bitter WP, Cole DA (1974) Comparisons between Troyer and Carrizo citrange. Citrograph 59:294–310

    Google Scholar 

  • Melgarejo Nárdiz P, García-Jiménez J, Jordá Gutiérrez MC, López González MM, Andrés Yebes MF, Duran-Vila N (2010) Patógenos de plantas descritos en España, 2nd edn. Ministerio de Medio Ambiente y Medio Rural y Marino, Madrid

  • Nitta H, Hatamoto M, Kurihisa H (2002) Control of white root rot on Japanese pear using dazomet micro-granules. Bull Hiroshima Pref Agr Res Cent 72:25–34

    Google Scholar 

  • Pal J, Sharma SK, Devi S, Sharma R, Raj H, Karn M, Verma S, Vedukola PR, Sharma A (2020) Screening, identification, and colonization of fungal root endophytes against Dematophora necatrix: a ubiquitous pathogen of fruit trees. Egypt J Biol Pest Control 30:112. https://doi.org/10.1186/s41938-020-00312-2

    Article  Google Scholar 

  • Pliego C, Ramos C, de Vicente A, Cazorla FM (2011) Screening for candidate bacterial biocontrol agents against soilborne fungal plant pathogens. Plant Soil 340:505–520. https://doi.org/10.1007/s11104-010-0615-8

    Article  CAS  Google Scholar 

  • R Development Core Team, 2022. R: a language and environment for statistical computing. R foundation for statistical computing, Vienna. ISBN 3-900051-07-0. http://www.r-project.org/. Accessed 29 June 2022

  • Reforgiato Recupero G, Caruso A, Russo G, Bertolami A (1992) The Flying Dragon trifoliate orange and BA-300 citrange: effects on scion performance. In: Proc. Int. Soc. Citriculture. Acireale, Italy, pp 286–290

  • Registro de Productos Fitosanitarios, 2023. Ministerio de Agricultura, Pesca y Alimentación. https://www.mapa.gob.es/es/agricultura/temas/sanidad-vegetal/productos-fitosanitarios/registro-productos/. Accessed 8 March 2023

  • Ruano-Rosa D, Arjona-Girona I, López-Herrera CJ (2017) Integrated control of avocado white root rot combining low concentrations of fluazinam and Trichoderma spp. Crop Prot 112:363–370. https://doi.org/10.1016/j.cropro.2017.06.024

    Article  CAS  Google Scholar 

  • Ruano-Rosa D, Cazorla FM, Bonilla N, Martínez-Pérez R, De Vicente A, López-Herrera CJ (2014) Biological control of avocado white root rot with combined applications of Trichoderma spp. and rhizobacteria. Eur J Plant Pathol 138:751–762. https://doi.org/10.1007/s10658-013-0347-8

    Article  Google Scholar 

  • Ruano-Rosa D, Del Moral-Navarrete L, Lopez-Herrera CJ (2010) Selection of Trichoderma spp. isolates antagonistic to Rosellinia necatrix. Spanish J Agric Res 8:1084–1097. https://doi.org/10.5424/sjar/2010084-1403

    Article  Google Scholar 

  • Ruano-Rosa D, López-Herrera CJ (2009) Evaluation of Trichoderma spp. as biocontrol agents against avocado white root rot. Biol Control 51:66–71. https://doi.org/10.1016/j.biocontrol.2009.05.005

    Article  Google Scholar 

  • Ruano-Rosa D, Lopez-Herrera CJ (2006) Biocontrol de la podredumbre blanca del aguacate con aislados no-patogénicos de Rosellinia necatrix. In: Montesinos E (ed). Sociedad Española de Fitopatología. XIII Congreso de la Sociedad Española de Fitopatología, Murcia, Spain, p 377

    Google Scholar 

  • Saunt J (1990) Citrus varieties of the world. An illustrated guide. Sinclair International Ltd., Norwich, UK

    Google Scholar 

  • Savage EM, Gardner FE (1965) The Troyer and Carrizo citranges. California Citrograph 50:112–116

    Google Scholar 

  • Schena L, Nigro F, Ippolito A (2002) Identification and detection of Rosellinia necatrix by conventional and real-time Scorpion-PCR. Eur J Plant Pathol 108:355–366. https://doi.org/10.1023/A:1015697813352

    Article  CAS  Google Scholar 

  • Siebert T, Krueger R, Kahn T, Bash J, Vidalakis G (2010) Descriptions of new varieties recently distributed from the Citrus Clonal Protection Program. Citrograph 1:20–26

    Google Scholar 

  • Simko I, Piepho H-P (2012) The area under the disease progress stairs: calculation, advantage, and application. Phytopathology 102:381–389. https://doi.org/10.1094/PHYTO-07-11-0216

    Article  PubMed  Google Scholar 

  • Sivanesan A, Holliday P (1972) Rosellinia necatrix. CMI Descriptions of Pathogenic Fungi and Bacteria. Commonwealth Mycological Institute, Kew, Surrey, England

    Google Scholar 

  • Steel RGD, Torrie JH (1960) Principles and procedures of statistics: with special reference to the biological sciences. McGraw-Hill Book Company, Inc., New York

    Google Scholar 

  • Sztejnberg A, Freeman S, Chet I, Katan J (1987) Control of Rosellinia necatrix in soil and in apple orchard by solarization and Trichoderma harzianum. Plant Dis 71:365–369. https://doi.org/10.1094/PD-71-0365

    Article  Google Scholar 

  • Sztejnberg A, Jabareen H (1985) Dematophora root rot disease in persimmon and studies on resistance of rootstocks to the disease. Alon Hanotea 39:757–762

    Google Scholar 

  • Sztejnberg A, Jabareen H (1986) Studies of resistance of persimmon rootstocks to Dematophora root rot. Phytoparasitica 14:240

    Google Scholar 

  • Sztejnberg A, Madar Z (1980) Host range of Dematophora necatrix, the cause of white root rot disease in fruit trees. Plant Dis 64:662–664. https://doi.org/10.1094/PD-64-662

    Article  Google Scholar 

  • Tallón Vila CI (2015) Biotechnology applied to the genetic improvement of citrus rootstocks. Development of a protocol for micropropagation and adventitious regeneration for use in generating salt toleran mutant lines. Universidad de Murcia, Murcia, Spain

    Google Scholar 

  • ten Hoopen GM, Krauss U (2006) Biology and control of Rosellinia bunodes, Rosellinia necatrix and Rosellinia pepo: a review. Crop Prot 25:89–107. https://doi.org/10.1016/j.cropro.2005.03.009

    Article  Google Scholar 

  • Tienda S, Vida C, Lagendijk E, de Weert S, Linares I, González-Fernández J, Guirado E, de Vicente A, Cazorla FM (2020) Soil application of a formulated biocontrol rhizobacterium, Pseudomonas chlororaphis PCL1606, induces soil suppressiveness by impacting specific microbial communities. Front Microbiol 11:1874. https://doi.org/10.3389/fmicb.2020.01874

    Article  PubMed  PubMed Central  Google Scholar 

  • Vincent JM (1947) Distortion of fungal hyphæ in the presence of certain inhibitors. Nature 159:850. https://doi.org/10.1038/159850b0

    Article  CAS  PubMed  Google Scholar 

  • Wickham H (2016) Data analysis. In: ggplot2. Use R! Springer, Cham, pp 189–201

    Chapter  Google Scholar 

Download references

Acknowledgements

The authors are highly thankful to Agromillora Group for providing the plant material, including Mariàngela Mestre and Joan Torrent, and to “Juan de la Cierva-training” postdoctoral grant from 2021 (FJC2021-047313-I) from Spanish Ministry of Science and Innovation (Ministerio de Ciencia e Innovación). We are also grateful for the technical assistance of Carlos Casanova (Institute for Sustainable Agriculture, Spanish Research Council) and Oliva Inmaculada López Castrillón.

Funding

This research received no external funding.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Juan M. Arjona-López.

Ethics declarations

Competing interests

The authors declare that they have no competing interests.

Additional information

Publisher’s Note

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

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Arjona-López, J., Monferrer-Salinas, J., Cantero-Sánchez, J. et al. Evaluation of susceptibility of commercial citrus rootstocks to white root rot incited by Rosellinia necatrix. J Plant Pathol (2024). https://doi.org/10.1007/s42161-024-01599-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s42161-024-01599-y

Keywords

Navigation