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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
REVIEW

Systematic review of defense responses against Phytophthora and strategies to manage Phytophthora diseases in citrus

Adielle R. da Silva https://orcid.org/0000-0003-1419-3061 A , Kaliane N. S. Pinto B , Bianca E. Maserti C , Hermes P. Santos-Filho D and Abelmon da S. Gesteira https://orcid.org/0000-0002-7590-0455 D E
+ Author Affiliations
- Author Affiliations

A Departamento de Ciências Biológicas, Universidade Estadual de Santa Cruz, Campus Soane Nazaré de Andrade, Rodovia Jorge Amado, km 16, 45662-900, Ilhéus, BA, Brazil.

B Departamento de Ciências Agrárias, Universidade Federal do Recôncavo da Bahia, Cruz das Almas, Bahia 44380-000, Brazil.

C Consiglio Nazionale delle Ricerche, Institute of Biophysics, Via S. Lorenzo, I–56100 Pisa, Italy.

D Embrapa Mandioca e Fruticultura. Cruz das Almas, Bahia 44380-000, Brazil.

E Corresponding author. Email: abelmon.gesteira@embrapa.br

Functional Plant Biology 48(10) 963-972 https://doi.org/10.1071/FP20349
Submitted: 7 November 2020  Accepted: 20 May 2021   Published: 15 June 2021

Abstract

Phytophthora spp. are the causal agents of gummosis or foot rot, fibrous root rot, and fruit brown rot diseases that affect the roots, trunk, and fruits of citrus trees, causing severe economic losses. This work presents an updated systematic review addressing the defence responses in citrus against Phytophthora and the strategies to manage Phytophthora diseases. Applying a new method of search based on an explicit, rigorous, and transparent methodology. For this purpose, a systematic literature review was conducted using the databases available for academic research. The main plant defence mechanisms reported in the cited papers are the hypersensitivity response, cell wall reinforcement, production of pathogenesis-related proteins, and expression of defence-related genes. Moreover, the main strategies to manage Phytophthora root rot are organic compounds in the soil and biological control with fungi and bacteria. In addition, inhibition of Phytophthora gummosis or canker by applying new oomycota fungicides and reducing the incidence of brown fruit rot through the application of potassium phosphite have also been reported. Moreover, modern plant biotechnology techniques can help to accelerate the selection of resistant rootstocks in breeding programs, as controlled crossings for the generation of hybrids, somatic hybridisation, transgenic citrus plants, mapped genomic regions of Quantitative Trait Loci (QTLs), candidate genes, metabolic markers and comparative transcriptomic. These innovative techniques represent a suitable tool to breed new Phytophthora resistant rootstocks, which is widely recognised as the best strategy to face gummosis or foot rot, fibrous root rot and ultimately minimise the expensive use of pesticides in crop protection.

Keywords: citrus, disease resistance, disease management, plant defense mechanisms, fungal pathogens, Phytophthora.


References

Adaskaveg JE, Forster H (2014) Integrated postharvest strategies for management of Phytophthora brown rot of Citrus in the United States. In Prusky D, Gullino ML Plant Pathology in the 21st Century: Post-Harvest Pathology, Eds. Springer International Publishing, Cham, Switzerland, pp. 123–131.

Adaskaveg JE, Hao W, Förster H (2015) Postharvest strategies for managing Phytophthora brown rot of citrus using potassium phosphite in combination with heat treatments. Plant Disease 99, 1477–1482.
Postharvest strategies for managing Phytophthora brown rot of citrus using potassium phosphite in combination with heat treatments.Crossref | GoogleScholarGoogle Scholar | 30695947PubMed |

Afek U, Sztejnberg A (1989) Effects of fosetyl-Al and phosphorous acid on scoparone, a phytoalexin associated with resistance of citrus to Phytophthora citrophthora. Phytopathology 79, 736–739.
Effects of fosetyl-Al and phosphorous acid on scoparone, a phytoalexin associated with resistance of citrus to Phytophthora citrophthora.Crossref | GoogleScholarGoogle Scholar |

Ahmed Y, D’Onghia AM, Ippolito A, Yaseen T (2014) First report of citrus root rot caused by Phytophthora palmivora in Egypt. Plant Disease 98, 155
First report of citrus root rot caused by Phytophthora palmivora in Egypt.Crossref | GoogleScholarGoogle Scholar | 30708589PubMed |

Ajengui A, Bertolini E, Ligorio A, Chebil S, Ippolito A, Sanzani SM (2018) Comparative transcriptome analysis of two citrus germplasms with contrasting susceptibility to Phytophthora nicotianae provides new insights into tolerance mechanisms. Plant Cell Reports 37, 483–499.
Comparative transcriptome analysis of two citrus germplasms with contrasting susceptibility to Phytophthora nicotianae provides new insights into tolerance mechanisms.Crossref | GoogleScholarGoogle Scholar | 29290008PubMed |

Alvarez LA, Vicent A, De Roca E, Bascón J, Abad-campos P, Armengol J (2008) Branch cankers on citrus trees in Spain caused by Phytophthora citrophthora. Plant Pathology 57, 84–91.
Branch cankers on citrus trees in Spain caused by Phytophthora citrophthora.Crossref | GoogleScholarGoogle Scholar |

Biasi A, Martin FN, Cacciola SO, di San Lio GM, Grünwald NJ, Schena L (2016) Genetic analysis of Phytophthora nicotianae populations from different hosts using microsatellite markers. Phytopathology 106, 1006–1014.
Genetic analysis of Phytophthora nicotianae populations from different hosts using microsatellite markers.Crossref | GoogleScholarGoogle Scholar | 27111805PubMed |

Boava LP, Cristofani-yaly M, Mafra VS, Kubo K, Kishi LT, Takita MA, Ribeiro-Alves M, Machado MA (2011) Global gene expression of Poncirus trifoliata, Citrus sunki and their hybrids under infection of Phytophthora parasitica. BMC Genomics 12, 39
Global gene expression of Poncirus trifoliata, Citrus sunki and their hybrids under infection of Phytophthora parasitica.Crossref | GoogleScholarGoogle Scholar | 21241495PubMed |

Boughalleb-M’hamdi N, Benfradj N, Migliorini D, Luchi N, Santini A (2018) Phytophthora nicotianae and P. cryptogea causing gummosis of citrus crops in Tunisia. Tropical Plant Pathology 43, 36–48.
Phytophthora nicotianae and P. cryptogea causing gummosis of citrus crops in Tunisia.Crossref | GoogleScholarGoogle Scholar |

Burdon JJ, Thrall PH (2009) Coevolution of plants and their pathogens in natural habitats. Science 324, 755–756.
Coevolution of plants and their pathogens in natural habitats.Crossref | GoogleScholarGoogle Scholar | 19423818PubMed |

Cacciola SO, Magnano Di San Lio G (2008) Management of citrus diseases caused by Phytophthora spp. In Phytoplasma and bacteria (eds) Integrated management of diseases caused by fungi. Springer Netherlands, pp. 61–84.

Calixto  MCMourão Filho  FDAMendes  BMJVieira  MLC2004 Somatic hybridization between Citrus sinensis (L.) Osbeck and C. grandis (L.) Osbeck.Pesquisa Agropecuária Brasileira 39 72172410.1590/S0100-204X2004000700015

Campanella V, Ippolito A, Nigro F (2002) Activity of calcium salts in controlling Phytophthora root rot of citrus. Crop Protection 21, 751–756.
Activity of calcium salts in controlling Phytophthora root rot of citrus.Crossref | GoogleScholarGoogle Scholar |

Colburn GC, Graham JH (2007) Protection of citrus rootstocks against Phytophthora spp. with a hypovirulent isolate of Phytophthora nicotianae. Phytopathology 97, 958–963.
Protection of citrus rootstocks against Phytophthora spp. with a hypovirulent isolate of Phytophthora nicotianae.Crossref | GoogleScholarGoogle Scholar | 18943635PubMed |

Dalio RJD, Magalhaes DM, Rodrigues CM, Arena GD, Oliveira TS, Souza-Neto RR, Picchi SC, Martins PMM, Santos PJC, Maximo HJ, Pacheco IS, De Souza AA, Machado MA (2017) PAMPs, PRRs, effectors and R-genes associated with Citrus-Pathogen interactions. Annals of Botany 119, 749–774.
PAMPs, PRRs, effectors and R-genes associated with Citrus-Pathogen interactions.Crossref | GoogleScholarGoogle Scholar | 28065920PubMed |

Dalio RJD, Máximo HJ, Oliveira TS, Azevedo T de M, Felizatti HL, Campos M de A, Machado MA (2018a) Molecular basis of citrus Sunki susceptibility and Poncirus trifoliata resistance upon Phytophthora parasitica Attack. Molecular Plant-Microbe Interactions 31, 386–398.
Molecular basis of citrus Sunki susceptibility and Poncirus trifoliata resistance upon Phytophthora parasitica Attack.Crossref | GoogleScholarGoogle Scholar | 29125028PubMed |

Dalio RJD, Maximo HJ, Oliveira TS, Dias RO, Breton MC, Felizatti H, Machado M (2018b) Phytophthora parasitica effector PpRxLR2 suppresses Nicotiana benthamiana immunity. Molecular Plant-Microbe Interactions 31, 481–493.
Phytophthora parasitica effector PpRxLR2 suppresses Nicotiana benthamiana immunity.Crossref | GoogleScholarGoogle Scholar | 29165046PubMed |

Drenth A, Guest DI (2004) Diversity and Management of Phytophthora in Southeast Asia. Australian Centre for international Agricultural Research, Canberra, Australia, p.238.

Fagoaga C, Rodrigo I, Conejero V, Hinarejos C, Tuset JJ, Arnau J, Pina JA, Navarro L, Peña L (2001) Increased tolerance to Phytophthora citrophthora in transgenic orange plants constitutively expressing a tomato pathogenesis related protein PR-5. Molecular Breeding 7, 175–185.
Increased tolerance to Phytophthora citrophthora in transgenic orange plants constitutively expressing a tomato pathogenesis related protein PR-5.Crossref | GoogleScholarGoogle Scholar |

Faldoni L, Cristofani-Yaly M, Boava LP, Schinor EH, Kupper KC (2015) Effect of organic manure in the induction of resistance of Citrus to Phytophthora parasitica. Journal of Agriculture Science 7, 135–143.
Effect of organic manure in the induction of resistance of Citrus to Phytophthora parasitica.Crossref | GoogleScholarGoogle Scholar |

Fang JG, Tsao PH (1995) Efficacy of Penicillium funiculosum as a biological control agent against Phytophthora root rots of azalea and citrus. Phytopathology 85, 871–878.
Efficacy of Penicillium funiculosum as a biological control agent against Phytophthora root rots of azalea and citrus.Crossref | GoogleScholarGoogle Scholar |

FAOSTAT (2020) Food and Agriculture Organization of the United Nations. http://www.fao.org/faostat/en/#data/QC/visualize

Flor HH (1971) The current status of the gene-for-gene concept. Annual Review of Phytopathology 9, 275–296.
The current status of the gene-for-gene concept.Crossref | GoogleScholarGoogle Scholar |

Graham J, Feichtenberger E (2015) Citrus Phytophthora diseases: Management challenges and successes. Journal of Citrus Pathology 2, iocv_journalcitruspathology_27203

Gray MA, Hao W, Förster H, Adaskaveg JE (2018) Baseline sensitivities of new fungicides and their toxicity to selected life stages of Phytophthora species from citrus in California. Plant Disease 102, 734–742.
Baseline sensitivities of new fungicides and their toxicity to selected life stages of Phytophthora species from citrus in California.Crossref | GoogleScholarGoogle Scholar | 30673403PubMed |

Hao W, Miles TD, Martin FN, Browne GT, Förster H, Adaskaveg JE (2018) Temporal occurrence and niche preferences of Phytophthora spp. causing brown rot of citrus in the central valley of California. Phytopathology 108, 384–391.
Temporal occurrence and niche preferences of Phytophthora spp. causing brown rot of citrus in the central valley of California.Crossref | GoogleScholarGoogle Scholar | 29053435PubMed |

Hao W, Gray MA, Förster H, Adaskaveg JE (2019) Evaluation of new oomycota fungicides for management of Phytophthora root rot of citrus in California. Plant Disease 103, 619–628.
Evaluation of new oomycota fungicides for management of Phytophthora root rot of citrus in California.Crossref | GoogleScholarGoogle Scholar | 30789317PubMed |

Harzing AW (2020). Harzing’s Publish or Perish software, version 7.19.2739. Available from: <https://harzing.com/resources/publish-or-perish>.

Ippolito A, Schena L, Nigro F, Soleti Ligorio V, Yaseen T (2004) Real-time detection of Phytophthora nicotianae and P. citrophthora in citrus roots and soil. European Journal of Plant Pathology 110, 833–843.
Real-time detection of Phytophthora nicotianae and P. citrophthora in citrus roots and soil.Crossref | GoogleScholarGoogle Scholar |

Leoni C, Ghini R (2006) Sewage sludge effect on management of Phytophthora nicotianae in citrus. Crop Protection 25, 10–22.
Sewage sludge effect on management of Phytophthora nicotianae in citrus.Crossref | GoogleScholarGoogle Scholar |

Lima RPM, Curtolo M, Merfa MV, Cristofani-Yaly M, Machado MA (2018a) QTLs and eQTLs mapping related to citrandarins’ resistance to citrus gummosis disease. BMC Genomics 19, 516
QTLs and eQTLs mapping related to citrandarins’ resistance to citrus gummosis disease.Crossref | GoogleScholarGoogle Scholar | 29969985PubMed |

Lima RPM, Máximo HJ, Merfa MV, Dalio RJD, Cristofani-Yaly M, Machado MA (2018b) Genetic tools and strategies for citrus breeding aiming at resistant rootstocks to gummosis disease. Tropical Plant Pathology 43, 279–288.
Genetic tools and strategies for citrus breeding aiming at resistant rootstocks to gummosis disease.Crossref | GoogleScholarGoogle Scholar |

Mammella MA, Cacciola SO, Martin F, Schena L (2011) Genetic characterization of Phytophthora nicotianae by the analysis of polymorphic regions of the mitochondrial DNA. Fungal Biology 115, 432–442.
Genetic characterization of Phytophthora nicotianae by the analysis of polymorphic regions of the mitochondrial DNA.Crossref | GoogleScholarGoogle Scholar | 21530925PubMed |

Matheron ME, Matejka JC (1990) Differential virulence of Phytophthora parasitica recovered from citrus and other plants to rough lemon and tomato. Plant Disease 74, 138–140.
Differential virulence of Phytophthora parasitica recovered from citrus and other plants to rough lemon and tomato.Crossref | GoogleScholarGoogle Scholar |

Matheron ME, Porchas M (2002) Comparative ability of six fungicides to inhibit development of Phytophthora gummosis on Citrus. Plant Disease 86, 687–690.
Comparative ability of six fungicides to inhibit development of Phytophthora gummosis on Citrus.Crossref | GoogleScholarGoogle Scholar | 30823246PubMed |

Matheron ME, Wright GC, Porchas M (1998) Resistance to Phytophthora citrophthora and P. parasitica and nursery characteristics of several Citrus rootstocks. Plant Disease 82, 1217–1225.
Resistance to Phytophthora citrophthora and P. parasitica and nursery characteristics of several Citrus rootstocks.Crossref | GoogleScholarGoogle Scholar | 30845409PubMed |

Máximo HJ, Dalio RJD, Rodrigues CM, Breton MC, Machado MA (2017) Reference genes for RT-qPCR analysis in Citrus and Poncirus infected by zoospores of Phytophthora parasitica. Tropical Plant Pathology 42, 76–85.
Reference genes for RT-qPCR analysis in Citrus and Poncirus infected by zoospores of Phytophthora parasitica.Crossref | GoogleScholarGoogle Scholar |

Meitz-Hopkins JC, Pretorius MC, Spies CFJ, Huisman L, Botha WJ, Langenhoven SD, McLeod A (2014) Phytophthora species distribution in South African citrus production regions. European Journal of Plant Pathology 138, 733–749.
Phytophthora species distribution in South African citrus production regions.Crossref | GoogleScholarGoogle Scholar |

Meng Y, Zhang Q, Ding W, Shan W (2014) Phytophthora parasitica: a model oomycete plant pathogen. Mycology 5, 43–51.
Phytophthora parasitica: a model oomycete plant pathogen.Crossref | GoogleScholarGoogle Scholar | 24999436PubMed |

Mourão Filho FA, Pio R, Madalena B, Mendes BMJ, Azevedo FA, Schinor EH, Entelmann FA, Alves ASR, Cantuarias-Avilés TE (2008) Evaluation of citrus somatic hybrids for tolerance to Phytophthora nicotianae and citrus tristeza virus. Scientia Horticulturae 115, 301–308.
Evaluation of citrus somatic hybrids for tolerance to Phytophthora nicotianae and citrus tristeza virus.Crossref | GoogleScholarGoogle Scholar |

Panabières F, Ali GS, Allagui MB, Dalio RJD, Gudmestad NC, Kuhn ML, Guha Roy S, Schena L, Antonios Z (2016) Phytophthora nicotianae diseases worldwide: new knowledge of a long-recognised pathogen. Phytopathologia Mediterranea 55, 20–40.
Phytophthora nicotianae diseases worldwide: new knowledge of a long-recognised pathogen.Crossref | GoogleScholarGoogle Scholar |

Puglisi I, De Patrizio A, Schena L, Jung T, Evoli M, Pane A, Van Hoa N, Van Tri M, Wright S, Ramstedt M, Olsson C, Faedda R, Magnano Di San Lio GM, Cacciola SO (2017) Two previously unknown Phytophthora species associated with brown rot of Pomelo (Citrus grandis) fruits in Vietnam. PLoS One 12, e0172085
Two previously unknown Phytophthora species associated with brown rot of Pomelo (Citrus grandis) fruits in Vietnam.Crossref | GoogleScholarGoogle Scholar | 28208159PubMed |

Queiroz BPV, Melo IS (2006) Antagonism of Serratia marcescens towards Phytophthora parasitica and its effects in promoting the growth of citrus. Brazilian Journal of Microbiology 37, 448–450.
Antagonism of Serratia marcescens towards Phytophthora parasitica and its effects in promoting the growth of citrus.Crossref | GoogleScholarGoogle Scholar |

Şahin-Çevik M, Çevik B, Karaca G (2014) Expression analysis of WRKY genes from Poncirus trifoliata in response to pathogen infection. Journal of Plant Interactions 9, 182–193.
Expression analysis of WRKY genes from Poncirus trifoliata in response to pathogen infection.Crossref | GoogleScholarGoogle Scholar |

Sakupwanya MN, Labuschagne N, Loots T, Apostolides Z (2018) Towards developing a metabolic-marker based predictive model for Phytophthora nicotianae tolerance in citrus rootstocks. Journal of Plant Pathology 100, 269–277.
Towards developing a metabolic-marker based predictive model for Phytophthora nicotianae tolerance in citrus rootstocks.Crossref | GoogleScholarGoogle Scholar |

Siviero A, Cristofani M, Furtado EL, Garcia AAF, Coelho ASG, Machado MA (2006) Identification of QTLs associated with citrus resistance to Phytophthora gummosis. Journal of Applied Genetics 47, 23–28.
Identification of QTLs associated with citrus resistance to Phytophthora gummosis.Crossref | GoogleScholarGoogle Scholar | 16424605PubMed |

Spies CFJ, Meitz-Hopkins JC, Langenhoven SD, Pretorius MC, McLeod A (2014) Two clonal lineages of Phytophthora citrophthora from citrus in South Africa represent a single phylogenetic species. Mycologia 106, 1106–1118.
Two clonal lineages of Phytophthora citrophthora from citrus in South Africa represent a single phylogenetic species.Crossref | GoogleScholarGoogle Scholar |

Timmer LW, Graham JH, Zitko SE (1998) Metalaxyl-resistant isolate of Phytophthora nicotianae: Occurrence, sensitivity, and competitive parasitic ability on citrus. Plant Disease 82, 254–261.
Metalaxyl-resistant isolate of Phytophthora nicotianae: Occurrence, sensitivity, and competitive parasitic ability on citrus.Crossref | GoogleScholarGoogle Scholar | 30856812PubMed |

Watanarojanaporn N, Boonkerd N, Wongkaew S, Prommanop P, Teaumroong N (2011) Selection of arbuscular mycorrhizal fungi for citrus growth promotion and Phytophthora suppression. Scientia Horticulturae 128, 423–433.
Selection of arbuscular mycorrhizal fungi for citrus growth promotion and Phytophthora suppression.Crossref | GoogleScholarGoogle Scholar |

Widmer TL, Graham JH, Mitchell DJ (1998) Composted municipal waste reduces infection of Citrus seedlings by Phytophthora nicotianae. Plant Disease 82, 683–688.
Composted municipal waste reduces infection of Citrus seedlings by Phytophthora nicotianae.Crossref | GoogleScholarGoogle Scholar | 30857022PubMed |

Yan H, Zhong Y, Jiang B, Zhou B, Wu B, Zhong G (2017) Guanggan (Citrus reticulata) shows strong resistance to Phytophthora nicotianae. Scientia Horticulturae 225, 141–149.
Guanggan (Citrus reticulata) shows strong resistance to Phytophthora nicotianae.Crossref | GoogleScholarGoogle Scholar |