Citrus Gummosis: A Formidable Challenge to Citrus Industry: A Review

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Review Paper 01/05/2020
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Citrus Gummosis: A Formidable Challenge to Citrus Industry: A Review

Nasir Ahmed Rajput, Muhammad Atiq, Hamza Tariq, Warda Modassar Saddique, Akhtar Hameed.
Int. J. Biosci.16( 5), 131-144, May 2020.
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Citrus is the most valuable fruit all over the world as well as Pakistan due to its taste, nutritional and medicinal qualities. All the citrus producing regions are facing threat due to a soil borne water loving pathogen Phytophthora species. Gummosis is the major disease which destroying the backbone of citrus industry. Several Phytophthora species was responsible for the citrus gummosis globally and leads to substantial yield losses annually. The infected tree shows decline symptom in combination with chlorosis of leaves, twigs dieback, discolored or poor colored fruits, wilting of tips and leaves withering. The infected twigs show gummosis, browning of the cortex, defoliation and desiccation. Symptoms are clearly seen on the above ground parts near the soil. Cracks and cankers are visible on the barks, branches and trunks and exude gum. Branches give a bleeding appearance. As it is a soil borne pathogen, so the symptoms are observed from the baseline to upward on the tree from main to secondary branches. While the taproots and crowns necrosis were observed with the increase severity of the infection expand necrotic lesions and the results showed tree declining and death. Many identification methods and control strategies are reviewed with more comprehensive management to use Phytophthora-free nursery, resistant rootstocks and economical phytochemical fungicides for the best management of citrus gummosis disease.


Ahmed Y, D’onghia AM, Ippolito A, El Shimy H, Cirvilleri G, Yaseen T. 2012. Phytophthora nicotianae is the predominant Phytophthora species in citrus nurseries in Egypt. Phytopathologia Mediterranea 1, 519-527.

Alvarez LA, Vicent A, Bascón J, Abad-Campos P, Armengol J. 2008. Branch cankers on citrus trees in Spain caused by Phytophthora citrophthora. Plant Pathology 57, 84–91.

Alves TCA, Tessmann DJ, Ivors KL, Ristaino JB, Santos AF. 2016. First Report of Gummosis Caused by Phytophthora frigida on Black Wattle in Brazil. Plant Disease 100, 2336.

Anil KS, Arun KS, Vashishtha B. 2004. Fruit breeding approach and achievements. Central Institute for Arid Horticulture Beechwal Industrial Area, Shri Ganganagar Highway Rajasthan, India.

Assuah M, Oduro K, Ofuso Budu K. 1999. Diplod ia natalensis Pole Evans, the causal agent of citrus gummosis disease in Ghana. Ghana Journal of Agricultural Science 32, 11-18.

Bairwa SR, Srivastava AK, Kumar P, Meena RS, Koli CR. 2015. Developing strategies for integrated management of Phytophthora root rot and gummosis in kinnow mandarin (Citrus reticulata). Indian Phytopathology 68, 101-105.

Beever RE, Waipara NW, Ramsfield TD, Dick MA, Horner IJ. 2009. Kauri (Agathis australis) under threat from Phytophthora. Phytophthoras in forests and natural ecosystems 74, p 74-85.

Benson DM, Grand LF, Vernia CS, Gottwald TR. 2006. Temporal and spatial epidemiology of Phytophthora root rot in Fraser fir plantations. Plant Disease 90, 1171-1180.

Benyahia H, Mouloud MAH, Jrifi A, Lamsettef Y. 2004. Effect of salinity in irrigation water on the colonization of citrus rootstocks by Phytophthora parasitica. Fruits 59, 101-108.

Brasier CM. 2000. The role of Phytophthora pathogens in forests and semi-natural communities in Europe and Africa. Phytophthora Diseases of Forest Trees p 6-13.

Boccas B, Leville E. 1978. Phytophthora diseases of Citrus (Les maladies a Phytophthora des agrumes. Institute de recherches sure les Fruits et Agrumes) 162 p.

Cacciola SO, di San Lio GM. 2008. Management of citrus diseases caused by Phytophthora spp. integrated management of diseases caused by fungi, Phytoplasma and bacteria (p 61-84). Springer, Dordrecht.

Cacciola SO, Raudino F, Lo Gidice V, Magnano San Lio G. 2007. Citrus root system disease. Phytopathological informant The defense of plants 57, 9-22.

Campanella V, Ippolito A, Nigro F. 2002. Activity of calcium salts in controlling Phytophthora root rot of citrus. Crop Protection 21, 751-756.

Choudhari RJ, Gade RM, Lad RS, Adinarayana J, Phanindra KB. 2018. Epidemiological relations to Phytophthora spp. causing citrus root rot in Nagpur Mandarin. International journal of current microbiology and applied sciences 6, 406-417.

Chowdappa P, Kumar BJN, Kumar SPM, Madhura S, Bhargavi BR, Lakshmi MJ. 2016. Population structure of Phytophthora nicotianae reveals host specific lineages on brinjal, ridge gourd, and tomato in South India. Phytopathology 106, 1553-1562.

Colburn GC, Graham JH. 2007. Protection of citrus rootstocks against Phytophthora spp. with a hypovirulent isolate of Phytophthora nicotianae. Phytopathology 97, 958-963.

Davison EM, Tay FC. 2005. How many soil samples are needed to show that Phytophthora is absent from sites in the south-west of Western Australia? Australasian Plant Pathology 34, 293-297.

Dhakad UK, Kaur S, Thind SK, Badaya VK. 2015. Factors favouring the development of foot rot pathogen (Phytophthora nicotianae var. parasitica) in Punjab. The Ecoscan 7, 135-138.

Drenth A, Guest DI. 2004. Diversity and management of Phytophthora in Southeast Asia. Australian Centre for International Agricultural Research.

Erwin DC, Ribeiro OK. 1996. Phytophthora Diseases Worldwide. American Phytopathological Society.

FAO – Food and Agricultural Organization of the United Nations, Rome. 2017. Citrus fruits fresh and processed statistical bulletin 2016. 1-53.

Fawcett HS. 1936. Citrus diseases and their control (Second Edition), p 656.

Feichtenberger E. 2001. Doenças incitadas por Phytophthora em citros. In: Luz EDMN, Matsuoka K, Santos AF, Bezerra JL, editors. Doenças causadas por Phytophthora no Brasil. Campinas. Livraria Rural p 283-342.

Feichtenberger E, Bassanezi RB, Spósito MB, Belasque J Jr. 2005. Doenças dos citros. In: Kimati H, Amorim L, Filho AB, Camargo LEA, Rezende JAM, editors. Manual de fitopatologia. 4th ed. São Paulo (BR): Editora Agronômica Ceres. (Doenças das plantas cultivadas) 2, 239-269.

Gade RM, Koche MD. 2012. Integrated disease management for root rot and gummosis in Nagpur mandarin. Indian Phytopathology 65, 272-275.

Gade RM, Lad RS. 2018. Biological management of major citrus diseases in Central India-a review. International Journal of Current Microbiology and Applied Sciences 6, 296-308.

Gade RM, Giri GK. 2005. Integration of soil solarization and fungicides for management of Phytophthora sp. in citrus nursery. Indian Phytopathology 58, 114-116.

GOP – Government of Pakistan. 2016. Ministry of National food security and research Economic wing Islamabad. Fruit, vegetables and condiments Statistics of Pakistan p 1-107.

Graham J, Feichtenberger E. 2015. Citrus Phytophthora diseases: Management challenges and successes. Journal of Citrus Pathology 2, 1-11.

Graham JH, Timmer LW. 2006. Phytophthora diseases of citrus. University of Florida, IFAS extension.

Graham  JH,  Bright  DB,  McCoy  CW.  2003. PhytophthoraDiaprepes weevil complex: Phytophthora spp. relationships with citrus rootstocks. Plant Disease 87, 85-90.

Grant T, Klotz L, Wallace J. 1953. Foot Rot of Citrus Trees. Yearbook of Agriculture p 734.

Guajardo J, Riquelme N, Tapia L, Larach A, Torres C, Camps R, Besoain X. 2018. First Report of Lasiodiplodia theobromae Causing Bot Gummosis in Citrus limon in Chile. Plant Disease 102, 818. 

Ho HH, Jong SC. 1989. Phytophthora nicotianae (P. parasitica). Mycotaxon 35, 243-275.

Hong CX, Moorman GW. 2005. Plant pathogens in irrigation water: challenges and opportunities. Critical Reviews in Plant Sciences 24, p 189-208.

Hulvey J, Gobena D, Finley L, Lamour K. 2010. Co-occurrence and genotypic distribution of Phytophthora species recovered from watersheds and plant nurseries of eastern Tennessee. Mycologia 102, 1127-1133.

Hyun IH, Choi W. 2014. Phytophthora species, new threats to the plant health in Korea. Plant Pathology Journal 30, 331-342.

Ippolito A, Schena L, Nigro F, Ligorio VS, Yaseen T. 2004. Real-time detection of Phytophthora nicotianae and P. citrophthorain citrus roots and soil. European Journal of Plant Pathology 110, 833-843.

Ippolito A, Schena L, Nigro F. 2002. Detection of Phytophthora nicotianae and P. citrophthora in citrus roots and soils by nested PCR. European Journal of Plant Pathology 108, 855-868.

Iqbal Z, Ahmad S, Asim M, Rehman MA, Rehman A, Raza W, Raza M, Bilal MS, Abid HU. 2020. Management of Phytophthora species associated with citrus decline in Pakistan. International Journal of Botany Studies 5, 98-103. 

Jagtap GP, Dhavale MC, Dey U. 2012a. Evaluation of natural plant extracts, antagonists and fungicides in controlling root rot, collar rot, fruit (brown) rot and gummosis of citrus caused by Phytophthora spp. in vitro. International journal of Microbiology 1, p 27-47.

Jagtap GP, Thosar RU, Dey U. 2012b. Evaluation of plant extracts and bioagents for the control of gummosis of mandarin orange (Citrus reticulata blanko) caused by Phytophthora species. African Journal of Agricultural Research 7, 4553-4558.

Jung T, Blaschke H, Obwald W. 2000. Involvement of soilborne Phytophthora species in Central European oak decline and the effect of site factors on the disease. Plant Pathology 49, 706-718.

Lende AS, Gade RM, Shitole AV. 2015. Management of Phytophthora root rot in Nagpur mandarin by using integrated approach. In: Proceedings of National Conference on Harmony with Nature in Context of Bioresources and Environmental Health. The Bioscan 332-336.

Leoni C, Ghini R. 2006. Sewage sludge effect on management of Phytophthora nicotianae in citrus. Crop Protection 25, 10-22.

Li B, Liu P, Xie S, Yin R, Weng Q, Chen Q. 2015. Specific and Sensitive Detection of Phytophthora nicotianae by Nested PCR and Loop-mediated Isothermal Amplification Assays. Journal of Phytopathology 163, 185-193.

Magnano di San Lio G, Cacciola SO, Marziano F, Pane A, Raudino F. 2002. Protezione integrate dell’agrumeto dalle malattie fungine. Informatore fitopatologico – La difesa delle piante 52, 13-23.

Mekonen M, Ayalew A, Weldetsadik K, Seid A. 2000. Assessing and Measuring of Citrus gummosis (Phytophthora spp.) in Major Citrus Growing Areas of Ethiopia. Journal of Horticulture 2, 1-4.

Melo JF, da Silva Martins E, Kupper KC. 2017. Production of antifungal compounds by Trichoderma spp. to control Phytophthora nicotianae, causal agent of gummosis on citrus. Citrus Research & Technology 36, 37-46.

Meng Y, Zhang Q, Ding W, Shan W. 2014. Phytophthora parasitica: a model oomycete plant pathogen. Mycology 5, 43-51.

Meng J, Wang Y. 2010. Rapid detection of Phytophthora nicotianae in infected tobacco tissues and soil samples based on its Ypt1 gene. Journal of Phytopathology 158, 1-7.

M’hamdi NB, 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.

Mounde LG, Ateka EM, Kihurani AW, Wasilwa L, Thuranira EG. 2009. Occurrence and distribution of citrus gummosis (Phytophthora spp.) in Kenya. African Journal of Horticultural Science 2, 56-68.

Naqvi SAMH, Singh S. 2002. Fungal diseases of citrus: Diagnosis and Management. Technical Bulletin National research Centre for citrus (NRCC) 5, 61-67.

Naqvi SAMH. 2000. Managing Phytophthora diseases on citrus. Indian Horticulture 44, 5-9.

Naqvi SAMH. 2004. Diagnosis and management of certain important fungal diseases of citrus. In Diseases of Fruits and Vegetables, Springer, Dordrecht 1, p 247-290.

Naqvi SAMH. 2006. Distribution of citrus Phytophthora spp. and mating types pathogenic to citrus in Central India. Journal of Mycology and Plant Pathology 36, 44-48.

Ohr HD, Menge JA. 2006. Diseases. UC IPM Online pest management guidelines: Citrus. UC ANR Publication 3441.

Prigigallo MI, Mosca S, Cacciola SO, Cooke DE, Schena L. 2015. Molecular analysis of Phytophthora diversity in nursery‐grown ornamental and fruit plants. Plant pathology 64, 1308-1319.

Quyet NT, Cuong HV, Hong LT, Soytong K. 2016. Control mechanism of Chaetomium spp. and its biological control of Citrus root rot in pot and field experiments in Vietnam. Journal of Agricultural Technology 12, 329-336.

Rajput NA, Zhang M, Shen D, Liu T, Zhang Q, Ru Y, Sun P, Dou D. 2015. Overexpression of a Phytophthora Cytoplasmic CRN Effector Confers Resistance to Disease, Salinity and Drought in Nicotiana benthamiana. Plant and Cell Physiology 56, 2423-2435.

Rather TR, Razdan VK, Tewari AK, Shanaz E, Bhat ZA, Hassan MG, Wani TA. 2012. Integrated management of wilt complex disease in bell pepper (Capsicum annuum L.). Journal of agricultural science 4, 141-147.

Ristaino JB, Gumpertz ML. 2000. New frontiers in the study of dispersal and spatial analysis of epidemics cause by species in the genus Phytophthora. Annual Review of Phytopathology 38, 541–576.

Sadeghy B, Salari M, Shahidi Bonjar GH, Panjekeh N, Aminnaee M. 2014. A preliminary study of biological control of citrus gummosis by soil-borne Streptomyces sp. isolates in vitro condition. Archives of Phytopathology and Plant Protection 47, 774-779.

Santos AF dos, Luz EDMN, Souza JT. 2005. Phytophthora nicotianae: agente etiológico da gomose da acácia negra no Brasil. Fitopatologia Brasileira 30, 81–84.

Savita GS, Nagpal A. 2012. Citrus diseases caused by Phytophthora species. Green Earth Research Foundation Bulletin of Biosciences 3, 18-27.

Schillaci G, Caruso L. 2006. Problematiche della difesa meccanizzata degli agrumi nel bacino del mediterraneo. Informatore Fitopatologico-La difesa delle piante 56, 21-24.

Swingle W T, Reece PC. 1967. The botany of Citrus and its wild relatives. In: Reuther W, Webber HJ, Batchelor LD (eds) The Citrus Industry, History, world distribution, botany, and varieties, Revised Edition. University of California Press, Berkeley 1, p 190-430.

Timmer LW, Peever TL, Solel Z, Akimitsu K. 2003. Alternaria diseases of citrus novel pathosystems. Phytopathologia Mediterranea 42, 99–112.

Tomita N, Mori Y, Kanda H, Notomi T. 2008. Loop-mediated isothermal amplification (LAMP) of gene sequences and simple visual detection of products. Nature Protocols 3, 877- 882.

Vannini A, Brown A, Brasier C, Vettraino AM. 2009. The search for Phytophthora centers of origin: Phytophthora species in mountain ecosystems in Nepal. Phytophthoras in Forests and Natural Ecosystems p 54-61.

Wagh SP, Gade RM, Lad RS, Adinarayana J, Phanindra KBVN. 2018. Epidemiological relations to population dynamics of Phytophthora spp. in mandarin. Indian Phytopathology 71, 213-218.

Wu GA, Terol J, Ibanez V, López-García A, Pérez-román E, Borredá C, Domingo C, Tadeo FR, Carbonell-caballero J, Alonso, R, Curk F, Du D, Ollitrault P, Roose ML, Dopazo J, Gmitter FG, Rokhsar DS, Talon M. 2018. Genomics of the origin and evolution of Citrus. Nature 554, 311–316.

Zitko SE, Timmer LW, Sandler HA. 1991. Isolation of Phytophthora palmivora pathogenic to citrus in Florida. Plant Disease 75, 532-535.