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Cronicon OPEN ACCESS EC EC AGRICULTURE AGRICULTURE Review Article Citrus Leprosis and its Impacts on Citrus Food Industry: A Review Fazal ur Rehman 1 *, Maria Kalsoom 2 , Sohail Ahmad 1 , Muhammad Asif Iqbal 1 , Sanwal Junaid 3 , Muhammad Abdullah Tariq 1 , Aftab Sultan 1 , Qaisar Hayat 1 and Javaid Khan 1 1 Department of Plant Pathology, College of Agriculture, University of Sargodha, Pakistan 2 Department of Food Science and Technology, University of Sargodha, Pakistan 3 Department of Entomology, College of Agriculture, University of Sargodha, Pakistan Citation: Fazal ur Rehman., et al. “Citrus Leprosis and its Impacts on Citrus Food Industry: A Review”. EC Agriculture 6.5 (2020): 34-39. *Corresponding Author: Fazal ur Rehman, Department of Plant Pathology, College of Agriculture, University of Sargodha, Pakistan. Received: March 24, 2020; Published: April 07, 2020 Abstract Citrus Leprosis is one of the major viral disease of citrus. It is caused by Laprosis virus that is transmitted by feeding of Brevipalpus phoenicis and Brevipalpus californicus, the female mites of Tenuipalpidae family. It contributes a lot to the total losses caused by citrus pathogens. Its effects both the production and the processing of citrus. Today about 100 millions of US dollars are spent to control the Brevipalpus phoenicis and Brevipalpus californicus, the vectors of Citrus Leprosis, annually. The symptoms of the diseased plants are zonate lesions on leaves and fruits and bark scaling on the trunk. It has confused symptomology with Citrus Psorosis disease caused by Citrus Psorosis Virus (CPsV). This review article has the information about the history of Citrus Leprosis, range of host, etiology, vector, symptoms, impacts on citrus industry and integrated management practices. Keywords: Brevipalpus Mites; Citrus Leprosis Virus; Citrus Food Industry; Secondary Metabolites; Integrated Management History of Citrus Leprosis Initially this disease was given the name of scaly bark disease because scaly symptoms were induced over the stem. It was also called Nail Head Rust because of symptomatic lesions on stem and fruit [1,2] . In 1901, in Florida, Hume observed and described the scaly symptoms that were present on the stem [3]. At the time, there were no consociated symptoms of the disease over the fruits and leaves. F.P. Patterson suggested that the fungus Hysterographium was might be its causal organism. Fawcett, in 1908, made the microscopic studies for demonstration and identification of its causal organism but he was failed to do so [4]. In 1909, Fawcett concluded that Hormodendron species was the causal organism of this disease [5]. Then Cladosporium herbarium Var. citri was reported as a causal organism of Citrus Leprosis in 1911 by Fawcett [6]. Still there were no evidence of its etiol- ogy. The recommended treatment was just spray of copper-based fungicides. But it was noticed that spray of copper based fungicides enhanced the incidence of scaly bark. The spray of oil mainly reduced the mite vector. The Citrus Leprosis was also given the name of “Va- riola” in 1930s in Brazil. In 1950, Knorr accounted that female spider mites were fraternized with Citrus Leprosis disease in Florida [7]. Later he demonstrated that Brevipalpus obovatus had an ability to induce the symptoms of Citrus Leprosis. He also demonstrated that the vector of CiLV in Florida was Brevipalpus californicus [8].

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Page 1: PDF - CroniconFazal ur Rehman 1*, Maria Kalsoom2, Sohail Ahmad, Muhammad Asif Iqbal1, Sanwal Junaid3, Muhammad Abdullah Tariq 1 , Aftab Sultan , Qaisar Hayat 1 and Javaid Khan 1 1

CroniconO P E N A C C E S S EC EC AGRICULTURE AGRICULTURE

Review Article

Citrus Leprosis and its Impacts on Citrus Food Industry: A Review

Fazal ur Rehman1*, Maria Kalsoom2, Sohail Ahmad1, Muhammad Asif Iqbal1, Sanwal Junaid3, Muhammad Abdullah Tariq1, Aftab Sultan1, Qaisar Hayat1 and Javaid Khan1

1Department of Plant Pathology, College of Agriculture, University of Sargodha, Pakistan 2Department of Food Science and Technology, University of Sargodha, Pakistan 3Department of Entomology, College of Agriculture, University of Sargodha, Pakistan

Citation: Fazal ur Rehman., et al. “Citrus Leprosis and its Impacts on Citrus Food Industry: A Review”. EC Agriculture 6.5 (2020): 34-39.

*Corresponding Author: Fazal ur Rehman, Department of Plant Pathology, College of Agriculture, University of Sargodha, Pakistan.

Received: March 24, 2020; Published: April 07, 2020

Abstract

Citrus Leprosis is one of the major viral disease of citrus. It is caused by Laprosis virus that is transmitted by feeding of Brevipalpus phoenicis and Brevipalpus californicus, the female mites of Tenuipalpidae family. It contributes a lot to the total losses caused by citrus pathogens. Its effects both the production and the processing of citrus. Today about 100 millions of US dollars are spent to control the Brevipalpus phoenicis and Brevipalpus californicus, the vectors of Citrus Leprosis, annually. The symptoms of the diseased plants are zonate lesions on leaves and fruits and bark scaling on the trunk. It has confused symptomology with Citrus Psorosis disease caused by Citrus Psorosis Virus (CPsV). This review article has the information about the history of Citrus Leprosis, range of host, etiology, vector, symptoms, impacts on citrus industry and integrated management practices.

Keywords: Brevipalpus Mites; Citrus Leprosis Virus; Citrus Food Industry; Secondary Metabolites; Integrated Management

History of Citrus Leprosis

Initially this disease was given the name of scaly bark disease because scaly symptoms were induced over the stem. It was also called Nail Head Rust because of symptomatic lesions on stem and fruit [1,2].

In 1901, in Florida, Hume observed and described the scaly symptoms that were present on the stem [3]. At the time, there were no consociated symptoms of the disease over the fruits and leaves. F.P. Patterson suggested that the fungus Hysterographium was might be its causal organism. Fawcett, in 1908, made the microscopic studies for demonstration and identification of its causal organism but he was failed to do so [4]. In 1909, Fawcett concluded that Hormodendron species was the causal organism of this disease [5]. Then Cladosporium herbarium Var. citri was reported as a causal organism of Citrus Leprosis in 1911 by Fawcett [6]. Still there were no evidence of its etiol-ogy. The recommended treatment was just spray of copper-based fungicides. But it was noticed that spray of copper based fungicides enhanced the incidence of scaly bark. The spray of oil mainly reduced the mite vector. The Citrus Leprosis was also given the name of “Va-riola” in 1930s in Brazil. In 1950, Knorr accounted that female spider mites were fraternized with Citrus Leprosis disease in Florida [7]. Later he demonstrated that Brevipalpus obovatus had an ability to induce the symptoms of Citrus Leprosis. He also demonstrated that the vector of CiLV in Florida was Brevipalpus californicus [8].

Page 2: PDF - CroniconFazal ur Rehman 1*, Maria Kalsoom2, Sohail Ahmad, Muhammad Asif Iqbal1, Sanwal Junaid3, Muhammad Abdullah Tariq 1 , Aftab Sultan , Qaisar Hayat 1 and Javaid Khan 1 1

Citation: Fazal ur Rehman., et al. “Citrus Leprosis and its Impacts on Citrus Food Industry: A Review”. EC Agriculture 6.5 (2020): 34-39.

35

Citrus Leprosis and its Impacts on Citrus Food Industry: A Review

Musumeci and Rossettic (1963) demonstrated that the transfer of Brevipalpus phoenicis was associated with the transfer of disease from diseased plant to the healthy plant and also produced the symptoms of Citrus Leprosis on the seedling of citrus [9]. After word there was a great controversy over the subject of its etiology. But there were many evidences of its viral etiology. It was demonstrated by the studies of Rodeigues., et al. (1997) that the particles similar to CiLV in lesions were also present in viruliferous Brevipalpus californicus. These particles were not present in the mites that were newly hatched from the eggs and they didn’t have the ability to produce symptoms. The CiLV was persistent virus and the viruliferous mites were able to reproduce the symptoms of Citrus Leprosis disease throughout their life. It was demonstrated that the virus had an ability to multiply itself in the body of Brevipalpus mites. The infestation of spider mites of genus Brevipalpus were directly associated with Citrus Leprosis disease.

Host range

Several species of Rutaceae family that are founded in the Asia. The plants of Rutaceae family are evergreen and are grown for the fruit and ornamental purposes. In Asia, Citrus sinensis is totally susceptible to Citrus Leprosis. Under natural conditions, Lemons (Citrus limon), mandarins (Citrus reticulata, Citrus reshni, Citrus deliciosa), grapefruits (Citrus paradisi) and hybrids (Murcott) are comparatively less in-fected by Citrus Leprosis Virus. There is no any other plant that can serve as the host of as CiLV. Although there are some other plants of herbaceous species including Chenopodium amaranticolor or Chenopodium quinoa etc. on which when virus is inoculated mechanically the same types of symptoms are produced [11]. It was also demonstrated that the virus, when isolated from the infected alternate host including Chenopodium amaranticolor or Chenopodium quinoa, was not able to transmit Citrus Leprosis Virus back into the plants of Ru-taceae family [12].

The pathogen

The Citrus Leprosis Virus belongs to family Rhabdovidae and is single stranded RNA negative virus. This virus is Bacillus like, short, cylindrical and rode shaped. They are about 120 - 130 nm and their width is about 50 nm [13]. The other dense and viroplasm like inclu-sion bodies are also associated with these particles. They are usually elliptical with about 4µm in diameter [14]. It is noted that single inclusion body is present in one cell. There viral particles may be present in nucleus or in cytoplasm and cause infection there [11,13,15]. It is observed that the both nuclear type and cytoplasmic type infection are mostly present in parenchyma and epidermal cells. But it is very less common to present in vascular parenchyma cells. The nuclear type Citrus Leprosis Virus is referred as CiLV-N and cytoplasmic type as CiLV-C. The CiLV- C prevails in citrus orchards and CiLV-N occurs rarely [16].

Symptoms

The symptoms lesions of Citrus Leprosis are visible over fruits, twigs and leaves. The severeness of these lesions varies according with the area and variety of the citrus. On leaves, there are dark brown central spots of diameter 2 to 3 mm and these spots are surrounded by yellow helo. There are 1 to 3 brown colored rings which circle around the brown colored spots. These lesions are also called zonate lesions because they are ring shaped [17]. It is noted that the overall size of zonate lesion is about 20mm and in some cases lesion coalesce with each other and form larger lesions. The fruit that have symptomatic lesion fall down before maturation, resulting in too much losses in yield. The symptoms of Citrus Leprosis are also confused with Citrus Canker (caused by Xanthomonas axonopodis) because of presence of brown spots with yellow helo [18]. The symptoms over the trunk are also like Citrus Psorosis (caused by Citrus Psorosis Virus), but the difference is that there is no wood staining in Citrus Leprosis that is present in case of Citrus Psorosis [19]. Bark scaling symptoms are present over the trunk.

Page 3: PDF - CroniconFazal ur Rehman 1*, Maria Kalsoom2, Sohail Ahmad, Muhammad Asif Iqbal1, Sanwal Junaid3, Muhammad Abdullah Tariq 1 , Aftab Sultan , Qaisar Hayat 1 and Javaid Khan 1 1

Citation: Fazal ur Rehman., et al. “Citrus Leprosis and its Impacts on Citrus Food Industry: A Review”. EC Agriculture 6.5 (2020): 34-39.

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Citrus Leprosis and its Impacts on Citrus Food Industry: A Review

Figure 1: Symptomatic lesions on the fruit.

Figure 2: Symptomatic Zonate lesions present on the leaves.

Figure 3: Bark scaling symptoms on twigs.

Page 4: PDF - CroniconFazal ur Rehman 1*, Maria Kalsoom2, Sohail Ahmad, Muhammad Asif Iqbal1, Sanwal Junaid3, Muhammad Abdullah Tariq 1 , Aftab Sultan , Qaisar Hayat 1 and Javaid Khan 1 1

Citation: Fazal ur Rehman., et al. “Citrus Leprosis and its Impacts on Citrus Food Industry: A Review”. EC Agriculture 6.5 (2020): 34-39.

37

Citrus Leprosis and its Impacts on Citrus Food Industry: A Review

Impact over food industry

Citrus Leprosis disease is a major, devastating and widespread disease. The potential of damage depends upon the susceptibility of citrus cultivar. This disease can cause up to 100% losses [20]. Other than the yield reduction by fall of fruit, this disease also effects the concentrate that is used in citrus juice and processing industries. The attractiveness of orange is determined by color and appearance of peel. Because in case of Citrus Leprosis disease, the peel of orange is adversely affected. Therefore, Citrus Leprosis has a great impact over the fresh fruit citrus industries. The symptomatic fruit are full of brown lesions. For determining the quality of orange juice produced, the physiochemical properties play an important role. The use of citrus products in our diet plays an important role in providing secondary metabolites, including limonoids, flavonoids, hydroxycinnamic acid and polyamines, that are vital for human health. When disease attacks over the fruit, the fruit becomes stressed. Under stressed conditions, the classes of secondary metabolites become changed [20]. Gener-ally, the quality of juice prepared from uninfected fruit is equal to the juice prepared from the orange that are infected by Citrus Leprosis Virus. But the juice from infected oranges have more amount of tangertin, hepta methoxy flavone, limonin glucoside and vicenin-2. Due to which, the quality of juice produced from diseased oranges is reduced.

Economic losses

In Pakistan total citrus growing area is about 206,569 hectares and total production of orange in Pakistan is 2.36 million tonns in 2015-16 and about 80.3% of total production is produced in Punjab [21]. Due to huge production of citrus in Sargodha, Sargodha is called the Florida of Pakistan. There are many citrus diseases that are contributing a lot in the reduction of yield of citrus. Therefore, firstly economic losses are caused by reduction in yield and secondly, if the mite vectors are not properly controlled, they will cause too much losses in quantity as well as quality. When the lesions due to Citrus Leprosis disease are present on fruit, they will lose their commercial values for both consumption and processing. The fruits with symptomatic lesions of Citrus Leprosis disease are also unfit for export and due to which the export is adversely affected.

It is particularly noted that when the commercial prices of fruit are high then former do more chemical and mechanical practices for controlling the mite vectors. But when the prices of fruit become down then there are reduced control measures for controlling the insect vectors. Due to this negligence of farmers, the incidence of Citrus Leprosis disease becomes increased in citrus orchards. This will result in too much economic losses only due to Citrus Leprosis disease.

Integrated management practices

As Citrus Leprosis Virus is transmitted by the vectors including Brevipalpus phoenicis and Brevipalpus californicus. When Brevipalpus species feed over the infected plants, they become viruliferous. When they feed over the uninfected plants, the virus is transmitted to that plants. Therefore, we must control the Brevipalpus mites for controlling the Citrus Leprosis disease. There are many recommended chemi-cal products that are being used in these days for controlling mites. These are Cyhexatin, Azocyclotin, Hexythiazon and Propargite. The other organoestanic acaricides may also be used [22]. The predaceous mites of Phytoseiidae family can also be used for controlling the female spider mites of Brevipalpus species. The other biofertilizers and entomophagous fungi can also be used to control mites. The other cultural practices including pruning, control of weeds and use of wind break can also reduce the reservoirs for the vector [23,24].

Conclusion

Majorly the economic importance of citrus lies in their fruit. But in the case of Citrus Leprosis disease, the fruit is adversely affected by this disease. Citrus Leprosis disease. caused by Citrus Leprosis Virus and transmitted by vector mites of Brevipalpus family, is widespread disease that affects millions of citrus plants every year. Due to alarming rate of spread of CiLV, particularly in South China, North India,

Page 5: PDF - CroniconFazal ur Rehman 1*, Maria Kalsoom2, Sohail Ahmad, Muhammad Asif Iqbal1, Sanwal Junaid3, Muhammad Abdullah Tariq 1 , Aftab Sultan , Qaisar Hayat 1 and Javaid Khan 1 1

Citation: Fazal ur Rehman., et al. “Citrus Leprosis and its Impacts on Citrus Food Industry: A Review”. EC Agriculture 6.5 (2020): 34-39.

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Citrus Leprosis and its Impacts on Citrus Food Industry: A Review

Japan, Philippines, Egypt, South Africa, Brazil, Argentina, Venezuela, Colombia, Panama, Nicaragua, Guatemala, Mexico etc., Integrated Management Practices are applied for the control of this disease. Citrus Leprosis disease has non-systematic nature of infection and it can be transmitted by vector mites of Brevipalpus family. We must make our control over vector mites to cope with and get rid of this disease.

Bibliography

1. Fawcett HS. “Citrus Diseases and Their Control”. 2nd edition. McGraw-Hill, New York (1936).

2. Rodrigues JCV., et al. “Occurrence and distribution of Citrus leprosis virus in Honduras”. Plant Pathology 56.2 (2007): 344.

3. Hume HH. “Some fungous diseases of citrus and others fruits”. Proceedings of the Florida State Horticultural Society 14 (1901): 64-70.

4. Fawcett HS. “Report of assistant plant pathologist”. Florida Agricultural Experiment Station, Rept (1908).

5. Fawcett HS. “Report of assistant plant pathologist”. Florida Agricultural Experiment Station, Gaines ville (1909).

6. Fawcett HS. “Scaly bark or nail-head rust of citrus”. Bulletin 106, Florida Agricultural Experiment Station, Gainesville, FA (1911): 41.

7. Knorr LC. “Etiological association of a Brevipalpus mite with Florida scaly bark of citrus”. Phytopathology 40 (1950): 15.

8. Knorr LC. “Studies on the etiology of leprosis in citrus”. Conference of the International Organization of Citrus Virologists 4 (1968): 332-340.

9. Musumeci MR and Rossetti V. “Transmissão dos sintomas da leprose pelo ácaro Brevipalpus phoenicis”. Ciência e Cultura 15 (1963): 228.

10. Rodrigues JCV and Machado MA. “Virus-Brevipalpus-plant relationships of the citrus leprosis pathosystem”. Proceedings of the Inter-national Society of Citriculture, Orlando (2000): 768-770.

11. Colariccio A., et al. “Mechanical transmission and ultrastructural aspects of citrus leprosis disease”. Fitopatologia Brasileira 20 (1995): 208-213.

12. Lovisolo 0. “Citrus leprosis virus. properties, diagnosis, agro-ecology, and phytosanitary importance”. EPPO Bulletin 31.1 (2001): 79-89.

13. Kitajima EW., et al. “Short rod-like particles associated with citrus leprosis”. Virology 50.1 (1972): 254-258.

14. Agrios, George N. “Plant pathology”. George Agrios. 5th edition (1936).

15. Kitajima EW., et al. “[Electron microscopy of leaf tissues of orange trees infected by “lepra explosiva” in Argentina]”. Fitopatologia (Lima) 9 (1974): 55-56.

16. Rodrigues JCV., et al. “Citrus leprosis virus vectored by Brevipalpus phoenicis (Acari: Tenuipalpidae) on citrus in Brazil”. Experimental and Applied Acarology 30.1-3 (2003): 161-179.

17. Gomes RT., et al. “Anatomical comparison of citrus leprosis (cytoplasmic and nuclear types), citrus zonate chlorosis and citrus chlo-rotic ringblotch lesions”. Virus Reviews and Research 9.1 (2004): 246.

18. Rossetti V. “[Differentiation between citrus canker and other diseases]”. Citrus 1 (1980): 23-26.

19. Anonymous. “Citrus leprosis virus (CiLV) Bitancourt”. NAPPO Phytosanitary Alert System (2006).

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Citation: Fazal ur Rehman., et al. “Citrus Leprosis and its Impacts on Citrus Food Industry: A Review”. EC Agriculture 6.5 (2020): 34-39.

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Citrus Leprosis and its Impacts on Citrus Food Industry: A Review

20. Poiroux-Gonord F., et al. “Metabolism in orange fruits is drive by photooxidative stress in the leaves”. Physiologia Plantarum 149.2 (2013): 175-187.

21. Muhammad Imran Siddique and Elena Garnevska. “Citrus Value Chain(s): A Survey of Pakistan Citrus Industry, Agricultural Value Chain, Gokhan Egilmez”. IntechOpen (2017).

22. Alves EB. “Dinâmica da resistência de Brevipalpus phoenicis (Geijskes, 1939) (Acari: Tenuipalpidae) ao acaricida dicofol”. Tese (Dou-torado em Ciências) - Escola Superior de Agricultura “Luiz de Queiroz”, Universidade de São Paulo, Piracicaba (2004).

23. Rodrigues JCV and Machado MA. “Virus-Brevipalpus-plant relationships of the citrus leprosis pathosystem”. Proceedings of the Inter-national Society of Citriculture, Orlando (2000): 768-770.

24. Salva RA and Massari CA. “Situação do ácaro da leprose no estado de São Paulo, levantamento – Fundecitrus”. In: Oliveira CAL; Dona-dio LC (ed.) Leprose dos citros. Jaboticabal: FUNEP (1995): 13-18.

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