Citrus Greening and Its Management in Citrus Trees

Ishwor Shrestha

Agricultural specialist and vice president of project planning at IAAS Nepal

13 min read
12/12/2024
Citrus Greening and Its Management in Citrus Trees

1. Introduction

Citrus is a globally important horticultural crop, producing an average annual yield of 124,246 thousand tons (FAOSTAT, 2016). Cultivated in over 140 countries (Zhong & Nicolosi, 2020), citrus thrives in diverse agroecological zones, including arid and semi-arid regions (Chandrasekaran et al., 2021). However, Huanglongbing (HLB), commonly known as citrus greening, poses a severe threat to global citrus production (Singerman & Rogers, 2020).

This devastating disease affects all citrus varieties within the Rutaceae family. Sweet oranges and mandarins are highly susceptible, while limes, lemons, and trifoliate oranges show greater resistance (Knapp et al., 2004). Losses caused by HLB are significant: 22% for Kinnow, 25-40% for sweet oranges, 15% for grapefruits, 10% for sweet limes, and 2% for lemons (Akhtar & Ahmed, 1999).

2. Causes of citrus greening

The primary vectors of citrus greening are the Asian Citrus Psyllid (ACP) (Diaphorina citri) and the African Citrus Psyllid (Trioza erytreae). ACP thrives in warm conditions (heat-resistant), while Trioza erytreae is rain- and humidity-tolerant but heat-sensitive (Bove, 2006). These psyllids transmit the gram-negative bacterium that causes HLB and damage plants by feeding on sap, excreting honeydew, and fostering sooty mold growth (Yan et al., 2015).

The three bacterial species responsible for HLB include:

  • Asian form: Candidatus Liberibacter asiaticus (heat-tolerant)
  • African form: Candidatus Liberibacter africanus (heat-sensitive)
  • American form: Candidatus Liberibacter americanus (heat-sensitive) (Tipu et al., 2020).

3. Symptoms

HLB symptoms depend on the tree's age, infection stage, and timing (Johnson et al., 2012). Key symptoms include:

  • Leaf mottling
  • Premature leaf drop
  • Bitter fruits
  • Poor root development
  • Plant death (Bist & Bista, 2020).

Symptoms of HLB in Citrus.jpg

Figure 1: Symptoms of HLB in Citrus: Leaf, Fruit, Pre-Harvest Drop, and Root Loss (Source: Nehela and Killiny,2020)

3.1 Leaf Symptoms

Infected trees experience excessive leaf shedding, off-season blooms, and severe dieback (Martinez, 1972). Symptoms fall into two categories:

  • Primary symptoms: Yellowing of leaves with blotchy mottling (Schneider, 1968).
  • Secondary symptoms: Smaller leaves with chlorotic patterns resembling zinc or iron deficiencies (Aubert, 1979).

LB disease is sometimes confused with micronutrient deficiencies such as zinc. Zinc deficiency typically results in symmetrical chlorosis on both sides of the leaves, while greening disease causes an irregular, asymmetrical mottling without a consistent pattern in citrus leaves (Mattos-Jr et al., 2020).

3.2 Yellow Shoots Symptoms

Blotchy mottling on shoots and branches is a distinctive HLB sign. The discoloration originates from veins and intensifies during cooler seasons (Weinert et al., 2004; McClean & Schwarz, 1970).

3.3 Fruit Symptoms

Affected fruits display green patches, yellowing near the peduncle, and waxy rind marks when pressed (Batool et al., 2007). Infected fruits are prone to decay, premature drop, and reduced sugar levels (Shahzad et al., 2022; Baldwin et al., 2018). Compared to healthy fruits, those impacted by HLB are less responsive to post-harvest degreening treatments (Shahzad et al., 2022). 

3.4 Juice quality

HLB-affected fruit exhibits off-flavors due to reduced sugar levels and increased concentrations of bitter compounds such as limonoids, flavonoids, and terpenoid volatiles (Baldwin et al., 2018). An alternative approach to lessen these bitter compounds in affected citrus fruits is the use of resins (Dala-Paula et al., 2019).

3.5 Root Symptoms

HLB severely damages fibrous roots, leading to poor nutrient distribution and root decay (Aubert, 1987; Zhao, 1981).

4. Management Strategies for Citrus Greening

Here are some management strategies aimed at controlling vectors and reducing the persistence of HLB disease:

4.1 Quarantine and Regulation

The geographic spread of Asian citrus psyllid and citrus greening continues to widen (Hall et al., 2013), with most management interventions proving largely ineffective (Taylor et al., 2019). The primary approach for managing HLB involves removing infected plants, which has a direct impact on the grower’s finances. Therefore, effective collaboration among growers is essential (Singerman & Rogers, 2020). Legislative actions have also been implemented to control the spread of pathogens. The following controls need to be established (Kawano, 1998):

  1. Regulated plants: Rutaceae family, Poncirus trifoliata, Fortunella species, and live citrus plants.
  2. Regulated pathogens and insects: Citrus greening bacteria and citrus psylla.
  3. Protection of mother stock.

4.2 Use of Tolerant Rootstocks

  • US-897 (Citrus reticulata Blanco × Poncirus trifoliata L. Ra.)
  • US-802 (Citrus maxima × Poncirus trifoliata ) and
  • US-812 (‘Sunki’ mandarin × ‘Benecke’ trifoliate orange)

(Source: Albrecht and Bowman, 2012)

4.3 Irrigation, Nutrition Management, and Hormones

Various commercial citrus varieties require an adequate supply of macronutrients to mitigate the effects of citrus greening disease. For mandarin trees, it is recommended to apply 475 g of nitrogen (N), 320 g of phosphorus (P₂O₅), and 355 g of potassium (K₂O) per tree annually (Koseoglu et al. 1995). In addition, micronutrient supplementation with copper sulfate, iron sulfate, and zinc sulfate are advised at a rate of 50 g per tree, either through soil application or via foliar spray at a 0.5% concentration (Shrivastav & Singh, 2009). Fertigation and controlled-release fertilizers have been identified as effective nutrient-delivery methods ( Phuyal et al., 2020). Brassinosteroids, a novel group of phytohormones, have shown potential in managing HLB by reducing symptoms during early bloom, reducing fruit drop, and enhancing yields (Alferez et al., 2019).

4.4 Biological Control

Biological agents like parasitoids (Tamarixia radiata, Diaphorencyrtus aligarhensis) and entomopathogenic fungi (Beauveria bassiana) effectively manage ACP populations (Ghosh et al., 2018).

4.5. Chemical Control

Applying dimethoate 30% EC to the leaves at a concentration of 1 ml/liter of water before the blossoming period effectively reduces psyllid populations (AITC, 2020). 50% Malathion EC, 44% Dimethoate, and 40.64% carbofuran FP revealed potent psylla control (Chen, 1998). Penicillin carbendazim also effectively controls psylla (Cheema et al.,1986). Intensive insecticide application during peak citrus flushes effectively reduces ACP populations (Hall et al., 2013). Horticultural oils and Insect Growth Regulators (IGRs) have proven more effective in targeting psyllid eggs and nymphs than adult psyllids (Grafton-Cardwell et al., 2013).

Carbenicillin, ampicillin, cephalexin, oxytetracycline (OTC), penicillin, rifampicin, streptomycin sulfate, and sulfadimethoxine have demonstrated significant effectiveness in reducing pathogen populations in affected trees (Zhang et al., 2014).

4.6 Intercropping with Guava

Inter-planting citrus with guava helps decrease Asian citrus psyllid infestations, thereby reducing the incidence of HLB (Beattie, 2006). This phenomenon is believed to result from the volatile compounds in guava that deter psyllids or hinder their ability to find and infest citrus trees. Specifically, terpenoids in guava are responsible for repelling psyllids (Silva et al., 2016).

 A newly interplanted Valencia sweet orange and white guava.jpg

Figure 2: A newly interplanted Valencia sweet orange and white guava in an experimental plot at USDA-ARS in Fort Pierce, Florida. (Source: Gottwald et al., 2010).

4.7 Physical and Chemical Repellents

Physical repellents such as kaolin clay particle film and metalized polyethylene mulch, which repel citrus psyllids (Hall et al., 2007; Grafton-Cardwell et al., 2013; Croxton & Stansly, 2014). Additionally, pest exclusion nets are effective in preventing psyllids from accessing citrus trees and crucial to keep trees HLB-free in the early growth stages (Alferez, 2019). Volatile compounds found in garlic chives such as disulfides and trisulfides, along with volatile oils from non-host plants like Lantana camara, Mikania micrantha and Eupatorium catarium, have been shown to effectively reduce psyllid populations (Yijing et al., 2005; Mann et al., 2011).

4.8 Tree Removal and Replacement

Severely infected trees (50–70%) should be removed to prevent further disease spread (Baniqued, 1998).

4.9 Other Management Practices

Effective management of citrus psyllids requires timely pesticide application, which involves pest monitoring through scouting and the use of yellow sticky traps to determine the optimal timing for control actions (Halbert & Manjunath, 2004; Hall et al., 2013). Research has shown that trees treated with oak extract showed improved stomatal conductance, increased chlorophyll content, and nitrogen uptake (Pitino et al., 2020).

Strategies for managing HLB include foliar spraying, root drenching, and trunk injection of antibiotics (Zhang et al., 2011; Puttamuk et al., 2014).

Cylinder traps were set up in a citrus grove in Temecula.png

Figure 3: Cylinder traps were set up in a citrus grove in Temecula, CA. (Source: Snyder et al., 2022)

Conclusion

Citrus greening is a major threat to the global citrus industry, manifesting through mottled leaves, defoliation, fruit distortion, and tree death. While there is no definitive cure, integrated management strategies—combining quarantine, biological control, nutrient management, and vector control—can mitigate the disease’s impact.

Sustained research and adoption of these measures are vital to restoring citrus orchard health and productivity worldwide.

Further reading

Pest, Disease and Weed Management

How to Cultivate Lemon Trees Commercially

Pest and Weed Management in Lemon Orchards

Important Citrus Diseases caused by Fungi

Important Virus Diseases in Citrus trees

Bacterial Citrus Diseases: Identification and Control

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Ishwor Shrestha
Agricultural specialist and vice president of project planning at IAAS Nepal

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