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Ghosh, D.;  Kokane, S.;  Savita, B.K.;  Kumar, P.;  Sharma, A.K.;  Ozcan, A.;  Kokane, A.;  Santra, S. Huanglongbing Pandemic: Current Challenges and Emerging Management Strategies. Encyclopedia. Available online: https://encyclopedia.pub/entry/40246 (accessed on 06 December 2025).
Ghosh D,  Kokane S,  Savita BK,  Kumar P,  Sharma AK,  Ozcan A, et al. Huanglongbing Pandemic: Current Challenges and Emerging Management Strategies. Encyclopedia. Available at: https://encyclopedia.pub/entry/40246. Accessed December 06, 2025.
Ghosh, Dilip, Sunil Kokane, Brajesh Kumar Savita, Pranav Kumar, Ashwani Kumar Sharma, Ali Ozcan, Amol Kokane, Swadeshmukul Santra. "Huanglongbing Pandemic: Current Challenges and Emerging Management Strategies" Encyclopedia, https://encyclopedia.pub/entry/40246 (accessed December 06, 2025).
Ghosh, D.,  Kokane, S.,  Savita, B.K.,  Kumar, P.,  Sharma, A.K.,  Ozcan, A.,  Kokane, A., & Santra, S. (2023, January 16). Huanglongbing Pandemic: Current Challenges and Emerging Management Strategies. In Encyclopedia. https://encyclopedia.pub/entry/40246
Ghosh, Dilip, et al. "Huanglongbing Pandemic: Current Challenges and Emerging Management Strategies." Encyclopedia. Web. 16 January, 2023.
Huanglongbing Pandemic: Current Challenges and Emerging Management Strategies
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This entry is adapted from the peer-reviewed paper 10.3390/plants12010160

Huanglongbing (HLB, aka citrus greening), one of the most devastating diseases of citrus, has wreaked havoc on the global citrus industry in recent decades. The culprit behind such a gloomy scenario is the phloem-limited bacteria “Candidatus Liberibacter asiaticus” (CLas), which are transmitted via psyllid. To date, there are no effective long-termcommercialized control measures for HLB, making it increasingly difficult to prevent the disease spread. To combat HLB effectively, introduction of multipronged management strategies towards controlling CLas population within the phloem system is deemed necessary. This entry presents a comprehensive review of up-to-date scientific information about HLB, including currently available management practices and unprecedented challenges associated with the disease control. Additionally, a triangular disease management approach has been introduced targeting pathogen, host, and vector. Pathogen-targeting approaches include (i) inhibition of important proteins of CLas, (ii) use of the most efficient antimicrobial or immunity-inducing compounds to suppress the growth of CLas, and (iii) use of tools to suppress or kill the CLas. Approaches for targeting the host include (i) improvement of the host immune system, (ii) effective use of transgenic variety to build the host’s resistance against CLas, and (iii) induction of systemic acquired resistance. Strategies for targeting the vector include (i) chemical and biological control and (ii) eradication of HLB-affected trees. Finally, a hypothetical model for integrated disease management has been discussed to mitigate the HLB pandemic.

HLB pandemic citrus greening Candidatus Liberibacter asiaticus

1. Introduction

Citrus is the most widely grown specialty fruit crop in the world, containing a variety of health-promoting compounds, including vitamin C. The crop is highly vulnerable to various fungal, bacterial, and viral diseases, owing to its narrow genetic diversity [1]. Huanglongbing (HLB, aka citrus greening) is one of the most devastating diseases, which has affected the global citrus industry during last few decades [2][3]. The disease was first reported in southern China [4]. The discovery of HLB in India was attributed to a citrus dieback in the 1700s [5][6], resulting in a hypothesis that the disease was established in India before spreading to China [3][7]. A similar malady was observed in South Africa in 1929 and named “citrus greening disease” based on the poor color development of the stylar end of affected fruit [8]. The disease was also confirmed in South America, in the state of Sao Paulo in Brazil in 2004 [9], and in the state of Florida in the USA [10]. It has seriously impacted the US citrus industry, with an approximate loss of USD 3.6 billion per year [11]. In the USA, the disease was also detected in other states, including two significant citrus-producing states, Texas [12] and California [13], as well as in South Carolina, Georgia, and Louisiana [14]. The disease had also become established in several Caribbean countries such as Cuba [15], Jamaica [16], Belize [17], and Mexico [18]. Other major citrus-growing areas of the Mediterranean Basin and Australia are under threat. The disease also has moved west from Pakistan into Iran [19] and is threatening the neighboring areas. Presently, the disease is distributed in over 58 countries of Asia, America, Africa, Oceania, and the Caribbean. Reports are based on symptomatology, DNA-DNA hybridization with specific probe, PCR followed by Xbal restriction digestion of the amplified DNA, electron microscopy, and real-time PCR (Figure 1, Table 1) [20].
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Figure 1. The world map represents geographical distribution of HLB based on DNA-DNA hybridization with probe, PCR followed by Xbal restriction digestion of the amplified DNA, electron microscopy, and symptomatology.
Table 1. Worldwide distribution of HLB disease.
Sr. No Continent/Country/Region Distribution of HLB Causal Organism Reference
  Asia      
1 Bangladesh Present Ca. Liberibacter asiaticus [21]
2 Bhutan Present Ca. Liberibacter asiaticus [22]
3 Cambodia Present Ca. Liberibacter asiaticus [23]
4 China Present Ca. Liberibacter asiaticus [22]
5 India Present, Widespread Ca. Liberibacter asiaticus [24]
6 Indonesia Present Ca. Liberibacter asiaticus [25]
7 Iran Present, Localized Ca. Liberibacter asiaticus [26]
8 Japan Present Ca. Liberibacter asiaticus [27]
9 Laos Present Ca. Liberibacter asiaticus [23]
10 Malaysia Present, Localized Ca. Liberibacter asiaticus [24]
11 Myanmar Present Ca. Liberibacter asiaticus [23]
12 Nepal Present, Widespread Ca. Liberibacter asiaticus [28]
13 Oman Present, Localized Ca. Liberibacter asiaticus [22]
14 Pakistan Present Ca. Liberibacter asiaticus [29]
15 Philippines Present, Widespread Ca. Liberibacter asiaticus [29]
16 Saudi Arabia Present, Localized Ca. Liberibacter asiaticus [30]
17 Sri Lanka Present Ca. Liberibacter asiaticus [22]
18 Taiwan Present, Widespread Ca. Liberibacter asiaticus [22]
19 Thailand Present Ca. Liberibacter asiaticus [31]
20 Vietnam Present, Localized Ca. Liberibacter asiaticus [32]
21 Yemen Present, Localized Ca. Liberibacter asiaticus [30]
  North America   Ca. Liberibacter asiaticus  
22 Barbados Present, Localized Ca. Liberibacter asiaticus [22]
23 Belize Present, Localized Ca. Liberibacter asiaticus [17]
24 Costa Rica Present, Localized Ca. Liberibacter asiaticus [22]
25 Cuba Present, Widespread Ca. Liberibacter asiaticus [22]
26 Dominica Present, Few occurrences Ca. Liberibacter asiaticus [22]
27 Dominican Republic Present, Localized Ca. Liberibacter asiaticus [22]
28 El Salvador Present Unknown [33]
29 Guadeloupe Present, Localized Unknown [34]
30 Guatemala Present Ca. Liberibacter asiaticus [22]
31 Honduras Present Ca. Liberibacter asiaticus [22]
32 Jamaica Present, Widespread Ca. Liberibacter asiaticus [22]
33 Martinique Present, Localized Ca. Liberibacter asiaticus [34]
34 Mexico Present, Localized Ca. Liberibacter asiaticus [22]
35 Nicaragua Present Ca. Liberibacter asiaticus [22]
36 Panama Present, Localized Ca. Liberibacter asiaticus [22]
37 Puerto Rico Present Ca. Liberibacter asiaticus [22]
38 Trinidad and Tobago Present, Localized Ca. Liberibacter asiaticus [22]
39 U.S. Virgin Islands Present, Few occurrences Ca. Liberibacter asiaticus [22]
40 United States Present, Localized Ca. Liberibacter asiaticus [22]
  South America      
41 Argentina Present, Localized Ca. Liberibacter asiaticus [22]
42 Brazil Present, Localized Ca. Liberibacter americanus and Ca. Liberibacter asiaticus [9]
43 Colombia Present, Few occurrences Ca.Liberibacter asiaticus [22]
44 Paraguay Present, Localized Ca. Liberibacter asiaticus [35]
45 Venezuela Present Ca. Liberibacter asiaticus [36]
  Africa      
46 Burundi Present Ca. Liberibacter africanus [37]
47 Cameroon Present Ca. Liberibacter africanus [37]
48 Central African Republic Present Ca. Liberibacter africanus [37]
49 Comoros Present Ca. Liberibacter africanus [22]
50 Eswatini Present Ca. Liberibacter africanus [38]
51 Ethiopia Present Ca. Liberibacter africanus and
Ca. Liberibacter asiaticus		 [37]
52 Kenya Present Ca. Liberibacter africanus [29]
53 Madagascar Present Ca. Liberibacter africanus [38]
54 Malawi Present Ca. Liberibacter africanus [37]
55 Mauritius Present Ca. Liberibacter africanus and
Ca. Liberibacter asiaticus		 [22]
56 Rwanda Present Ca. Liberibacter africanus [37]
57 Somalia Present Ca. Liberibacter africanus [22]
58 South Africa Present, Localized Ca. Liberibacter africanus [39]
59 Tanzania Present, Localized Ca. Liberibacter africanus [38]
60 Uganda Present Ca. Liberibacter africanus [40]
61 Zimbabwe Present, Localized Ca. Liberibacter africanus [29]
Typical symptoms of the disease are yellowing of shoots with mottled blotchy leaves (partly yellow/green, with several shades of yellow blending), corky veins, and green islands as depicted in Figure 2 [41][42]. The localized symptoms of greening eventually spread on the entire canopy and finally cause defoliation and tree dieback [43]. The symptoms of the chlorotic pattern often resemble zinc and iron deficiencies, as well as other diseases such as citrus tristeza, citrus stubborn, and phytophthora infection [44][45][46]. It is often seen that fruits from infected trees are small, lopsided, poorly colored, and bitter in taste (Figure 2). The root system is found to be underdeveloped due to starvation that leads to loss of fibrous roots [47]. All the species and hybrids of citrus, irrespective of their rootstock, are susceptible to the greening disease. However, symptoms vary from cultivar to cultivar, with the most severe found on sweet orange (C. sinensis), mandarin (C. reticulata), tangelo (C. tangelo), and grapefruit (C. grandis). Less severe symptoms are observed on lemon, rough lemon, and sour orange [2]. There are no known resistant citrus species for the disease, but some cultivars are more tolerant. For example, grapefruit is more tolerant than sweet orange. The pomelo (Citrus maxima) and kumquat (Fortunella margarita) cultivar were initially considered as tolerant but eventually became infected and started showing mottling symptoms [2][48].
Plants 12 00160 g002
Figure 2. (A) HLB-infected sweet orange plant in the field showing characteristic yellow shoot symptoms at initial stage. (B) HLB-infected sweet orange in the field at severe stage. (C) Healthy leaf. (D) Vein yellowing and corking. (E) Vein corking. (F) Blotchy mottle (a random pattern of chlorosis). (G) Narrow leaf with blotchy mottle. (H) Green island. (I) HLB-affected with color inversion and misshapen sweet orange fruit (lopsided) with aborted seeds.

2. Causative Agent, Genomics, and Pathogenesis Mechanism

The pathogen associated with HLB was initially thought to be a mycoplasma-like organism. Subsequent electron microscopic studies confirmed that the causative organism is a bacterium. The fastidious nature of the pathogen was an impediment in traditional taxonomical classification like the study of morphology and growth characteristics. The phloem-limited causal agent was classified based on the 16S rRNA gene sequence and grouped under the α-subdivision of proteobacteria, genus Candidatus Liberibacter in the family Rhizobiaceae [49][50]. So far, three species of bacterium are known to be associated with citrus greening disease: ‘Candidatus Liberibacter asiaticus’ (CLas), ‘Candidatus Liberibacter africanus’ (CLaf), and ‘Candidatus Liberibacter americanus’ (CLam). To date, no successful attempts have been made to grow these bacteria in culture.
Among them, CLas is the most destructive, widely prevalent, highly divergent, and has caused significant economic loss in citrus production globally [51]. CLam and CLaf are only present in Brazil and Africa, respectively. CLam, originally identified in Brazil, was the major species, but later CLas became the most prevalent species [52]. This intracellular plant pathogen acts as an insect symbiont and is transmitted by two sap-sucking insect species, Diaphorinacitri and Triozaerytreae. D. citri isalso known as the Asian citrus psyllid (ACP) (Figure 3). The ACP is responsible for the spread of CLas and CLam in Asia as well as in the Americas [53]. The ACP is heat-tolerant and can withstand high temperatures (up to 45 °C) but is sensitive to high humidity (above 90%) [54]. On the other hand, T. erytreae, African citrus psyllid (AfCP), the vector for spread of CLaf in Africa [29], is heat-sensitive. The adult and juvenile forms grow in a cool, moist environment and cannot withstand temperatures above 32 °C [55]. The rapid spread of HLB throughout the globe sparked research interest in understanding the genomics, transcriptomics, and proteomics of the host/vector/pathogen virulence and diversity.
Plants 12 00160 g003
Figure 3. (A) ACP nymph on a citrus plant in the field. (B) ACP adults feeding on the leaf. (C) Infestation of ACP nymph and adults on curry leaf plants.
Despite the unculturable nature of CLas, the complete circular genome sequence was generated from CLas-infected psyllid by metagenomics, which became the foundation platform for further research in functional genomics [56]. Presently, 42 complete isolate sequences of CLas are available in GenBank.Ten genomes are fully assembled in a single scaffold: psy62 [56], gxpsy [57], Ishi-1 [58], A4 [59], JXGC [60], AHCA1 [61], JRPAMB1 [62], TaiYZ2 [63], CoFLP1 [64], and ReuSP1 [65] (Table 2). A total of 4.5% and 8% of genes are involved in cell motility and active transport mechanism, respectively, and they might contribute to its virulence activity in the citrus plant phloem system [56]. Bacterial plant pathogens use the secreted proteins (effectors) in their defense mechanism to suppress plant immunity and create a favorable environment for colonization and proliferation [66][67]. The CLas genome consists of all Type I secretion system genes that encode proteins involved in multidrug efflux and toxin effectors: HlyD (membrane fusion protein, CLIBASIA_01355), PrtD (ABC transporter, CLIBASIA_1350), and TolC (outer membrane export protein, CLIBASIA_04145). However, CLas lacks type III, type IV, and type VI secretion systems and typical degradative enzymes, which are required for its free-living state [67][68][69].
CLas also possesses the general Sec secretion system/Sectransloconcapable of pathogenicity to the host plants by secreting effectors directly outside bacterial cells. CLas secretory proteins CLIBASIA 05315, CLIBASIA 03875, CLIBASIA 00460, and CLIBASIA 04025 have been reported as Sec-dependent secretory proteins engaged in starch accumulation, cell death, and host plant infections [67][68][69][70][71]. Different peroxidase enzymes, such as SC2_gp095 and CLIBASIA_RS00445, have been identified as non-classical secretory proteins in CLas, which counter the reactive-oxygen-species (ROS)-mediated defense-signaling response, including H2O2, used by plants to combat disease progression [69]. This indicates that CLas may have developed a non-classical secretion pathway to release virulence proteins to combat the host. According to secretome analysis, the CLas genome contains a total of 27 non-classically secreted proteins (ncSecPs), the majority of which are involved in suppressing early plant defense mechanisms by diminishing the hypersensitive response [69]. The peroxiredoxin (Prx) superfamily proteins are ubiquitous cysteine-based non-heme peroxidases present in CLas. For example, bacterioferritin comigratory protein (BCP) is involved in the oxidative stress defense system of CLas due to its ROS scavenging activity [72]. Lipopolysaccharides (LPS), the most important outer membrane module of CLas encoded by 21 genes, not only play a critical role in maintaining the robust structural integrity to the bacterial cell, but also play a role in the virulence mechanism. However, there are some differences between CLas, CLaf, and CLam for type I secretion system, and LPS production has been reported [67][73].
Quorum sensing is a cell-to-cell signaling cascade where chemical-based regulatory communications occur among bacterial populations for their motility, biofilm formation, and virulence mechanism [11]. The mechanism of quorum sensing is regulated by two genes: luxI and luxR. The luxI gene encodes different quorum-sensing molecules, acyl-homoserine lactone (AHL), which induce biofilm formation by activation of luxR genes [68]. As CLas has a solo LuxR system but lacks LuxI [56], there is currently no evidence on how the CLas pathogen employs a quorum-sensing-based mechanism to cause the pathogenicity in citrus plants, although it is speculated that the disease is established like other phytopathogens [74][75]. It has been hypothesized that the communication among the CLas, endosymbiont, and psyllid is based on luxR and luxl genes [74]. CLas potentially communicates with the endosymbiont (Wolbachia spp.) and psyllid after adhering in the saliva sheath. Proteins like Mucin-5AC protein (23.46 kDa) were identified in D. citri saliva in a proteome study, which might be involved in the formation of the salivary sheath. Studies have shown that the down-regulation of Mucin 5AC results in reduced bacterial pathogen acquisition by inhibiting bacterial adhesion to the insect gut [76]. It has been reported that some proteins of psyllid (haemocyanin protein and myosin protein) and CLas (phosphopantothenoylcysteine synthetase and pantothenate kinase) interact with each other after the acquisition of CLas [76]. Therefore, a comprehensive understanding of the quorum-sensing system in CLas and the interaction with the citrus and the vector with respect to co-evolved protein interaction networksmay provide a target for combating HLB by hampering acquisition, growth, and biofilm formation of CLas.
Table 2. Details of sequenced genomes of CLas, CLam, and CLaf.
Sr. No Candidatus Liberibacter spp. Strain Host Sample Origin Genome Size (Mb) Number CDS Present in the Genome Reference
1 Candidatus Liberibacter asiaticus A4
(CP010804.1)		 Citrus reticulata China: Guangdong 1.23025 1067 [59]
2 Candidatus Liberibacter asiaticus Gxpsy
(CP004005.1)		 Diaphorinacitri China: Guangxi 1.26824 1094 [57]
3 Candidatus Liberibacter asiaticus JRPAMB1
(CP040636.1)		 Diaphorinacitri USA: Florida 1.23716 1072 [62]
4 Candidatus Liberibacter asiaticus TaiYZ2 (CP041385.1) Citrus maxima Thailand: Songkhla 1.23062 1067 [77]
5 Candidatus Liberibacter asiaticus psy62
(CP001677.5)		 - USA: Florida 1.22732 1049 [56]
6 Candidatus Liberibacter asiaticus JXGC
(CP019958.1)		 Citrus China: Jiangxi 1.22516 1033 [60]
7 Candidatus Liberibacter asiaticus Ishi-1
(AP014595.1)		 Diaphorinacitri Japan: Ishigaki 1.19085 1001 [58]
8 Candidatus Liberibacter asiaticus AHCA1
(CP029348.1)		 Diaphorinacitri USA: California 1.23375 1056 [61]
9 Candidatus Liberibacter asiaticus FL17
(JWHA00000000.1)		 Citrus USA: Florida 1.22725 1019 [78]
10 Candidatus Liberibacter asiaticus YNJS7C
(QXDO00000000)		 Citrus China: Yunnan 1.25898 1102 [79]
11 Candidatus Liberibacter asiaticus YCPsy
LIIM00000000)		 Diaphorinacitri China: Guangdong 1.233647 1037 [80]
12 Candidatus Liberibacter asiaticus LBR19TX2
(VTMA00000000		 - USA: Texas 1.20275 1008 [67]
13 Candidatus Liberibacter asiaticus LBR23TX5
(VTMB00000000)		 - USA: Texas 1.20347 1009 [67]
14 Candidatus Liberibacter asiaticus AHCA17
(VNFL00000000)		 Citrus maxima USA: California 1.20862 1036 [81]
15 Candidatus Liberibacter asiaticus YNXP-1
(VIGA00000000)		 Cuscuta China: Yunnan 1.20707 1031 -
16 Candidatus Liberibacter asiaticus SGCA16
(VTLZ00000000)		 - USA: San Gabriel 1.20994 1015 [67]
17 Candidatus Liberibacter asiaticus JXGZ-1
(VIQL00000000)		 Cuscuta China: JiangXi 1.21799 1040 -
18 Candidatus Liberibacter asiaticus DUR1TX1
VTLT00000000.1)		 - USA: Texas 1.20629 1011 [67]
19 Candidatus Liberibacter asiaticus Mex8
(VTLU00000000.1)		 - Mexico: Mexicali 1.24313 1042 [67]
20 Candidatus Liberibacter asiaticus SGCA5
(LMTO00000000.1)		 Orange citrus USA: San Gabriel 1.20138 1001 [80]
21 Candidatus Liberibacter asiaticus CHUC
(VTLV00000000)		 - China 1.20845 1032 [67]
22 Candidatus Liberibacter asiaticus TX2351
(MTIM00000000)		 Asian citrus psyllid USA: Texas 1.252 1129 [82]
23 Candidatus Liberibacter asiaticus GFR3TX3
(VTLR00000000)		 - USA: Texas 1.20932 1013 [67]
24 Candidatus Liberibacter asiaticus HHCA16
(VTLY00000000)		 - USA: Hacienda Heights 1.20705 1012 [67]
25 Candidatus Liberibacter asiaticus MFL16
(VTLX00000000)		 - USA: Florida 1.19922 1012 [67]
26 Candidatus Liberibacter asiaticus DUR2TX1
(VTLS00000000)		 - USA: Texas 1.21232 1009 [67]
27 Candidatus Liberibacter asiaticus CRCFL16
(VTLW00000000)		 - USA: Florida 1.20828 1028 [67]
28 Candidatus Liberibacter asiaticus HHCA
(JMIL00000000.2)		 Citrus sp. USA: Hacienda Heights 1.15062 867 [59]
29 Candidatus Liberibacter asiaticus TX1712
(QEWL00000000)		 Citrus sinensis USA: Texas 1.20333 0 [83]
30 Candidatus Liberibacter asiaticus SGpsy
(QFZJ00000000.1)		 Diaphorinacitri USA: San Gabriel 0.769888 0 [61]
31 Candidatus Liberibacter asiaticus SGCA1
(QFZT00000000.1)		   USA: San Gabriel 0.233414 557 [61]
32 Candidatus Liberibacter asiaticus YCPsy
(LIIM00000000)		 Diaphorinacitri Guangdong, China 1.233647 - [80]
33 Candidatus Liberibacter asiaticus PA19 (WOXD01000000) Kinnow mandarin Pakistan 1.224156 1059 [84]
34 Candidatus Liberibacter asiaticus PA20 (WOUN01000000) Kinnow mandarin Pakistan 1.226225 1062 [84]
35 Candidatus Liberibacter asiaticus CoFLP1
(CP054558.1)		 Diaphorinacitri Colombia:
Municipio Dibulla		 1.231639 1048 [64]
36 Candidatus Liberibacter asiaticus 9PA (JABDRZ000000000.1) Citrus sinensis Brazil (South America) 1.231881 - [85]
37 Candidatus Liberibacter asiaticus MFL16
(VTLX00000000)		 Citrus USA: Florida 1,199,225 bp - [67]
38 Candidatus Liberibacter asiaticus CRCFL16 (VTLW00000000) Citrus USA: Florida 1,208,280 bp - [67]
39 Candidatus Liberibacter asiaticus ReuSP1
(CP061535.1)		 Diaphorinacitri France: La Reunion 1.230064 1043 [65]
40 Candidatus Liberibacter asiaticus Tabriz.3(JAKQYA000000000.1) Elaeagnus angustifolia Iran: East Azerbaijan, Tabriz 1.22409 589 -
41 Candidatus Liberibacter asiaticus YNHK-2
(WUUB01000000.1)		 Citrus China: Yunnan 1.08957 - [86]
42 Candidatus Liberibacter asiaticus A-SBCA19
(JADBIB010000000.1)		 Diaphorinacitri USA: California, San Bernardino County 1.18688 1067 [87]
43 Candidatus Liberibacter americanus Sao Paulo (NC_022793) Citrus sinensis Brazil 1.1952 945 [73]
44 Candidatus Liberibacter americanus PW_SP Catharanthus roseus Brazil: Sao Paulo 1.17607 924 -
45 Candidatus Liberibacter africanus PTSAPSY Psyllid South Africa: Pretoria 1.19223 1036 -

Pathogen Virulence Factors

Recent studies have put emphasis on understanding the virulence mechanisms of CLas in the citrus host. The contribution of prophages in CLas pathogenicity towards the suppression of plant defense has been reported [88]. Initially, it was reported that CLas bacterium carries two prophages, Type 1 (SC1) and Type 2 (SC2). Recently, the prophages have been classified into three types, i.e., Type 1 (SC1), Type 2 (SC2), and Type 3 (P-JXGC-3), based on functional and comparative genomic analysis of 15 different CLas genomes [89]. The SC1 prophage is reported tobe lytic as it produces proteins necessary for the lytic cycle and becomes replicative in plants [90]. Phage particles were observed in the phloem of infected periwinkle and sweet orange plants [91]. SC2, on the other hand, is a replicative excision plasmid that lacks lytic genes and may play a role in the lysogenic cycle. SC2 encodes proteins, i.e., peroxidase (SC2_gp095) and glutathione peroxidase (SC2_gp100); it has been observed that transient expression of SC2 gp095 leads to suppression of H2O2-mediated defense signaling in plants [88][90]. The CLas may use the peroxidase enzyme as a defense mechanism against the host immune response by suppressing the plant’s H2O2-mediated hypersensitive response [88][90]. Zheng et al. (2016) studied the dominating CLas strains in southern China, revealing a single prophage, SC1 (90.4%) or SC2 (82.6%), over other strains [92]. The in silico analyses of CGdP2 have identified the presence of CRISPR/cas systems in SC1 and SC2 prophages. Based on this analysis, it was hypothesized that the presence of a CRISPR/cas system in dominating species allows them to overcome an invading phage/prophage into the CLas genome. CLas also contains other virulence factors, like serralysin (CLIBASIA_01345) and hemolysin (CLIBASIA_01555). Serralysin is a metalloprotease, which inactivates various antimicrobial proteins involved in the plant defense mechanism. This enzyme is believed to be used by the CLas to defend against the citrus immune response [93]. To promote virulence, the endosymbiont-like pathogen ‘Ca. L. psyllaurous’ suppresses the expression of genes involved in the plant defense mechanism, i.e., genes regulated by jasmonic acid (JA) and salicylic acid (SA), by introducing protein effectors [94]. CLas also degrades SA, which plays a critical role in the plant defense mechanism against pathogens using salicylate hydroxylase.Salicylate hydroxylase reduces the defense action of the citrus plant by attenuating the response to exogenous SA [95]. The secretion and transport of the effector proteins in the host plant cells is one of the most important virulence factors of the bacterial pathogen [66]. Thevirulence factor CaLas5315 (Sec-delivered effector 1) hinders the papain-like cysteine protease’s activity to suppress the defense mechanism of citrus. It also induces the callose deposition inside the vascular tissue, starch formation, chlorosis, and plant cell death after localization in the chloroplast of Nicotiana benthamiana [69][71][96]. Ying et al. (2019) have assessed 60 total putative virulence factors of CLas and identified four candidates (detrimental virulence factors) which are responsible for growth inhibition (CLIBASIA_00470 and CLIBASIA_04025) and cell death (CLIBASIA_05150 and CLIBASIA_04065C) in N. benthamiana [97].

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