1. Origin and History
Xanthomonas citri subsp.
citri (
Xcc) and
Xanthomonas citri subsp.
aurantifolii (
Xca) are causal agents of Citrus Bacterial Canker (CBC), a devastating disease that severely affects citrus plants. Citrus, Poncirus, Fortunella, and their hybrids are the most common natural host genera
[1]. In addition, natural infections have been described in
Atalantiabuxifolia,
Casimiroa edulis,
Citropsisdaweana,
Clausenaharmandiana,
Eremocitrus glauca,
Microcitrus spp.,
Naringicrenulata,
Swingleaglutinosa, and
Zanthoxylum ailanthoides [2]. Canker lesions on the oldest citrus herbaria have been observed at the Royal Botanic Gardens in Kew, England, suggesting that citrus canker (CC) originated in India and Java rather than other countries of the Orient. The authors of the reference
[3] found citrus canker symptoms in herborized plant samples collected in 1827–1831 (
Citrus medica) from India, in 1842–1844 (
C. aurantifolia) from Indonesia, and in 1865 (from Japanese citrus samples erroneously identified as a citrus scab at this time); thus, it is likely that the disease began in tropical Asia, probably in South China, Indonesia, and India, before spreading to other citrus-growing regions via citrus species
[4]. According to the authors of the reference
[5], although citrus canker was reported for the first time in 1914 in the USA
[6], the disease was actually a serious problem in Florida several years earlier following its official detection around 1910
[6][7]. Citrus canker is believed to have been first reported in Texas in 1911, in the Upper Gulf Coast area
[6]. CC was later reported in the Gulf countries region of the United States in 1915, and it is supposed that a shipment of diseased nursery stock from Asia is what caused the outbreak there
[4]. Before the turn of the century, the disease had also surfaced in South Africa
[5], South America
[6], and Australia
[7]. According to these reports, quarantines, inspections of nurseries and orchards, and the on-site burning of sick trees eliminated the disease in these nations and the Gulf States. Eradication attempts have been made in several places but have failed in the face of epidemiological outbreaks in Australia, Uruguay, Brazil, Argentina, Oman, Reunion Island, and Saudi Arabia, whereas there are still many ongoing active eradication programs in Florida, Uruguay, and Brazil
[8]. Citrus is the third most popular fruit in India, after mango and banana, and CC is one of the main obstacles to its growth. It was first reported from Punjab
[9][10][11]. More instances of it were also noted in the following states: Assam
[11], Andhra Pradesh
[12], Tamil Nadu
[13], Karnataka
[14], Madhya Pradesh
[15], Rajasthan
[15], and Uttar Pradesh
[16]. Others have mentioned the occurrence of CC on limes and other citrus cultivars. Furthermore, the cultivation of lime has become a major issue for citrus growers across the nation due to the persistence of the disease.
2. Taxonomy
The genus
Xanthomonas comprises of150 pathovars and 28 species
[17]; due to pathogenicity tests, bacterium was given the name
Pseudomonas citri in the early 1900s
[18]. The bacterium was later divided into other genera, including
Phytomonas, and was finally classified as
X. citri in late 1930
[19]. The
Xanthomonas genus contains 27 phytopathogens that are responsible for serious diseases in crops and ornamental plants
[20]. The genus has 150 distinct pathovars, 240 genera, and 68 host families
[17][18][19][21].
Xanthomonas infection affects a wide range of plants, fruits, cereals, and nuts from the
Solanaceae and
Brassicaceae families, which include around 350 species. Among them, 124 species are monocots and 268 are dicots
[20].
CC is classified into three distinct types: A, B, and C;
Xcc is the causative agent of canker A and no citrus species are immune to
Xcc after being artificially inoculated, indicating that genetic resistance is not an option and that field tolerance is mainly due to the difference in growth habits
[22]. In 2002, the genome of the
Xcc strain 306 was completely sequenced and compared to the genomes of other
Xanthomonas spp. that cause pathogenicity in different plants
[23][24][25].
X. fuscans subsp.
aurantifolii type B (
XauB), is the pathogen of canker B. compared to canker A, where symptoms take longer to appear, likely due to the slower growth rate of
XauB in culture
[26][27][28].
X. fuscans subsp.
aurantifolii type C (
XauC) is also the causal agent Canker C, is similar to type A, but is only found in
C. aurantifolia [29]. Recently, a new strain of
X. fuscans subsp.
aurantifolii has been identified and is associated with swingle citrumelo in Brazil
[30].
To demonstrate the association of CC type A,
Xanthomonas citri strains within this species were given the title of strain A
[20]. In the 1970s, two new bacterial CC-causing Xanthomonads were found, initially classified as Group C strains, which only produce canker lesions in key lime, and Group B strains, which have a broader host range
[31][32]. The bacterium was still classified as
X. citri until 1978, when it was moved to
X. campestris pv.
citri in order to maintain
citri at the specific level
[33]. Gabriel proposed the reclassification of the bacterium as
X. citri in 1989
[34]. Vauterin identified the bacteria as
Xanthomonas axonopodis pv.
citri using DNA-DNA hybridization and denaturation rates
[33]. Recent suggestions for significant changes to the classification of
Xanthomonas, based on multilocus sequence analysis and digital DNA-DNA hybridization of full genome nucleotides, were made in 2016 by Constantin and their team. They recommended the name
Xanthomonas citri pv.
citri for the causal agent of CC type A
[35]. Their suggestions were accepted and published in the
International Journal of Systematic and Evolutionary Microbiology [36]. The bacteria are polar flagellated, rod-shaped, and Gram-negative. In addition, colonies on petri plates produce yellow colors as a result of the presence of a carotenoid pigment called Xanthomonadin, also referred to as xanthan, which has a glossy look due to an exopolysaccharide (EPS)
[37][38][39]. The bacterial classification consists of the kingdoms Prokaryote, phylum Proteobacteria, class Gamma-proteobacteria, order Xanthomonadales, family Xanthomonadaceae, genus
Xanthomonas, species
citri, and pathovar
citri [40] (
Table 1).
Table 1. X. citri subsp. citri Asiaticum (Canker A) classification details, from the start of the studies.
3. Control
For many years, the most widely used methods for disease control were to cut down infected trees to prevent the spread of the infection
[43]. However, some citrus growers use varieties that are resistant to disease and are grown in nurseries free of CC. Additionally, copper-based bactericides have been used to control CC for over two decades
[20]. Unfortunately, the repeated application of these bactericides has led to the emergence of copper-resistant strains of
Xanthomonas spp.
[44][45]. Moreover, copper-based bactericides can potentially cause phytotoxicity and other adverse environmental impacts, such as leaving copper residues on plants and cultivated soils. These consequences ultimately increase the cost of production
[46].
International cooperation and research are crucial for effectively reducing the effects of this disease. The origins of infection must be found, efficient disease control strategies must be created, and researchers must collaborate to share resources and best practices. This endeavor to coordinate research and create policies to aid in reducing the spread of the disease has to involve international organizations and governments. To study the epidemiology, biology, and management of CC, international research initiatives like the global citrus canker research and development project have been developed. These initiatives have the ability to offer insightful information on the illness and create efficient controls and prevention measures. Researchers can develop better management and containment measures and a better understanding of the disease thanks to this kind of research.
Additionally, it is crucial to improve a nation’s ability to track and detect CC while international organizations and states must collaborate to create and implement efficient surveillance systems and capacity-building initiatives if they are to achieve this. This will make it more likely that outbreaks will be identified early and controlled in a timely way. Ultimately, worldwide cooperation and research can lessen the effect of CC on the world’s citrus business. By taking these steps, researchers can improve disease control techniques, strengthen surveillance systems, and guarantee that outbreaks are rapidly identified and efficiently treated.
3.1. Cultural Control
If a disease is not common in a certain area, its best measure is to eradicate it
[40]. Quarantine and elimination are two effective management methods employed in many countries to control pathogen introduction and spread
[47]. Eradication efforts often involve destroying citrus species by cutting them down and burning them
[48]. The infested property is quarantined and then the eradication process is implemented for a period of up to one year, with inspections occurring at least twice a year
[48]. Regulatory measures have been implemented to allow survey teams to look for infected citrus trees, cut them down, and eliminate them. Moreover, survey teams will take action to identify and remove susceptible trees within 125 feet of a diseased tree
[49][50]. In response to the changing prevalence of CC in Brazilian plantations, authorities now suggest planting less susceptible varieties and practicing appropriate orchard management to prevent and control the disease. In Brazil, if the infection rate is 0.5% or less, then all plants within a 30 m radius of affected plantation will be cut down. However, if the infection rate exceeds 0.5%, then the entire block will be removed
[50].
In addition, Brazilian authorities have also implemented various other strategies to control citrus canker in the affected areas. These include monitoring and controlling the spread of the disease, using fungicides to prevent and treat the disease, and removing and destroying any infected plants. More recently, Brazilian authorities have also implemented a mass vaccination program in some areas to reduce the risk of CC. The Brazilian government has recently declared that areas and states where CC is endemic are no longer bound by the requirement to eliminate canker-affected or suspected trees [IN21, Ministry of Agriculture Livestock and Supply, MAPA; São Paulo, Brazil, 2018]. At a height of roughly 1900 feet, new canker infections appear in known source trees
[51]. The “1900 ft rule” was a brand-new regulation that went into effect in January 2000. The destruction of all ill citrus trees, as well as any healthy trees that were within 1900 feet of an infected tree, was mandated by this law, which went into effect in March 2000
[51]. The 1900 ft rule can be used to eradicate dooryard citrus from contaminated areas because each circle with a radius of 1900 feet has a surface area of 1.06 km
2 (0.41 miles)
[47]. Prior to the onset of the monsoon, trimming the diseased twigs and applying a 1% Bordeaux mixture on a regular basis both proved to be quite effective in managing the illness. Likewise, Bordeux contains copper and it prevents the secondary infection by the pathogen at the point of wound where pruning has been performed; however, now-a-days nano particles have been performing much more than the bactericides alone, or with the loading of nanoparticles that may be of copper, zinc, iron, titanium oxide, etc. These are the nano compounds which can have much impact if used after loading upon bactericides
[52][53][54][55].
3.2. Chemical Control
Studies have shown that the application of 3–4 sprays of a 1% Bordeaux mixture to pruned, diseased twigs between November and December can be an effective management strategy for CC
[56][57][58]. Furthermore, applying 1% Bordeaux with 4 sprays of a 5000 ppm copper–oxychloride combination has yielded positive results in controlling the disease
[57][58]. Additionally, chemicals such as Ultrasulphur, Perenox, and a combination of Blitox–nickel chloride, and sodium arsenate–copper sulphate, have been used to treat citrus cankers
[59][60]. To manage acid lime cankers, a 1% glycerin spray and 500–1000 ppm streptomycin-sulphate have been used
[61]. Moreover, two prunings and 6 sprays of 1000 ppm streptomycin have been found to minimize acid lime cankers
[62]. Finally, a combination of Agrimycin and streptocycline–Bordeaux mixture has been reported to be an efficient antibiotic treatment for CC
[63].
The Paushamycin–Blitox and Bordeaux mixture showed the most effective control of CC in field experiments with several chemicals
[64]. Young plants have reportedly been treated in nurseries by having a neem cake solution applied to their leaves
[65]. Streptocycline with copper oxychloride (0.1%) applied ideally every 7 and 15 days has been reported to be particularly efficient against CC
[65]. A neem powder solution with streptomycin (100 ppm) and copper oxychloride (0.3%) applied together on clipped affected twigs has proven to be particularly effective at controlling the disease
[66]. Three applications of copper hydroxide or copper ammonium carbonate with maneb with completely ripe grapefruit trees were evaluated in field studies. The applications reduced the number of lesions on fruits but not on foliage, according to the results. The most effective product for treating cankers was discovered to be copper ammonium carbonate with 8% metallic copper
[67]. Mancozeb was added to copper spray in order to combat copper resistance
[68]. It was advised to apply sprayable ammonium detergent disinfectants on individuals or equipment coming into contact with citrus in quarantine areas for hygiene reasons
[69].
3.3. Biological Control
It has become more and more common to create ecologically friendly treatments for plant illnesses
[40]. Researchers are looking into more ecological techniques to control phytopathogens in the field because of the development of chemical residue in soils and water supplies, as well as consumer concerns
[40]. Recent research has used the antagonistic behavior of bacteria and chemicals produced from plants to control the CC pathogen
[40]. Studies on the biological control of CC are, however, still in their infancy
[38][70]. Certain bacterial strains have been reported to have aggressive anti-CC properties in vitro, including
Bacillus subtilis,
Pseudomonas syringae,
Pseudomonas fluorescence, and
Erwinia herbicola, isolated from citrus phylloplane
[71][72][73][74]. It has been found to be difficult, however, to find antagonistic bacteria that can survive on mature citrus tree leaves
[75]. For instance,
Pseudomonas aeruginosa produces a secondary metabolite that is an antibiotic of organ copper, which can reduce the formation of canker lesions on Valencia oranges by as much as 90%
[75].
Streptomycin sulphate is commonly used to control CC caused by
Xcc [76]. However, due to the possibility of strains developing resistance to streptomycin and the risk of antibiotic resistance in other bacteria, regular spraying of streptomycin has been prohibited by European authorities
[77]. Therefore, it is essential to identify more effective ways to control CC as it is still spreading, and an estimated 12 million USD is spent on its control annually
[78][79].
When it comes to the management and control of plant diseases, biocontrol agents, such as chemical bactericides, are gaining attention. These agents are environmentally friendly and have a range of modes of action, making them a recommended option for managing pathogenic microbes
[80][81]. Nearly three-hundred-thousand species of plants on Earth are hosts for endophytes
[82]. The term “endophyte” was first used by De Bary in 1866, and he classified them as microorganisms, usually bacteria or fungi, which live inside healthy plants without causing any visible signs of infection to the host
[83][84][85]. However, under favorable conditions, some endophytic bacteria, to some extent, behave like dormant pathogens that help in the infection of the host plant
[85]. By producing antimicrobial compounds and phytohormones, endophytic bacteria can aid in plant development, defense, stimulate host plant immunity by SAR and ISR, and disease resistance
[85][86]. Numerous
Bacillus spp., in particular
B. oryzicola,
B. subtilis,
B. velezensis,
B. amyloliquefaciens FZB42,
B. methylotrophicus, and
B. amyloliquefaciens subsp.
plantarum, have been observed for their capability to biocontrol a range of bacterial phytopathogens, such as
X. oryzae pv.
oryzae [87]. The commercial availability of bacillus-based products has increased recently. Some examples include RhizoPlus, RhizoVital, Amylo-X WG, and Sonata
[88].
The researchers observed a bacteriolytic effect on
Xcc, but no evidence of phytotoxicity was identified
[89]. Several
P. aeruginosa secondary metabolites decreased canker formation when used at low micromolar quantities
[90][91].
P. aeruginosa must be carefully controlled because it is an opportunistic human infection, making it dangerous to use as a BCA
[47]. BCAs have also been recommended as
Bacillus spp. because they reduced
Xcc growth both in vivo and in vitro
[92][93][94].
Xcc quorum sensing molecule DSFisdegraded; numerous species of
Pseudomonas and
Bacillus, as well as
Citrobacter, isolated from phylloplane of a sweet orange inhibit the growth and development of cankers
[95]. The defense mechanisms of these bacterial species against CC infected trees were not studied. By generating bacteriocins, other bacterial species, including Cronobacter and Enterobacter, also prevented
Xcc development in vitro
[96].
Bacteriophages can be used to differentiate between different subgroups of bacteria within a species
[96]. A commonly used technique for identifying
X. citri strains is the use of Cp1 and Cp2 phages
[97]. However, utilizing phages for biological control is not without its difficulties
[98]. High quantities of phages must be sprayed on the surface of the leaf in order for them to be effective, as they have a limited active life span
[99].
XacN1, a giant phage, is capable of infecting a variety of
X. citri isolates, making it a suitable candidate for further field studies
[100]. A combination of phages from orange orchards and ASM has been demonstrated to lessen canker symptoms in both greenhouse and outdoor experiments
[101]. Phage and copper–mancozeb used together, however, did not result in an improvement in CC control over copper–mancozeb used alone
[102]. Its interesting to note that filamentous integrative phages, such as XACF1, have been demonstrated to lessen the pathogenicity of
Xcc, suggesting that they might be employed as CC biocontrol agents
[103].
3.4. Resistant Varieties
Citrus varieties that are more resistant to cankers, such as ‘Valencia’ oranges and mandarins, may be beneficial in countries where the condition is both widespread and severe. For example, the ‘CC’ strain has been reported to be resistant to seedless limes
[58]. In Japan, the ‘Tangi’ cultivar has been reported to have resistance to the cankers
[104]. Furthermore, some aggressive citrus cultivars have been found to have narrow stomatal openings, lower stomatal frequencies, and greater amounts of phenols and amino acids
[105]. The number of lesions per inoculation site can be measured to determine a citrus’ genotype resistance to CC type A without the necessity for bacterial population research. The “Lakeland” type of limequat might be a good seed parent for the development of sour citrus fruit
[106]. Tangerine (
Citrus sinensis,
C. reticulata) cultivar “Setoka”, an improved Kuchinotsu No. 37–Murcott variety, was introduced in 1998. It is known as “Tangor Norin No. 8” in Japan, and its fruits ripen in February. This new variety of tree contains fruits that are almost entirely seedless, have few thorns, strong parthenocarpic tendencies, polyembryonic seeds, and trees with intermediate-to-decreased vigor. It is resistant to both CC and citrus scab. Its 200–280 g, oblate-shaped fruit has a thin, orange-to-deep-orange skin, extremely soft and juicy flesh, a flavor that is pleasant and aromatic, a low amount of acid content of 0.8 to 1.2 g per 100 mL, and a high concentration of soluble solids of 12 to 13%
[107]. Citrus scab and cankers are resistant to certain late-maturing cultivars, such as “Shiranuhi”, “Youkou”, “Miho-core”, and “Hareyaka”
[108][109][110]. It has also been discovered that Amaka, a tangor created by crossing “Kiyomi” tangor (
C. unshiu;
C. sinensis), is relatively resistant to CC
[107]. As they exhibit resistance to citrus scab, but only modest resistance to CC, the mid- to late-maturing cultivars “Akemi” and “Harumi” have been recommended for cultivation in Japan
[111][112]. Ultimately, introducing resistance genes into cultivars that are susceptible is the most efficient strategy to stop these diseases. For transformation, embryogenic calluses from navel orange “Newhall”, one of China’s most widely used commercial cultivars because of its seedlessness and benefits, “Early Gold” sweet orange, and “Murcott” tangerine were used to separate protoplasts. GFP-expressing transgenic embryoids were observed. The three cultivars’ regenerated shoots were grafted in vitro to accelerate their growth. The six “Early Gold” sweet orange shoots that were treated to PCR analysis all contained the Xa21 gene, whereas none of the nineteen samples of navel orange Newhall did
[113].
Citrus bacterial spot and
Xcc were examined in the greenhouse by foliar spraying of induced systemic resistance (ISR) compounds, harpin protein and acibenzolar-S-methyl against them. This was done 3–7 days prior to inoculation. In spray programsutilizing copper hydroxide (CuOH) and copper oxychloride (COC) in sweet orange orchards in southern Brazil with low-to-moderate disease incidence of citrus canker, the ISRs were studied in terms of this activity. Sprays of COC and CuOH considerably and modestly decreased the incidence of cankers and early fruit drop. Actigard, COC, and CuOH did not significantly lessen citrus canker and early fruit drop on citrus leaves as compared to Cu alone. ISRs cannot currently be suggested to support Cu programs for the management of CC because of a lack of further control
[114]. Citrus rootstocks can significantly influence both fruit yield and susceptibility to CC.
Citrumelo Swingle, and Flying dragon rootstocks were found to have the highest productivity index and the lowest occurrences of CC disease. However, Rangpur and Volkameriana rootstocks, while encouraging a higher crop load, demonstrated a greater susceptibility to CC
[115].
3.5. Induced Systemic Resistance
Plants possess an active resistance mechanism, known as induced systemic resistance (ISR), which can be triggered by either biotic or abiotic infection. This technique enhances the plant’s physical and chemical defenses against infection
[116]. Chemicals such as salicylic acid, benzothiadiazoles, and harpin protein are being used successfully to increase the plant’s resistance to diseases
[117][118]. ISR can also prevent the emergence of pathogen resistance and control the disease
[94]. Early in the season, ISR activity can be used to amplify the protective effects of copper, which inhibit the growth of bacteria on expanding leaves
[119]. Examples of chemicals used for the treatment of CC include Actigard (a benzothiadiazole approved for use in the USA) and Eden Bioscience (a harpin protein product approved for use in Europe and South America)
[120]. Moreover, several ISR inducers are currently being studied for their potential to control
Xcc in Florida. These include Messenger, Nutri-phite, Oxycom, and FNX-100
[47]. Transgenesis has also been used against the CC for increasing tolerance to
Xcc. When three lines of sweet orange—Hamlin, Pera, and Natal—had their genomes modified with the Xa21gene, the severity of the disease was considerably reduced. When produced in the extremely sensitive Anliucheng, the Xa21gene’s promoter appeared to be more successful in promoting disease resistance. RpfF, which encodes for a quorum-sensing gene that can disrupt bacterial communication by reducing the activation of virulence proteins, was introduced into transgenic Carrizo citrange and sweet orange plants in order to improve their tolerance to pathogen infection. The expression of the flesh fly AMP sarcotoxin also improved the tolerance to
Xcc [121].
3.6. Leaf Miner Control
Cankers that are not spread by leaf miners, but a large influx of bacteria through leaf miner galleries, can increase the severity of the disease, making it difficult to control
[48]. To reduce the risk of the disease, it is important to control leaf miners during the initial summer growth period; however, there is no effective way to manage leaf miners during the later summer flushes. As there is no visible damage during the spring growth, it is important to take preventive action
[120]. Applying petroleum oil, Agri-mek, Spintor, Micromite, and Assail immediately can help to reduce leaf minor damage
[48][121].
A conventional Chinese management method was used to achieve even budding, which entails pruning to delay budding until late autumn, and the gathering and removal of fallen leaves during the winter
[122]. This restricts growth to the period of the year when
P. citrella moths are at their lowest population. Additionally, fertilizing trees regularly and preventing drought boosts their resilience to attack by
P. citrella. According to studies, citrus trees treated with avermectin have an 86.2–100% success rate in controlling
P. citrella [123]. These two extracts can also effectively control
P. citrella by preventing mating at very low pheromone deployment rates
[124]. Moreover, Smith and Hoy (1995) reported the use of parasitoids
Ageniaspiscitricola as a successful means of controlling
P. citrella [125].
Studies have found that
P. citrella has mortality rates of 80–97% when exposed to
Bacillus thuringiensis strains 04-1, 454, and HD-1
[122]. To prevent the recent spread of the species, programs for biological control have been implemented in Israel, Australia, and Florida in the United States, wherein natural enemies have been introduced
[126][127]. These programs have included cultural practices, the potential release of parasitoids and predators, and precisely-timed injections of
Bacillus thuringiensis [122]. Mating disruption can be a highly effective management technique when combined with biological control and minimal chemical control, provided growers have access to pheromone dispensers.
3.7. Control through Plant Extracts
Alternative strategies for controlling plant pathogenic bacteria must be developed in order to reduce or mitigate the negative effects of synthetic pesticides on the environment
[128][129]. Green plants can be utilized as a valuable source of natural pesticides and have been demonstrated to be an effective chemotherapeutic alternative to synthetic pesticides
[130]. Numerous studies have displayed the potential of various plant byproducts, such as extracts and diffusates, to combat different pathogenic bacteria and fungi
[131][132][133][134][135]. Unfortunately, antibiotics are often beyond the financial reach of the average farmer in Pakistan due to their comparatively high costs and the fact that small farmers’ economic circumstances are not ideal
[136]. In light of this, it appears that plant extracts and diffusates may be a suitable solution for treating bacterial plant diseases
[137]. To reduce the spread of
Xcc, farming communities have utilized a variety of plant extracts, including
Azadirachtaindica,
Dalbrgia sissoo,
Allium sativum L.,
Calotropis gigantea,
Allium cepa L.,
Melia azedarach,
Eucalyptuscamelduensis, and
Gardenia florida [137]. A general term used to describe any volatile, aromatic chemical produced by plants is “essential oil”
[138].
Antibacterial effects of essential oils against pathogenic and phytopathogenic microorganisms have long been recognized
[139]. Numerous essential oils from the citrus species
Fortunella spp.,
Citrus aurantifolia, and
Citrus aurantium have been proven to eradicate
Xcc [140]. In disc diffusion trials, citral from
C. aurantifolia significantly reduced the development of
Xcc, while geranyl acetate, limonene, and transcaryophyllene from the
Fortunella species had small effects
[140]. Considering that citral has an MIC of 0.5 mg/mL, large doses are required to manage
Xcc in vitro conditions
[140]. The development of
Xcc was reduced by Chinese sumac (
Rhus chinensis) leaf gallnut extracts in water and acetone at a concentration of 1 mg/mL, suggesting that other plant-derived compounds can be helpful against CC
[141]. The bioactive compounds were methyl gallates and gallic acids after the gallnut leaf extracts had been further isolated
[141]. Comparing methyl gallates (MIC 0.1 mg/mL) to gallic acids (MIC 4 mg/mL), the latter was substantially less active
[141]. Synthetic gallates inhibited
Xcc host colonization following artificial infiltration at low micromolar concentrations in vitro, but when applied to already developed cankers, these substances decreased the bacterial population
[142].
Similar to pyridinium-tailored compounds, alkyl gallate amphiphile structures display improved chemical entry in target cells; in
Xcc, membrane permeabilization and the divisional septum have been identified as the chemicals’ main targets
[143]. Further molecular development produced more lipophilic and deadly monoacetylated alkyl gallates from these substances, which were initially discovered to be low in toxicity in human cells
[143].
C. coriariaisis a potential host plant for controlling
Xanthomonas [144]; the diffusates of
Terminalia chebula,
Phyllanthus emblica,
Sapindusmukoross, and
Acacia nilotica were found to be the most effective ones against
Xcc in forest trees
[145].
Psidium guajava L. leaf extracts in methanol could be used to produce antibacterial treatments to manage plant pathogenic bacteria because they could prevent the growth of
Xanthomonas spp. at all concentrations
[146].
3.8. Control of Citrus Canker through Wind Break Systems
In a particular reference
[147], it was emphasized that the interaction between precipitation and high-speed winds plays a crucial role in the dispersal of substantial amounts of bacteria from infected citrus trees. The authors of this research suggested that reducing the sources of inoculum and controlling wind speed could be effective strategies for mitigating the spread of the disease. In some regions of northeastern Argentina, natural windbreaks are commonly used to shield citrus orchards from the prevailing southern winds
[148]. This choice of location for the windbreaks is supported by an analysis of the synoptic-scale atmospheric circulation pattern that accompanies precipitation events in the area. The typical large-scale atmospheric circulation pattern begins with southerly winds blowing from the South Atlantic Anticyclone (located around 30° S latitude) over the South American continent, accompanied by anticyclonic conditions in the mid-troposphere
[149][150]. This pattern usually persists for a few days, after which a wave front originating from the Pacific Ocean crosses the Andes and generates an extratropical cyclone in the eastern or northeastern part of Argentina. This cyclone is typically associated with a cold front that advances towards the northeastern region, resulting in significant precipitation events. During this stage, the prevailing wind direction over northeastern Argentina is generally from the south or southwest. A study conducted by the authors of reference
[151][152][153][154][155] in Concordia, which is located in the northeastern region of Entre Ríos Province in Argentina, demonstrated that implementing windbreaks, either alone or in combination with copper-based bactericides, resulted in a significant decrease in the advancement of citrus canker disease.
The impact of windbreaks on the incidence of citrus canker disease was investigated by the authors of references
[156][157][158][159][160] in Bella Vista. Three separate blocks of Citrus species were planted at increasing distances to the north of a natural windbreak, and the researchers monitored the disease intensity weekly. Regression analysis revealed a significant positive correlation (R2: 0.62–0.96) between the distance from the windbreak and the observed disease intensity. At a distance of 117 m from the windbreak (i.e., the last row of the grove), the intensity of citrus canker was found to be 2- to 10-fold greater than that observed at a distance of 19 m (i.e., the first row), for all cultivars and on various dates. In the same experimental grove, the authors of references
[161][162] aimed to identify the weather variables that were most strongly associated with mid-season grapefruit canker disease. They based their analysis on the average observations of three blocks and conducted their investigations over 14 and 18 growing seasons, respectively, without taking into account the distance from the windbreak. In both studies, the weather variables calculated during the spring were examined, and it was found that the total number of days with precipitation exceeding 12 mm, the total number of days with concurrent precipitation exceeding 12 mm, and mean daily wind speeds (measured at the Bella Vista meteorological station) exceeding 2.6 km/h were the most strongly correlated variables
[163].
3.9. Factors Affecting Successful Eradication of Citrus Canker
Xcc’s possess distinct features that make them highly appropriate for eradication, as they cannot survive outside their host lesion for an extended period of time. Additionally,
Xcc’s lack a reliable vector for transmission, while their increased lesions can be rapidly and accurately identified. Furthermore, the majority of commercially cultivated citrus plants are extremely sensitive to these bacteria, making disease control measures only marginally successful and relatively costly, even though they were successful in eliminating the disease in Florida, Australia, and South Africa in the past
[47].