Abstract
One of the most common fruit crops cultivated worldwide is citrus, which is also a significantly traded horticulture product. In places of the world where citrus is grown, Tylenchulus semipenetrans, one of the main nematode pest that parasitizes plants, significantly reduces yields in the world where citrus is grown. The management of plant parasitic nematodes in citrus can be done alternatively by using biological control because of its lower toxicity to the environment, specificity of the target, and safety for nontarget organisms. Even though various bacteria, mites, and fungi have been employed to reduce T. semipenetrans population in citrus, a dedication to the creation of high-quality products, extension programs, and industrial partnerships will help to promote the widespread use of biological control agents.
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1 Introduction
One of the most popular fruit crops and a significant horticulture traded commodity in the globe is citrus (Matheyambath et al. 2016). Oranges account for 55% of all citrus production worldwide, followed by 25% mandarins, 13% lemons, and 7% grapefruits (Global Citrus Outlook 2019). One of the main reasons restricting citrus production globally is plant-parasitic nematode infection. Since citrus crops become perennial, they nourish and encourage nematode population growth throughout the year around (Reddy 2018). There are many plant nematodes associated to the citrus rhizosphere; however, only a small number of species affect the trees (Khan 2023). Tylenchulus semipenetrans, Pratylenchus coffeae, Radopholus citrophilus, and Meloidogyne indica are among the groups of plant-parasitic nematodes that significantly reduce citrus crop yields worldwide (Kumar and Das 2019; Duncan 2009; Verdejo-Lucas and McKenry 2004).
The main pathogenic species almost every region where citrus is grown in the world is the citrus nematode, T. semipenetrans. The young adult females enter the cortical cortex more deeply, settle down, and create nurse cells, which serve as a permanent feeding site and food sink for the nematode (Khan 2008). Depending on the level of infestation, yield losses brought on by this nematode are predicted to range from 10% to 30% globally (Verdejo-Lucas and McKenry 2004). However, researchers estimate those orchard infestations in many regions of the world range from 50% to 90% due to insufficient regulatory exclusion measures (Sorribas et al. 2008, 2000; Maafi and Damadzadeh 2008; Iqbal et al. 2006; de Campos et al. 2002). Citrus is slowly declining as a result of it, and it is also responsible for other complexities like citrus dieback. The age and health of the tree, the nematode population density, and the rootstock’s vulnerability all have a role in how much damage a nematode infection causes (Ravichandra 2014). Some of the symptoms that are noticeable include chlorosis, leaf defoliation, smaller fruit, fruit loss before maturity, and twig dieback from above branches. In contrast to healthy roots, the branch rootlets on the infected feeder roots are shorter, darker, and covered in soil (Abd-Elgawad 2020; Duncan 2009).
The most effective preplant nematicides employed in citrus nurseries and orchards against T. semipenetrans were fumigants such as 1,3-dichloropropene, metham sodium, and methyl bromide (Shokoohi and Duncan 2018). Due to their toxicity to the environment and negative effects on human health, many pesticides have been taken off the market. In some cases, using resistant rootstocks to control T. semipenetrans has been effective (Verdejo-Lucas and McKenry 2004; Verdejo-Lucas et al. 2000; Gottlieb et al. 1987; Kaplan and O’Bannon 1981), but these hybrids perform poorly in alkaline soils, and over time, resistance-breaking biotypes were developed (Abd-Elgawad 2020). Citrus plant-parasitic nematodes can be managed through biological control since these are less hazardous to the environment, more particular in their target species, and safe for nontarget creatures. The world’s citrus-growing regions have been subject to biological control methods based on fungi, bacteria, and mites or their bioactive components.
The current chapter examines the potential for biological control agents in citrus to evolve in the future and provides an overview of the biological control agents now being used in citrus to combat T. semipenetrans.
2 Biological Control of T. semipenetrans in Citrus
Biocontrol fungi/bacteria alone (Stirling 1991; Khan 2007; Khan and Anwer 2011) or along with oil, neem cakes (Sikora and Roberts 2018; Khan et al. 2021) or pesticides (Mohiddin and Khan 2013) are getting popularity in achieving sustainable nematode management in agricultural crops (Khan 2023; Khan et al. 2023). The microbial antagonists, Aspergilus niger, Pochonia chlamydosporia, Purpureocellium lilacinum, Pasturia penetrans etc. (Jatala 1986; Stirling 1991; Kerry 2000; Khan 2016), and phosphate solubilizing microorganisms such as Aspergillus, Bacillus, Penicillium, Pseudomonas etc. (Khan et al. 2009, 2016a, b; Sikora and Roberts 2018) may significantly contribute in the sustainable management of plant nematodes.
2.1 Fungi
2.1.1 Trichoderma spp.
As a biocontrol agent, Trichoderma spp. has been utilized extensively against plant pathogens like bacteria, plant and soil nematodes, and fungus. The chitinases, glucanases, and proteases generated by fungi are crucial in the fight against diseases (Sharon et al. 2001). In recent years, Trichoderma has also been found effective in suppressing plant nematodes (Mohiddin et al. 2010; Khan and Mohiddin 2018). Various species of Trichoderma were employed to combat citrus nematodes. The effectiveness of Trichoderma spp. has been established in numerous experiments carried out under various circumstances. According to Narendra et al. (2008), when T. harzianum (4 kg/soil) was applied to C. jambhiri under pot conditions, the juvenile and female populations of T. semipenetrans were reduced by 30.58% and 64.85%, respectively, in comparison to the untreated control. The commercial formulations of Trichoderma spp. are available in market (Khan et al. 2011), which are quite effective against soil nematodes and other pathogens (Mohammed and Khan 2021; Sikora and Roberts 2018; Shahid and Khan 2019).
T. hamatum, however, significantly reduced the amount of delicious orange under greenhouse conditions (86.68% and 61% at 3 × 108 spore/mL, respectively) (Hanawi 2016). While applying T. harzianum (3 × 108 spore/mL) to citrus cv. volkameriana resulted in the highest control (91.1%) in J2 population compared to other treatments, according to Montasser et al. (2012). The same findings were reported by Shawky and Al-Ghonaimy (2015) who found an 86.3% decrease in T. semipenetrans J2 on volkameriana seedlings when T. harzianum was administered at the highest rate (5 × 108 cfu/pot). According to recent studies, combining T. harzianum with Nemastop (natural oils) boosted the mortality rate of T. semipenetrans juveniles from 46% to 80% in vitro experiments (Ibrahim et al. 2019).
Based on field trials on sweet orange, T. viride (3 × 108 spores/mL) decreased J2 and female T. semipenetrans populations by 64.9% and 44.8%, respectively (Hanawi 2016). While a month after, T. harzianum (5 × 108 cfu) was applied to volkameriana. According to Shawky and Al-Ghonaimy (2015), citrus nematode in the soil as well as roots had decreased by 55%. However, 4 months after application in the field, a striking suppression (72%) in the nematode population was seen in comparison to untreated control plots. Ibrahim et al. (2019) investigated the effectiveness of T. harzianum alone or combined with nemastop (natural oils), other biocontrol agents, and chemical pesticide to maintaining citrus nematode under control on Washington navel orange trees in Menia EL-kamh, Sharkia governorate, Egypt (Nemaphos). After 12 months of treatments in the field, T. harzianum mixed with Nemastop and when applied as a soil drench (500 mL/tree), compared to 33.1% for Nemaphos and 35.85% for T. harzianum alone, it caused a 51.7% reduction in the number of nematodes.
More successful nematode control was achieved by combining hostile bacteria with agricultural waste, such as compost, than by employing only one microbial strain or compost. It was reported that T. semipenetrans population density was less in the soil and roots by the application of T. harzianum mixed with neem, karanj, and castor oil cakes, and acid lime seedling growth was found to be boosted (Reddy et al. 1996). El-Mohamedy et al. (2016) reported that the population of citrus nematode that developed on sour oranges under greenhouse conditions decreased from 0.73 to 0.80 after the application of compost containing either T. harzianum or T. viride (1 × 106 cfu/mL) to 0.38 and 0.41, respectively. Similar results were achieved by combining compost with T. viride or T. harzianum at the same rate, which led to a lower nematode population (0.40, 0.42) as a comparison to the fungal cultrate alone (1.1, 0.76) in volkameriana (Hammam et al. 2016).
2.1.2 Purpureocillium lilacinum (=Paecilomyces lilacinus)
This fungus can parasitize citrus nematode eggs, egg masses, and females (Kumar 2020). Seven different P. lilacinus-based treatments are utilized globally to control citrus nematodes at different phases of their life cycles. According to Maznoor et al. (2002), the application of P. lilacinus (8 g/kg soil) made with rice bran-reduced nematode populations on khasi mandarin in India by 64.4% compared to nematode populations reduced by formulations with mustard oil cake (63.9%). However, in terms of nematode population decrease, the bioefficacy of the fungi developed in both environments was comparable. While Narendra et al. (2008) reported that when P. lilacinus (4 kg/soil) was applied to C. jambhiri plant, J2 and the female population of T. semipenetrans were significantly reduced (64.7% and 75.7%, respectively), compared to the control under pot conditions. When P. lilacinus, T. harzianum, and G. fasciculatum were all applied together, the population of T. semipenetrans was decreased by 73.04% and 89.08%, respectively. This helped C. jambhiri plants grow more quickly. Similar to this, applying 10 g of P. lilacinus, 10 g of Pseudomonas fluorescens, and 250 g of neem seed cake per tree once every 6 months for 2 years decreased the plant nematodes and increased the yield (30.24 kg/tree) in comparison to control (17.20 kg/tree) (Rao 2008). In future, market growth for P. lilacinus-based commercialization products manages the domestic citrus nematode strains. Verdejo discovered 20 fungal strains from citrus rhizosphere in Spain, among them P. lilacinus and Talaromyces cyanescens showed promising against citrus nematode infesting Carrizo citrange and Cleopatra mandarin in greenhouse conditions.
2.1.3 Pochonia chlamydosporia
P. chlamydosporia-based talc formulation was applied to the soil, Kumar and Prabhu (2009) claim that this resulted in a considerable reduce citrus nematode after 30 days over control (52.5, 9.5, respectively), under nursery conditions. As P. chlamydosporia (20 g/tree) was applied in orchard, Deepa et al. (2011) reported that the population of citrus nematode decreased by 42.76% when compared to untreated controls. Successful reduction of the M. javanica infects root gall in nursery by adding P. chlamydosporia and P. lilacinus to the soil @ 5 and 10 g/kg, respectively (Rao 2005).
2.1.4 Mycorrhizae (Glomus spp.)
These are the obligate root symbionts, which increase nutrient intake to promote plant growth and reduce plant stress brought on by nematodes that parasitize plants (Schouteden et al. 2015; Vos et al. 2012). Nematode and mycorrhizal fungal interactions depend on the association of plant cultivars, fungi, and nematode species and appear to be highly particular (Ingham 1988). In a preliminary greenhouse investigation, rough lemon seedlings grew more quickly than nonmycorrhizal seedlings after being transplanted into soil contaminated with Glomus mosseae and infected with T. semipenetrans (O’Bannon et al. 1979). Radopholus citrophilus, a citrus-burrowing nematode, was later found to have lower population densities in mycorrhizal-infested or nonmycorrhizal, high-phosphorus plants than in nonmycorrhizal, low-P plants of rough lemon. However, there was no discernible difference in the seedlings’ growth. According to Reddy et al. (1995), citrus nematode was successfully controlled after G. fasciculatum was treated with neem cake in nursery. The soil treatment of G. fasciculatum (@ 500 spores/kg soil) reduced the citrus nematode infesting C. jambhiri by 66.77–82.22% (Narendra et al. 2008). While Ravichandra (2014) reported that, T. semipenetrans-infesting citrus might be controlled by applying G. fasciculatum or G. mossae @ 50–100 g/plant. Despite having a biocontrol effect on PPN, arbuscular mycorrhizal fungi’s usage in citrus is fairly limited because of variable results.
2.1.5 Nematophagous Fungi
Nematophagous fungus and citrus nematodes coexist in the rhizosphere of the soil. They are successful in controlling these nematode species. According to Martinelli et al. (2012), the abundance of the Pratylenchus jaehni in pera orange under natural conditions in Spain was successfully reduced by applying formulations of Arthrobotrys robusta, A. musiformis, A. oligospora, Monacrosporium eudermatum, and Dactylella leptospora, enriched with sugarcane bagasse and rice bran mixture separately at doses of 1 and 2 L/plant. However, Noweer (2018) reported that the use of a combination of egg-parasitizing fungus Verticillium chlamydosporium and nematode-trapping fungus Dactylaria brochopaga (0.5 kg/tree) for 2 seasons caused a significant decline in the population of T. semipenetrans (97% and 70%, respectively) compared to control in mandarin trees.
2.2 Bacteria
Among the most effective and extensively used bacteria against several plant nematodes infecting citrus over the world include Bacillus spp., Pseudomonas spp., and Streptomyces spp. Pasteuria species have also been utilized as biocontrol agents in addition to these Serratia marcescens.
2.2.1 Bacillus spp.
This genus has successfully controlled plant nematodes at an amazing level on a variety of horticulture crops in multiple instances. B. thuringiensis, B. firmus, B. subtilis, and B. megaterium species have all been investigated in citrus under various circumstances. According to Montasser et al. (2012), of the seven isolates of fungi and bacteria used as biocontrol agents that were tested in vitro, B. subtilis had the highest level of success against T. semipenetrans (J2) (100% mortality at 3 × 108 cfu/mL), followed by S. marcescens (99.9%) after 72 h of exposure. When compared to untreated plots, field tests in Egypt using the commercial formulation of Bacillus thuringiensis—Agerin® (3 kg/4200 m2) grafted onto 15-year-old baladi mandarin (Citrus reticulata) trees on sour orange (Citrus aurantium) trees boosted yields by 52.9–69.2% over two seasons (El-Nagdi et al. 2010). On 16-year-old Valencia sweet orange trees, Abd-Elgawad et al. (2010) showed a sharp decrease in T. semipenetrans juveniles and the maximum fruit output (85.6–90.2 kg/tree) following the application of B. subtilis (107 cells/mL).
Hammam et al. (2016) reported that, the effectiveness of T. semipenetrans population was higher when B. subtilis combined with compost (1016 cfu/mL) was administered to the soil of volkameriana seedlings in Egypt after 3 months of treatment under greenhouse conditions. B. subtilis had similar results in sour oranges (1 × 106 cfu/mL) mixed with compost, which caused 73.7% more T. semipenetrans death across all life stages than B. subtilis alone (66.8%) (El-Mohamedy et al. 2016). El-Tanany et al. (2018) found that soil treatment of a combination of commercial formulations including B. megaterium and T. album (Bio Arc + Bio Zeid) over two seasons boosted fruit yield and significantly decreased (66.20–78.79%) T. semipenetrans populations in Washington navel orange trees over two seasons under field conditions in Egypt.
B. megaterium, a similar species, has become a promising citrus biocontrol agent. According to Elzawahry et al. (2015), the use of the commercial formulation Bioarc TM (30 g/L) resulted in 90.5% T. semipenetrans J2 mortality following a 72-h exposure period in the laboratory. While a greenhouse study revealed a considerable reduction (89.0%, 89.5%, and 76.6%, 82.9%) in juvenile in the soil and females in the root of baladi orange and lime, respectively.
2.2.2 Pseudomonas fluorescens
It is possible to control Meloidogyne spp. and T. semipenetrans in citrus successfully by using P. fluorescens as a biocontrol agent (Rajendran et al. 2001). For instance, after 72 h of exposure under in vitro conditions, Montasser et al. (2012) reported the maximum death (99.9%) of T. semipenetrans juveniles. Hanawi (2016), however, found that after 48 h of exposure, 94% of juveniles died at a dosage of 3 × 108 cfu/mL. In comparison to untreated control plots under natural conditions in India, the application of commercial talc-based P. fluorescens formulation (20 g/tree) to the soil decreased T. semipenetrans infesting C. limon and increased the yield (Deepa et al. 2011). Despite the fact that the use of experimental culture filtrate led to a sharp decline in T. semipenetrans juveniles on sweet orange trees in Egypt when compared to control plots (48.2% at 25 mL/tree—3 × 108 cfu/mL) (Hanawi 2016). Applying neem cake (25 g/plant) and P. fluorescens (2 × 109 spores) together considerably decreased the population of T. semipenetrans in the soil and on the roots of acid lime seedlings as compared to the control (Reddy et al. 2000).
2.2.3 Streptomyces avermitilis
The naturally occurring fermentation byproduct of S. avermitilis, Abamectin, has enormous promise as a biocontrol agent for a variety of plant nematodes (Saad et al. 2017). El-Nagdi et al. (2010) reported that the application of commercial formulations of S. avermitilis—abamectin to mandarin trees grafted on sour orange (Citrus aurantium) enhanced yield by 84.6–115.4% over two seasons compared with control plots under field conditions. El-Tanany et al. (2018) evaluated abamectin (Tervigo®), oxamyl (Vydate®), and botanical insecticide to manage T. semipenetrans infesting Washington navel orange trees in Egypt. In comparison to oxamyl and azadirachtin (Achook®), the substance used in the soil (2.5 L per feddan) caused a reduction of 78.12–87.06% throughout two growing seasons. However, compared to abamectin (41.45 kg/tree), the average fruit output was much higher with oxamyl treatment (51.87 kg/tree). A similar reduction in T. semipenetrans population was found by El-Saedy et al. (2019) following the administration of Tervigo® (15 mL/tree), which also led to an increase in fruit yield (71.1 kg/tree) throughout two seasons among orange trees in Valencia
2.2.4 Pasteuria spp.
The Pasteuria sp. has been associated to T. semipenetrans in reports from various citrus-growing regions across the globe (Ciancio et al. 2016; Sorribas et al. 2000, 2008; Gené et al. 2005; Kaplan 1994; Ciancio and Roccuzzo 1992). It could function as an efficient biocontrol agent for T. semipenetrans and other plant nematodes due to the density of its endospores and their long-term persistence in soil under challenging conditions (Ciancio 2018). The population of T. semipenetrans was effectively reduced by the combined application of P. penetrans (2109 spores/plant) and P. lilacinum (50 g/plant with 4107 spores/g) (Reddy and Nagesh 2000). The limited host range and obligatory character of this genus have limited the experimental investigations that have been done utilizing it to combat T. semipenetrans. The application of these bacteria in the biocontrol of citrus nematode will be further improved by further knowledge of their biology and field ecology as well as artificial culturing of the bacteria employing fermented technology.
2.3 Mites
It has been determined that mites may be used as plant nematode biocontrol agents. Investigations on various species of mites such as Macrocheles muscaedomestica, Cosmolaelaps simplex, Macrocheles matrius, and Gaeolaelaps acule against T. semipenetrans have been undertaken on citrus, with the majority of the studies taking place in greenhouses. Al Rehiayani and Fouly (2005) found that the simultaneous application of C. simplex (200 individuals/pot) and T. semipenetrans juvenile inoculation to citrus seedlings significantly reduced the nematode’s reproduction capacity, although mite individuals were less effective than aldicarb (614 juveniles/100 cm3 soil). Salehi et al. (2014) found that key lime plants that were not treated (398.25 J2/100 cm3 soil) produced considerably more juvenile T. semipenetrans plants than those that were treated (20 individuals/pot), ranging from 126 to 161. Similar research was conducted by Abo-Korah (2017) on the efficiency of M. matrius against citrus nematode and found that it reduced T. semipenetrans juvenile population by the highest percentage (77.5%) when compared to carbofuran (76.9%), and that seedling growth was also increased. However, compared to T. semipenetrans, P. penetrans had a reduced predation efficiency. Despite the possibility of managing T. semipenetrans, problems with mass production, soil delivery, and nonspecificity prevent predatory mites from being widely used in the biocontrol of plant nematodes (Cumagun and Moosavi 2015; Viaene et al. 2006). However, the advancement of mass production, delivery, and soil ecological knowledge may boost the use of these agents shortly.
3 Biotechnological Interventions in Citrus Nematode Management
There is a dearth of information on biotechnological methods for controlling T. semipenetrans. To handle T. semipenetrans, methods including gene silencing (RNAi) and the introduction of harmful substances to the invading nematode should be taken into consideration. Natural variation for resistance, extensive germ plasm screening, and genetic markers should all be investigated to find the genes that confer resistance to T. semipenetrans. To reduce effective establishment in host cells on a sensitive or tolerant host, transgenic techniques that take advantage of an understanding of nematode-host interactions and direct the infective stage to prevent locating host roots are used (Fosu-Nyarko and Jones 2015). To counteract T. semipenetrans, citrus breeding programs are using genomic editing techniques like CRISPR/Cas (Abd-Elgawad 2022). Nanotechnology is a most recent branch of science and offers satisfactory solutions for plant disease management (Khan and Rizvi 2014; Khan et al. 2019a, b, c) and disease detection (Khan and Akram 2020; Khan and Rizvi 2016; Khan et al. 2020). Nano-sensors are the most important product of nanotechnology, and have great potential for use in plant disease diagnosis (Khan 2023). Sellappan et al. (2022) developed nanobiosensor to early detection and prevention of agricultural crops from harmful microorganisms. Using specific nanoparticles as nano-sensors to detect the plant pathogen early can reduce the plant disease damage and help in proper management of the disease (Khan and Rizvi 2018).
4 Conclusion and Future Perspectives
In addition to acting as a safer alternative to toxic chemical pesticides in citrus, biological control is crucial in the management of nematode infections. Although several fungi, bacteria, and mites have been used in citrus, a dedication to the development of high-quality products, extension programs, and collaboration between researchers, farmers, and industry will more strongly advocate the use of biological control agents against plant nematodes in citrus. To create cultivars with long-lasting resistance, major resistance genes or quantitative trait locus (QTLs) must be introgressed alongside low-impact QTLs. The next goal is to precisely identify these low-effect QTLs. This suggests that to acquire a high heritability trait, all resistance testing must be taken into account. Due to the availability of complete genome sequences for the major crops, nematode resistance genes can be found, localized, diagnosed, and cloned, a goal that is likely to be accomplished shortly. This will give breeders a flexible tool for precise resistance breeding.
References
Abd-Elgawad MMM (2020) Managing nematodes in Egyptian citrus orchards. Bull Natl Res Cent 44:1–15
Abd-Elgawad MM (2022) Understanding molecular plant–nematode interactions to develop alternative approaches for nematode control. Plants 11:2141
Abd-Elgawad MMM, El-Mougy N, El-Gamal N, Abdel-Kader M, Mohamed M (2010) Protective treatments against soil borne pathogens in citrus orchards. J Plant Prot Res 50:512–519
Abo-Korah MS (2017) Biological control of Tylenchulus semipenetrans and Pratylenchus penetrans infecting citrus trees by the predaceous mite, Macrocheles matrius. Menoufia J Plant Prot 2:291–297
Al Rehiayani SM, Fouly AH (2005) Cosmolaelaps simplex (Berlese), a polyphagous predatory mite feeding on root-knot nematode Meloidogyne javanica and citrus nematode Tylenchulus semipenetrans. Pak J Biol Sci 8:168–174
Ciancio A (2018) Biocontrol potential of Pasteuria spp. for the management of plant parasitic nematodes. CAB Rev 13:1–13
Ciancio A, Roccuzzo G (1992) Observations on a Pasteuria sp. parasitic in Tylenchulus semipenetrans. Nematologica 38:403–404
Ciancio A, Roccuzzo G, Longaron CO (2016) Regulation of the citrus nematode Tylenchulus semipenetrans by a Pasteuria sp. endoparasite in a naturally infested soil. BioControl 61:337–347
Cumagun CJR, Moosavi MR (2015) Significance of biocontrol agents of phytonematodes. In: Askary TH, Martinelli PRP (eds) Biocontrol agents of phytonematodes. CABI, Wallingford, pp 50–78
de Campos AS, dos Santos JM, Duncan LW (2002) Nematodes of citrus in open nurseries and orchards in Sao Paulo State, Brazil. Nematology 4:263–264
Deepa SP, Subramanian S, Ramakrishnan S (2011) Biomanagement of citrus nematode, Tylenchulus semipenetrans Cobb on lemon (Citrus limonia L.). J Biopest 4:205–207
Duncan LW (2009) Managing nematodes in citrus orchards. In: Ciancio A, Mukerji KG (eds) Integrated management of fruit crops nematodes. Springer, Dordrecht, pp 135–174
El-Mohamedy RSR, Hammam MMA, Abd-El-Kareem F, Abd-Elgawad MMM (2016) Biological soil treatment to control Fusarium solani and Tylenchulus semipenetrans on sour orange seedlings under greenhouse conditions. Int J Chem Tech Res 9:73–85
El-Nagdi WMA, Yossef MMA, Hafez OM (2010) Effects of commercial formulations of Bacillus thuringiensis and Streptomyces avermitilis on Tylenchulus semipenetrans and on nutrition status, yield and fruit quality of mandarin. Nematol Mediterr 38:147–157
El-Saedy MAM, Hammad SE, Awd Allah SFA (2019) Nematocidal effect of abamectin, boron, chitosan, hydrogen peroxide and Bacillus thuringiensis against citrus nematode on Valencia orange trees. J Plant Sci Phytopathol 3:111–117. https://doi.org/10.29328/journal.jpsp.1001041
El-Tanany MM, El-Shahaat MS, Khalil MS (2018) Efficacy of three bio-pesticides and oxamyl against citrus nematode (Tylenchulus semipenetrans) and on productivity of Washington Navel orange trees. Egypt J Hortic 45:275–287
Elzawahry AM, Khalil AEM, Allam ADA, Mostafa RG (2015) Effect of the bio-agents (Bacillus megaterium and Trichoderma album) on citrus nematode (Tylenchulus semipenetrans) infecting baladi orange and lime seedlings. J Phytopathol Pest Manag 2:1–8
Fosu-Nyarko J, Jones MG (2015) Application of biotechnology for nematode control in crop plants. In: Escobar C, Fenoll C (eds) Advances in botanical research, vol 73. Academic, New York, pp 339–376
Gené J, Verdejo-Lucas S, Stchigel AM, Sorribas FJ, Guarro J (2005) Microbial parasites associated with Tylenchulus semipenetrans in citrus orchards of Catalonia, Spain. Biocontrol Sci Technol 15:721–731
Global Citrus Outlook (2019). https://worldcitrusorganisation.org/wp-content/uploads/2020/01/Citrus-Market-Trends-2019.pdf
Gottlieb Y, Cohen E, Spiegel-Roy P (1987) Assessing resistance of citrus rootstocks to Tylenchulus semipenetrans with rooted leaves. Revue de Nematologie 10:119–121
Hammam MMA, El-Mohamedy RSR, Abd-El-Kareem F, Abd-Elgawad MMM (2016) Evaluation of soil amended with bio-agents and compost alone or in combination for controlling citrus nematode Tylenchulus semipenetrans and Fusarium dry root rot on Volkamer lime under greenhouse conditions. Int J Chem Tech Res 9:86–96
Hanawi MJ (2016) Fungal and bacterial bio-control agents in controlling citrus nematode Tylenchulus semipenetrans Cobb in greenhouse and field. Eur Acad Res 4:7824–7841
Ibrahim D, Ali A, Metwaly H (2019) Bio-management of citrus nematode, Tylenchulus semipenetrans and dry root rot fungi, Fusarium solani under laboratory and field conditions. Egypt J Agronematol 18:118–128
Ingham RE (1988) Interactions between nematodes and vesicular-arbuscular mycorrhizae. Agric Ecosyst Environ 24:169–182
Iqbal MA, Mukhtar T, Ahmad R, Khan HU (2006) Ecological prevalence of Tylenchulus semipenetrans in four districts of the Punjab province, Pakistan. Pak J Nematol 24:19–26
Jatala P (1986) Biological control of plant-parasitic nematodes. Annu Rev Phytopathol 24(1):453–489
Kaplan DT (1994) Partial characterization of a Pasteuria sp. attacking the citrus nematode, Tylenchulus semipenetrans, in Florida. Fundam Appl Nematol 17:509–512
Kaplan DT, O’Bannon JH (1981) Evaluation and nature of citrus nematode resistance in Swingle citrumelo. Proc Florida State Hortic Soc 94:33–36
Kerry BR (2000) Rhizosphere interactions and the exploitation of microbial agents for the biological control of plant-parasitic nematodes. Annu Rev Phytopathol 38:423–441. https://doi.org/10.1146/annurev.phyto.38.1.423
Khan MR (2007) Prospects of microbial control of root-knot nematodes infecting vegetable crops. In: Sharma N, Singh HB (eds) Biotechnology: plant heatlh management. International Book Distributing, Co., pp 643–665
Khan MR (2008) Plant nematodes- methodology, morphology, systematics, biology and ecology. Science Publishers, New Hampshire, p 360
Khan MR (2016) Nematode biocontrol agents: diversity and effectiveness against phytonematodes in sustainable crop protection. Indian Phytopathol 69(4s):453–463
Khan MR (2023) Plant nematodes, hidden constraints in the global crop production. In: Khan MR, Quintanilla M (eds) Nematode diseases of crops and their sustainable management. Elsevier Publishers, pp 3–23
Khan MR, Akram M (2020) Nanoparticles and their fate in soil ecosystem. In: Biogenic nano-particles and their use in agro-ecosystems. Springer, Singapore, pp 221–245
Khan MR, Anwer A (2011) Fungal bioinoculants for plant disease management. In: Paul M, Clinton M, Ahmad I (eds) Microbes and microbial technology. Springer, pp 447–488
Khan MR, Mohiddin FA (2018) Trichoderma: its multifarious utility in crop improvement. In Crop Improvement Through Microbial Biotechnology (pp. 263–291). Elsevier.
Khan MR, Rizvi TF (2014) Nanotechnology: scope and application in plant disease management. Plant Pathol J 13(3):214–231
Khan MR, Rizvi TF (2016) Application of nanofertilizer and nanopesticides for improvements in crop production and protection. In: Ghorbanpour M, Manika K, Varma A (eds) Nanoscience and plant–soil systems. Springer, pp 405–428
Khan MR, Rizvi TF (2018) Nanotechnology, a tool for reducing pesticide input in plant protection. In: Khan MR, Mukhopadhyay AN, Pandey RN, Thakur MP, Singh D, Siddiqui MA, Akram MD, Haque Z (eds) Bio-intensive approaches: application and effectiveness in plant diseases management. Today and Tomorrow Publishes, New Delhi, pp 225–242
Khan MR, Altaf S, Mohiddin FA, Khan U, Anwer A (2009) Biological control of plant nematodes with phosphate solubilizing microorganisms. In: Khan MS, Zaidi A (eds) Phosphate solubilizing microbes for crop improvement. Nova science publishers, Inc., New York, pp 395–426
Khan MR, Majid S, Mohidin FA, Khan N (2011) A new bioprocess to produce low cost powder formulations of biocontrol bacteria and fungi to control fusarial wilt and root-knot nematode of pulses. Biol Control 59(2):130–140. https://doi.org/10.1016/j.biocontrol.2011.04.007
Khan MR, Mohidin FA, Khan U, Ahamad F (2016a) Inoculant rhizobia suppressed root-knot disease, and enhanced plant productivity and nutrient uptake of some field-grown food legumes. Acta Agriculturae Scandinavica Section B 68(2):1–9
Khan MR, Mohidin FA, Khan U, Ahamad F (2016b) Native Pseudomonas spp. suppressed the root-knot nematode in in-vitro and in-vivo, and promoted the nodulation and grain yield in the field grown mungbean. Biol Control 101:159–168. https://doi.org/10.1016/j.biocontrol.2016.06.012
Khan MR, Ahamad F, Rizvi TF (2019a) Application of nanomaterials in plant disease diagnosis and management. In: Nanobiotechnology applications in plant protection. Springer Nature Switzerland, pp 1–21. https://doi.org/10.1007/978-3-030-13296-5_2
Khan MR, Ahamad F, Rizvi TF (2019b) Effect of nanoparticles on plant pathogens. In: Ghobanpour M, Wani SH (eds) Advances in phytonanotechnology: from synthesis to appilication. Elsevier/Acadmic Press, pp 215–240
Khan MR, Adam V, Rizvi TF, Zhang B, Ahamad F, Jośko I, Zhu Y, Yang M, Mao M (2019c) Nanoparticle–plant interactions: a two-way traffic. Small. https://doi.org/10.1002/smll.201901794
Khan MR, Fromm KM, Rizvi TF, Giese B, Ahamad F, Turner RJ, Füeg M, Marsili E (2020) Metal nanoparticle-microbe interactions: synthesis and antimicrobial effects. In: Particle and particle systems characterization. https://doi.org/10.1002/ppsc.201900419
Khan MR, Ahamad I, Shah H (2021) Emerging important nematode problems in field crops and their management. In: Singh KP, Jahagirdar S, Sarma BK (eds) Emerging trends in plant pathology. Springer Nature, pp 33–62
Khan MR, Ruiu L, Akram M, Qasim ABR (2023) Nematode problems in cucurbits and their sustainable management. In: Khan MR, Quintanilla M (eds) Nematode diseases of crops and their sustainable management. Elsevier Publishers
Kumar KK (2020) Fungi: a bio-resource for the control of plant parasitic nematodes. In: Yadav A, Mishra S, Kour D, Yadav N, Kumar A (eds) Agriculturally important fungi for sustainable agriculture. Springer, Cham, pp 285–311
Kumar KK, Das AK (2019) Diversity and community analysis of plant parasitic nematodes associated with citrus at citrus research station, Tinsukia. Assam. J Entomol Zool Stud 7:187–189
Kumar S, Prabhu S (2009) Biological control of citrus nematode, Tylenchulus semipenetrans in citrus nursery. Indian J Nematol 39:249–250
Maafi ZT, Damadzadeh M (2008) Incidence and control of the citrus nematode, Tylenchulus semipenetrans Cobb, in the north of Iran. Nematology 10:113–122
Martinelli PRP, Santos JM, Barbosa JC (2012) Efficacy of formulations containing five nematophagous fungi for the management of Pratylenchus jaehni in Citrus. Nematol Brasil 36:1–8
Matheyambath AC, Padmanabhan P, Paliyath G (2016) Citrus fruits. In: Benjamin C, Finglas PM, Toldra F (eds) Encyclopedia of food and health. Academic, New York, pp 136–140
Maznoor S, Sinha AK, Bora BC (2002) Management of citrus nematode, Tylenchulus semipenetrans on Khasi Mandarin, by Paecilomyces lilacinus. Indian J Nematol 32(2):153–155
Mohammed RKA, Khan MR (2021) Management of root-knot nematode in cucumber through seed treatment with multifarious beneficial microbes under protected cultivation. Indian Phytopathol 74(4):1035–1043. https://doi.org/10.1007/s42360-021-00422-3
Mohiddin FA, Khan MR (2013) Tolerance of fungal and bacterial biocontrol agents to six pesticides commonly used in the control of soil borne plant pathogens. Afr J Agric 8(43):5272–5275
Mohiddin FA, Khan MR, Khan SM, Bhat BH (2010) Why Trichoderma is considered super hero (super fungus) against the evil parasites? Plant Pathol J 9(3):92–102. https://doi.org/10.3923/ppj.2010.92.102
Montasser SA, Abd El-Wahab AE, Abd-Elgawad MMM, Abd-El-Khair H, Faika FHK, Hammam MMA (2012) Effects of some fungi and bacteria as bio-control agents against citrus nematode Tylenchulus semipenetrans Cobb. J Appl Sci Res 8:5436–5444
Narendra BW, Sinha AK, Neog PP (2008) Biological control of citrus nematode Tylenchulus semipenetrans on Citrus jambhiri. Indian J Nematol 38:244–246
Noweer EMA (2018) Effect of the nematode-trapping fungus Dactylaria brochopaga and the nematode egg parasitic fungus Verticilium chlamydosporium in controlling citrus nematode infesting mandarin, and inter relationship with the co inhabitant fungi. Int J Eng Technol 7:19–23
O’Bannon JH, Inserra RN, Nemec S, Vovlas N (1979) The Influence of Glomus mosseae on Tylenchulus semipenetrans-infected and uninfected citrus limon seedlings. J Nematol 11:247–250
Rajendran G, Ramakrishnan S, Subramanian S (2001) Biomanagement of nematodes in horticultural crops. South Ind Hortic 49:227–230
Rao MS (2005) Management of Meloidogyne javanica on acid lime nursery seedlings by using formulations of Pochonia chlamydosporia and Paecilomyces lilacinus. Nematol Mediterr 33:145–148
Rao MS (2008) Management of Meloidogyne javanica on acid lime using Paecilomyces lilacinus and Pseudomonas fluorescens. Nematol Mediterr 36:45–50
Ravichandra NG (2014) Nematode diseases of horticultural crops. In: Ravichandra NG (ed) Horticultural nematology. Springer, New Delhi, pp 127–205. https://doi.org/10.1007/978-81-322-1841-8_8
Reddy PP (2018) Emerging nematode problems in fruit crops. In: Reddy PP (ed) Emerging crop pest problems: redefining management strategies. Scientific Publishers, Delhi, pp 196–216
Reddy PP, Nagesh M (2000) Integrated management of the citrus nematode using bacterial (Pasteuria penetrans) and fungal (Paecilomyces lilacinus) biocontrol agents. In: Proceedings, international symposium on citriculture, pp 825–829
Reddy PP, Rao MS, Mohandas S, Nagesh M (1995) Integrated management of the citrus nematode, Tylenchulus semipenetrans Cobb using VA mycorrhiza, Glomus fasciculatum (Thaxt.) Gerd & Trappe and oil cakes. Pest Manag Hortic Ecosyst 1:37–41
Reddy PP, Rao MS, Nagesh M (1996) Management of citrus nematode, Tylenchulus semipenetrans, by integration of Trichoderma harzianum with oil cakes. Nematol Mediterr 24:265–267
Reddy PP, Nagesh M, Rao MS, Rama N (2000) Management of Tylenchulus semipenetrans by integration of Pseudomonas fluorescens with oil cakes. In: Proceedings of the international symposium on citriculture, pp 830–833
Saad ASA, Radwan MA, Mesbah HA, Ibrahim HS, Khalil MS (2017) Evaluation of some non-fumigant nematicides and the biocide avermectin for managing Meloidogyne incognita in tomatoes. Pak J Nematol 35:85–92
Salehi A, Ostovan H, Modarresi M (2014) Evaluation of the efficiency of Gaeolaelaps aculeifer in control of plant parasitic nematode Tylenchulus semipenetrans under greenhouse conditions. J Entomol Nematol 6:150–153
Schouteden N, De Waele D, Panis B, Vos CM (2015) Arbuscular mycorrhizal fungi for the biocontrol of plant-parasitic nematodes: a review of the mechanisms involved. Front Microbiol 6:1280. https://doi.org/10.3389/fmicb.2015.01280
Sellappan L, Manoharan S, Sanmugam A, Anh NT (2022) Role of nanobiosensors and biosensors for plant virus detection. In: Denizli A, Nguyen TA, Rajendran S, Yasin G, Nadda AK (eds) Micro and nano technol nanosens smart agric. Elsevier, Amsterdam, p 493
Shahid S, Khan MR (2019) Evaluation of biocontrol agents for the management of root-rot of mung bean caused by Macrophomina phaseolina. Indian Phytopathol 72:89–98
Sharon E, Bar-Eyal M, Chet I, Herrera-Estrella A, Kleifeld O, Spiegel Y (2001) Biological control of the root-knot nematode Meloidogyne javanica by Trichoderma harzianum. Phytopathology 91:687–693
Shawky S, Al-Ghonaimy A (2015) Efficacy of some bioagents and plant extracts in controlling Tylenchulus semipenetrans on citrus in Egypt. Egypt J Agronematol 14:45–61
Shokoohi E, Duncan LW (2018) Nematode parasites of citrus. In: Sikora R, Timper P, Coyne D (eds) Plant-parasitic nematodes in tropical & subtropical agriculture, 3rd edn. CAB International, St. Albans, pp 446–476
Sikora RA, Roberts PA (2018) Management practices: an overview of integrated nematode management technologie. In: Plant parasitic nematodes in subtropical and tropical agriculture, pp 795–838
Sorribas FJ, Verdejo-Lucas S, Forner JB, Alcaidel A, Pons J, Ornat C (2000) Seasonality of Tylenchulus semipenetrans Cobb and Pasteuria sp. in citrus orchards in Spain. J Nematol 32:622–632
Sorribas FJ, Verdejo-Lucas S, Pastor J, Ornat C, Pons J, Valero J (2008) Population densities of Tylenchulus semipenetrans related to physicochemical properties of soil and yield of clementine mandarin in Spain. Plant Dis 92:445–450
Stirling GR (1991) Biological control of plant parasitic nematodes: progress, problems and prospects: by GR Stirling. CAB International. 282 pp
Verdejo-Lucas S, McKenry MV (2004) Management of the citrus nematode, Tylenchulus semipenetrans. J Nematol 36:424–432
Verdejo-Lucas S, Sorribas FJ, Forne FB, Alcaide A (2000) Resistance of hybrid citrus rootstocks to a Mediterranean biotype of Tylenchulus semipenetrans Cobb. HortScience 35:269–273
Viaene N, Coyne DL, Kerry BR (2006) Biological and cultural management. In: Perry RN, Moens M (eds) Plant nematology. CAB International, Wallingford, pp 346–369
Vos C, Geerinckx K, Mkandawire R, Panis B, De Waele D, Elsen A (2012) Arbuscular mycorrhizal fungi affect both penetration and further life stage development of root-knot nematodes in tomato. Mycorrhiza 22:157–163
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Kumar, K.K., Pervez, R. (2023). Citrus Nematode in Fruit Crops and Their Management by Biological and Biotechnological Interventions. In: Khan, M.R. (eds) Novel Biological and Biotechnological Applications in Plant Nematode Management. Springer, Singapore. https://doi.org/10.1007/978-981-99-2893-4_20
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