Disease Control Strategies in Citrus Plants

A special issue of Plants (ISSN 2223-7747). This special issue belongs to the section "Plant Protection and Biotic Interactions".

Deadline for manuscript submissions: closed (30 September 2023) | Viewed by 16744

Special Issue Editors


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Guest Editor
Plant Pathologist/Program Director, Citrus Pest Detection Program (CPDP), Central California Tristeza Eradication Agency (CCTEA), 22847 Road 140, Tulare, CA 93274-9367, USA
Interests: survey and detection of citrus pest and diseases; high-throughput diagnostics; plant disease management; citrus viruses and viroids; citrus psyllid; Huanglongbing (HLB)

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Guest Editor
1. Associate Professor of Research, Horticulture and Plant Pathology, Kingsville Citrus Center, Texas A&M University, Weslaco, TX 78599, USA
2. Agriculture, Agribusiness, and Environmental Sciences Department, Texas A&M University-Kingsville, Kingsville, TX 78363, USA
Interests: plant pathology; pathogen identification and diagnostics; biotechnology; and disease management; citrus psyllid; Huanglongbing (HLB)

Special Issue Information

Dear Colleagues,

Historically, citrus production has faced many serious problems including but not limited to fungal, bacterial, viral and viroid diseases. Certain parts of the world face unique challenges due to their unique environments, use of specific citrus scion and rootstock, and cultural practices. Arrival of the HLB disease in Florida (USA) has encouraged the citrus industries in other states and countries to follow basic plant disease control strategies such as exclusion, eradication and/or suppression of the disease. In addition, research on therapy, resistance, or tolerance development in cultivars has driven the research community to explore cutting-edge technologies such as citrus tristeza virus vectors, RNA interference, CRISPR/Cas9, and nanoparticle-based chemical therapy. Efficient and sustainable citrus plant protection is of great economic and ecological significance for global crop production. With this Special Issue, we invite the submission of original research articles, short communications, and comprehensive reviews to share the latest research on control strategies for any biotic factors including but not limited to fungal, bacterial, and viral pathogens of citrus.

Dr. Subhas Hajeri
Dr. Madhurababu Kunta
Guest Editors

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Published Papers (9 papers)

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Research

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26 pages, 2959 KiB  
Article
Next Generation Sequencing, and Development of a Pipeline as a Tool for the Detection and Discovery of Citrus Pathogens to Facilitate Safer Germplasm Exchange
by Manjunath Keremane, Khushwant Singh, Chandrika Ramadugu, Robert R. Krueger and Todd H. Skaggs
Plants 2024, 13(3), 411; https://doi.org/10.3390/plants13030411 - 30 Jan 2024
Cited by 2 | Viewed by 1351
Abstract
Citrus is affected by many diseases, and hence, the movement of citrus propagative materials is highly regulated in the USA. Currently used regulatory pathogen detection methods include biological and laboratory-based technologies, which are time-consuming, expensive, and have many limitations. There is an urgent [...] Read more.
Citrus is affected by many diseases, and hence, the movement of citrus propagative materials is highly regulated in the USA. Currently used regulatory pathogen detection methods include biological and laboratory-based technologies, which are time-consuming, expensive, and have many limitations. There is an urgent need to develop alternate, rapid, economical, and reliable testing methods for safe germplasm exchange. Citrus huanglongbing (HLB) has devastated citrus industries leading to an increased need for germplasm exchanges between citrus growing regions for evaluating many potentially valuable hybrids for both HLB resistance and multilocational performance. In the present study, Next-Generation Sequencing (NGS) methods were used to sequence the transcriptomes of 21 test samples, including 15 well-characterized pathogen-positive plants. A workflow was designed in the CLC Genomics Workbench software, v 21.0.5 for bioinformatics analysis of the sequence data for the detection of pathogens. NGS was rapid and found to be a valuable technique for the detection of viral and bacterial pathogens, and for the discovery of new citrus viruses, complementary to the existing array of biological and laboratory assays. Using NGS methods, we detected beet western yellows virus, a newly reported citrus virus, and a variant of the citrus yellow vein-associated virus associated with the “fatal yellows” disease. Full article
(This article belongs to the Special Issue Disease Control Strategies in Citrus Plants)
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16 pages, 5173 KiB  
Article
Co-Occurrence Analysis of Citrus Root Bacterial Microbiota under Citrus Greening Disease
by Jong-Won Park, W. Evan Braswell and Madhurababu Kunta
Plants 2024, 13(1), 80; https://doi.org/10.3390/plants13010080 - 26 Dec 2023
Viewed by 1136
Abstract
Candidatus Liberibacter asiaticus (CLas) is associated with Citrus Huanglongbing (HLB), a devastating disease in the US. Previously, we conducted a two-year-long monthly HLB survey by quantitative real-time PCR using root DNA fractions prepared from 112 field grapefruit trees grafted on sour orange rootstock. [...] Read more.
Candidatus Liberibacter asiaticus (CLas) is associated with Citrus Huanglongbing (HLB), a devastating disease in the US. Previously, we conducted a two-year-long monthly HLB survey by quantitative real-time PCR using root DNA fractions prepared from 112 field grapefruit trees grafted on sour orange rootstock. Approximately 10% of the trees remained CLas-free during the entire survey period. This study conducted 16S metagenomics using the time-series root DNA fractions, monthly prepared during twenty-four consecutive months, followed by microbial co-occurrence network analysis to investigate the microbial factors contributing to the CLas-free phenotype of the aforementioned trees. Based on the HLB status and the time when the trees were first diagnosed as CLas-positive during the survey, the samples were divided into four groups, Stage H (healthy), Stage I (early), II (mid), and III (late) samples. The 16S metagenomics data using Silva 16S database v132 revealed that HLB compromised the diversity of rhizosphere microbiota. At the phylum level, Actinobacteria and Proteobacteria were the predominant bacterial phyla, comprising >93% of total bacterial phyla, irrespective of HLB status. In addition, a temporal change in the rhizosphere microbe population was observed during a two-year-long survey, from which we confirmed that some bacterial families differently responded to HLB disease status. The clustering of the bacterial co-occurrence network data revealed the presence of a subnetwork composed of Streptomycetaceae and bacterial families with plant growth-promoting activity in Stage H and III samples. These data implicated that the Streptomycetaceae subnetwork may act as a functional unit against HLB. Full article
(This article belongs to the Special Issue Disease Control Strategies in Citrus Plants)
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30 pages, 5532 KiB  
Article
Gamma-Aminobutyric Acid Accumulation Contributes to Citrus sinensis Response against ‘Candidatus Liberibacter Asiaticus’ via Modulation of Multiple Metabolic Pathways and Redox Status
by Yasser Nehela and Nabil Killiny
Plants 2023, 12(21), 3753; https://doi.org/10.3390/plants12213753 - 2 Nov 2023
Cited by 2 | Viewed by 1654
Abstract
Huanglongbing (HLB; also known as citrus greening) is the most destructive bacterial disease of citrus worldwide with no known sustainable cure yet. Herein, we used non-targeted metabolomics and transcriptomics to prove that γ-aminobutyric acid (GABA) accumulation might influence the homeostasis of several metabolic [...] Read more.
Huanglongbing (HLB; also known as citrus greening) is the most destructive bacterial disease of citrus worldwide with no known sustainable cure yet. Herein, we used non-targeted metabolomics and transcriptomics to prove that γ-aminobutyric acid (GABA) accumulation might influence the homeostasis of several metabolic pathways, as well as antioxidant defense machinery, and their metabolism-related genes. Overall, 41 metabolites were detected in ‘Valencia’ sweet orange (Citrus sinensis) leaf extract including 19 proteinogenic amino acids (PAA), 10 organic acids, 5 fatty acids, and 9 other amines (four phenolic amines and three non-PAA). Exogenous GABA application increased most PAA in healthy (except L-threonine, L-glutamine, L-glutamic acid, and L-methionine) and ‘Candidatus L. asiaticus’-infected citrus plants (with no exception). Moreover, GABA accumulation significantly induced L-tryptophan, L-phenylalanine, and α-linolenic acid, the main precursors of auxins, salicylic acid (SA), and jasmonic acid (JA), respectively. Furthermore, GABA supplementation upregulated most, if not all, of amino acids, phenolic amines, phytohormone metabolism-related, and GABA shunt-associated genes in both healthy and ‘Ca. L. asiaticus’-infected leaves. Moreover, although ‘Ca. L. asiaticus’ induced the accumulation of H2O2 and O2•− and generated strong oxidative stress in infected leaves, GABA possibly stimulates the activation of a multilayered antioxidative system to neutralize the deleterious effect of reactive oxygen species (ROS) and maintain redox status within infected leaves. This complex system comprises two major components: (i) the enzymatic antioxidant defense machinery (six POXs, four SODs, and CAT) that serves as the front line in antioxidant defenses, and (ii) the non-enzymatic antioxidant defense machinery (phenolic acids and phenolic amines) that works as a second defense line against ‘Ca. L. asiaticus’-induced ROS in citrus infected leaves. Collectively, our findings suggest that GABA might be a promising alternative eco-friendly strategy that helps citrus trees battle HLB particularly, and other diseases in general. Full article
(This article belongs to the Special Issue Disease Control Strategies in Citrus Plants)
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21 pages, 739 KiB  
Article
Modeling Study of the Effects of Ageratum conyzoides on the Transmission and Control of Citrus Huanglongbing
by Ying Wang, Shujing Gao, Yujiang Liu and Huaiping Zhu
Plants 2023, 12(20), 3659; https://doi.org/10.3390/plants12203659 - 23 Oct 2023
Viewed by 1029
Abstract
Ageratum conyzoides (A. conyzoides) is commonly found or intentionally planted in citrus orchards due to its ability to provide habitat and breeding grounds for the natural enemies of citrus pests. This study aims to expand from a switching Huanglongbing model by [...] Read more.
Ageratum conyzoides (A. conyzoides) is commonly found or intentionally planted in citrus orchards due to its ability to provide habitat and breeding grounds for the natural enemies of citrus pests. This study aims to expand from a switching Huanglongbing model by incorporating the effects of A. conyzoides, vector preferences for settling, and pesticide application intervals on disease transmission. Additionally, we establish the basic reproduction number R0 and its calculation for a general switching compartmental epidemic model. Theoretical findings demonstrate that the basic reproduction number serves as a threshold parameter to characterize the dynamics of the models: if R0<1, the disease will disappear, whereas if R0>1, it will spread. Numerical results indicate that the recruitment rate of A. conyzoides not only affects the spread speed of Huanglongbing but also leads to paradoxical effects. Specifically, in cases of high infection rates, a low recruitment rate of A. conyzoides can result in a decrease, rather than an increase, in the basic reproduction number. Conversely, a high recruitment rate can accelerate the spread of Huanglongbing. Furthermore, we show how different vector bias and pesticide spraying periods affect the basic reproduction number. Full article
(This article belongs to the Special Issue Disease Control Strategies in Citrus Plants)
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25 pages, 4982 KiB  
Article
Gamma-Aminobutyric Acid Supplementation Boosts the Phytohormonal Profile in ‘Candidatus Liberibacter asiaticus’-Infected Citrus
by Yasser Nehela and Nabil Killiny
Plants 2023, 12(20), 3647; https://doi.org/10.3390/plants12203647 - 22 Oct 2023
Cited by 1 | Viewed by 1270
Abstract
The devastating citrus disease, Huanglongbing (HLB), is associated with ‘Candidatus Liberibacter sp.’ and transmitted by citrus psyllids. Unfortunately, HLB has no known sustainable cure yet. Herein, we proposed γ-aminobutyric acid (GABA) as a potential eco-friendly therapeutic solution to HLB. Herein, we used [...] Read more.
The devastating citrus disease, Huanglongbing (HLB), is associated with ‘Candidatus Liberibacter sp.’ and transmitted by citrus psyllids. Unfortunately, HLB has no known sustainable cure yet. Herein, we proposed γ-aminobutyric acid (GABA) as a potential eco-friendly therapeutic solution to HLB. Herein, we used GC/MS-based targeted metabolomics combined with gene expression to investigate the role of GABA in citrus response against HLB and to better understand its relationship(s) with different phytohormones. GABA supplementation via root drench boosts the accumulation of endogenous GABA in the leaves of both healthy and ‘Ca. L. asiaticus’-infected trees. GABA accumulation benefits the activation of a multi-layered defensive system via modulating the phytohormone levels and regulating the expression of their biosynthesis genes and some pathogenesis-related proteins (PRs) in both healthy and ‘Ca. L. asiaticus’-infected plants. Moreover, our findings showed that GABA application stimulates auxin biosynthesis in ‘Ca. L. asiaticus’-infected plants via the activation of the indole-3-pyruvate (I3PA) pathway, not via the tryptamine (TAM)-dependent pathway, to enhance the growth of HLB-affected trees. Likewise, GABA accumulation was associated with the upregulation of SA biosynthesis genes, particularly the PAL-dependent route, resulting in higher SA levels that activated CsPR1, CsPR2, CsPR5, and CsWRKY70, which are prominent to activation of the SA-mediated pathway. Additionally, higher GABA levels were correlated with an enhanced JA profile and linked with both CsPR3 and CsPR4, which activates the JA-mediated pathway. Collectively, our findings suggest that exogenous GABA application might be a promising alternative and eco-friendly strategy that helps citrus trees battle HLB. Full article
(This article belongs to the Special Issue Disease Control Strategies in Citrus Plants)
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13 pages, 2140 KiB  
Article
Alternative Tissue Sampling for Improved Detection of Candidatus Liberibacter asiaticus
by Subhas Hajeri, Sandra Olkowski, Lucita Kumagai, Neil McRoberts and Raymond K. Yokomi
Plants 2023, 12(19), 3364; https://doi.org/10.3390/plants12193364 - 23 Sep 2023
Viewed by 1014
Abstract
Early detection and prompt response are key factors in the eradication of ‘huanglongbing’ (HLB) in California. Currently, qPCR testing of leaf tissue guides the removal of infected trees. However, because of the uneven distribution of ‘Candidatus Liberibacter asiaticus’ (CLas) in [...] Read more.
Early detection and prompt response are key factors in the eradication of ‘huanglongbing’ (HLB) in California. Currently, qPCR testing of leaf tissue guides the removal of infected trees. However, because of the uneven distribution of ‘Candidatus Liberibacter asiaticus’ (CLas) in an infected tree and asymptomatic infection, selecting the best leaves to sample, from a mature tree with more than 200,000 estimated leaves, is a major hurdle for timely detection. The goal of this study was to address this issue by testing alternative tissues that might improve the CLas detection rate. Using two years of field data, old and young leaves, peduncle bark of fruit, and feeder roots were evaluated for the presence of CLas. Quadrant-peduncle (Q-P) tissue sampling consistently resulted in better CLas detection than any other tissue type. Q-P samples had a 30% higher qPCR positivity rate than quadrant-leaf (Q-L) samples. No significant seasonal patterns were observed. Roots and single peduncles had similar detection rates; both were higher than single leaves or Q-L samples. If symptoms were used to guide sampling, 30% of infected trees would have been missed. Taken together, these results suggest that Q-P tissue sampling is the optimal choice for improved CLas detection under California growing conditions. Full article
(This article belongs to the Special Issue Disease Control Strategies in Citrus Plants)
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17 pages, 1040 KiB  
Article
Differential Expression of miRNAs Involved in Response to Candidatus Liberibacter asiaticus Infection in Mexican Lime at Early and Late Stages of Huanglongbing Disease
by Ana Marlenne Bojórquez-Orozco, Ángela Paulina Arce-Leal, Ricardo A. Chávez Montes, María Elena Santos-Cervantes, Abraham Cruz-Mendívil, Jesús Méndez-Lozano, Araceli G. Castillo, Edgar A. Rodríguez-Negrete and Norma Elena Leyva-López
Plants 2023, 12(5), 1039; https://doi.org/10.3390/plants12051039 - 24 Feb 2023
Cited by 1 | Viewed by 1897
Abstract
Huanglongbing (HLB) is one of the most destructive diseases threatening citriculture worldwide. This disease has been associated with α-proteobacteria species, namely Candidatus Liberibacter. Due to the unculturable nature of the causal agent, it has been difficult to mitigate the disease, and nowadays a [...] Read more.
Huanglongbing (HLB) is one of the most destructive diseases threatening citriculture worldwide. This disease has been associated with α-proteobacteria species, namely Candidatus Liberibacter. Due to the unculturable nature of the causal agent, it has been difficult to mitigate the disease, and nowadays a cure is not available. MicroRNAs (miRNAs) are key regulators of gene expression, playing an essential role in abiotic and biotic stress in plants including antibacterial responses. However, knowledge derived from non-model systems including Candidatus Liberibacter asiaticus (CLas)-citrus pathosystem remains largely unknown. In this study, small RNA profiles from Mexican lime (Citrus aurantifolia) plants infected with CLas at asymptomatic and symptomatic stages were generated by sRNA-Seq, and miRNAs were obtained with ShortStack software. A total of 46 miRNAs, including 29 known miRNAs and 17 novel miRNAs, were identified in Mexican lime. Among them, six miRNAs were deregulated in the asymptomatic stage, highlighting the up regulation of two new miRNAs. Meanwhile, eight miRNAs were differentially expressed in the symptomatic stage of the disease. The target genes of miRNAs were related to protein modification, transcription factors, and enzyme-coding genes. Our results provide new insights into miRNA-mediated regulation in C. aurantifolia in response to CLas infection. This information will be useful to understand molecular mechanisms behind the defense and pathogenesis of HLB. Full article
(This article belongs to the Special Issue Disease Control Strategies in Citrus Plants)
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16 pages, 8636 KiB  
Article
Custom-Developed Reflection–Transmission Integrated Vision System for Rapid Detection of Huanglongbing Based on the Features of Blotchy Mottled Texture and Starch Accumulation in Leaves
by Qian Xu, Jianrong Cai, Lixin Ma, Bin Tan, Ziqi Li and Li Sun
Plants 2023, 12(3), 616; https://doi.org/10.3390/plants12030616 - 30 Jan 2023
Cited by 1 | Viewed by 1341
Abstract
Huanglongbing (HLB) is a highly contagious and devastating citrus disease that causes huge economic losses to the citrus industry. Because it cannot be cured, timely detection of the HLB infection status of plants and removal of diseased trees are effective ways to reduce [...] Read more.
Huanglongbing (HLB) is a highly contagious and devastating citrus disease that causes huge economic losses to the citrus industry. Because it cannot be cured, timely detection of the HLB infection status of plants and removal of diseased trees are effective ways to reduce losses. However, complex HLB symptoms, such as single HLB-symptomatic or zinc deficiency + HLB-positive, cannot be identified by a single reflection imaging method at present. In this study, a vision system with an integrated reflection–transmission image acquisition module, human–computer interaction module, and power supply module was developed for rapid HLB detection in the field. In reflection imaging mode, 660 nm polarized light was used as the illumination source to enhance the contrast of the HLB symptoms in the images based on the differences in the absorption of narrow-band light by the components within the leaves. In transmission imaging mode, polarization images were obtained in four directions, and the polarization angle images were calculated using the Stokes vector to detect the optical activity of starch. A step-by-step classification model with four steps was used for the identification of six classes of samples (healthy, HLB-symptomatic, zinc deficiency, zinc deficiency + HLB-positive, magnesium deficiency, and boron deficiency). The results showed that the model had an accuracy of 96.92% for the full category of samples and 98.08% for the identification of multiple types of HLB (HLB-symptomatic and zinc deficiency + HLB-positive). In addition, the classification model had good recognition of zinc deficiency and zinc deficiency + HLB-positive samples, at 92.86%. Full article
(This article belongs to the Special Issue Disease Control Strategies in Citrus Plants)
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Review

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57 pages, 12228 KiB  
Review
Huanglongbing Pandemic: Current Challenges and Emerging Management Strategies
by Dilip Ghosh, Sunil Kokane, Brajesh Kumar Savita, Pranav Kumar, Ashwani Kumar Sharma, Ali Ozcan, Amol Kokane and Swadeshmukul Santra
Plants 2023, 12(1), 160; https://doi.org/10.3390/plants12010160 - 29 Dec 2022
Cited by 20 | Viewed by 4749
Abstract
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 [...] Read more.
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 article 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. Full article
(This article belongs to the Special Issue Disease Control Strategies in Citrus Plants)
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