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      A Pathogen Secreted Protein as a Detection Marker for Citrus Huanglongbing

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          Abstract

          The citrus industry is facing an unprecedented crisis due to Huanglongbing (HLB, aka citrus greening disease), a bacterial disease associated with the pathogen Candidatus Liberibacter asiaticus ( CLas) that affects all commercial varieties. Transmitted by the Asian citrus psyllid (ACP), CLas colonizes citrus phloem, leading to reduced yield and fruit quality, and eventually tree decline and death. Since adequate curative measures are not available, a key step in HLB management is to restrict the spread of the disease by identifying infected trees and removing them in a timely manner. However, uneven distribution of CLas cells in infected trees and the long latency for disease symptom development makes sampling of trees for CLas detection challenging. Here, we report that a CLas secreted protein can be used as a biomarker for detecting HLB infected citrus. Proteins secreted from CLas cells can presumably move along the phloem, beyond the site of ACP inoculation and CLas colonized plant cells, thereby increasing the chance of detecting infected trees. We generated a polyclonal antibody that effectively binds to the secreted protein and developed serological assays that can successfully detect CLas infection. This work demonstrates that antibody-based diagnosis using a CLas secreted protein as the detection marker for infected trees offers a high-throughput and economic approach that complements the approved quantitative polymerase chain reaction-based methods to enhance HLB management programs.

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          Most cited references42

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          Current epidemiological understanding of citrus Huanglongbing .

          Huanglongbing (HLB) is the most destructive citrus pathosystem worldwide. Previously known primarily from Asia and Africa, it was introduced into the Western Hemisphere in 2004. All infected commercial citrus industries continue to decline owing to inadequate current control methods. HLB increase and regional spatial spread, related to vector populations, are rapid compared with other arboreal pathosystems. Disease dynamics result from multiple simultaneous spatial processes, suggesting that psyllid vector transmission is a continuum from local area to very long distance. Evolutionarily, HLB appears to have originated as an insect endosymbiont that has moved into plants. Lack of exposure of citrus to the pathogen prior to approximately 100 years ago did not provide sufficient time for development of resistance. A prolonged incubation period and regional dispersal make eradication nonviable. Multiple asymptomatic infections per symptomatic tree, incomplete systemic distribution within trees, and prolonged incubation period make detection difficult and greatly complicate disease control.
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            A review of advanced techniques for detecting plant diseases

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              Phytoplasma protein effector SAP11 enhances insect vector reproduction by manipulating plant development and defense hormone biosynthesis.

              Phytoplasmas are insect-transmitted phytopathogenic bacteria that can alter plant morphology and the longevity and reproduction rates and behavior of their insect vectors. There are various examples of animal and plant parasites that alter the host phenotype to attract insect vectors, but it is unclear how these parasites accomplish this. We hypothesized that phytoplasmas produce effectors that modulate specific targets in their hosts leading to the changes in plant development and insect performance. Previously, we sequenced and mined the genome of Aster Yellows phytoplasma strain Witches' Broom (AY-WB) and identified 56 candidate effectors. Here, we report that the secreted AY-WB protein 11 (SAP11) effector modulates plant defense responses to the advantage of the AY-WB insect vector Macrosteles quadrilineatus. SAP11 binds and destabilizes Arabidopsis CINCINNATA (CIN)-related TEOSINTE BRANCHED1, CYCLOIDEA, PROLIFERATING CELL FACTORS 1 and 2 (TCP) transcription factors, which control plant development and promote the expression of lipoxygenase (LOX) genes involved in jasmonate (JA) synthesis. Both the Arabidopsis SAP11 lines and AY-WB-infected plants produce less JA on wounding. Furthermore, the AY-WB insect vector produces more offspring on AY-WB-infected plants, SAP11 transgenic lines, and plants impaired in CIN-TCP and JA synthesis. Thus, SAP11-mediated destabilization of CIN-TCPs leads to the down-regulation of LOX2 expression and JA synthesis and an increase in M. quadrilineatus progeny. Phytoplasmas are obligate inhabitants of their plant host and insect vectors, in which the latter transmits AY-WB to a diverse range of plant species. This finding demonstrates that pathogen effectors can reach beyond the pathogen-host interface to modulate a third organism in the biological interaction.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                23 October 2017
                2017
                : 8
                : 2041
                Affiliations
                [1] 1Department of Microbiology and Plant Pathology, University of California, Riverside , Riverside, CA, United States
                [2] 2Center for Plant Cell Biology, University of California, Riverside , Riverside, CA, United States
                [3] 3Citrus Research and Education Center, University of Florida , Lake Alfred, FL, United States
                [4] 4Department of Plant Pathology, University of California, Davis , Davis, CA, United States
                [5] 5Department of Chemical and Environmental Engineering, University of California, Riverside , Riverside, CA, United States
                [6] 6Department of Plant Pathology, University of Florida , Gainesville, FL, United States
                [7] 7Texas A&M University – Kingsville Citrus Center , Weslaco, TX, United States
                Author notes

                Edited by: Hua Lu, University of Maryland, Baltimore County, United States

                Reviewed by: Zonghua Wang, Fujian Agriculture and Forestry University, China; Vardis Ntoukakis, University of Warwick, United Kingdom

                *Correspondence: Wenbo Ma, wenbo.ma@ 123456ucr.edu

                This article was submitted to Plant Microbe Interactions, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2017.02041
                5776943
                29403441
                63dce498-d636-4bf9-83de-b615b38d8bb8
                Copyright © 2017 Pagliaccia, Shi, Pang, Hawara, Clark, Thapa, De Francesco, Liu, Tran, Bodaghi, Folimonova, Ancona, Mulchandani, Coaker, Wang, Vidalakis and Ma.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 11 July 2017
                : 06 October 2017
                Page count
                Figures: 6, Tables: 2, Equations: 0, References: 54, Pages: 13, Words: 0
                Funding
                Funded by: U.S. Department of Agriculture 10.13039/100000199
                Award ID: 15-8130-0494-CA
                Award ID: 2014-67021-21589
                Award ID: 2016-70016-24833
                Funded by: Citrus Research Board 10.13039/100008563
                Award ID: 5300-149
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                citrus greening disease,hlb,effectors,disease diagnosis,antibody-based detection,bacterial secreted proteins

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