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Co-infection of Sweet Orange with Severe and Mild Strains of Citrus tristeza virus Is Overwhelmingly Dominated by the Severe Strain on Both the Transcriptional and Biological Levels.

ABSTRACT: Citrus tristeza is one of the most destructive citrus diseases and is caused by the phloem-restricted Closterovirus, Citrus tristeza virus. Mild strain CTV-B2 does not cause obvious symptoms on indicators whereas severe strain CTV-B6 causes symptoms, including stem pitting, cupping, yellowing, and stiffening of leaves, and vein corking. Our laboratory has previously characterized changes in transcription in sweet orange separately infected with CTV-B2 and CTV-B6. In the present study, transcriptome analysis of Citrus sinensis in response to double infection by CTV-B2 and CTV-B6 was carried out. Four hundred and eleven transcripts were up-regulated and 356 transcripts were down-regulated prior to the onset of symptoms. Repressed genes were overwhelmingly associated with photosynthesis, and carbon and nucleic acid metabolism. Expression of genes related to the glycolytic, oxidative pentose phosphate (OPP), tricarboxylic acid cycle (TCA) pathways, tetrapyrrole synthesis, redox homeostasis, nucleotide metabolism, protein synthesis and post translational protein modification and folding, and cell organization were all reduced. Ribosomal composition was also greatly altered in response to infection by CTV-B2/CTV-B6. Genes that were induced were related to cell wall structure, secondary and hormone metabolism, responses to biotic stress, regulation of transcription, signaling, and secondary metabolism. Transport systems dedicated to metal ions were especially disturbed and ZIPs (Zinc Transporter Precursors) showed different expression patterns in response to co-infection by CTV-B2/CTV-B6 and single infection by CTV-B2. Host plants experienced root decline that may have contributed to Zn, Fe, and other nutrient deficiencies. Though defense responses, such as, strengthening of the cell wall, alteration of hormone metabolism, secondary metabolites, and signaling pathways, were activated, these defense responses did not suppress the spread of the pathogens and the development of symptoms. The mild strain CTV-B2 did not provide a useful level of cross-protection to citrus against the severe strain CTV-B6.

SUBMITTER: Fu S

PROVIDER: S-EPMC5583216 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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Co-infection of Sweet Orange with Severe and Mild Strains of <i>Citrus tristeza virus</i> Is Overwhelmingly Dominated by the Severe Strain on Both the Transcriptional and Biological Levels.

Fu Shimin S Shao Jonathan J Zhou Changyong C Hartung John S JS

Frontiers in plant science 20170831

Citrus tristeza is one of the most destructive citrus diseases and is caused by the phloem-restricted Closterovirus, <i>Citrus tristeza virus</i>. Mild strain CTV-B2 does not cause obvious symptoms on indicators whereas severe strain CTV-B6 causes symptoms, including stem pitting, cupping, yellowing, and stiffening of leaves, and vein corking. Our laboratory has previously characterized changes in transcription in sweet orange separately infected with CTV-B2 and CTV-B6. In the present study, tra ...[more]

PMID: 28912786

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Project description:BackgroundCitrus worldwide is threatened by huanglongbing (HLB) and tristeza diseases caused by 'Candidatus Liberibacter asiaticus' (CaLas) and Citrus tristeza virus (CTV). Although the pathogens are members of the α-proteobacteria and Closteroviridae, respectively, both are restricted to phloem cells in infected citrus and are transmitted by insect vectors. The response of sweet orange to single infection by either of these two pathogens has been characterized previously by global gene expression analysis. But because of the ubiquity of these pathogens where the diseases occur, co-infection by both pathogens is very common and could lead to increased disease severity based on synergism. We therefore co-inoculated sweet orange trees with CaLas and either a mild or a severe strain of CTV, and measured changes of gene expression in host plants.ResultsIn plants infected with CaLas-B232, the overall alteration in gene expression was much greater in plants co-inoculated with the severe strain of CTV, B6, than when co-infected with the mild strain of CTV, B2. Plants co-infected with CaLas-B232 and either strain of CTV died but trees co-infected with CTV-B2 survived much longer than those co-infected with CTV-B6. Many important pathways were perturbed by both CTV-B2/CaLas-B232 and/or CTV-B6/CaLas-B232, but always more severely by CTV-B6/CaLas-B232. Genes related to cell wall modification and metal transport responded differently to infection by the pathogens in combination than by the same pathogens singly. The expressions of genes encoding phloem proteins and sucrose loading proteins were also differentially altered in response to CTV-B2 or CTV-B6 in combination with CaLas-B232, leading to different phloem environments in plants co-infected by CaLas and mild or severe CTV.ConclusionsMany host genes were expressed differently in response to dual infection as compared to single infections with the same pathogens. Interactions of the pathogens within the host may lead to a better or worse result for the host plant. CTV-B6 may exert a synergistic effect with CaLas-B232 in weakening the plant; on the other hand, the responses activated by the mild strain CTV-B2 may provide some beneficial effects against CaLas-B232 by increasing the defense response of the host.

Project description:Huanglongbing (HLB) and tristeza, are diseases of citrus caused by a member of the ?-proteobacteria, 'Candidatus Liberibacter asiaticus' (CaLas), and Citrus tristeza virus (CTV) respectively. HLB is a devastating disease, but CTV strains vary from very severe to very mild. Both CaLas and CTV are phloem-restricted. The CaLas-B232 strain and CTV-B6 cause a wide range of severe and similar symptoms. The mild strain CTV-B2 doesn't induce significant symptoms or damage to plants.Transcriptome profiles obtained through RNA-seq revealed 611, 404 and 285 differentially expressed transcripts (DETs) after infection with CaLas-B232, CTV-B6 and CTV-B2. These DETs were components of a wide range of pathways involved in circadian rhythm, cell wall modification and cell organization, as well as transcription factors, transport, hormone response and secondary metabolism, signaling and stress response. The number of transcripts that responded to both CTV-B6 and CaLas-B232 was much larger than the number of transcripts that responded to both strains of CTV or to both CTV-B2 and CaLas-B232. A total of 38 genes were assayed by RT-qPCR and the correlation coefficients between Gfold and RT-qPCR were 0.82, 0.69, 0.81 for sweet orange plants infected with CTV-B2, CTV-B6 and CaLas-B232, respectively.The number and composition of DETs reflected the complexity of symptoms caused by the pathogens in established infections, although the leaf tissues sampled were asymptomatic. There were greater similarities between the sweet orange in response to CTV-B6 and CaLas-B232 than between the two CTV strains, reflecting the similar physiological changes caused by both CTV-B6 and CaLas-B232. The circadian rhythm system of plants was perturbed by all three pathogens, especially by CTV-B6, and the ion balance was also disrupted by all three pathogens, especially by CaLas-B232. Defense responses related to cell wall modification, transcriptional regulation, hormones, secondary metabolites, kinases and stress were activated by all three pathogens but with different patterns. The transcriptome profiles of Citrus sinensis identified host genes whose expression is affected by the presence of a pathogen in the phloem without producing symptoms (CTV-B2), and host genes whose expression leads to induction of symptoms in the plant (CTV-B6, CaLas-B232).

Project description:The presence of Citrus tristeza virus (CTV) has previously been reported in citrus growing regions of Turkey. All serologically and biologically characterized isolates including Iğdır, which was the first identified CTV isolates from Turkey, were considered mild isolates. In this study, molecular characteristics of the Iğdır isolate were determined by different methods. Analysis of the Iğdır isolate by western blot and BD-RT-PCR assays showed the presence of MCA13 epitope, predominantly found in severe isolates, in the Iğdır isolate revealing that it contains a severe component. For further characterization, the coat protein (CP) and the RNA-dependent RNA polymerase (RdRp) genes representing the 3' and 5' half of CTV genome, respectively, were amplified from dsRNA by RT-PCR. Both genes were cloned separately and two clones for each gene were sequenced. Comparisons of nucleotide and deduced amino acid sequences showed that while two CP gene sequences were identical, two RdRp clones showed only 90% and 91% sequence identity in their nucleotide and amino acid sequences, respectively, suggesting a mixed infection with different strains. Phylogenetic analyses of the CP and RdRp genes of Iğdır isolate with previously characterized CTV isolates from different citrus growing regions showed that the CP gene was clustered with NZRB-TH30, a resistance breaking isolate from New Zealand, clearly showing the presence of severe component. Furthermore, two different clones of the RdRp gene were clustered separately with different CTV isolates with a diverse biological activity. While the RdRp-1 was clustered with T30 and T385, two well-characterized mild isolates from Florida and Spain, respectively, the RdRp-2 was most closely related to NZRB-G90 and NZRB-TH30, two well-characterized resistance breaking and stem pitting (SP) isolates from New Zealand confirming the mixed infection. These results clearly demonstrated that the Iğdır isolate, which was previously described as biologically a mild isolate, actually contains a mixture of mild and severe strains.

Project description:Citrus tristeza virus (CTV, family Closteroviridae) is an economically important pathogen of citrus. CTV resides in the phloem of the infected plants and induces a range of disease phenotypes, including stem pitting and quick decline as well as a number of other deleterious syndromes. To uncover the biological processes underlying the poorly understood damaging symptoms of CTV, we profiled the transcriptome of sweet orange (Citrus sinensis) phloem-rich bark tissues of non-infected, mock-inoculated trees and trees singly infected with two distinct variants of CTV, T36 or T68-1. The T36 and T68-1 variants accumulated in the infected plants at similar titers. With that, young trees infected with T68-1 were markedly repressed in growth, while the growth rate of the trees infected with T36 was comparable to the mock-inoculated trees. Only a small number of differentially expressed genes (DEGs) were identified in the nearly asymptomatic T36-infected trees, whereas almost fourfold the number of DEGs were identified with the growth-restricting T68-1 infection. DEGs were validated using quantitative reverse transcription-PCR. While T36 did not induce many noteworthy changes, T68-1 altered the expression of numerous host mRNAs encoding proteins within significant biological pathways, including immunity and stress response proteins, papain-like cysteine proteases (PLCPs), cell-wall modifying enzymes, vascular development proteins and others. The transcriptomic alterations in the T68-1-infected trees, in particular, the strong and persistent increase in the expression levels of PLCPs, appear to contribute to the observed stem growth repression. On the other hand, analysis of the viral small interfering RNAs revealed that the host RNA silencing-based response to the infection by T36 and that by T68-1 was comparable, and thus, the induction of this antiviral mechanism may not contribute to the difference in the observed symptoms. The DEGs identified in this study promote our understanding of the underlying mechanisms of the yet unexplained growth repression induced by severe CTV isolates in sweet orange trees.

Dataset Information

Co-infection of Sweet Orange with Severe and Mild Strains of Citrus tristeza virus Is Overwhelmingly Dominated by the Severe Strain on Both the Transcriptional and Biological Levels.

Publications

Co-infection of Sweet Orange with Severe and Mild Strains of <i>Citrus tristeza virus</i> Is Overwhelmingly Dominated by the Severe Strain on Both the Transcriptional and Biological Levels.

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