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

Authors: SHIMIN, FU - Southwest University; Shao, Jonathan; ZHAO, CHANGYONG - Southwest University; Hartung, John

Submitted to: Frontiers in Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/31/2017
Publication Date: 8/31/2017
Citation: Shimin, F., Shao, J.Y., Zhao, C., Hartung, J.S. 2017. 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. Frontiers in Plant Science. https://doi.org/10.3389/fpls.2017.01419.
DOI: https://doi.org/10.3389/fpls.2017.01419

Interpretive Summary: Citrus tristeza nearly destroyed the citrus industry in the first half of the 20th century remains one of the most destructive of all citrus diseases. Tristeza and is caused by any of a group of viruses named after the disease. Disease symptoms range from none at all to rapid plant death and all variations between these extremes. These differences in symptoms are due to differences in each virus strain, but in nature several strains of the virus can infect orange trees at the same time. Strain CTV-B2 does not cause obvious symptoms but strain CTV-B6 causes symptoms, including stem pitting, cupping, yellowing and stiffening of leaves, and vein corking. Little is known about the mechanisms used by the sweet orange tree to respond to virus infection. We have previously characterized the response of sweet orange to each of these viruses in isolation. In the present study, we studied the response of sweet orange to simultaneous infection by CTV-B2 and CTV-B6 was carried out. The expression of about 20,000 genes was analyzed, and about 750 showed dramatic differences in response to infection. These genes caused dramatic reduction in photosynthesis, and thus production of sugar, in response to a shortage of iron and zinc caused by infection by CTV-B2/CTV-B6. Perhaps ironically, although production of sugar was reduced in the leaves, so was the ability of the plant to move it to where it needed to go. Leaves became stiff and distorted due to thickened cell walls and accumulation of sugars. Interestingly, although CTVB2 causes no symptoms and CTV-B6 causes severe symptoms, there was no 'compromise' in the symptoms observed in the double infected trees. The symptoms were very severe, as though CTV-B2 was not present at all. Although various genes related to defense responses were strongly activated, these defense responses did not prevent 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. Our results will be of interest to other researchers working with citrus diseases.

Technical 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. 411 transcripts were up-regulated and 356 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.