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Transcriptomic analyses reveal physiological changes in sweet orange roots affected by citrus blight.

ABSTRACT: BACKGROUND:Citrus blight is a very important progressive decline disease of commercial citrus. The etiology is unknown, although the disease can be transmitted by root grafts, suggesting a viral etiology. Diagnosis is made by demonstrating physical blockage of xylem cells that prevents the movement of water. This test was used to identify symptomatic trees from four commercial groves in Florida. Total RNA extracts of phloem-enriched scaffold root tissues were prepared from seven trees that failed to take up water and from one healthy tree. These RNA extracts were used for transcriptomic analyses using paired end RNA-Seq from an Illumina 2500 system. The expression of transcripts annotated as polyprotein of citrus endogenous pararetrovirus were estimated by both RT-qPCR and RNA-Seq. RESULTS:Transcripts from seven RNA-Seq libraries from trees affected by citrus blight were compared to a control tree. 129-148 million RNA fragments (two paired-end reads/fragment) were generated per library and were mapped to the sweet orange reference genome. In response to citrus blight stress, genes encoding aquaporins, proteins with water channel activity and several cellulose synthase genes were down-regulated, whereas genes involved in lignin and glucosinolate biosynthesis were up-regulated. Transcripts encoding proteins in pathways of carbohydrate metabolism, nucleotide synthesis, signaling, hormone metabolism, secondary metabolism, transport, and biotic stress pathways were overwhelmingly down regulated in all libraries. CONCLUSION:Reduced water intake and xylem plugging were observed in the trees tested and the changes in their transcriptome were analyzed. Plants adapted to reduced water flow by regulating primary and secondary metabolism, nuclear transport and hormone associated pathways. The patterns of energy generation, transcription, translation and protein degradation were consistent with irreversible decline. The down regulation of cellulose synthase transcripts and up regulation of transcripts related to lignin production likely lead to an imbalance in the pathways leading to wood formation, and may lead to the blockage of the xylem vessels seen as the cardinal symptom of citrus blight. Transcripts of a pararetrovirus were elevated in the transcriptome of roots used in this study.

SUBMITTER: Fu S

PROVIDER: S-EPMC6907255 | biostudies-literature | 2019 Dec

REPOSITORIES: biostudies-literature

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Project description:To evaluate the transcriptome response of roots towards Hoagland solution of two-year-old healthy (C) and HLB-affected (T) sweet orange (Citrus sinensis L.) cultivar Midsweet grafted on Kuharskei Carrizo rootstock at three different time points; D1 (at the start of the experiment), D2 (After 3 days of Hoagland solution), D3 (After nine days of Hoagland solution), were performed using RNA sequencing analysis. A total of 9, 19, and 2324 DEGs were expressed in HLB-affected and healthy trees feeder roots on D1, D2, and D3, respectively. Due to a small number of DEGs in HLB-affected and healthy trees roots on D1 and D2, enrichment analysis could not be performed. At D3, Gene Ontology (GO) enrichment analysis was performed using upregulated and downregulated DEGs in HLB-affected roots compared to healthy roots. For the upregulated DEGs in HLB-affected roots, the most enriched biological GO categories were related to transport, cellular amino acid metabolic process, oxoacid metabolic process, organic acid metabolic processes, phenylpropanoid biosynthesis process, response to carbohydrate stimulus, ethylene and the jasmonic acid-mediated signaling pathway, and regulation of plant hormone. The biological GO categories based on the number of DEGs associated with downregulated DEGs were the developmental process, phosphate metabolic process, protein modification process, defense response, growth, cell cycle, cell death, and ABA-mediated signaling pathway. The results of this study strongly suggest; although, the reduced biomass limits the nutrient uptake capacity in the plants as a whole, so in order to compensate for reduced root to shoot ratio the existing root undergo anatomical and transcriptomic changes to improve nutrient uptake efficiency to meet the nutrient demand of shoot systems. It is likely that higher inputs of energy in nutrient uptake possibly results in reducing the root longevity of HLB-affected trees. Good nutrition management practices are critical for the survival of HLB-affected trees as the availability and uptake of nutrients allow HLB-affected trees in response to abiotic and biotic stress.

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.

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Transcriptomic analyses reveal physiological changes in sweet orange roots affected by citrus blight.

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