Transcriptional reprogramming caused by the geminivirus Tomato yellow leaf curl virus in local or systemic infections in Nicotiana benthamiana

Abstract

Background Viruses have evolved to create a cellular environment permissive for viral replication in susceptible hosts. Possibly both enabling and resulting from these virus-triggered changes, infected hosts undergo a dramatic transcriptional reprogramming, the analysis of which can shed light on the molecular processes underlying the outcome of virus-host interactions. The study of the transcriptional changes triggered by the plant DNA viruses geminiviruses is potentially hampered by the low representation of infected cells in the total population, a situation that becomes extreme in those cases, like that of Tomato yellow leaf curl virus (TYLCV), in which the virus is restricted to phloem companion cells. Results In order to gain insight into how different the transcriptional landscapes of TYLCV-infected cells or whole tissues of TYLCV-infected plants might be, here we compare the transcriptional changes in leaf patches infected with TYLCV by agroinfiltration or in systemic leaves of TYLCV-infected plants in Nicotiana benthamiana . Our results show that, in agreement with previous works, infection by TYLCV induces a dramatic transcriptional reprogramming; the detected changes, however, are not equivalent in local and systemic infections, with a much larger number of genes differentially expressed locally, and some genes responding in an opposite manner. Interestingly, a transcriptional repression of the auxin signalling pathway and a transcriptional activation of the ethylene signalling pathway were detected in both local and systemically infected samples. A transcriptional activation of defence was also detectable in both cases. Comparison with the transcriptional changes induced by systemic infection by the geminivirus Tobacco curly shoot virus (TbSV) shows common subsets of up- and down-regulated genes similarly affected by both viral species, unveiling a common transcriptional repression of terpenoid biosynthesis, a process also suppressed by the geminivirus Tomato yellow leaf curl China virus. Conclusions Taken together, the results presented here not only offer insight into the transcriptional changes derived from the infection by TYLCV in N. benthamiana , but also demonstrate that the resolution provided by local and systemic infection approaches largely differs, highlighting the urge to come up with a better system to gain an accurate view of the molecular and physiological changes caused by the viral invasion. Electronic supplementary material The online version of this article (10.1186/s12864-019-5842-7) contains supplementary material, which is available to authorized users.

Insight into the Role of Epigenetic Processes in Abiotic and Biotic Stress Response in Wheat and Barley

“…The past decade has seen unprecedented progress in understanding the signaling pathways controlling the plant responses to stresses, which has been summarized in prior reviews [16][17][18]. Activation of these signaling pathways usually results in the dramatic transcriptional reprogramming to initiate a set of stress responses [19][20][21]. There is increasing evidence indicating that this transcriptional reprogramming and regulation of stress-responsive genes involves diverse epigenetic processes and elements, such as DNA methylation, histone modification, chromatin remodeling and non-coding RNAs [22][23][24].…”

The C4 Protein from Tomato Yellow Leaf Curl Virus Can Broadly Interact with Plant Receptor-Like Kinases

“…Mounting evidence suggests that PRRs might play a role also in plant-virus interactions. Although this has not been proven for geminiviruses yet, TYLCV infection can activate plant defense responses [28,29], and activation of PTI by flg22 treatment can trigger the release of C4 from the plasma membrane and its translocation to the chloroplast, suggesting that this viral protein is somehow associated with and responsive to the activation of the FLS2 receptor complex (Medina-Puche et al, unpublished). To date, however, NIK1 is the only RLK shown to have a prominent role in the geminivirus infection.…”

Plant DNA polymerases α and δ mediate replication of geminiviruses

“…Orthologs of Arabidopsis POLA1/2, POLD1/2, POLE1/2, and REV3 proteins in N. benthamiana were identified by BLAST (Supplementary Table 1 ). The proteins and coding genes used in this work were selected among the corresponding orthologs based on their gene expression in TYLCV-infected N. benthamiana samples ( 38 ; Supplementary Table 1 ).…”

“…Local and systemic viral infection assays were done as described in ref. 38 . In brief, Agrobacterium cells carrying the TYLCV-WT, TYLCV-C3mut, or BCTV infectious clones, or an empty vector (EV) as control, were liquid-cultured in LB with appropriate antibiotics overnight.…”