Abstract
BackgroundThe Beet curly top virus C4 oncoprotein is a pathogenic determinant capable of inducing extensive developmental abnormalities. No studies to date have investigated how the transcriptional profiles differ between plants expressing or not expressing the C4 oncoprotein.ResultsWe investigated early transcriptional changes in Arabidopsis associated with expression of the Beet curly top virus C4 protein that represent initial events in pathogenesis via a comparative transcriptional analysis of mRNAs and small RNAs. We identified 48 and 94 differentially expressed genes at 6- and 12-h post-induction versus control plants. These early time points were selected to focus on direct regulatory effects of C4 expression. Since previous evidence suggested that the C4 protein regulated the brassinosteroid (BR)-signaling pathway, differentially expressed genes could be divided into two groups: those responsive to alterations in the BR-signaling pathway and those uniquely responsive to C4. Early transcriptional changes that disrupted hormone homeostasis, 18 and 19 differentially expressed genes at both 6- and 12-hpi, respectively, were responsive to C4-induced regulation of the BR-signaling pathway. Other C4-induced differentially expressed genes appeared independent of the BR-signaling pathway at 12-hpi, including changes that could alter cell development (4 genes), cell wall homeostasis (5 genes), redox homeostasis (11 genes) and lipid transport (4 genes). Minimal effects were observed on expression of small RNAs.ConclusionThis work identifies initial events in genetic regulation induced by a geminivirus C4 oncoprotein. We provide evidence suggesting the C4 protein regulates multiple regulatory pathways and provides valuable insights into the role of the C4 protein in regulating initial events in pathogenesis.
Highlights
The Beet curly top virus C4 oncoprotein is a pathogenic determinant capable of inducing extensive developmental abnormalities
Transcriptional analysis design To begin understanding gene expression changes induced by the Beet curly top virus (BCTV) C4 protein, we performed RNA-seq analysis on RNA extracted from seedlings of Arabidopsis line Inducible promoter C4–28 (IPC4–28) expressing or not expressing the C4 protein at 6- and 12-h post-induction or post-mock induction (Fig. 1a)
Initial symptoms of an abnormal development phenotype occurred in IPC4–28 seedlings geminated in liquid media in the presence of 10 μM ß-est as early as 2-days postinduction [6]
Summary
The Beet curly top virus C4 oncoprotein is a pathogenic determinant capable of inducing extensive developmental abnormalities. Plant virus proteins are adept at co-opting cellular machinery and metabolic pathways to alter the host physiology to benefit the virus life cycle [1]. One such virus protein is the small C4 protein (~ 10 kDa) (AC4 in geminiviruses with bipartite genomes) encoded by some members of the Geminiviridae [2]. The oncogenic nature of C4/AC4 proteins has been shown to, at least in part, result from their ability to interfere with the function of shaggy-like protein kinases [8–10]. In Arabidopsis, seven shaggy-like protein kinases (AtSKs) of the ten-member multigene family have been implicated in negatively regulating the brassinosteroid (BR) signaling pathway (BRSP) [11–14]. AtSKs have been implicated in crosstalk between the BRSP and other hormone signaling pathways, biotic and abiotic stress responses, root and stomata development, flower development, xylem differentiation, phloem development, and patterntriggered immunity [13, 14, 16–19]
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