Tobacco mosaic virus-directed reprogramming of auxin/indole acetic acid protein transcriptional responses enhances virus phloem loading

Abstract

Vascular phloem loading has long been recognized as an essential step in the establishment of a systemic virus infection. In this study, an interaction between the replication protein of tobacco mosaic virus (TMV) and phloem-specific auxin/indole acetic acid (Aux/IAA) transcriptional regulators was found to modulate virus phloem loading in an age-dependent manner. Promoter expression studies show that in mature tissues TMV 126/183-kDa-interacting Aux/IAAs predominantly express and accumulate within the nuclei of phloem companion cells (CCs). Furthermore, CC Aux/IAA nuclear localization is disrupted upon infection with an interacting virus. In situ analysis of virus spread shows that the inability to disrupt Aux/IAA CC nuclear localization correlates with a reduced ability to load into the vascular tissue. Subsequent systemic movement assays also demonstrate that a virus capable of disrupting Aux/IAA localization is significantly more competitive at moving out of older plant tissues than a noninteracting virus. Similarly, CC expression and overaccumulation of a degradation-resistant Aux/IAA-interacting protein was found to inhibit TMV accumulation and phloem loading selectively in flowering plants. Transcriptional expression studies demonstrate a role for Aux/IAAinteracting proteins in the regulation of salicylic and jasmonic acid host defense responses as well as virus-specific movement factors, including pectin methylesterase, that are involved in regulating plasmodesmata size-exclusion limits and promoting virus cell-to-cell movement. Combined, these findings indicate that TMV directs the reprogramming of auxin-regulated gene expression within the vascular phloem of mature tissues as a means to enhance phloem loading and systemic spread.pathogen defense | plant hormone signaling | virus movement | plasmodesmata gating | age-related resistance

Potato Mop-Top Virus Co-Opts the Stress Sensor HIPP26 for Long-Distance Movement

“…They suggest 440 that nuclear association of plant RNA virus components can manipulate transcriptional 441 regulation and re-programme gene expression in vascular tissue and that this may be a more 442 general strategy used by plant viruses to facilitate long-distance movement than previously 443 supposed (Solovyev and Savenkov, 2014;Collum et al, 2016 NbHIPP26 would result in increased spread of infection and not inhibition as we observed.…”

“…The eukaryotic cell nucleolus contains the factors needed for its main function in ribosome 422 subunit production, and this is where ribosomal RNA transcription, processing, and and spread in the phloem of older leaves (Collum et al, 2016).…”

Massive up‐regulation of LBD transcription factors and EXPANSINs highlights the regulatory programs of rhizomania disease

“…Previous studies have reported that plant viruses can hijack the auxin signalling pathway to promote virus infection and virus movement in the host plants (Collum et al., ; Jin et al., ). The capsid protein of Rice dwarf virus (RDV) interferes with auxin signalling by binding to the rice AUX/IAA protein OsIAA10, thereby protecting it from degradation by the 26S proteasome and resulting in typical RDV symptoms in infected plants (Jin et al., ).…”

“…These transcriptional repressors have been suggested to regulate genes involved in phloem loading. TMV infection inhibits the nuclear localization of AUX/IAA proteins, resulting in the transcriptional reprogramming of mature vascular tissue, which is correlated with enhanced TMV spread in the phloem of older leaves (Collum et al., ). Taken together, these data are consistent with our findings showing that BNYVV P25 interacts with BvAUX28, presumably inactivating its function as a transcriptional repressor through the disruption of its nuclear localization.…”

Modulation of host plant immunity by Tobamovirus proteins

“…The TMV replicase complex also interacts with a specific auxin/indole acetic acid (Aux/IAA) host transcriptional regulator. This interaction disrupts the control of host genes implicated in virus movement, plasmodesmata gating and defence in the companion cells, enhancing TMV phloem loading (Padmanabhan et al, 2008;Collum et al, 2016).…”