Tobacco mosaic virus-directed reprogramming of auxin/indole acetic acid protein transcriptional responses enhances virus phloem loading.
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/IAA-interacting 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.
Department of Cell Biology and Molecular Genetics, University of Maryland, College Park, MD 20742;
Tamara D
TD
Collum
Department of Cell Biology and Molecular Genetics, University of Maryland, College Park, MD 20742;
Meenu S
MS
Padmanabhan
Institute for Bioscience and Biotechnology Research, University of Maryland, College Park, MD 20742;
Yi-Cheng
YC
Hsieh
Institute for Bioscience and Biotechnology Research, University of Maryland, College Park, MD 20742; Department of Plant Science and Landscape Architecture, University of Maryland, College Park, MD 20742 jculver@umd.edu.
James N
JN
Culver
D018506:Gene Expression Regulation, Plant / Q000502:physiology; D007210:Indoleacetic Acids / Q000378:metabolism*; D052585:Phloem / Q000378:metabolism* / Q000821:virology*; D014026:Nicotiana / Q000378:metabolism / Q000821:virology*; D014027:Tobacco Mosaic Virus / Q000502:physiology*; D015533:Transcriptional Activation / Q000502:physiology; D019562:Viral Load / Q000502:physiology*; D053586:Virus Internalization
D007210:Indoleacetic Acids; C030737:indoleacetic acid
age-related resistance; pathogen defense; plant hormone signaling; plasmodesmata gating; virus movement