Tamara D. Collum, Meenu S. Padmanabhan, Yi-Cheng Hsieh, and James N. Culver

Significance

For plant viruses a successful infection correlates with the ability to access the vascular phloem and move systemically into distal tissues. However, how viruses gain access to and usurp vascular tissues is poorly understood. Here we show how tobacco mosaic virus (TMV) enhances its access to the phloem of mature plant tissues through the targeted disruption of auxin/indole acetic acid (Aux/IAA) transcriptional regulators that control expression of host genes involved in virus cell-to-cell movement, plasmodesmata gating, and defense. TMV’s ability to disrupt Aux/IAA function successfully confers a significant advantage in the systemic spread of this virus, allowing it to outcompete nondisrupting viruses. In summary, TMV interacts with Aux/IAA proteins to reprogram the vascular phloem, making it more conducive to systemic movement.

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/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.

See: http://www.pnas.org/content/113/19/E2740.abstract.html?etoc

PNAS May 10 2016; vol. 113; no.19: E2740–E2749

Fig. 1.

Histochemical analysis of pIAA26::GUS, pIAA27::GUS, and pIAA18::GUS expression in A. thaliana Shahdara leaves, petioles, and stems. (A) GUS expression in 7-wk-old leaves after staining overnight. (Scale bars, 2 mm.) (B) Petiole cross-sections. (Scale bars, 200 μm.) (C) Stem cross-sections. (Scale bars, 100 μm.)