Tobacco TTG2 Quells Resistance to Pathogens by Sequestering NPR1 from Nuclear Localisation

Abstract

SummaryTRANSPARENT TESTA GLABRA (TTG) proteins that contain the WD40 protein interaction domain are implicated in many signalling pathways in plants. The salicylic acid (SA) signalling pathway regulates the resistance of plants to pathogens through defence responses involving pathogenesis-related (PR) gene transcription, activated by the NPR1 (nonexpresser of PR genes 1) protein, which contains WD40-binding domains. We report that tobacco (Nicotiana tabacum) NtTTG2 suppresses the resistance to viral and bacterial pathogens by repressing the nuclear localisation of NPR1 and SA/NPR1-regulated defence in plants. Prevention of NtTTG2 protein production by silencing of the NtTTG2 gene resulted in the enhancement of resistance and PR gene expression, but NtTTG2 overexpression or NtTTG2 protein overproduction caused the opposite effects. Concurrent NtTTG2 and NPR1 gene silencing or NtTTG2 silencing in the absence of SA accumulation compensated for the compromised defence as a result of the NPR1 single-gene silencing or the absence of SA. However, NtTTG2 did not interact with NPR1 but was able to modulate the subcellular localisation of the NPR1 protein. In the absence of NtTTG2 production NPR1 was found predominantly in the nucleus and the PR genes were expressed. By contrast, when NtTTG2 accumulated in transgenic plants, a large proportion of NPR1 was retained in the cytoplasm and the PR genes were not expressed. These results suggest that NtTTG2 represses SA/NPR1-regulated defence by sequestering NPR1 from the nucleus and the transcriptional activation of the defence-response genes.

Early Disruption of Maternal–Zygotic Interaction and Activation of Defense-Like Responses inArabidopsisInterspecific Crosses

“…It is possible that the induced NBS-LRR, including NPR1, may serve a regulatory role during seed development. NPR1 is known to interact with TTG2 in tobacco (Nicotiana tabacum; Li et al, 2012); perhaps in Arabidopsis it senses disrupting events in the cell and signals the maternal seed coat or endosperm to subvert development.…”

TTG2-regulated development is related to expression of putative AUXIN RESPONSE FACTOR genes in tobacco

“…TTGs are characterized by the presence of the WD40 motif [5–7], which refers to the conserved tryptophan (W) and aspartate (D) dipeptide and the length of approximately 40 amino acid residues in a protein sequence [8]. This motif is present as a series of repeats to form protein interaction domain in a variety of proteins [9–11], including all TTGs so far identified except for Arabidopsis thaliana AtTTG2, which is a WRKY transcription factor [12].…”

“…As the WD40 domain has multiple modes for recruiting different substrates, WD40-containing proteins can serve as interchangeable substrate receptors and interact with diverse types of proteins [11, 13]. Due to this characteristic, TTGs have the potential of regulating both development and defenses in plants [5, 7, 14, 15]. …”

“…The NtTTG1-ParA1 interaction was essential for the induction of cell death first in leaf trichomes and then in mesophyll cells [7]. NtTTG2 is an analog of NtTTG1 and both proteins share four WD40 repeats [5, 7, 19]. Recently we showed that NtTTG2 suppressed tobacco resistance to pathogens by indirectly modulating subcellular localization of the NPR1 protein [5], which is a transcriptional regulator of defense responses to pathogens [20–22].…”

CsTTG1 Encodes a WD-repeat Protein That Regulates Fruit Wart Formation in Cucumis sativus through Interaction with the Homeodomain-leucine Zipper I Protein Mict

“…In addition, the tobacco NtTTG1 protein, a trichome protein with a high degree of sequence identity to AtTTG1, plays an essential role in hypersensitive cell death signal transduction from leaf trichomes to mesophyll cells (Glover et al, 1998;Wang et al, 2009). However, NtTTG2, a paralog of NtTTG1, not only plays a role in suppressing SA/NPR1-regulated defense against pathogens but also regulates development by affecting the expression of ARF genes (Li et al, 2012;Zhu et al, 2013). These studies suggest that WDR proteins, which are structurally strongly conserved, have diverse functions in different species.…”