Research Article: Novel Positive Regulatory Role for the SPL6 Transcription Factor in the N TIR-NB-LRR Receptor-Mediated Plant Innate Immunity

Date Published: March 14, 2013

Publisher: Public Library of Science

Author(s): Meenu S. Padmanabhan, Shisong Ma, Tessa M. Burch-Smith, Kirk Czymmek, Peter Huijser, Savithramma P. Dinesh-Kumar, Frederick M. Ausubel.


Following the recognition of pathogen-encoded effectors, plant TIR-NB-LRR immune receptors induce defense signaling by a largely unknown mechanism. We identify a novel and conserved role for the SQUAMOSA PROMOTER BINDING PROTEIN (SBP)-domain transcription factor SPL6 in enabling the activation of the defense transcriptome following its association with a nuclear-localized immune receptor. During an active immune response, the Nicotiana TIR-NB-LRR N immune receptor associates with NbSPL6 within distinct nuclear compartments. NbSPL6 is essential for the N-mediated resistance to Tobacco mosaic virus. Similarly, the presumed Arabidopsis ortholog AtSPL6 is required for the resistance mediated by the TIR-NB-LRR RPS4 against Pseudomonas syringae carrying the avrRps4 effector. Transcriptome analysis indicates that AtSPL6 positively regulates a subset of defense genes. A pathogen-activated nuclear-localized TIR-NB-LRR like N can therefore regulate defense genes through SPL6 in a mechanism analogous to the induction of MHC genes by mammalian immune receptors like CIITA and NLRC5.

Partial Text

Plants employ the Nucleotide Binding-Leucine Rich Repeat (NB-LRR) family of intracellular receptors to detect pathogens and initiate defense signaling [1], [2]. NB-LRRs have structural similarity with the mammalian NOD-like receptors (NLRs), but unlike NLRs that recognize conserved Pathogen Associated Molecular Patterns (PAMPs), each plant NB-LRR recognizes a unique pathogen-encoded effector protein. NB-LRR association with an effector and subsequent receptor activation leads to a number of cellular responses that includes massive transcriptional reprogramming [3]. Ultimately, these responses often culminate in a specialized form of programmed cell death (PCD) – the hypersensitive response (HR) that restricts pathogen to the infection site thereby protecting the rest of the plant from disease [4].

We have identified, for the first time, a novel conserved role for the SPL6 transcription factor in innate immunity. We provide evidence to show that it is a key nuclear partner that aids defense responses mediated by N and possibly RPS4 TIR-NB-LRR immune receptors. We show that SPL6 is required for N-mediated resistance to TMV in Nicotiana. N and SPL6 associate in planta, within subnuclear bodies only during an active immune response. SPL6 is also required in Arabidopsis for the induction of defense by the nuclear-localized TIR-NB-LRR RPS4 but not for defense mediated by plasma membrane localized RPM1 and RPS2. Preliminary gene regulation assay suggest that SPL6 is a positive regulator of defense. Thus, SPL6 plays a conserved role in the TIR-NB-LRR mediated immune response across different plant species. Based on our data, we present a model for N-mediated immune response activation that details pathogen recognition by N in the cytoplasm followed by its activation and subsequent regulation of defense genes through nuclear SPL6 activity (Figure 7).




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