Functional requirement of the Arabidopsis importin‐α nuclear transport receptor family in autoimmunity mediated by the NLR protein SNC1

Abstract

IMPORTIN-a3/MOS6 (MODIFIER OF SNC1, 6) is one of nine importin-a isoforms in Arabidopsis that recruit nuclear localization signal-containing cargo proteins to the nuclear import machinery. IMP-a3/MOS6 is required genetically for full autoimmunity of the nucleotide-binding leucine-rich repeat immune receptor mutant snc1 (suppressor of npr1-1, constitutive 1) and MOS6 also contributes to basal disease resistance. Here, we investigated the contribution of the other importin-a genes to both types of immune responses, and we analyzed potential interactions of all importin-a isoforms with SNC1. By using reverse-genetic analyses in Arabidopsis and proteinÀprotein interaction assays in Nicotiana benthamiana, we provide evidence that among the nine a-importins in Arabidopsis, IMP-a3/MOS6 is the main nuclear transport receptor of SNC1, and that IMP-a3/MOS6 is required selectively for autoimmunity of snc1 and basal resistance to mildly virulent Pseudomonas syringae in Arabidopsis.

Nucleocytoplasmic Communication in Healthy and Diseased Plant Tissues

“…Alternatively, a largely redundant repertoire of import adaptors could present a strategy to effectively buffer and protect vital signaling pathways. Indeed, the loss of a single importin -α gene has no obvious morphological consequences in Arabidopsis , while higher order mutants of IMP-α1 / 2 / 3 display a stunted growth morphology ( Chen et al, 2020 ; Lüdke et al, 2021 ). Chen et al (2020) also reported that triple mutant plants of IMP-α1 / 2 / 3 flower early and accordingly, the authors identified the three α-importins as adaptors that import LIKE HETEROCHROMATIN PROTEIN1 (LHP1; Table 1 ).…”

“…Besides its partially redundant role with IMP-α1 and -α2 in plant development, a selective role of IMP-α3 has been described in immunity ( Lüdke et al, 2021 ). Based on the genetic requirement for the autoimmune phenotype of suppressor of npr1−1, constitutive1 ( snc1 ), a gain-of-function mutant of a nucleotide−binding leucine−rich repeat (NLR) immune receptor, IMP-α3 was named MODIFIER OF SNC1, 6 ( MOS6 ; Palma et al, 2005 ).…”

“…NLRs usually detect the presence or actions of immune suppressive pathogen effector molecules, but a nuclear function of SNC1 in the transcriptional regulation of defense genes and miRNAs has also been described ( Zhu et al, 2010 ; Xu et al, 2014 ; Cai et al, 2018 ). Recent work suggests that MOS6 is the main import adapter for SNC1 ( Table 1 ; Lüdke et al, 2021 ). This is consistent with the finding that the loss of MOS6 , but not of any other α-importin , partially suppresses the autoimmune phenotype of snc1 ( Palma et al, 2005 ; Lüdke et al, 2021 ).…”

“…Recent work suggests that MOS6 is the main import adapter for SNC1 ( Table 1 ; Lüdke et al, 2021 ). This is consistent with the finding that the loss of MOS6 , but not of any other α-importin , partially suppresses the autoimmune phenotype of snc1 ( Palma et al, 2005 ; Lüdke et al, 2021 ). In addition, the genetic requirement of MOS6 but not of other α-importins for basal resistance, together with the finding that MOS6 but not its closest homolog IMP-α6 interacts with the truncated NLR TIR-NB13 (TN13), further suggests a specialization of MOS6/IMP-α3 in immunity-related cargo transport ( Roth et al, 2017 ).…”

“…For instance, cargo selectivity has been described for MINIYO (IYO), which interacts with IMP-α4, but not with IMP-α3 or IMP-α6 in transient assays and mass spectrometry analysis ( Table 1 ; Muñoz et al, 2017 ; Contreras et al, 2019 ). MINIYO plays a vital role in stem cell differentiation, but no morphological phenotype has been described for imp-α4 mutant plants, suggesting additional import routes for MINIYO ( Helizon et al, 2018 ; Lüdke et al, 2021 ). On the other hand, loss of IMP-α4 but not of other α-importins affects transformation of Arabidopsis roots by the plant pathogen Agrobacterium tumefaciens , although IMP-α4 and several other importin-α transport adapters are capable to interact with Agrobacterium effector proteins that mediate nuclear import of the T-DNA/protein complex (T-complex; Bhattacharjee et al, 2008 ).…”