TALE‐carrying bacterial pathogens trap host nuclear import receptors for facilitation of infection of rice

Abstract

Summary Many plant‐pathogenic Xanthomonas rely on the secretion of virulence transcription activator‐like effector (TALE) proteins into plant cells to activate plant susceptibility genes to cause disease. The process is dependent on the binding of TALEs to specific elements of host target gene promoters in the plant nucleus. However, it is unclear how TALEs, after injection into host cells, are transferred from the plant cytoplasm into the plant nucleus, which is the key step of successful pathogen infection. Here, we show that the host plant cytoplasm/nuclear shuttle proteins OsImpα1a and OsImpα1b are key components for infection by the TALE‐carrying bacterial pathogens Xanthomonas oryzae pv. oryzae ( Xoo ) and Xanthomonas oryzae pv. oryzicola ( Xoc ), the causal agents of bacterial leaf blight and bacterial leaf streak, respectively, in rice. Direct interaction between the second nuclear localization signal of TALEs of Xoo or Xoc and OsImpα1a or OsImpα1b is required for the transportation of TALEs into the nucleus. Conversely, suppression of the expression of OsImp α 1a and OsImp α 1b genes attenuates the shuttling of TALEs from the cytoplasm into the nucleus and the induction of susceptibility genes, thus improving the broad‐spectrum disease resistance of rice to Xoo and Xoc . These results provide an applicable strategy for the improvement of resistance to TALE‐carrying pathogens in rice by moderate suppression of the expression of plant nuclear import receptor proteins.

Importin-αs are required for the nuclear localization and function of the Plasmopara viticola effector PvAVH53

“…oryzae (Xoo) and Xanthomonas oryzae pv. oryzicola (Xoc) target OsImpα1a and OsImpα1b to facilitate infection 46 . However, multiple imp-α homologs/isoforms exist in plants 12 , and these may associate with distinct groups of cargo proteins.…”

OsWRKY62 and OsWRKY76 interact with Importin α1s for Negative Regulation of Defensive Responses in Nucleus

“…oryzicola (Xoc), the causal agents of bacterial leaf blight and leaf streak, respectively (Hui et al, 2019). Nuclear localization of TALEs increases host susceptibility and modulates host gene expression (Hui et al, 2019;Szurek et al, 2001). The results suggest that nuclear transportation of proteins play a signi cant role in response to biotic and abiotic challenges.…”

“…Silencing importin αs expression in N. benthamiana or Vitis vinifera leads to increased susceptibility to pathogens(Chen et al, 2021), suggesting a positive role of the importin αs against the pathogens tested. Importin αs also mediate transportation of bacterial TALEs to the host nucleus for regulatory functions(Hui et al, 2019;Szurek et al, 2001). Nuclear import of Xoo or Xoc TALEs increases rice susceptibility to the pathogen, and silencing OsIMα1a and OsIMα1b enhances resistance to Xoc and suppresses the expression of rice susceptibility gene(Hui et al, 2019).…”

OsPGIP1-Mediated Resistance to Bacterial Leaf Streak in Rice is Beyond Responsive to the Polygalacturonase of Xanthomonas oryzae pv. oryzicola

“…For example, the overexpression of the broad-spectrum disease resistance gene OsMPK6 , an indole-3-acetic acid amido synthetase ( GH3–2 ), a nucleotide binding and leucine-rich repeat domain (NLR) protein heteropairs RGA4/RGA5 , OsPGIP4 , OsMAPK10.2 , the small heat shock protein gene OsHSP18.0-CI and the phytosulfokine receptor 1 ( OsPSKR1 ) enhanced the resistance of rice to BLS (Shen et al 2010; Fu et al 2011; Feng et al 2016; Hutin et al 2016; Ma et al 2017; Ju et al 2017; Yang et al 2019). The repression of OsWRKY45–1 , a receptor-like cytoplasmic kinase ( NRRB ), OsImpα1a and OsImpα1b also enhanced the resistance of rice to Xoc (Tao et al 2009; Guo et al 2014; Hui et al 2019).…”