Transgenic Expression of the Dicotyledonous Pattern Recognition Receptor EFR in Rice Leads to Ligand-Dependent Activation of Defense Responses

Abstract

Plant plasma membrane localized pattern recognition receptors (PRRs) detect extracellular pathogen-associated molecules. PRRs such as Arabidopsis EFR and rice XA21 are taxonomically restricted and are absent from most plant genomes. Here we show that rice plants expressing EFR or the chimeric receptor EFR::XA21, containing the EFR ectodomain and the XA21 intracellular domain, sense both Escherichia coli- and Xanthomonas oryzae pv. oryzae (Xoo)-derived elf18 peptides at sub-nanomolar concentrations. Treatment of EFR and EFR::XA21 rice leaf tissue with elf18 leads to MAP kinase activation, reactive oxygen production and defense gene expression. Although expression of EFR does not lead to robust enhanced resistance to fully virulent Xoo isolates, it does lead to quantitatively enhanced resistance to weakly virulent Xoo isolates. EFR interacts with OsSERK2 and the XA21 binding protein 24 (XB24), two key components of the rice XA21-mediated immune response. Rice-EFR plants silenced for OsSERK2, or overexpressing rice XB24 are compromised in elf18-induced reactive oxygen production and defense gene expression indicating that these proteins are also important for EFR-mediated signaling in transgenic rice. Taken together, our results demonstrate the potential feasibility of enhancing disease resistance in rice and possibly other monocotyledonous crop species by expression of dicotyledonous PRRs. Our results also suggest that Arabidopsis EFR utilizes at least a subset of the known endogenous rice XA21 signaling components.

Receptor Kinases in Plant-Pathogen Interactions: More Than Pattern Recognition

“…PLL4 and PLL5 are close homologs of rice XANTHOMONAS RESISTANCE21 (XA21) BINDING PROTEIN15 (XB15), which was previously shown to dephosphorylate XA21 in vitro and negatively affect XA21-mediated immunity to the bacterium Xanthomonas oryzae pv oryzae (Park et al, 2008). These results also indicate conserved regulatory mechanisms for Xa21 and EFR, a notion supported by XA21-EFR domain swapping experiments (Holton et al, 2015;Schwessinger et al, 2015).…”

“…This feature not only helps the identification of PRRs, but also allows deployment of disease resistance by cross-species/genus transfer of PRR-coding genes. Indeed, transgenic overexpression of EFR confers elf18 sensitivity and elevated resistance to cereal bacterial pathogens in rice and wheat (Triticum aestivum) plants, which do not encode EFR (Schwessinger et al, 2015;Schoonbeek et al, 2015).…”

uORF-mediated translation allows engineered plant disease resistance without fitness costs

“…The first line of active defence in plants involves recognition of microbial/damage-associated molecular patterns (M/DAMPs) by host pattern-recognizing receptors (PRRs) in pattern-triggered immunity (PTI) 5 . Ectopic expression of PRRs for MAMPs 6, 7 and the DAMP signal eATP 8 , as well as in vivo release of the DAMP molecules, oligogalacturonides 9 , have all been shown to enhance resistance in transgenic plants. Besides PRR-mediated basal resistance, plant genomes encode hundreds of intracellular nucleotide-binding and leucine-rich repeat (NB-LRR) immune receptors (also known as “R proteins”) to detect the presence of pathogen effectors delivered inside plant cells 10 .…”

Pattern Recognition Receptors—Versatile Genetic Tools for Engineering Broad-Spectrum Disease Resistance in Crops

“…One feature makes PRRs particularly attractive targets for genetic engineering of plant immunity: signaling networks downstream of PRRs are sufficiently conserved (Figure 1), not only within but also between plant families and even between monocot and dicot classes, to facilitate functional transfer of PRRs between them [53][54][55]. Apparently, PRRs can plug into the existing signaling network by engaging with conserved interacting signaling partners (e.g., SOBIR, BAK1 or CERK1) (Figure 2) [54,55].…”

“…Apparently, PRRs can plug into the existing signaling network by engaging with conserved interacting signaling partners (e.g., SOBIR, BAK1 or CERK1) (Figure 2) [54,55]. Because PRRs as the ligand binding components of PTI receptor complexes determine the epitope specificity, introducing a PRR with a novel epitope specificity can confer recognition of this epitope onto previously insensitive plant species.…”