Ectopic activation of the rice NLR heteropair RGA4/RGA5 confers resistance to bacterial blight and bacterial leaf streak diseases

Abstract

Bacterial blight (BB) and bacterial leaf streak (BLS) are important diseases in Oryza sativa caused by Xanthomonas oryzae pv. oryzae (Xoo) and Xanthomonas oryzae pv. oryzicola (Xoc), respectively. In both bacteria, transcription activator-like (TAL) effectors are major virulence determinants that act by transactivating host genes downstream of effector-binding elements (EBEs) bound in a sequence-specific manner. Resistance to Xoo is mostly related to the action of TAL effectors, either by polymorphisms that prevent the induction of susceptibility (S) genes or by executor (R) genes with EBEs embedded in their promoter, and that induce cell death and resistance. For Xoc, no resistance sources are known in rice. Here, we investigated whether the recognition of effectors by nucleotide binding and leucine-rich repeat domain immune receptors (NLRs), the most widespread resistance mechanism in plants, is also able to stop BB and BLS. In one instance, transgenic rice lines harboring the AVR1-CO39 effector gene from the rice blast fungus Magnaporthe oryzae, under the control of an inducible promoter, were challenged with transgenic Xoo and Xoc strains carrying a TAL effector designed to transactivate the inducible promoter. This induced AVR1-CO39 expression and triggered BB and BLS resistance when the corresponding Pi-CO39 resistance locus was present. In a second example, the transactivation of an auto-active NLR by Xoo-delivered designer TAL effectors resulted in BB resistance, demonstrating that NLR-triggered immune responses efficiently control Xoo. This forms the foundation for future BB and BLS disease control strategies, whereupon endogenous TAL effectors will target synthetic promoter regions of Avr or NLR executor genes.

Pathogen‐informed breeding for crop disease resistance

“…For example, scientists generated transgenic rice ( Oryza sativa ) plants harboring the AVR1‐CO39 effector gene of rice blast fungus M. oryzae or the NLR gene RGA4 , under the control of a TALE‐inducible promoter. Both transgenic lines exhibited enhanced resistance when challenged with pathogen strains carrying the corresponding TAL effectors (Hutin et al, 2016). Furthermore, both rice and pepper have evolved “executor” genes with TAL effector binding sites in their promoters, such as Xa27 from rice and Bs3 and Bs4c from pepper, the products of which induce hypersensitive cell death to confine pathogen proliferation (Dangl et al, 2013).…”

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

“…Research has shown that modifying the expression of defense-related ( DR ) genes alters the resistance of rice to Xoc . 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).…”

Recent advances in developing disease resistance in plants

“…R gene promoters have been modified to include a concatemer of EBE sites for TALes from multiple strains of a pathogen 60, 61 . TAL EBEs can also be added to promoters to recruit TALe-mediated expression of autonomous R genes or avirulence proteins leading to resistance reactions 62, 63 .…”