The CC-NB-LRR-Type Rdg2a Resistance Gene Confers Immunity to the Seed-Borne Barley Leaf Stripe Pathogen in the Absence of Hypersensitive Cell Death

Abstract

BackgroundLeaf stripe disease on barley (Hordeum vulgare) is caused by the seed-transmitted hemi-biotrophic fungus Pyrenophora graminea. Race-specific resistance to leaf stripe is controlled by two known Rdg (Resistance to Drechslera graminea) genes: the H. spontaneum-derived Rdg1a and Rdg2a, identified in H. vulgare. The aim of the present work was to isolate the Rdg2a leaf stripe resistance gene, to characterize the Rdg2a locus organization and evolution and to elucidate the histological bases of Rdg2a-based leaf stripe resistance.Principal FindingsWe describe here the positional cloning and functional characterization of the leaf stripe resistance gene Rdg2a. At the Rdg2a locus, three sequence-related coiled-coil, nucleotide-binding site, and leucine-rich repeat (CC-NB-LRR) encoding genes were identified. Sequence comparisons suggested that paralogs of this resistance locus evolved through recent gene duplication, and were subjected to frequent sequence exchange. Transformation of the leaf stripe susceptible cv. Golden Promise with two Rdg2a-candidates under the control of their native 5′ regulatory sequences identified a member of the CC-NB-LRR gene family that conferred resistance against the Dg2 leaf stripe isolate, against which the Rdg2a-gene is effective. Histological analysis demonstrated that Rdg2a-mediated leaf stripe resistance involves autofluorescing cells and prevents pathogen colonization in the embryos without any detectable hypersensitive cell death response, supporting a cell wall reinforcement-based resistance mechanism.ConclusionsThis work reports about the cloning of a resistance gene effective against a seed borne disease. We observed that Rdg2a was subjected to diversifying selection which is consistent with a model in which the R gene co-evolves with a pathogen effector(s) gene. We propose that inducible responses giving rise to physical and chemical barriers to infection in the cell walls and intercellular spaces of the barley embryo tissues represent mechanisms by which the CC-NB-LRR-encoding Rdg2a gene mediates resistance to leaf stripe in the absence of hypersensitive cell death.

Programmed cell death in the plant immune system

“…Since then, several natural examples of plant-pathogen interactions resulting in resistance without cell death have been reported, in particular the potato Rx and barley Rrs1 disease resistance genes. [117][118][119][120][121][122][123][124] Additionally, suppressing caspase-like activities (unrelated to metacaspases) in plants inhibits pathogen-induced cell death without affecting disease resistance. 89,125 As described above, elimination of the metacaspase AtMC1 results in drastically reduced HR after infection with incompatible pathogens, but bacterial growth restriction remains unaffected in this mutant.…”

The Coiled-Coil and Nucleotide Binding Domains of BROWN PLANTHOPPER RESISTANCE14 Function in Signaling and Resistance against Planthopper in Rice

“…Support for this hypothesis comes from studies on Rx (Slootweg et al, 2010), RPS4 (Heidrich et al, 2011), and N (Bhattacharjee et al, 2009). Moreover, cell death appears to be uncoupled from the defense mechanisms induced by plant disease resistance genes encoding R proteins such as Rdg2a (Bulgarelli et al, 2010), Rrs1 (Lehnackers and Knogge, 1990), Mla1 (Freialdenhoven et al, 1994), Rx (Bendahmane et al, 1999), RPS4, RPS6 (Gassmann, 2005), and Mi-1 (Martinez de Ilarduya et al, 2003). These findings indicate that plant immunity can be effective without programmed host cell death.…”

Retromer Contributes to Immunity-Associated Cell Death in Arabidopsis

“…However, it is still debated whether effector-triggered hypersensitive PCD is a cause or consequence of disease resistance. While some evidence supports the contribution of HR to growth restriction of strictly biotrophic pathogens (Wang et al, 2011), other evidence indicates that ETI can be separated from the HR (Bendahmane et al, 1999;Bulgarelli et al, 2010;Coll et al, 2010;Heidrich et al, 2011).…”