Two Distinct EF-Tu Epitopes Induce Immune Responses in Rice and Arabidopsis

Abstract

Plants sense potential pathogens by recognizing conserved pathogen-associated molecular patterns (PAMPs) that cause PAMP-triggered immunity (PTI). We previously reported that rice recognizes flagellin from the rice-incompatible N1141 strain of Acidovorax avenae and subsequently induces immune responses. Cell extracts isolated from flagellin-deficient N1141 (Δfla1141) still induced PTI responses, suggesting that Δfla1141 possesses an additional PAMP distinct from flagellin. Here, we show that elongation factor Tu (EF-Tu), one of the most abundant bacterial proteins, acts as a PAMP in rice and causes several PTI responses. In Brassicaceae species, EF-Tu and an N-acetylated peptide comprising the first 18 amino acids of the N-terminus, termed elf18, are fully active as inducers of PTI responses. By contrast, elf18 did not cause any immune responses in rice, whereas an EF-Tu middle region comprising Lys176 to Gly225, termed EFa50, is fully active as a PAMP in rice. In the leaves of rice plants, EF-Tu induced H2O2 generation and callose deposition, and also triggered resistance to coinfection with pathogenic bacteria. Taken together, these data demonstrate that rice recognizes EFa50, which is distinct from elf18, and that this epitope induces PTI responses.

Understanding Plant Immunity as a Surveillance System to Detect Invasion

“…Plants outside of the Brassicaceae do not respond to elf18 and presumably do not contain a functional homolog of EFR (13,81). Recently, a second immunogenic epitope of EF-Tu, termed EFa50, was discovered from P. avenae, which elicits numerous immune responses in rice cells but not in Arabidopsis (51). Thus, similar to flagellin perception, independent evolution of receptors to different epitopes of EF-Tu has likely occurred, suggestive of specific host-pathogen evolution rather than general perception.…”

“…The number and diversity of IPs generated and perceived during any given invasion are relatively unknown. A number of microbe-produced structural immunogenic epitopes were identified from culture-grown microbial fractionations (7,31,41,42,51,67). This process has been key to identifying many immunogenic molecules, but it requires significant investment and potentially results in immunogenic epitopes from a single organism.…”

A Conserved Peptide Pattern from a Widespread Microbial Virulence Factor Triggers Pattern-Induced Immunity in Arabidopsis

“…Likewise, more recently identified Sclerotinia sclerotiorum -derived proteinaceous SSCF1 or Xanthomonas campestris -derived EMAX are recognized by Brassicaceae only [14], [15]. Moreover, identification of a tomato flagellin perception system that recognizes flagellin epitopes different from flg22 [16], or of a rice receptor that recognizes a central fragment of EF-Tu structurally unrelated to elf18 [17], suggest substantial dynamics in PRR evolution. More systematic studies on PRR distribution patterns among Arabidopsis thaliana ecotypes have further revealed that individual pattern recognition specificities might also be lost during evolution [14], [15], [18].…”

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

“…Tomato, for instance, has a second flagellin receptor, FLS3, that detects an epitope (termed flgII-28) distinct from flg22 (sensed by FLS2) [38]. Similarly, rice can sense another EF-Tu epitope (EFa50) distinct from elf18 which is sensed in Brassicaceae [39]. Thus, the genetic diversity of plants provides a rich source of PRRs not only for a multitude of different MAMPs from various kinds of invaders but also for distinct MAMP epitopes.…”