Layered pattern receptor signaling via ethylene and endogenous elicitor peptides during Arabidopsis immunity to bacterial infection

Abstract

Recognition of molecular patterns characteristic of microbes or altered-self leads to immune activation in multicellular eukaryotes. In Arabidopsis thaliana, the leucine-rich-repeat receptor kinases FLAGELLIN-SENSING2 (FLS2) and EF-TU RECEPTOR (EFR) recognize bacterial flagellin and elongation factor EF-Tu (and their elicitor-active epitopes flg22 and elf18), respectively. Likewise, PEP1 RECEP-TOR1 (PEPR1) and PEPR2 recognize the elicitor-active Pep epitopes conserved in Arabidopsis ELICITOR PEPTIDE PRECURSORs (PROPEPs). Here we reveal that loss of ETHYLENE-INSENSITIVE2 (EIN2), a master signaling regulator of the phytohormone ethylene (ET), lowers sensitivity to both elf18 and flg22 in different defense-related outputs. Remarkably, in contrast to a large decrease in FLS2 expression, EFR expression and receptor accumulation remain unaffected in ein2 plants. Genome-wide transcriptome profiling has uncovered an inventory of EIN2-dependent and EFR-regulated genes. This dataset highlights important aspects of how ET modulates EFR-triggered immunity: the potentiation of salicylate-based immunity and the repression of a jasmonate-related branch. EFR requires ET signaling components for PROPEP2 activation but not for PROPEP3 activation, pointing to both ET-dependent and -independent engagement of the PEPR pathway during EFR-triggered immunity. Moreover, PEPR activation compensates the ein2 defects for a subset of EFR-regulated genes. Accordingly, ein2 pepr1 pepr2 plants exhibit additive defects in EFR-triggered antibacterial immunity, compared with ein2 or pepr1 pepr2 plants. Our findings suggest that the PEPR pathway not only mediates ET signaling but also compensates for its absence in enhancing plant immunity.microbe-associated molecular pattern | danger-associated molecular pattern | disease resistance | plant hormone | defense-related genes

Structural basis for recognition of an endogenous peptide by the plant receptor kinase PEPR1

“…However, protonation of some key residues such as PEPR1 Arg487 that forms salt bonds with the free carboxy group of AtPep1 ( Figure 3B) might contribute to this process. A number of studies suggest that AtPeps function as an amplifier of PTI [25][26][27][28], one hallmark of which is an increase in medium pH [36,37]. Although further in vivo studies are required to investigate whether and how PTI is associated with the pH-dependent PEPR1LRR recognition of AtPep1, this observation indicates that changes in pH during PTI can affect the biochemical activities of signaling molecules involved.…”

“…Similar to FLS2 and EFR, PEPR1 stably associates with BAK1 in response to treatment with AtPeps [23,24]. A number of studies suggest that PEPR-mediated immune responses serve to amplify PTI signaling [25][26][27][28] via the JA/ET (jasmonic acid-ethylene) and SA (salicylic acid) pathways [25,28]. A more recent study suggests that PEPR1,2-mediated signaling has a critical role in coupling local and systemic immunity [29].…”

BIK1 interacts with PEPRs to mediate ethylene-induced immunity

“…However, emerging evidence indicates that ET can also enhance PAMP-triggered immunity by inducing FLS2 transcription (25,26). The companion article by Tintor et al (34) shows that EIN2 and EIN3/EIL1 are required for elf18-induced signaling and that PEPR1/PEPR2 contributes to EFR-triggered immunity. These results are consistent with our observation that PEPRs and BIK1 are required for ET-triggered defense responses and disease resistance to B. cinerea.…”

Salicylic Acid Regulates Arabidopsis Microbial Pattern Receptor Kinase Levels and Signaling

“…Signaling upon flg22 perception involves the increased accumulation of SA (Mishina and Zeier, 2007;Tsuda et al, 2008). Other PAMPs induce the SA marker PR1 and, therefore, also are likely to cause increased SA levels (Gust et al, 2007;Tintor et al, 2013). We envision that PAMPs released from pathogens stimulate PRRs, resulting in higher levels of SA that is made in and/or mobilized to neighboring cells/tissues (Shulaev et al, 1995;Costet et al, 1999), stimulate ACD6 and PRR-dependent callose, and over time cause increased (co)receptor levels.…”