Mutual Potentiation of Plant Immunity by Cell-surface and Intracellular Receptors

Abstract

The plant immune system involves cell-surface receptors that detect intercellular pathogenderived molecules, and intracellular receptors that activate immunity upon detection of 10 pathogen-secreted effectors that act inside the plant cell. Surface receptor-mediated immunity has been extensively studied but in authentic interactions between plants and microbial pathogens, its presence impedes study of intracellular receptor-mediated immunity alone. How these two immune pathways interact is poorly understood. Here, we reveal mutual potentiation between these two recognition-dependent defense pathways. 15Recognition by surface receptors activates multiple protein kinases and NADPH oxidases, whereas intracellular receptors primarily elevate abundance of these proteins. Reciprocally, the intracellular receptor-dependent hypersensitive cell death response is strongly enhanced by activation of surface receptors. Activation of either immune system alone is insufficient to provide effective resistance against Pseudomonas syringae. Thus, immune pathways 20 activated by cell-surface and intracellular receptors mutually potentiate to activate strong defense that thwarts pathogens. By studying the activation of intracellular receptors in the absence of surface receptor-mediated immunity, we have dissected the relationship between the two distinct immune systems. These findings reshape our understanding of plant immunity and have broad implications for crop improvement. 25

Use of virus‐induced gene silencing to characterize genes involved in modulating hypersensitive cell death in maize

“…MAMP recognition leads to activation of the MAMP‐triggered immunity (MTI) response, which is qualitatively similar to ETI though quantitatively lower, usually not involving an HR (Newman et al, 2013). Recent studies suggest that a functional MTI response is important to enable a full ETI response (Ngou et al, 2020; Yuan et al, 2020).…”

“…VPS37-1 colocalized with FLS2 at endosome upon flagellin elicitation and vps37-1 mutants compromised vacuolar sorting of FLS2 and flagellin-triggered stomatal closure, and displayed impaired immunity to the bacterial pathogen P. syringae and to the biotrophic oomycete Hyaloperonospora arabidopsidis(Lu et al, 2012). While FLS2 activation and the resulting MTI do not generally lead to an HR, a strong connection has recently been shown between a functional MTI response and a full ETI response, including HR(Ngou et al, 2020;Yuan et al, 2020).Silencing of VPS37 suppressed Rp1-D21-induced HR in maize(Figure 4a,c). The VPS37 transcript level was reduced by 1.63fold in plants infected with pFoMV-VPS37 compared to control F I G U R E 3 Suppression of Rp1-D21-induced cell death by coexpression of SGT15019 but not SGT9704 in Nicotiana benthamiana.…”

Pattern recognition receptors confer plant salt tolerance via WRKY18/WRKY40 transcription factors

“…This predicts the existence of a critical threshold beyond which further immune activation comes at a cost for salt stress tolerance. Recent studies show that PRR signaling provides an integrating basis for ETI, and that mutual PTI-ETI potentiation is required for effective pathogen resistance (Ngou et al, 2020;Yuan et al, 2020). At present, how NLR signaling exceeds the predicted threshold during ETI remains poorly understood.…”

A molecular roadmap to the plant immune system

“…Intriguingly, a new body of work has emerged, which has begun to uncover interplay between cell-surface and intracellular immunity ( 43 , 44 ). These papers demonstrate that cell-surface immunity is required to potentiate intracellular immunity, enhancing NLR responses such as cell death.…”

“…Activation of intracellular immunity is generally considered a more robust response and can be associated with localized cell death that constrains the spread of infection. Although often presented as distinct signaling pathways, insights into how cell-surface and intracellular immune pathways in plants overlap and work synergistically to resist infection have recently begun to emerge ( 43 , 44 ).…”