Convergent loss of an EDS1/PAD4 signalling pathway in several plant lineages predicts new components of plant immunity and drought response

Abstract

Drought and immunity pathway reduction in aquatic environments 2 AbstractThe transition of plants from sea to land sparked an arms race with pathogens. The increased susceptibility of land plants is largely thought to be due to their dependence on micro-organisms for nutrients; the ensuing co-evolution has shaped the plant immune system. By profiling the immune receptors across flowering plants, we identified species with low numbers of NLR immune receptors. Interestingly, four of these species represent distinct lineages of monocots and dicots that returned to the aquatic lifestyle. Both aquatic monocot and dicot species lost the same well-known downstream immune signalling complex (EDS1-PAD4). This observation inspired us to look for other genes with a similar loss pattern and allowed us to predict putative new components of plant immunity. Gene expression analyses confirmed that a group of these genes was differentially expressed under pathogen infection. Excitingly, another subset of these genes was differentially expressed upon drought. Collectively, our study reveals the minimal plant immune system required for life under water, and highlights additional components required for the life of land plants.Drought and immunity pathway reduction in aquatic environments 3 Author summaryPlant resistance to pathogens is commonly mediated by a complex gene family, known as NLRs. Upon pathogen infection, changes in the cellular environment trigger NLR activation and subsequent defence responses. Despite the dependence of agricultural practices on NLR genes to control pathogen load, relatively little is known about this gene family outside of model crop species. In this study, we identified a convergent reduction in the NLR gene family among two lineages of aquatic plants. Furthermore, we established that NLR reduction occurred in conjunction with the loss of a common immune signalling pathway. Subsequently, we identified other genes convergently lost in aquatic species and propose these as candidate components of the plant immune signalling pathway. In addition, we revealed components of the agronomically important drought response to be lost in aquatic plants. This study adds to our understanding of the complex interactions between environment and response to biotic stress, widely known as the disease triangle. The pathways identified in this study shed further light on the link between responses to drought and disease.Drought and immunity pathway reduction in aquatic environments

Plant NLRs get by with a little help from their friends

“…Conceivably, each subclade may have specialized downstream of a specific set of sensors, or alternatively, some strawberry, grapevine and/or lettuce RNLs have evolved a sensor function. Conversely, RNLs are absent in several different aquatic plant families, which correlates with absence of TNLs and the lipase-like EDS1, SAG101 and PAD4 proteins [49]. Furthermore, there is a strong indication of a co-evolved functional relationship specifically between TNLs, NRG1, and SAG101, as all three are absent from monocotyledon, and certain dicotyledon, genomes [3,17,49].…”

“…Conversely, RNLs are absent in several different aquatic plant families, which correlates with absence of TNLs and the lipase-like EDS1, SAG101 and PAD4 proteins [49]. Furthermore, there is a strong indication of a co-evolved functional relationship specifically between TNLs, NRG1, and SAG101, as all three are absent from monocotyledon, and certain dicotyledon, genomes [3,17,49]. This supports the hypothesis that RNLs play a role in EDS1/SAG101/PAD4 signaling downstream of TNL activation [50].…”

Enzymatic Functions for Toll/Interleukin-1 Receptor Domain Proteins in the Plant Immune System

“…Canonical TNLtype resistance genes are absent from all examined monocot genomes, as are the TIR-pathway mediators, SAG101 and NRG1 (Collier et al, 2011;Wagner et al, 2013). Remarkably, convergent loss of TNLs and downstream genes has occurred several times during plant evolution (Collier et al, 2011;Baggs et al, 2019). Monocots do, however, encode several TIR-NBS and TIR-only genes, although in low abundance relative to the high number of TNLs commonly present in dicots (Sun et al, 2014;Gao et al, 2018).…”

“…While TNLs are absent from monocots (and several dicot lineages), they are present broadly across the plant phylogeny, including bryophytes and conifers (see also Figure 2C) (Baggs et al, 2019). For instance, the moss Physcomitrella patens carries TNL loci, as does the western white pine, Pinus monticola (Liu and Ekramoddoullah, 2011;Tanigaki et al, 2014).…”