The Evolution of Symbiotic Plant–Microbe Signalling

Abstract

Plants form beneficial symbioses with a variety of different microbes. Among these, the root associated arbuscular mycorrhizal fungi, ectomycorrhizal fungi, rhizobial, and actinobacterial symbioses are some of the best understood. The successful establishment of these symbioses relies on a complex, coordinated signal exchange that arose from hundreds of millions of years of coevolution between plants and their associated microbes. Despite the diversity of these microbial symbionts, common signalling mechanisms were evolved that include the manipulation of host immunity and the use of similar plant‐ and microbe‐derived signals and receptors. Owing to the plethora of information on these diverse symbioses, their signalling mechanisms are rarely reviewed together and even less so within an evolutionary context. We provide an overview of what is known regarding the evolution of these signals in an effort to highlight knowledge gaps in our understanding of plant–microbe symbiosis.

Hormones as go‐betweens in plant microbiome assembly

“…SLs are a group of compounds relatively recently recognised as plant hormones with functions in shoot branching, root system architecture, parasitic weed germination and plant–microbe communication (Yoneyama et al ., 2008 ; Al‐Babili and Bouwmeester, 2015 ; Clear and Hom, 2019 ; Aliche et al ., 2020 ). They also display complex cross‐talk with other hormones and are therefore involved in many aspects of plant growth and development (Cheng et al ., 2013 ; Omoarelojie et al ., 2019 ).…”

“…They also display complex cross‐talk with other hormones and are therefore involved in many aspects of plant growth and development (Cheng et al ., 2013 ; Omoarelojie et al ., 2019 ). SLs have a role in classical plant symbioses with AMF and nodulating rhizobia (Steinkellner et al ., 2007 ; Foo and Davies, 2011 ; Clear and Hom, 2019 ). Although an SL receptor has not been characterised in AMF, so far, treatment with SL induces a variety of fungal responses, including morphological and transcriptional changes, and the stimulation of the release of secreted proteins, which support plant colonisation (Lanfranco et al ., 2018 ).…”

Towards a Systems Biology Approach to Understanding the Lichen Symbiosis: Opportunities and Challenges of Implementing Network Modelling

“…In symbiotic systems, signalling pathways have been a topic of particular focus for legumes-rhizobia and plants-root fungi (mycorrhiza) symbioses ( Bonfante and Genre, 2010 ; Bonfante and Requena, 2011 ; Oldroyd, 2013 ; Venkateshwaran et al, 2013 ; Mohanta and Bae, 2015 ; Martin et al, 2017 ; Poole et al, 2018 ; Clear and Hom, 2019 ). However, modelling the signalling networks in these systems has not received much attention, perhaps due largely to the knowledge gap in certain key signalling steps.…”

“…For example, some of the most detailed and comprehensive predictive signalling models have been developed for complex but known signalling networks of human B-cells (Papin and Palsson, 2004), prostate cancer cells (Dasika et al, 2006;Vardi et al, 2012), and Toll-like receptors (TLRs) functioning in immune system (Li et al, 2009). In symbiotic systems, signalling pathways have been a topic of particular focus for legumes-rhizobia and plants-root fungi (mycorrhiza) symbioses (Bonfante and Genre, 2010;Bonfante and Requena, 2011;Oldroyd, 2013;Venkateshwaran et al, 2013;Mohanta and Bae, 2015;Martin et al, 2017;Poole et al, 2018;Clear and Hom, 2019). However, modelling the signalling networks in these systems has not received much attention, perhaps due largely to the knowledge gap in certain key signalling steps.…”

Distinguishing Allies from Enemies—A Way for a New Green Revolution

“…In contrast to plant–pathogen interactions, studies on plant responses towards mutualist microbes are scarcer, mainly focusing on associations with mycorrhizal fungi and rhizobia. In the four types of root mutualist relationships (arbuscular mycorrhizae—AM, ectomycorrhizae—ECM, rhizobia and Frankia ), a similar strategy seems to be used for host infection [ 15 ]. Plants secrete compounds for the recruitment of mutualist partners near their roots, which in turn will respond by secreting compounds that induce plant physiological changes.…”