Flourishing in water: the early evolution and diversification of plant receptor‐like kinases

Abstract

SUMMARY Receptor‐like kinases (RLKs) play significant roles in mediating innate immunity and development of plants. The evolution of plant RLKs has been characterized by extensive variation in copy numbers and domain configurations. However, much remains unknown about the origin, evolution, and early diversification of plant RLKs. Here, we perform phylogenomic analyses of RLKs across plants (Archaeplastida), including embryophytes, charophytes, chlorophytes, prasinodermophytes, glaucophytes, and rhodophytes. We identify the presence of RLKs in all the streptophytes (land plants and charophytes), nine out of 18 chlorophytes, one prasinodermophyte, and one glaucophyte, but not in rhodophytes. Interestingly, the copy number of RLKs increased drastically in streptophytes after the split of the clade of Mesostigmatophyceae and Chlorokybophyceae and other streptophytes. Moreover, phylogenetic analyses suggest RLKs from charophytes form diverse distinct clusters, and are dispersed along the diversity of land plant RLKs, indicating that RLKs have extensively diversified in charophytes and charophyte RLKs seeded the major diversity of land plant RLKs. We identify at least 81 and 76 different kinase‐associated domains for charophyte and land plant RLKs, 23 of which are shared, suggesting that RLKs might have evolved in a modular fashion through frequent domain gains or losses. We also detect signatures of positive selection for many charophyte RLK groups, indicating potential functions in host–microbe interaction. Taken together, our findings provide significant insights into the early evolution and diversification of plant RLKs and the ancient evolution of plant–microbe symbiosis.

Transcriptomic and Metabolomic Approaches Deepen Our Knowledge of Plant–Endophyte Interactions

“…The second is via a plant-symbiont-pathogen interaction that results in a continuous formation of novel defenses in hosts (Delaux and Schornack, 2021). In the course of evolution of host defense, plant-symbiont-pathogen interactions generated conserved gene modules, such as receptor-like kinases (Gong and Han, 2021), that are central to the plant innate immunity (Bentham et al, 2020). Notably, in the interaction with the fungal endophyte Colletotrichum tofieldiae, the fungus activates the plant's PHT1 phosphate transporters which is beneficial under phosphorus-deficient conditions, while inducing plant defense by stimulating indole glucosinolate synthesis via the innate immune system (Hiruma et al, 2016).…”

Cryogenian glacial habitats as a plant terrestrialisation cradle – the origin of the anydrophytes and Zygnematophyceae split

“…It was proposed the different mechanisms of cell division between land plants and Zygnematophyceae results partially from simplification of the phragmoplast of the putative common ancestor (Anydrophyte) in the Zygnematophyceae; in more derived desmids phragmoplast is lost totally (Buschmann and Zachgo, 2016). To support the idea of secondary Zygnematophyceae simplification we propose using recently published analyses of early evolution of land plant receptor kinases (Gong and Han 2021) and several reports on transcription factors evolution. Comparison of independently evolved multicellular organisms indicates evolutionary multiplication of receptor kinases and transcription factors -both crucial mediators of intercellular communication and tissue differentiation -are a convergent feature of multicellular animals, land plants, Chlorophytes and brown algae (Cock et al, 2010;de Clerk et al 2018).…”

“…Comparison of independently evolved multicellular organisms indicates evolutionary multiplication of receptor kinases and transcription factors -both crucial mediators of intercellular communication and tissue differentiation -are a convergent feature of multicellular animals, land plants, Chlorophytes and brown algae (Cock et al, 2010;de Clerk et al 2018). Comparing data from Cheng et al (2019), Gong and Han (2021) and Jiao et al (2020) we conclude that not only Lys-M symbiosis-related and SD receptor kinases are lost in Zygnematophyceae (Cheng et al, 2019;Gong and Han 2021), but overall kinase-associated domains types are significantly reduced in Zygnematophyceae as compared to Chara or Embryophytes (Gong and Han 2021). But the exceptionally high number of different types of transcription factors still retained in single-cell Zygnematophyceae might be understood considering secondary reductions in structural complexity into the unicellular status are not necessarily accompanied by reductions in total transcription factors complements as proposed by Jiao et al (2020).…”

The APAF1_C/WD40 repeat domain-encoding gene from the sea lettuce Ulva mutabilis sheds light on the evolution of NB-ARC domain-containing proteins in green plants

“…Finally, it will be fascinating to discover which effector molecules interact with algal R proteins, from which (microbial) organism they originate, and if these molecules are the result of harmful or symbiotic interactions. In addition to effector-triggered immunity, pattern-triggered immunity involving receptor-like kinases (Gong and Han 2021 ) is also an important mediator of plant immunity. Further investigations of both modes of action, which evolved in parallel (de Vries et al 2018 ; Gong and Han 2021 ) will likely deepen our understanding of the nature of early plant–microbe interactions.…”

“…In addition to effector-triggered immunity, pattern-triggered immunity involving receptor-like kinases (Gong and Han 2021 ) is also an important mediator of plant immunity. Further investigations of both modes of action, which evolved in parallel (de Vries et al 2018 ; Gong and Han 2021 ) will likely deepen our understanding of the nature of early plant–microbe interactions.…”