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Rich, M. K.

Publications and source records attributed to Rich, M. K..

6 recordsLinked to original sources

Stepwise evolution of the developmental and symbiotic functions of DELLA in land plants

DELLA proteins play diverse roles in development, plant-microbe interactions and stress responses, and are regulated by the hormone gibberellic acid (GA) in flowering plants. Here, we investigated the evolutionary conservation of functions of the single DELLA ortholog in the non-vascular model liverwort Marchantia paleacea, which lacks genes for perception and biosynthesis of bioactive GA. We found that GA-independent developmental phenotypes are conserved in M. paleacea, while neither DELLA, nor its close paralog GRAS13 are involved in establishment of arbuscular mycorrhizal symbiosis. We propose that symbiosis-related functions of DELLA evolved and have been maintained in vascular plants because GA-dependent regulation offered an additional, systemic, control layer on symbiosis.

plant biology↗

EPP1 is an ancestral component of the plant Common SymbiosisPathway

The success of plants on land has been enabled by mutualistic intracellular associations with microbes for 450 million years (Delaux and Schornack 2021). Because of their intracellular nature, the establishment of these interactions requires tight regulation by the host plants. In particular, three genes - SYMRK, CCaMK and CYCLOPS - form the core of an ancestral common symbiosis pathway (CSP) for intracellular symbioses, and are conserved since the most recent common ancestor of land plants (Radhakrishnan et al. 2020; Delaux et al. 2015; Wang et al. 2010; Parniske 2008). Here, we describe EPP1 as a fourth gene committed to the CSP. Among land plants, EPP1 is conserved only in species able to associate with at least one type of intracellular symbiont. We found that loss-of-function epp1 mutants or EPP1 knock-down lines in four clades of land plants - legumes, Solanaceae, monocots and bryophytes - are all impaired in their ability to associate with arbuscular mycorrhizal fungi. We discovered that the plasma membrane-localized receptor-like SYMRK phosphorylates EPP1 on a conserved serine residue and that this phosphorylation is essential for symbiosis. Using a gain-of-function approach, we demonstrate that EPP1 is upstream of the nuclear kinase CCaMK. We propose that EPP1 is an ancestral component of the essential pathway that has regulated plant symbiosis for half a billion years.

plant biology↗

Conservation of symbiotic signalling across 450 million years of plant evolution

HighlightO_LIThe common symbiotic pathway is activated during arbuscular mycorrhizal symbiosis in Marchantia paleacea C_LIO_LIThe three core members of the common symbiotic pathway are essential for symbiosis in Marchantia paleacea C_LIO_LIThe molecular function of the CCaMK/CYCLOPS module is conserved across land plants C_LIO_LISymbiotic signalling has been conserved in plants for 450 million years C_LI The colonization of land by plants 450 million years ago revolutionized life on Earth1. The fossil record2 and genetic evidence in extant species3 suggest that this transition was facilitated by interactions with symbiotic arbuscular mycorrhizal (AM) fungi4. This ancestral symbiosis relied on the biosynthesis of chemicals by the host plant, both as signals5 and as nutrients3. In angiosperms, a signalling pathway involving the receptor-like kinase SYMRK/DMI26,7, the Calcium and Calmodulin-dependent protein kinase CCaMK/DMI38 and the transcription factor CYCLOPS/IPD39,10 has been described as the common symbiosis pathway (CSP), essential for the establishment of the AM symbiosis and the root-nodule symbiosis11. Phylogenetic and comparative phylogenomic analyses indicated an ancient origin of the CSP, present in all extant land plants forming intracellular symbioses12-15. Trans-complementation assays of the angiosperm mutants with orthologs from diverse species further indicated the conservation of the molecular function of the CSP across the embryophytes9,12,14-16. However, this correlative evidence did not allow testing the ancestral biological function of the CSP. In this study we demonstrate that SYMRK, CCaMK and CYCLOPS are essential for the colonization by AM fungi in bryophytes, indicating that plants have maintained a dedicated signalling pathway to support symbiotic interactions for 450 million years.

plant biology↗

LysM-RLK plays an ancestral symbiotic function in plants

Arbuscular mycorrhiza (AM) with soilborne Glomeromycota fungi was pivotal in the conquest of land by plants almost half a billion years ago. In flowering plants, it is hypothesised that AM is initiated by the perception of AM-fungi-derived chito- and lipochito-oligosaccharides (COs/LCOs) in the host via Lysin Motif Receptor-Like Kinases (LysM-RLKs). However, it remains uncertain whether plant perception of these molecules is a prerequisite for AM establishment and for its origin. Here, we made use of the reduced LysM-RLK complement present in the liverwort Marchantia paleacea to assess the conservation of the role played by this class of receptors during AM and in COs/LCOs perception. Our reverse genetic approach demonstrates the critical function of a single LysM-RLK, LYKa, in AM formation, thereby supporting an ancestral function for this receptor in symbiosis. Binding studies, cytosolic calcium variation recordings and genome-wide transcriptomics indicate that another LysM-RLK of M. paleacea, LYR, is also required for triggering a response to COs/LCOs, despite being dispensable for AM formation. Collectively, our results demonstrate that the perception of symbionts by LysM-RLK is an ancestral feature in land plants, and suggest the existence of yet-uncharacterised AM-fungi signals.

plant biology↗

An ancestral function of strigolactones as symbiotic rhizosphere signals

In flowering plants, carotenoid-derived strigolactones (SLs) have dual functions as hormones that regulate growth and development, and as rhizosphere signaling molecules that induce symbiosis with arbuscular mycorrhizal (AM) fungi. Here, we report the identification of bryosymbiol (BSB), a previously unidentified SL from the bryophyte Marchantia paleacea. BSB is also found in vascular plants, indicating that it is ancestral in land plants. BSB synthesis is enhanced at AM symbiosis permissive conditions and BSB deficient mutants are impaired in AM symbiosis. In contrast, the absence of BSB synthesis has little effect on the growth and gene expression. We show that the introduction of the SL receptor of Arabidopsis renders M. paleacea cells BSB-responsive. These results suggest that BSB is not perceived by M. paleacea cells due to the lack of cognate SL receptors. We propose that SLs originated as AM symbiosis-inducing rhizosphere signaling molecules and were later recruited as plant hormone.

plant biology↗

An ancestral signalling pathway is conserved in plant lineages forming intracellular symbioses

Plants are the foundation of terrestrial ecosystems and their colonization of land was facilitated by mutualistic associations with arbuscular mycorrhizal fungi. Following that founding event, plant diversification has led to the emergence of a tremendous diversity of mutualistic symbioses with microorganisms, ranging from extracellular associations to the most intimate intracellular associations, where fungal or bacterial symbionts are hosted inside plant cells. Through analysis of 271 transcriptomes and 122 plant genomes, we demonstrate that the common symbiosis signalling pathway controlling the association with arbuscular mycorrhizal fungi and with nitrogen-fixing bacteria specifically co-evolved with intracellular endosymbioses, including ericoid and orchid mycorrhizae in angiosperms and ericoid-like associations of bryophytes. In contrast, species forming exclusively extracellular symbioses like ectomycorrhizae or associations with cyanobacteria have lost this signalling pathway. This work unifies intracellular symbioses, revealing conservation in their evolution across 450 million years of plant diversification.

plant biology↗