An ancient route towards salicylic acid and its implications for the perpetual<i>Trichormus–Azolla</i>symbiosis

SUMMARY Land plants constantly respond to fluctuations in their environment. Part of their response is the production of a diverse repertoire of specialized metabolites. One of the foremost sources for metabolites relevant to environmental responses is the phenylpropanoid pathway, which was long thought to be a land‐plant‐specific adaptation shaped by selective forces in the terrestrial habitat. Recent data have, however, revealed that streptophyte algae, the algal relatives of land plants, have candidates for the genetic toolkit for phenylpropanoid biosynthesis and produce phenylpropanoid‐derived metabolites. Using phylogenetic and sequence analyses, we here show that the enzyme families that orchestrate pivotal steps in phenylpropanoid biosynthesis have independently undergone pronounced radiations and divergence in multiple lineages of major groups of land plants; sister to many of these radiated gene families are streptophyte algal candidates for these enzymes. These radiations suggest a high evolutionary versatility in the enzyme families involved in the phenylpropanoid‐derived metabolism across embryophytes. We suggest that this versatility likely translates into functional divergence, and may explain the key to one of the defining traits of embryophytes: a rich specialized metabolism.

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“…, 2018; de Vries et al. , 2021). It is noteworthy that kfl00104_0290_v1.1 has with Tyr113 another aromatic amino acid adjacent to G114.…”

Section: Resultsmentioning

confidence: 99%

The evolution of the phenylpropanoid pathway entailed pronounced radiations and divergences of enzyme families

et al. 2021

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“…The phytohormone salicylic acid (SA), which is involved in biotic stress in land plants (Pieterse et al, 2009), alters cyanobiont abundance and nifE gene expression . Vice versa, transcriptomics and comparative genomic analyses highlight that the presence or absence of the cyanobiont alters the expression of homologous genes putatively involved in SA biosynthesis and signalling (de Vries et al, 2021a). More experimental and comparative data are needed to understand (a) how stress-responsive signalling integrates into Azolla's symbiosis and (b) whether this can be transferred to non-permanent cyanobacterial symbioses.…”

Section: Symbiotic Communication and Integration Into Stress Responsesmentioning

confidence: 99%

Evolutionary genomic insights into cyanobacterial symbioses in plants

Vries

2022

Quant Plant Bio.

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Photosynthesis, the ability to fix atmospheric carbon dioxide, was acquired by eukaryotes through symbiosis: the plastids of plants and algae resulted from a cyanobacterial symbiosis that commenced more than 1.5 billion years ago and has chartered a unique evolutionary path. This resulted in the evolutionary origin of plants and algae. Some extant land plants have recruited additional biochemical aid from symbiotic cyanobacteria; these plants associate with filamentous cyanobacteria that fix atmospheric nitrogen. Examples of such interactions can be found in select species from across all major lineages of land plants. The recent rise in genomic and transcriptomic data has provided new insights into the molecular foundation of these interactions. Furthermore, the hornwort Anthoceros has emerged as a model system for the molecular biology of cyanobacteria–plant interactions. Here, we review these developments driven by high-throughput data and pinpoint their power to yield general patterns across these diverse symbioses.

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“…Together with jasmonates, salicylic acid (SA) also plays an important role in the defense against pathogens in vascular plants (Ding and Ding, 2020). SA has been proposed to be involved in the signaling between host plant and the cyanobiont in the Azolla-Nostoc symbiosis ( de Vries et al, 2018de Vries et al, , 2023. While most biosynthetic enzymes of SA are present in the hornwort genome, we found none of them upregulated during nitrogen starvation.…”

Section: Hormonal Responsementioning

confidence: 77%

Nitrogen starvation response in hornworts and liverworts provides little evidence for complex priming to the cyanobiont

Yue,

Sablok,

Neubauer

et al. 2024

Preprint

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Mutualistic plant-microbe symbiotic interactions are thought to have evolved from a loose association often observed between host plants and microbes when nutrients are limited and caused by chemical attractants released by the host plant. Therefore, the molecular network enabling intimate mutualistic plant-microbe symbioses may have evolved from a general nutrient starvation response shared by all land plants (embryophytes). Nevertheless, this hypothesis remains to be tested because information on the consequences of nutrient starvation is mainly available for vascular plants but missing for most non-vascular plant lineages. While well-studied in vascular plants, particularly in arbuscular mycorrhizal fungi- and nodule-forming bacteria-plant symbioses, the molecular link between nutrient status and symbiotic interaction remains poorly understood in other systems. This is especially true to the symbiotic associations between plants and cyanobacteria, in which host plants release so-called hormogonia inducing factors (HIF) only under nutrient limited conditions to mobilize the cyanobiont and initiate the interaction. Nevertheless, in contrast to the well-investigated mycorrhiza- and nodule-forming bacteria-plant associations, plant-cyanobacteria interactions are extracellular and morphological structures hosting the cyanobionts are formed even in the absence of the microbial partner. Therefore, nutrient starvation may induce a less complex genetic network in plant-cyanobacteria systems in contrast to intracellular symbioses (plant-AMF/nodule-forming bacteria). To test the hypothesis of a conserved starvation network across land plants and to investigate the link between nutrient starvation and symbiosis initiation in the plant-cyanobacteria symbiosis, we explore the transcriptional responses to nutrient starvation in two non-vascular plant species, a hornwort Anthoceros agrestis and a liverwort Blasia pusilla, serving as ideal model systems for plant-cyanobacteria endophytic symbioses. By analyzing time-series RNA-seq data, we investigate gene expression changes associated with nutrient starvation in these bryophyte species and compare them with data available for vascular plants. Our study aims to identify convergent and divergent transcriptomic responses and to uncover transcriptomic signatures specific to cyanobacteria symbiosis-capable organisms. Our results reveal that A. agrestis and B. pusilla exhibit similar transcriptional responses to the nitrogen starvation, characterized by the upregulation of genes involved in nitrogen uptake and assimilation, hormonal regulation, stress response, and signal transduction pathways. Moreover, our findings suggest that bioactive molecules, particularly flavonoids produced under nutrient starvation, may play a role in initiating the plant-mycorrhiza and nodule-forming bacteria symbioses, particularly serving as HIF in plant-cyanobacteria symbioses.

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An ancient route towards salicylic acid and its implications for the perpetualTrichormus–Azollasymbiosis

Cited by 4 publications

References 120 publications

The evolution of the phenylpropanoid pathway entailed pronounced radiations and divergences of enzyme families

The evolution of the phenylpropanoid pathway entailed pronounced radiations and divergences of enzyme families

Evolutionary genomic insights into cyanobacterial symbioses in plants

Nitrogen starvation response in hornworts and liverworts provides little evidence for complex priming to the cyanobiont

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