Regulation of symbiotic interactions and primitive lichen differentiation by UMP1 MAP kinase in Umbilicaria muhlenbergii

Wang, Yanyan; Li, Rong; Wang, Diwen; Qian, Ben; Bian, Zhuyun; Wei, Jiangchun; Wei, Xinli; Xu, Jin-Rong

doi:10.1038/s41467-023-42675-8

Cited by 4 publications

(1 citation statement)

References 69 publications

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“…On the mycobiont side, fungal stimuli may encompass the activities of carbohydrate-active enzymes (CAZymes), potentially enhancing the permeability of algal cell walls 27 . Sugars, sugar alcohols, along with other compound groups like secondary metabolites and antioxidants, are proposed as key elements in maintaining the intricately balanced symbiotic interplay between fungi and algae in lichens 26, 28 . This process implies that LAS should manifest distinct genomic features compared to algae unable to establish symbiotic associations 29–32 .…”

Section: Introductionmentioning

confidence: 99%

Phylogenomics reveals the evolutionary origins of lichenization in chlorophyte algae

Keller

Puginier

Libourel

et al. 2022

Preprint

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Mutualistic symbioses, such as lichens formed between fungi and green algae or cyanobacteria, have contributed to major transitions in the evolution of life and are at the center of extant ecosystems. However, our understanding of their evolution and function remains elusive in most cases. Here, we investigated the evolutionary history and the molecular innovations at the origin of lichens in green algae. We de novo sequenced the genomes or transcriptomes of 15 lichen-forming and closely-related non-lichen-forming algae and performed comparative phylogenomics with 22 genomes previously generated. We identified more than 350 functional categories significantly enriched in chlorophyte green algae able to form lichens. Among them, functions such as light perception or resistance to dehydration were shared between lichenizing and other terrestrial algae but lost in non-terrestrial ones, indicating that the ability to live in terrestrial habitats is a prerequisite for lichens to evolve. We detected lichen-specific expansions of glycosyl hydrolase gene families known to remodel cell walls, including the glycosyl hydrolase 8 which was acquired in lichenizing Trebouxiophyceae by horizontal gene transfer from bacteria, concomitantly with the ability to form lichens. Mining genome-wide orthogroups, we found additional evidence supporting at least two independent origins of lichen-forming ability in chlorophyte green algae. We conclude that the lichen-forming ability evolved multiple times in chlorophyte green algae, following a two-step mechanism which involves an ancestral adaptation to terrestrial lifestyle and molecular innovations to modify the partners cell walls.

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Section: Introductionmentioning

confidence: 99%

Phylogenomics reveals the evolutionary origins of lichenization in chlorophyte algae

Keller

Puginier

Libourel

et al. 2022

Preprint

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Phylogenomics reveals the evolutionary origins of lichenization in chlorophyte algae

Puginier,

Libourel,

Otte

et al. 2024

Nat Commun

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Mutualistic symbioses have contributed to major transitions in the evolution of life. Here, we investigate the evolutionary history and the molecular innovations at the origin of lichens, which are a symbiosis established between fungi and green algae or cyanobacteria. We de novo sequence the genomes or transcriptomes of 12 lichen algal symbiont (LAS) and closely related non-symbiotic algae (NSA) to improve the genomic coverage of Chlorophyte algae. We then perform ancestral state reconstruction and comparative phylogenomics. We identify at least three independent gains of the ability to engage in the lichen symbiosis, one in Trebouxiophyceae and two in Ulvophyceae, confirming the convergent evolution of the lichen symbioses. A carbohydrate-active enzyme from the glycoside hydrolase 8 (GH8) family was identified as a top candidate for the molecular-mechanism underlying lichen symbiosis in Trebouxiophyceae. This GH8 was acquired in lichenizing Trebouxiophyceae by horizontal gene transfer, concomitantly with the ability to associate with lichens fungal symbionts (LFS) and is able to degrade polysaccharides found in the cell wall of LFS. These findings indicate that a combination of gene family expansion and horizontal gene transfer provided the basis for lichenization to evolve in chlorophyte algae.

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Conserved signaling modules regulate filamentous growth in fungi: a model for eukaryotic cell differentiation

Vandermeulen,

Lorenz,

Cullen

2024

Genetics

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Eukaryotic organisms are composed of different cell types with defined shapes and functions. Specific cell types are produced by the process of cell differentiation, which is regulated by signal transduction pathways. Signaling pathways regulate cell differentiation by sensing cues and controlling the expression of target genes whose products generate cell types with specific attributes. In studying how cells differentiate, fungi have proved valuable models because of their ease of genetic manipulation and striking cell morphologies. Many fungal species undergo filamentous growth—a specialized growth pattern where cells produce elongated tube-like projections. Filamentous growth promotes expansion into new environments, including invasion into plant and animal hosts by fungal pathogens. The same signaling pathways that regulate filamentous growth in fungi also control cell differentiation throughout eukaryotes and include highly conserved mitogen-activated protein kinase (MAPK) pathways, which is the focus of this review. In many fungal species, mucin-type sensors regulate MAPK pathways to control filamentous growth in response to diverse stimuli. Once activated, MAPK pathways reorganize cell polarity, induce changes in cell adhesion, and promote the secretion of degradative enzymes that mediate access to new environments. However, MAPK pathway regulation is complicated because related pathways can share components with each other yet induce unique responses (i.e. signal specificity). In addition, MAPK pathways function in highly integrated networks with other regulatory pathways (i.e. signal integration). Here, we discuss signal specificity and integration in several yeast models (mainly Saccharomyces cerevisiae and Candida albicans) by focusing on the filamentation MAPK pathway. Because of the strong evolutionary ties between species, a deeper understanding of the regulation of filamentous growth in established models and increasingly diverse fungal species can reveal fundamentally new mechanisms underlying eukaryotic cell differentiation.

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Regulation of symbiotic interactions and primitive lichen differentiation by UMP1 MAP kinase in Umbilicaria muhlenbergii

Cited by 4 publications

References 69 publications

Phylogenomics reveals the evolutionary origins of lichenization in chlorophyte algae

Phylogenomics reveals the evolutionary origins of lichenization in chlorophyte algae

Phylogenomics reveals the evolutionary origins of lichenization in chlorophyte algae

Conserved signaling modules regulate filamentous growth in fungi: a model for eukaryotic cell differentiation

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