Evolutionary genomic insights into cyanobacterial symbioses in plants

Vries, Sophie de; Vries, Jan de

doi:10.1017/qpb.2022.3

Cited by 19 publications

(24 citation statements)

References 134 publications

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“…Other COG categories with a high proportion of unique genes were those dedicated to intracellular trafficking, motility and signal transduction mechanisms (). The importance of these mechanisms in cyanobiont symbiosis has been previously reported [25, 27, 28]. Interestingly, genomes from clade SYMB-1 contained a lower fraction of unique genes from these categories than those from SYMB-2 and 3 (), in line with what was observed in the pangenomic analysis, namely that based on composition, genomes from SYMB-1 are closer to FL-II than SYMB-2 and 3 are to their sister clade FL-XI ().…”

Section: Discussionsupporting

confidence: 83%

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Phylometagenomics of cycad coralloid roots reveals shared symbiotic signals

Bustos-Diaz,

Cruz-Perez,

Garfias-Gallegos

et al. 2024

Microbial Genomics

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Cycads are known to host symbiotic cyanobacteria, including Nostocales species, as well as other sympatric bacterial taxa within their specialized coralloid roots. Yet, it is unknown if these bacteria share a phylogenetic origin and/or common genomic functions that allow them to engage in facultative symbiosis with cycad roots. To address this, we obtained metagenomic sequences from 39 coralloid roots sampled from diverse cycad species and origins in Australia and Mexico. Culture-independent shotgun metagenomic sequencing was used to validate sub-community co-cultures as an efficient approach for functional and taxonomic analysis. Our metanalysis shows a host-independent microbiome core consisting of seven bacterial orders with high species diversity within the identified taxa. Moreover, we recovered 43 cyanobacterial metagenome-assembled genomes, and in addition to Nostoc spp., symbiotic cyanobacteria of the genus Aulosira were identified for the first time. Using this robust dataset, we used phylometagenomic analysis to reveal three monophyletic cyanobiont clades, two host-generalist and one cycad-specific that includes Aulosira spp. Although the symbiotic clades have independently arisen, they are enriched in certain functional genes, such as those related to secondary metabolism. Furthermore, the taxonomic composition of associated sympatric bacterial taxa remained constant. Our research quadruples the number of cycad cyanobiont genomes and provides a robust framework to decipher cyanobacterial symbioses, with the potential of improving our understanding of symbiotic communities. This study lays a solid foundation to harness cyanobionts for agriculture and bioprospection, and assist in conservation of critically endangered cycads.

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Section: Discussionsupporting

confidence: 83%

“…An alpha value of <1 from the power law was obtained for the entire Nostocales super-clade, indicating an open pangenome [72] consistent with the multiple lifestyles characteristic of these species [73]. Similarly, the symbiotic clades exhibited an open pangenome, which is consistent with a facultative symbiotic lifestyle [28, 74] ().…”

Section: Resultsmentioning

confidence: 93%

Phylometagenomics of cycad coralloid roots reveals shared symbiotic signals

Bustos-Diaz,

Cruz-Perez,

Garfias-Gallegos

et al. 2024

Microbial Genomics

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“…Hornworts host the cyanobacteria in mucilage cavities that can be accessed through ventral mucilage clefts, which superficially resemble stomata ( Renzaglia et al., 2000 ; Villarreal A and Renzaglia, 2006 ). An exception is L. dussii that hosts cyanobacteria in canals that branch and form an integrated network within the thallus ( de Vries and de Vries ; Meeks, 2003 ).…”

Section: The Unique Biology Of Hornwortsmentioning

confidence: 99%

What can hornworts teach us?

et al. 2023

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The hornworts are a small group of land plants, consisting of only 11 families and approximately 220 species. Despite their small size as a group, their phylogenetic position and unique biology are of great importance. Hornworts, together with mosses and liverworts, form the monophyletic group of bryophytes that is sister to all other land plants (Tracheophytes). It is only recently that hornworts became amenable to experimental investigation with the establishment of Anthoceros agrestis as a model system. In this perspective, we summarize the recent advances in the development of A. agrestis as an experimental system and compare it with other plant model systems. We also discuss how A. agrestis can help to further research in comparative developmental studies across land plants and to solve key questions of plant biology associated with the colonization of the terrestrial environment. Finally, we explore the significance of A. agrestis in crop improvement and synthetic biology applications in general.

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“…Data from the Arctic Ocean revealed that approximately 50 mya, an abundance of Azolla characterized an 800 000‐year interval called the “ Azolla event,” which possibly had a role in global cooling by sequestering atmospheric carbon dioxide (Brinkhuis et al., 2006; Speelman et al., 2009). Azolla is further remarkable due to its obligate symbiosis with the N‐fixing cyanobacterium Nostoc azollae in specialized leaf cavities (de Vries et al., 2018; de Vries & de Vries, 2022; Li et al., 2018). Ceratopteris richaridii is also adapted to water and is known as the genetically tractable fern model organism (“C‐Fern”; Plackett et al., 2015) and as a teaching tool in biology (Renzaglia & Warne, 1995).…”

Section: Introductionmentioning

confidence: 99%

Fern cell walls and the evolution of arabinogalactan proteins in streptophytes

et al. 2023

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Significant changes have occurred in plant cell wall composition during evolution and diversification of tracheophytes. As the sister lineage to seed plants, knowledge on the cell wall of ferns is key to track evolutionary changes across tracheophytes and to understand seed plant-specific evolutionary innovations. Fern cell wall composition is not fully understood, including limited knowledge of glycoproteins such as the fern arabinogalactan proteins (AGPs). Here, we characterize the AGPs from the leptosporangiate fern genera Azolla, Salvinia, and Ceratopteris. The carbohydrate moiety of seed plant AGPs consists of a galactan backbone including mainly 1,3-and 1,3,6-linked pyranosidic galactose, which is conserved across the investigated fern AGPs. Yet, unlike AGPs of angiosperms, those of ferns contained the unusual sugar 3-Omethylrhamnose. Besides terminal furanosidic arabinose, Ara (Araf), the main linkage type of Araf in the ferns was 1,2-linked Araf, whereas in seed plants 1,5-linked Araf is often dominating. Antibodies directed against carbohydrate epitopes of AGPs supported the structural differences between AGPs of ferns and seed plants. Comparison of AGP linkage types across the streptophyte lineage showed that angiosperms have rather conserved monosaccharide linkage types; by contrast bryophytes, ferns, and gymnosperms showed more variability. Phylogenetic analyses of glycosyltransferases involved in AGP biosynthesis and bioinformatic search for AGP protein backbones revealed a versatile genetic toolkit for AGP complexity in ferns. Our data reveal important differences across AGP diversity of which the functional significance is unknown. This diversity sheds light on the evolution of the hallmark feature of tracheophytes: their elaborate cell walls.

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Evolutionary genomic insights into cyanobacterial symbioses in plants

Cited by 19 publications

References 134 publications

Phylometagenomics of cycad coralloid roots reveals shared symbiotic signals

Phylometagenomics of cycad coralloid roots reveals shared symbiotic signals

What can hornworts teach us?

Fern cell walls and the evolution of arabinogalactan proteins in streptophytes

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