Dataset Information

Lack of a universal genomic toolkit for animal terrestrialisation

ABSTRACT: Animal terrestrialisation, the transition from aquatic to land environments, is one of the most impactful events in animal evolution, having occurred independently across several phyla. Yet, whether these transitions relied on a conserved genomic toolkit remains unexplored. To address this gap, we integrated large-scale comparative genomics and machine learning from close to 1,000 animal genomes with experimentally induced abiotic stress responses, transcriptomics, and proteomics across diverse aquatic and terrestrial invertebrates. Here, we show that no universal genetic toolkit underlies animal terrestrialisation. Instead, species-specific gene coexpression networks inferred from stress experiments, mimicking key selective pressures related to life on land (e.g., exposure to UV-B light, osmotic stress, and different oxygen availability), revealed hub genes that were largely unique to each lineage. Despite this divergence, independent lineages co-opted distinct sets of ancient gene families, most predating terrestrial life, resulting in functionally convergent genomic responses. This pattern was congruent with phylogenomic analyses, which indicated that most gene families originated early in animal evolution, with limited gene gain and extensive gene loss associated with the emergence of terrestrial lineages. Machine learning identified a small set of gene families predictive of habitat type, enriched in stress-related functions such as cytochrome P450 metabolism and vitamins A and E. Many of these also functioned as hub genes in the coexpression networks, linking them to key positions in species-specific regulatory architectures. These findings challenge the notion of a shared terrestrialisation program and instead reveal a model of functional convergence through lineage-specific genomic repurposing of ancient genes.

INSTRUMENT(S):

ORGANISM(S): Ligia Oceanica Siphonaria Pectinata Schmidtea Mediterranea (freshwater Planarian Flatworm) Leptonemertes Chalicophora Caenorhabditis Elegans Phorcus Turbinatus Physella Hirudo Medicinalis Lineus Sanguineus Ooperipatellus Viridimaculatus Obama Nungara Porcellio Scaber Theba Pisana Arenicola Marina Litoditis Marina Eisenia Fetida

TISSUE(S): Multicellular Organism

SUBMITTER: Cristina Chiva

LAB HEAD: Rosa Fernández

PROVIDER: PXD064337 | Pride | 2026-06-15

REPOSITORIES: Pride

ACCESS DATA

Dataset's files

Source:

			Action	DRS
	2023MQ065_RQGA_001_01_1ug.raw	Raw
	2023MQ065_RQGA_002_01_1ug.raw	Raw
	2023MQ065_RQGA_003_01_1ug.raw	Raw
	2023MQ065_RQGA_TPIS-S1-S3-DB-2501.pdResult	Other
	2023MQ066_RQGA_001_01_1ug.raw	Raw

Items per page:

1 - 5 of 65

Similar Datasets

Project description:During the evolution of life on Earth, the conquest of land by plants played a pivotal role producing a boost in land biomass, a substantial drop in atmospheric CO2, an increase in oxygen and the emergence of new terrestrial habitats facilitating land colonization by animals. Therefore, the characterization of the molecular mechanisms that allowed plant terrestralization is a cornerstone in evolutionary studies. Viridiplantae or the green lineage is divided into two clades Chlorophyta or green microalgae and Streptophyta that in turn splits into Embryophyta or land plants and Charophyta. The latest are mainly considered aquatic algae although some facultative terrestrial species has been identified. Charophyta are generally accepted as the extant algal species most closely related to current land plants and, therefore, they are used in evolutionary studies on plant terrestralization. High light irradiance was one of the major stressors that ancestral charophytic algae needed to overcome during the transition from aquatic to terrestrial environments. In this study, we have chosen the facultative terrestrial early charophytic alga Klebsormidium nitens to perform an integrative transcriptomic and metabolomic analysis under high light in order to unveil key mechanisms involved in the early steps of plants terrestralization. We found a fast chloroplast retrograde signaling possibly mediated by reactive oxygen species and the inositol polyphosphate 1-phosphatase (SAL1) and 3′-phosphoadenosine-5′-phosphate (PAP) pathways inducing gene expression and accumulation of specific metabolites. Systems used by both Chlorophyta and Embryophyta were activated such as the xanthophyll cycle with an accumulation of zeaxanthin and protein folding and repair mechanisms constituted by NADPH-dependent thioredoxin reductases, thioredoxin-disulfide reductases and peroxiredoxins. Similarly, cyclic electron flow, specifically the pathway dependent on Proton Gradient Regulation 5, was strongly activated under high light. We detected a simultaneous co-activation of the non-photochemical quenching mechanisms based on LHC-like Stress Related protein and the photosystem II subunit S that are specific to Chlorophyta and Embryophyta respectively. Exclusive Embryophyta systems for the synthesis, sensing and response to the phytohormone auxin were also activated under high light in Klebsormidium leading to an increase in auxin content with the concomitant accumulation of amino acids such as tryptophan, histidine and phenylalanine.

Project description:Study abstract: Axolotl salamanders (Ambystoma mexicanum) remain aquatic in their natural state, during which biomechanical forces on their diarthrodial limb joints are likely reduced relative to salamanders living on land. However, even as sexually mature adults, these amphibians can be induced to metamorphose into a weight-bearing terrestrial stage by environmental stress or the exogenous administration of thyroxine hormone. In some respects, this aquatic to terrestrial transition of axolotl salamanders through metamorphosis may model developmental and changing biomechanical skeletal forces in mammals during the prenatal to postnatal transition at birth and in the early postnatal period. To assess differences in the appendicular skeleton as a function of metamorphosis, anatomical and gene expression parameters were compared in skeletal tissues between aquatic and terrestrial axolotls that were the same age and genetically full siblings. The length of long bones and area of cuboidal bones in the appendicular skeleton, as well as the cellularity of cartilaginous and interzone tissues of femorotibial joints were generally higher in aquatic axolotls compared to their metamorphosed terrestrial siblings. A comparison of steady state mRNA transcripts encoding aggrecan core protein (ACAN), type II collagen (COL2A1), and growth and differentiation factor 5 (GDF5) in femorotibial cartilaginous and interzone tissues did not reveal any significant differences between aquatic and terrestrial axolotls. RNAseq samples: Total RNA was isolated from whole body tissue samples of Mexican axolotl salamanders (Ambystoma mexicanum) at the following developmental stages: Embryo at the tail bud stage, newly hatched larva, larva at the limb bud stage, juvenile at 8.5 centimeters, and adult using variations of guanidinium-based protocols. RNA quantity, purity, and integrity of both the individual samples and the resulting pool were determined with an Agilent 2100 Bioanalyzer using the Eukaryotic Total RNA nano series II analysis kit. The pooled RNA sample was poly-A selected and used for Illumina random priming directional library prep. Four lanes were sequenced only on one end providing single end reads and 4 lanes were sequenced at both ends giving paired-end reads. The library was sequenced on an Illumina HiSeq 2000 for 75bp reads producing 147,248,512 single end reads and 2 x 153,254,667 paired-end reads.

Dataset Information

Lack of a universal genomic toolkit for animal terrestrialisation

Dataset's files

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets