The structure of the Physcomitrium Patens Photosystem I Reveals a Unique Lhca2 Paralogue replacing Lhca4

The moss Physcomitrium patens diverged from green algae shortly after the colonization of land by ancient plants. This colonization posed new environmental challenges which drove evolutionary processes. The photosynthetic machinery of modern flowering plants is adapted to the high light conditions on land. Red shifted Lhca4 antennae are present in the photosystem I light harvesting complex of many green lineage plants but absent from P. patens. The Cryo-EM structure of the P. patens photosystem I light harvesting complex I supercomplex (PSI-LHCI) at 2.8 Å reveals that Lhca4 is replaced by a unique Lhca2 paralogue in moss. This PSI-LHCI supercomplex also retains the PsaM subunit, present in cyanobacteria and several algal species but lost in higher plants, and the PsaO subunit responsible for binding light harvesting complex II. The blue shifted Lhca2 paralogue and chlorophyll b enrichment relative to higher plants make the P. patens PSI-LHCI spectroscopically unique among other green lineage supercomplexes. Overall, the structure represents an evolutionary intermediate PSI with the crescent shaped LHCI common in higher plants and contains a unique Lhca2 paralogue which facilitates the mosses adaptation to low light niches.

Intrasexual cuticular hydrocarbon dimorphism in a wasp sheds light on hydrocarbon biosynthesis genes in Hymenoptera

Cuticular hydrocarbons (CHCs) cover the cuticle of insects and serve as desiccation barrier and for chemical communication. While the main enzymatic steps of CHC biosynthesis are well understood, few of the underlying genes have been identified. Here we show how exploitation of intrasexual CHC dimorphism in a mason wasp, Odynerus spinipes, in combination with whole-genome sequencing and comparative transcriptomics facilitated identification of such genes. RNAi-mediated knockdown of twelve candidate gene orthologs in honey bees, Apis mellifera, confirmed nine genes impacting CHC profile composition. Most of them have predicted functions consistent with current knowledge of CHC metabolism. However, we found first-time evidence for a fatty acid amide hydrolase also influencing CHC profile composition. In situ hybridization experiments furthermore suggest trophocytes participating in CHC biosynthesis. Our results set the base for experimental CHC profile manipulation in Hymenoptera and imply that the evolutionary origin of CHC biosynthesis predates the arthropods' colonization of land.

Divergent evolutionary trajectories of bryophytes and tracheophytes from a complex common ancestor of land plants

The origin of plants and their colonization of land resulted in the transformation of the terrestrial environment. Here we investigate the evolution of the land plants (embryophytes) and their two main lineages, the tracheophytes (vascular plants) and bryophytes (non vascular plants). We used new fossil calibrations, relative lineage dating implied by horizontal gene transfer, and new phylogenomic methods for mapping gene family origins. Distinct rooting strategies resolve tracheophytes and bryophytes as monophyletic sister groups that diverged in the Cambrian, 515-494 Ma. The embryophyte stem is characterised by a burst of gene innovation, while bryophytes subsequently experienced a no less dramatic episode of reductive genome evolution in which they lost genes associated with the elaboration of vasculature and the stomatal complex. Overall, our analyses confirm that extant tracheophytes and bryophytes are both highly derived; as a result, understanding the origin of land plants requires tracing character evolution across the diversity of modern lineages.

Evolution of chlorophyll degradation is associated with plant transition to land

Colonization of land by green plants (Viridiplantae) some 500 million years ago was made possible by large metabolic and biochemical adaptations. Chlorophyll, the central pigment of photosynthesis, is highly photo-active. In order to mitigate deleterious effects of pigment accumulation, some plants have evolved a coordinated pathway to deal with chlorophyll degradation end-products, so-called phyllobilins. This pathway has been so far mostly unravelled in Arabidopsis thaliana. Here, large-scale comparative phylogenomic coupled to an innovative biochemical characterization strategy of phyllobilins allow a better understanding how such a pathway appeared in Viridiplantae. Our analysis reveals a stepwise evolution of the canonical pheophorbide a monooxygenase/phyllobilin pathway. It appears to have evolved gradually, first in chlorophyte’s chloroplasts, to ensure multicellularity by detoxifying chlorophyll catabolites, and in charophytes outside chloroplasts to allow adaptation of embryophytes to land. At least six out of the eight genes involved in the pathway were already present in the last common ancestor of green plants. This strongly suggests parallel evolution of distinct enzymes catalysing similar reactions in various lineages, particularly for the dephytylation step. Together, our study suggests that chlorophyll degradation accompanied the transition from water to land, and was therefore of great importance for plant diversification.

Reproductive colonization of land by frogs: embryos and larvae excrete urea to avoid ammonia toxicity

Vertebrate colonization of land occurred multiple times, including over 50 origins of terrestrial eggs in frogs. Some environmental factors and phenotypic responses that facilitated these transitions are known, but responses to water constraints and risk of ammonia toxicity during early development are poorly understood. We tested if ammonia accumulation and dehydration risk induce a shift from ammonia to urea excretion during in early stages of four anurans, from three origins of terrestrial development. We quantified ammonia and urea concentrations during early development on land, under well-hydrated and dry conditions. Where we found urea excretion, we tested for a plastic increase under dry conditions and with ammonia accumulation in developmental environments. We assessed the potential adaptive role of urea excretion by comparing ammonia tolerance measured in 96h-LC50 tests with ammonia levels in developmental environments. Ammonia accumulated in foam nests and perivitelline fluid, increasing over development and reaching higher concentrations under dry conditions. All four species showed high ammonia tolerance, compared to fishes and aquatic-breeding frogs. Both nest-dwelling larvae of Leptodactylus fragilis and late embryos of Hyalinobatrachium fleischmanni excreted urea, showing a plastic increase under dry conditions. These two species can develop the longest on land and urea excretion appears adaptive, preventing their exposure to potentially lethal levels of ammonia. Neither late embryos of Agalychnis callidryas nor nest-dwelling larvae of Engystomops pustulosus risked toxic ammonia levels under dry conditions, and neither excreted urea. Our results suggests that an early onset of urea excretion, its increase under dry conditions, and elevated ammonia tolerance, can all help prevent ammonia toxicity during terrestrial development. High ammonia represents a general risk for development that can be exacerbated as climate change increases dehydration risk for terrestrial-breeding frogs. It may also be a cue that elicits adaptive physiological responses during early development.

Lipid exchanges drove the evolution of mutualism during plant terrestrialization

Symbiosis with arbuscular mycorrhizal fungi (AMF) improves plant nutrition in most land plants, and its contribution to the colonization of land by plants has been hypothesized. Here, we identify a conserved transcriptomic response to AMF among land plants, including the activation of lipid metabolism. Using gain of function, we show the transfer of lipids from the liverwort Marchantia paleacea to AMF and its direct regulation by the transcription factor WRINKLED (WRI). Arbuscules, the nutrient-exchange structures, were not formed in loss-of-function wri mutants in M. paleacea, leading to aborted mutualism. Our results show the orthology of the symbiotic transfer of lipids across land plants and demonstrate that mutualism with arbuscular mycorrhizal fungi was present in the most recent ancestor of land plants 450 million years ago.

An angiosperm NLR atlas reveals that NLR gene reduction is associated with ecological specialization and signal transduction component deletion

Nucleotide-binding site-leucine-rich repeat receptor (NLR) genes comprise the largest family of plant disease resistance genes. NLR genes are phylogenetically divided into the TNL, CNL, and RNL subclasses. NLR copy numbers and subclass composition vary tremendously across angiosperm genomes. However, the evolutionary associations between genomic NLR content and plant lifestyle, or between NLR content and signal transduction components, are poorly characterized due to limited genome availability. Here, we established an angiosperm NLRatlas (ANNA, http://compbio.nju.edu.cn/app/ANNA/), which includes NLR genes from over 300 angiosperm genomes. Using ANNA, we revealed that NLR copy numbers differ up to 66-fold among closely related species due to rapid gene loss and gain. Interestingly, NLR contraction was associated with adaptations to aquatic, parasitic, and carnivorous lifestyles. The convergent NLR reduction in aquatic plants resembles the long-term evolutionary silence of NLR genes in green algae before the colonization of land. A co-evolutionary pattern between NLR subclasses and plant immune-pathway components was also identified, suggesting that immune pathway deficiencies may drive TNL loss. Finally, we recovered a conserved TNL lineage that may function independently of the RNL pathway. Our findings provide new insights into the evolution of NLR genes in the context of plant lifestyles and genome content variation.

Cryptic terrestrial fungus-like fossils of the early Ediacaran Period

The colonization of land by fungi had a significant impact on the terrestrial ecosystem and biogeochemical cycles on Earth surface systems. Although fungi may have diverged ~1500–900 million years ago (Ma) or even as early as 2400 Ma, it is uncertain when fungi first colonized the land. Here we report pyritized fungus-like microfossils preserved in the basal Ediacaran Doushantuo Formation (~635 Ma) in South China. These micro-organisms colonized and were preserved in cryptic karstic cavities formed via meteoric water dissolution related to deglacial isostatic rebound after the terminal Cryogenian snowball Earth event. They are interpreted as eukaryotes and probable fungi, thus providing direct fossil evidence for the colonization of land by fungi and offering a key constraint on fungal terrestrialization.

Draft genome of the aquatic moss Fontinalis antipyretica (Fontinalaceae, Bryophyta)

Mosses comprise one of three lineages forming a sister group to extant vascular plants. Having emerged from an early split in the diversification of embryophytes, mosses may offer complementary insights into the evolution of traits following the transition to, and colonization of, land. Here, we report the draft nuclear genome of Fontinalis antipyretica (Fontinalaceae, Hypnales), a charismatic aquatic moss that is widespread in temperate regions of the Northern Hemisphere. We sequenced and de novo-assembled its genome using the 10X Genomics method. The genome comprises 385.2 Mbp, with a scaffold N50 of 45.8 Kbp. The assembly captured 87.2% of the 430 genes in the BUSCO Viridiplantae odb10 dataset. The newly generated F. antipyretica genome is the third moss genome, and the second seedless aquatic plant genome, to be sequenced and assembled to date.