Project description:225 years ago, Alexander von Humboldt documented his first observations of a peculiar phenomenon in Clusia rosea (Clusiaceae), the first tree known to perform crassulacean acid metabolism (CAM). Since then, the photosynthetic and ecophysiological plasticity of Clusia species have captivated the minds of plant scientists worldwide. CAM is a physiological adaptation to low water availability. While stomata are closed during the day, RuBisCO is supplied with CO2 via decarboxylation of organic acids that have been stored and synthesized during the night by phosphoenolpyruvate carboxylases (PEPC). How the physiological reprogramming necessary for CAM evolved remains enigmatic. Photosynthetic physiotypes of CAM, including weak CAM, inducible CAM, and CAM-cycling have additionally fueled a debate on the evolutionary constraints of CAM and the prospects of engineering CAM into C3 crops. Here, we de novo sequenced the genomes of three Clusia species to capture genetic snapshots along an evo-ecophysiological continuum from weak over inducible to strong CAM. Through a combination of phased chromosome level assembly and annotation, comparative multiomics, and physiological experiments, we demonstrate that diploidization of polyploids explains the physiotype diversity of CAM. We illustrate that Clusia major, a plant that exhibits a C3-type mode of photosynthesis, retained almost all hallmarks of CAM. Transposon-mediated genic diploidization, however, acted upon homoeologs in CAM-related gene families, preferentially those involved in phosphoenolpyruvate (PEP) recycling via phosphorolytic leaf starch metabolization. In effect this rendered a plant capable of constitutive C3+CAM with open stomata during the day by shifting carbohydrate supply (PEP) to viable soluble sugars. Our findings indicate that polyploidization during genus evolution and subsequent diploidization shaped the emergence of extant C3+CAM physiotypes in Clusia. This study of evolutionary intermediates provides crucial insights into the convergent evolution of physiotype diversity and plasticity of CAM.
Project description:More than 200 years ago, Alexander von Humboldt documented his first observations of a peculiar phenomenon in Clusia rosea (Clusiaceae), the first tree known to perform crassulacean acid metabolism (CAM). Since then, the photosynthetic and ecophysiological plasticity of Clusia species have captivated the minds of plant scientists worldwide. CAM is a physiological adaptation to low water availability. While stomata are closed during the day, RuBisCO is supplied with CO2 via decarboxylation of organic acids that have been stored and synthesized during the night by phosphoenolpyruvate carboxylases (PEPC). How the physiological reprogramming necessary for CAM evolved remains enigmatic. Photosynthetic physiotypes of CAM, including weak CAM, inducible CAM, and CAM-cycling have additionally fueled a debate on the evolutionary constraints of CAM and the prospects of engineering CAM into C3 crops. Here, we de novo sequenced the genomes of three Clusia species to capture genetic snapshots along an evo-ecophysiological continuum from weak over inducible to strong CAM. Through a combination of chromosome level assembly and annotation, comparative multiomics, and physiological phenotyping, we identify a strong association between diploidization of polyploids and the physiotype diversity of CAM. We illustrate that Clusia major, a plant that seems to exhibits a C3-type mode of photosynthesis, retained almost all hallmarks of CAM. Transposon-mediated genic diploidization, however, acted upon homoeologs in CAM-related gene families, particularly those involved in phosphoenolpyruvate (PEP) recycling via phosphorolytic leaf starch metabolization. In effect, this rendered a plant capable of C3+CAM with open stomata during the day by shifting carbohydrate supply (PEP) to viable soluble sugars. Our findings indicate that polyploidization during genus evolution and subsequent diploidization shaped the emergence of extant physiotypes in Clusia.
Project description:Root nodule symbiosis (RNS) represents a significant phenotypic adaptation in plants to thrive in nitrogen-deficient environments. Recent findings propose a single gain of RNS at the crown of the nitrogen-fixing clade (NF clade). However, the genetic mechanisms underlying the origin and subsequent evolution of RNS remain largely unexplored. Here, we newly sequenced and assembled eleven genomes from the NF clade and studied genetic change along the evolution of RNS. Our results elucidated three key evolutionary stages leading to the formation of stable RNS between plants and symbiotic nitrogen-fixing bacteria.
Project description:Root nodule symbiosis (RNS) represents a significant phenotypic adaptation in plants to thrive in nitrogen-deficient environments. Recent findings propose a single gain of RNS at the crown of the nitrogen-fixing clade (NF clade). However, the genetic mechanisms underlying the origin and subsequent evolution of RNS remain largely unexplored. Here, we newly sequenced and assembled eleven genomes from the NF clade and studied genetic change along the evolution of RNS. Our results elucidated three key evolutionary stages leading to the formation of stable RNS between plants and symbiotic nitrogen-fixing bacteria.
Project description:Many aspects of an individual's biology derive from its interaction with symbiotic microbes, which further define many aspects of the ecology and evolution of the host species. The centrality of microbes in the function of individual organisms has given rise to the concept of the holobiont-that an individual's biology is best understood as a composite of the 'host organism' and symbionts within. This concept has been further elaborated to posit the holobiont as a unit of selection. In this review, I critically examine whether it is useful to consider holobionts as a unit of selection. I argue that microbial heredity-the direct passage of microbes from parent to offspring-is a key factor determining the degree to which the holobiont can usefully be considered a level of selection. Where direct vertical transmission (VT) is common, microbes form part of extended genomes whose dynamics can be modelled with simple population genetics, but that nevertheless have subtle quantitative distinctions from the classic mutation/selection model for nuclear genes. Without direct VT, the correlation between microbial fitness and host individual fitness erodes, and microbe fitness becomes associated with host survival only (rather than reproduction). Furthermore, turnover of microbes within a host may lessen associations between microbial fitness with host survival, and in polymicrobial communities, microbial fitness may derive largely from the ability to outcompete other microbes, to avoid host immune clearance and to minimize mortality through phage infection. These competing selection pressures make holobiont fitness a very minor consideration in determining symbiont evolution. Nevertheless, the importance of non-heritable microbes in organismal function is undoubted-and as such the evolutionary and ecological processes giving rise to variation and evolution of the microbes within and between host individuals represent a key research area in biology.
Project description:Angiosperms represent one of the most spectacular terrestrial radiations on the planet1, but their early diversification and phylogenetic relationships remain uncertain2-5. A key reason for this impasse is the paucity of complete genomes representing early-diverging angiosperms. Here, we present high-quality, chromosomal-level genome assemblies of two aquatic species-prickly waterlily (Euryale ferox; Nymphaeales) and the rigid hornwort (Ceratophyllum demersum; Ceratophyllales)-and expand the genomic representation for key sectors of the angiosperm tree of life. We identify multiple independent polyploidization events in each of the five major clades (that is, Nymphaeales, magnoliids, monocots, Ceratophyllales and eudicots). Furthermore, our phylogenomic analyses, which spanned multiple datasets and diverse methods, confirm that Amborella and Nymphaeales are successively sister to all other angiosperms. Furthermore, these genomes help to elucidate relationships among the major subclades within Mesangiospermae, which contain about 350,000 species. In particular, the species-poor lineage Ceratophyllales is supported as sister to eudicots, and monocots and magnoliids are placed as successively sister to Ceratophyllales and eudicots. Finally, our analyses indicate that incomplete lineage sorting may account for the incongruent phylogenetic placement of magnoliids between nuclear and plastid genomes.
Project description:Clarifying the evolutionary processes underlying species diversification and adaptation is a key focus of evolutionary biology. Begonia (Begoniaceae) is one of the most species-rich angiosperm genera with c. 2000 species, most of which are shade-adapted. Here, we present chromosome-scale genome assemblies for four species of Begonia (B. loranthoides, B. masoniana, B. darthvaderiana and B. peltatifolia), and whole genome shotgun data for an additional 74 Begonia representatives to investigate lineage evolution and shade adaptation of the genus. The four genome assemblies range in size from 331.75 Mb (B. peltatifolia) to 799.83 Mb (B. masoniana), and harbor 22 059-23 444 protein-coding genes. Synteny analysis revealed a lineage-specific whole-genome duplication (WGD) that occurred just before the diversification of Begonia. Functional enrichment of gene families retained after WGD highlights the significance of modified carbohydrate metabolism and photosynthesis possibly linked to shade adaptation in the genus, which is further supported by expansions of gene families involved in light perception and harvesting. Phylogenomic reconstructions and genomics studies indicate that genomic introgression has also played a role in the evolution of Begonia. Overall, this study provides valuable genomic resources for Begonia and suggests potential drivers underlying the diversity and adaptive evolution of this mega-diverse clade.