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Christin, P.-A.

Publications and source records attributed to Christin, P.-A..

10 recordsLinked to original sources

Gene turnover and contingency facilitated the repeated evolution of C4 photosynthesis in grasses

SummaryO_LIIn grasses, almost all species belong to two evenly sized clades (BOP and PACMAD), yet the >20 independent origins of C4 photosynthesis in this family only occur in the PACMAD lineage. Here, we identify potential genetic precursors for C4 photosynthesis that were present at the base of the PACMAD clade, representing the last common ancestor of all C4 grasses. C_LIO_LIWe generated the first reference genomes for Aristidoideae species (Aristida adscensionis and Stipagrostis hirtigluma), the sister lineage of all other PACMAD grasses. In combination with 34 other Poales genomes, we identify gene gains at the base of the PACMAD clade, and genes lost in the sister BOP lineage. C_LIO_LICandidate C4 precursors include {beta}-carbonic anhydrase, as well as genes involved in amino acid and nitrate transport, carbon metabolism, oxidative stress management and transcription regulation. C_LIO_LIGene turnover created the necessary genetic contingency, facilitating the independent recruitment and refinement of C4 genes in multiple independent origins. Our results support the idea that the repeated evolution of C4 photosynthesis in PACMAD grasses was not driven by a single genetic event but was instead underwritten by chance genetic changes that originated long before there was selection for the trait itself. C_LI

evolutionary biology↗

Nuclear phylogenomics of grasses (Poaceae) supports current classification and reveals repeated reticulation

O_LIGrasses (Poaceae) comprise around 11,800 species and are central for human livelihoods and terrestrial ecosystems. Knowing their relationships and evolutionary history is key to comparative research and crop breeding. Advances in genome-scale sequencing allow for increased breadth and depth of phylogenomic analyses, making it possible to infer a new reference species tree of the family. C_LIO_LIWe inferred a comprehensive species tree of grasses by combining new and published sequences for 331 nuclear genes from genome, transcriptome, target enrichment and shotgun data. Our 1,153-tip tree covers 79% of grass genera (including 21 genera sequenced for the first time) and all but two small tribes. We compared it to a 910-tip plastome tree. C_LIO_LIThe nuclear phylogeny matches that of the plastome at most deep branches, with only a few instances of incongruence. Gene tree-species tree reconciliation suggests that reticulation events occurred repeatedly in the history of grasses. C_LIO_LIWe provide a robust framework for the grass tree of life to support research on grass evolution, including modes of reticulation, and genetic diversity for sustainable agriculture. C_LI

plant biology↗

Identifying leaf anatomy and metabolic regulators that underpin C4 photosynthesis in Alloteropsis semialata

O_LIC4 photosynthesis is a complex trait requiring multiple developmental and metabolic alterations. Despite this complexity, it has independently evolved over 60 times. However, our understanding of the transition to C4 is complicated by the fact that variation in photosynthetic type is usually segregated between species. C_LIO_LIHere, we perform a genome wide association study (GWAS) using the grass Alloteropsis semialata, the only known species to have C3, intermediate, and C4 accessions. We aimed to identify genomic regions associated with the strength of the C4 cycle (measured using {delta}13C), and the development of C4 leaf anatomy. C_LIO_LIGenomic regions correlated with {delta}13C include regulators of C4 decarboxylation enzymes (RIPK), non-photochemical quenching (SOQ1), and the development of Kranz anatomy (SCARECROW-LIKE). Regions associated with the development of C4 leaf anatomy in the intermediate accessions contain additional leaf anatomy regulators, including those responsible for vein patterning (GSL8) and meristem determinacy (GRF1). C_LIO_LIThe detection of highly correlated genomic regions with a modest sample size indicates that the emergence of C4 photosynthesis in A. semialata required a few loci of large effect. The candidate genes could prove to be relevant for engineering C4 leaf anatomy in C3 species. C_LI

plant biology↗

Variation in the rate lateral gene transfers accumulate in a grass lineage

Lateral gene transfer (LGT) has been reported in multiple eukaryotes. This process seems particularly widespread in the grass family, although we know very little about the underlying dynamics and how it impacts gene content variation within a species. Alloteropsis semialata is a tropical grass, and multiple LGT were detected in a reference genome assembled from an Australian individual. As part of this study we assemble three additional de novo genomes for A. semialata and one for its sister species Alloteropsis angusta. In total we detect 168 LGT across the five reference genomes. Using whole-genome resequencing data for a further 40 individuals we establish the distribution of these transfers and map their origin along the species phylogeny. This shows that many LGTs were acquired relatively recently, with numerous secondary losses. Exponential decay models indicate that the rate of LGT acquisitions varied significantly among lineages [6-28 per Ma], with a high rate of subsequent LGT losses [11-24% per Ma] that largely exceeds that of native loci [0.02-0.8% per Ma]. This high turnover creates large intraspecific structural variants, with a preponderance of LGT occurring as accessory genes in the Alloteropsis pangenome. The acquired genes represent unparalleled genetic novelties, having independently evolved for tens of millions of years before they were transferred. Ultimately, the rapid LGT turnover generates standing variation that can fuel local adaptation.

evolutionary biology↗

Upregulation of C4 characteristics does not consistently improve photosynthetic performance in intraspecific hybrids of a grass

C4 photosynthesis is thought to have evolved via intermediate stages, with changes towards the C4 phenotype gradually enhancing photosynthetic performance. This hypothesis is widely supported by modelling studies, but experimental tests are missing. Mixing of C4 components to generate artificial intermediates can be achieved via crossing, and the grass Alloteropsis semialata represents an outstanding system since it includes C4 and non-C4 populations. Here, we analyse F1 hybrids between C3 and C4, and C3+C4 and C4 genotypes to determine whether the acquisition of C4 characteristics increases photosynthetic performance. The hybrids have leaf anatomical characters and C4 gene expression profiles that are largely intermediate between those of their parents. Carbon isotope ratios are similarly intermediate, which suggests that a partial C4 cycle coexists with C3 carbon fixation in the hybrids. This partial C4 phenotype is associated with C4-like photosynthetic efficiency in C3+C4 x C4, but not in C3 x C4 hybrids, which are overall less efficient than both parents. Our results support the hypothesis that the photosynthetic gains from the upregulation of C4 characteristics depend on coordinated changes in anatomy and biochemistry. The order of acquisition of C4 components is thus constrained, with C3+C4 species providing an essential step for C4 evolution.

plant biology↗

Hybridisation boosts dispersal of two contrasted ecotypes in a grass species

O_LIIn the absence of strong reproductive barriers, genetic exchanges between closely related groups of organisms with different adaptations have well-documented beneficial and detrimental consequences. In plants, pollen-mediated exchanges affect the sorting of alleles across physical landscapes, and influence rates of hybridisation. How these dynamics affect the emergence and spread of novel ecological strategies remains only partially understood. C_LIO_LIWe use phylogenomics and population genomics to retrace the origin of two geographically overlapping ecotypes of the African grass Alloteropsis angusta. C_LIO_LIWe report the existence of a previously undescribed ecotype inhabiting miombo woodlands and grasslands. The two ecotypes have divergent nuclear genomes. However, the seed-transported chloroplast genomes are consistently shared by distinct ecotypes inhabiting the same region. These patterns suggest that the nuclear genome of one ecotype can reach the seeds of the other via pollen movements, with strong selection subsequently sorting nuclear alleles by habitat. C_LIO_LIThe contrasting ecotypes of A. angusta can use each other as a gateway to new locations across a large part of Africa. Coupled with newly discovered hybridisation with the sister species A. semialata, our results show that hybridisation can facilitate the geographical dispersal of distinct ecotypes of the same grass species. C_LI

evolutionary biology↗

Physiological diversity enhanced by recurrent divergence and secondary gene flow within a grass species

O_LIC4 photosynthesis evolved multiple times independently in angiosperms, but most origins are relatively old so that the early events linked to photosynthetic diversification are blurred. The grass Alloteropsis semialata is an exception, as this single species encompasses C4 and non-C4 populations. C_LIO_LIUsing phylogenomics and population genomics, we infer the history of dispersal and secondary exchanges before, during, and after photosynthetic divergence in A. semialata. We further establish the genetic origins of polyploids in this species. C_LIO_LIOrganelle phylogenies indicate limited seed dispersal within the Central Zambezian region of Africa, where the species originated [~] 2-3 Ma. Outside this region, the species spread rapidly across the paleotropics to Australia. Comparison of nuclear and organelle phylogenies and analyses of whole genomes reveal extensive secondary gene flow. In particular, the genomic group corresponding to the C4 trait was swept into seeds from distinct geographic regions. Multiple segmental allopolyploidy events mediated additional secondary genetic exchanges between photosynthetic types. C_LIO_LILimited dispersal and isolation allowed lineage divergence, while episodic secondary exchanges led to the pollen-mediated, rapid spread of the derived C4 physiology. Overall, our study suggests that local adaptation followed by recurrent secondary gene flow promoted physiological diversification in this grass species. C_LI

evolutionary biology↗

Phylogenetic relatedness, co-occurrence, and rhizomes increase lateral gene transfer among grasses

O_LILateral gene transfer (LGT) has been documented in a broad range of prokaryotes and eukaryotes, and it can promote adaptation. LGT of functional nuclear genes has been reported among some plants, but systematic studies are needed to assess the frequency and facilitators of LGT in the group. C_LIO_LIWe scan the genomes of a diverse set of 17 grass species that span more than 50 million years of divergence and include major crops to identify grass-to-grass protein-coding LGT. C_LIO_LIWe identify LGT in 13 species, with significant variation in the amount each received. Rhizomatous species acquired statistically more genes, probably because this growth habit boosts opportunities for transfer into the germline. In addition, the amount of LGT increases with phylogenetic relatedness, which might reflect genomic compatibility amongst close relatives facilitating successful transfers. However, genetic exchanges among highly divergent species with overlapping distributions also occur, pointing to an additional role of biogeography. C_LIO_LIOverall, we show that LGT is a widespread phenomenon in grasses, which has moved functional genes across the entire grass family into domesticated and wild species alike. The dynamics of successful LGT appears to be dependent on both opportunity (co-occurrence and rhizomes) and compatibility (phylogenetic distance). C_LI

evolutionary biology↗

Phylogenomics supports a Cenozoic rediversification of the "living fossil" Isoetes

The fossil record provides an invaluable insight into the temporal origins of extant lineages of organisms. However, establishing the relationships between fossils and extant lineages can be difficult in groups with low rates of morphological change over time. Molecular dating can potentially circumvent this issue by allowing distant fossils to act as calibration points, but rate variation across large evolutionary scales can bias such analyses. In this study, we apply multiple dating methods to genome-wide datasets to infer the origin of extant species of Isoetes, a group of mostly aquatic and semi-aquatic isoetalean lycopsids, which closely resemble fossil forms dating back to the Triassic. Rate variation observed in chloroplast genomes hampers accurate dating, but genome-wide nuclear markers place the origin of extant diversity within this group in the mid-Paleogene, 45-60 million years ago. Our genomic analyses coupled with a careful evaluation of the fossil record indicate that despite resembling forms from the Triassic, extant Isoetes species do not represent the remnants of an ancient and widespread group, but instead have spread around the globe in the relatively recent past.

evolutionary biology↗

Biochemical mechanisms driving rapid fluxes in C4 photosynthesis

Biochemical mechanisms driving rapid fluxes in C4 photosynthesis Biochemical mechanisms driving... Modeling Plant growth RNA-seq Enzyme measurements Quantum yield measurements Data availability Material and Methods References Sufficient flux through pathways is critical to their function within the metabolic network. A high flux cycle called C4 photosynthesis evolved in some plants to combat the slow speed and low specificity of the plants carbon fixation enzyme Rubisco1. In these plants, flux through the C4 photosynthetic cycle eclipses flux through Rubisco making it the highest flux in planta2,3. Engineering efforts are underway ...

plant biology↗