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Biology subjects

Osborne, C. P.

Publications and source records attributed to Osborne, C. P..

7 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↗

Future heatwave conditions inhibit CO2-induced stomatal closure in wheat

Rising atmospheric CO2 concentrations are driving ongoing climatic changes, leading to agricultural crops increasingly experiencing extreme weather events1. Stomata serve as gatekeepers on plant leaves, regulating both CO2 capture for photosynthesis and the concomitant release of water. At higher CO2 concentrations or higher vapour pressure deficit (VPD), stomatal pores narrow, reducing stomatal conductance to water vapour (gsw) and transpiration (E)2-6. Increasing temperatures and/or nitrogen fertilisation promote an opposite stomatal response, enhancing gsw and E7,8. With atmospheric CO2 concentration, temperature and VPD predicted to rise throughout this century1, it is unclear how crops will modify stomatal gaseous exchanges, particularly under differing N-fertilisation regimes. Here, we show in wheat (Triticum aestivum), that elevated CO2 does not reduce gsw or E during heatwaves when VPD is high, instead plant water usage increases. High-VPD heatwave events also impact stomatal responsiveness to N-fertiliser application, prompting significantly higher gas exchange contributions from abaxial leaf surfaces, irrespective of CO2 growth conditions. Dynamic stomatal responsiveness to light and high CO2 are also attenuated during heatwaves in a CO2-independent manner. Taken together, our data suggests that future wheat crops will use significantly more water during heatwaves than might be expected, which has substantial implications for future global food security.

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↗

Implementing a framework of carbon and nitrogen feedback responses into a plant resource allocation model

O_LIThe allocation of resources to roots and shoots can greatly alter total plant mass. Allocation is thought to be the consequence of growth processes (i.e uptake rates, transport rates, growth rates) and the communication between them via signalling mechanisms. Feedbacks that alter growth processes are induced in nature by changes in the internal pools of carbon and nitrogen, but how these function together to define allocation remains unclear. C_LIO_LIWe introduce a framework model of internal feedback responses to changes in plant carbon and nitrogen concentrations. We evaluate how well the model responds to changes in carbon and nitrogen availability by simulating external environmental perturbations that influence the uptake of resources. C_LIO_LIThe model reflects experimental results when looking at the effect of atmospheric CO2 and soil nitrogen concentrations on total plant mass and replicates observed responses to leaf defoliation events. Overall this shows that a combination of known signalling mechanisms are sufficient to reproduce experimentally observed responses to external resource availability. C_LIO_LIModel simulations highlight key areas of uncertainty where more empirical data is needed. In particular, quantitative data is needed to establish the strengths and rates at which feedback responses to carbon and nitrogen substrate concentrations alter growth and uptake rates. C_LI

plant 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↗

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↗

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↗