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Evolvability and drivers of photosynthetic transitions in flowering plants

Final Report Summary - PHOTOTRANS (Evolvability and drivers of photosynthetic transitions in flowering plants)

Executive Summary:

The functional diversification of organisms and their adaptation to changing environmental conditions has often involved the acquisition of novel traits, some of which are of impressive complexity. The capacity to evolve such traits varies among organisms, but the factors determining whether particular lineages evolve novel complex traits are still poorly understood. In this project, we studied the factors that determine the evolvability of alternative photosynthetic pathways, such as C4 photosynthesis and CAM photosynthesis. These traits are complex assemblages of anatomical and biochemical novelties that result in the concentration of CO2 before its fixation by the ancestral photosynthetic machinery. The CO2-concentrating mechanisms (CCM) operate spatially within the leaf of C4 plants, and temporally in CAM plants. They provide an advantage warm and dry habitats. Despite their complexity, these traits have each evolved numerous times independently within flowering plants. Transitions between photosynthetic types are however not randomly distributed among groups of plants and while some lineages completely lack CCMs, others include a large number of C4 plants, CAM plants, or both.

The Phototrans project aimed to understand the factors determining the evolvability of alternative photosynthetic pathways in flowering plants. Phylogenetic methods were used to establish the relationships between species with different photosynthetic types, to reconstruct the timing of photosynthetic transitions, and to test for the effect of different factors on the evolvability of alternative photosynthetic pathways.

Phylogenetic analyses showed that C4 photosynthesis evolved numerous times independently in flowering plants. Although they were spread through time, all these origins happened during the past 35 million years. Statistical modelling suggested that a decrease of atmospheric CO2 concentration during the Oligocene created the general precondition for C4 evolution. This event was however not sufficient for C4 to evolve. The acquisition of the C4 pathway was possible only in plant lineages with a suitable foliar anatomy. At the time CO2 levels became low enough to favour C4 evolution, such anatomy was restricted to certain lineages due to independent alterations of the size and number of different types of cells during the evolutionary diversification of plants.

Besides anatomical preconditions, we showed the existence of genomic preconditions using transcriptomics and genomics. Most C4 and CAM enzymes are encoded by multigene families, with different genes encoding different isoforms that vary in their function, but also their expression pattern and catalytic properties. Despite the existence of numerous gene lineages in grass genomes, three independent C4 origins co-opted the exact same genes for the C4 function. This recruitment bias could be due to predispositions of the expression patterns, the isoforms already expressed in leaves of C3 plants being preferentially co-opted for C4 photosynthesis. This bias in recruitment extends to CAM lineage. Indeed, we have shown that independent origins of both CAM and C4 photosynthesis in Caryophyllales co-opted the same genes for a function in CCMs, suggesting that both photosynthetic types might rely on similar genomic preconditions.

Detailed investigations of some groups of grasses with an exceptional diversity of photosynthetic types revealed multiple C4 origins from recent ancestors with suitable foliar anatomies. In several instances, evolution of the C4 machinery was fuelled by the acquisition of genes already optimized for the C4 pathway in other species. These findings highlight the importance of non-vertical gene transmission for adaptation, but the mechanisms behind these gene transfers between closely and distantly related species are still to be elucidated.

The phylogenetic investigations performed during this project at broad and fine taxonomic scales together show that the astonishing number of convergent photosynthetic transitions results from a combination of anatomical and genomic preconditions, and lateral gene transfers, which strongly increased the capacity of some lineages of plants to adapt to environmental changes during the last tens of millions of years.