Evidence for plant adaptation to a future high CO₂ world

Abstract

Plant morphology and function are sensitive to rising atmospheric carbon dioxide (CO₂) concentrations, but evidence that CO₂ concentration can act as a selective pressure driving evolution is sparse. Plants originating from naturally high CO₂ springs are subjected to elevated CO₂ concentration over multiple generations, providing an opportunity to predict how adaptation to future atmospheres may occur, with important implications for future plant conservation and crop breeding strategies. Using Plantago lanceolata L. from such a site (the ‘spring’ site) and from an adjacent ambient CO₂ site (‘control’ site), and growing the populations in ambient and elevated CO₂ at 700 ?mol mol-1, I have characterised, for the first time, the functional and population genomics, alongside morphology and physiology, of plant adaptation to elevated CO₂ concentrations. Growing plants in elevated CO₂ caused relatively modest changes in gene expression, with fewer changes evident in the spring than control plants (33 vs 131 genes differentially expressed [DE], in spring and control plants respectively). In contrast, when comparisons were made between control and spring plants grown in either ambient or elevated CO₂, there were a much larger number of loci showing DE (689 in the ambient and 853 in the elevated CO₂ environment). Population genomic analysis revealed that genetic differentiation between the spring and control plants was close to zero with no fixed differences, suggesting that plants are adapted to their native CO₂ environment at the level of gene expression. Growth at elevated CO₂ led to an unusual phenotype, with an increase in stomatal density and index in the spring, but not in control plants. Focussing on previously characterised stomatal patterning genes revealed significant DE (FDR < 0.05) between spring and control plants for three loci (YODA, CDKB1;1, and SCRM2) and between ambient and elevated CO₂ for four (ER, YODA, MYB88, and BCA1). We propose that the up-regulation in spring plants of two positive regulators of stomatal numbers (SCRM2 and CDKB1;1) act here as key controllers of stomatal adaptation to elevated CO₂ on an evolutionary timescale. Significant transcriptome reprogramming of the photosynthetic pathway was identified, with an overall decrease in expression across the pathway in control plants, and an increase in spring plants, in response to elevated CO₂. This was followed up by physiological measurements, where a significant increase (P < 0.05) in photosynthetic capacity and regeneration rate was exhibited in spring plants, compared to control plants, at both elevated and ambient CO₂ concentrations. Through this comprehensive analysis, we have identified the basis of plant adaptation to elevated CO₂ likely to occur in the future.

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ORCID for Mark Chapman: orcid.org/0000-0002-7151-723X

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