Abstract
Atmospheric carbon dioxide (CO2 ) directly determines the rate of plant photosynthesis and indirectly effects plant productivity and fitness and may therefore act as a selective pressure driving evolution, but evidence to support this contention is sparse. Using Plantago lanceolata L. seed collected from a naturally high CO2 spring and adjacent ambient CO2 control site, we investigated multigenerational response to future, elevated atmospheric CO2 . Plants were grown in either ambient or elevated CO2 (700μmolmol-1 ), enabling for the first time, characterization of the functional and population genomics of plant acclimation and adaptation to elevated CO2 . This revealed that spring and control plants differed significantly in phenotypic plasticity for traits underpinning fitness including above-ground biomass, leaf size, epidermal cell size and number and stomatal density and index. Gene expression responses to elevated CO2 (acclimation) were modest [33-131 genes differentially expressed (DE)], whilst those between control and spring plants (adaptation) were considerably larger (689-853 DE genes). In contrast, population genomic analysis showed that genetic differentiation between 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. An unusual phenotype of increased stomatal index in spring but not control plants in elevated CO2 correlated with altered expression of stomatal patterning genes between spring and control plants for three loci (YODA, CDKB1;1 and SCRM2) and between ambient and elevated CO2 for four loci (ER, YODA, MYB88 and BCA1). We propose that the two positive regulators of stomatal number (SCRM2) and CDKB1;1 when upregulated act as key controllers of stomatal adaptation to elevated CO2 . Combined with significant transcriptome reprogramming of photosynthetic and dark respiration and enhanced growth in spring plants, we have identified the potential basis of plant adaptation to high CO2 likely to occur over coming decades.
Highlights
Since industrialization, global atmospheric CO2 concentrations ([CO2]) have risen steadily from ca. 280 ppm to present-day concentrations of ca. 400 ppm and are predicted to rise to between 700 and 900 ppm
Single leaf dry mass showed a significant location effect (P < 0.05), with the spring plants having consistently greater single leaf dry mass across CO2 treatments
Past studies show that the majority of plants exposed to elevated [CO2] have reduced numbers of stomata (measured as stomatal index (SI) or density (Hetherington & Woodward, 2003), here we found SI was significantly increased for spring plants in response to exposure to elevated [CO2] (Fig. 1h, i), a finding reported previously in P. lanceolata (Marchi et al, 2004) Up to 30% of species within certain subclasses show increased and not decreased stomatal density (SD) and index in response to elevated [CO2] (Woodward & Kelly, 1995), as well as cases of greater SD within naturally high CO2 springs, and that the finding here for P. lanceolata was observed in three separate experiments and is robust and should be considered further
Summary
Global atmospheric CO2 concentrations ([CO2]) have risen steadily from ca. 280 ppm to present-day concentrations of ca. 400 ppm and are predicted to rise to between 700 and 900 ppm. The small number of studies provided inconclusive findings (Leakey & Lau, 2012) This is surprising given the elevated [CO2] including Bromus madritensis exposed for several years to elevated [CO2] in a free-air CO2 enrichment (FACE) experiment and subjected to either ambient or elevated CO2 in a controlled environment. These experiments suggest strongly that plants are likely to show adaptive responses to this important facet of the changing climate but that as yet, these responses are not fully understood. Few multigenerational exposures to elevated CO2 have been undertaken Coupled with this is the limited genomic and genetic characterization of plants from long-term experiments. The availability of new molecular tools, in particular high-throughput and inexpensive RNA and DNA sequencing, suggests that this bottleneck may be addressed using previously impossible approaches that combine phenotyping, functional genomic and population genetic analysis in nonmodel systems
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