Dynamic acclimation of photosynthesis increases plant fitness in changing environments

Abstract

Plants growing in different environments develop with different photosynthetic capacities--developmental acclimation of photosynthesis. It is also possible for fully developed leaves to change their photosynthetic capacity--dynamic acclimation. The importance of acclimation has not previously been demonstrated. Here, we show that developmental and dynamic acclimation are distinct processes. Furthermore, we demonstrate that dynamic acclimation plays an important role in increasing the fitness of plants in natural environments. Plants of Arabidopsis (Arabidopsis thaliana) were grown at low light and then transferred to high light for up to 9 d. This resulted in an increase in photosynthetic capacity of approximately 40%. A microarray analysis showed that transfer to high light resulted in a substantial but transient increase in expression of a gene, At1g61800, encoding a glucose-6-phosphate/phosphate translocator GPT2. Plants where this gene was disrupted were unable to undergo dynamic acclimation. They were, however, still able to acclimate developmentally. When grown under controlled conditions, fitness, measured as seed output and germination, was identical, regardless of GPT2 expression. Under naturally variable conditions, however, fitness was substantially reduced in plants lacking the ability to acclimate. Seed production was halved in gpt2- plants, relative to wild type, and germination of the seed produced substantially less. Dynamic acclimation of photosynthesis is thus shown to play a crucial and previously unrecognized role in determining the fitness of plants growing in changing environments.

Figure 1.

Dynamic photosynthetic acclimation in Arabidopsis. A, Maximum photosynthetic capacity, measured at 1,500 μmol m⁻² s⁻¹ white light and 2,000 μL L⁻¹ CO₂ in eight accessions of Arabidopsis grown for 8 weeks at an irradiance of 100 μmol m⁻² s⁻¹ and then maintained in the same conditions (white bars) or transferred to 400 μmol m⁻² s⁻¹ light (hatched bars) for 9 d. Accessions measured were Ws-2, Col-0, Landsberg erecta (Ler), Nossen (No), Oystese (Oy), Martuba (Mt), Cape Verdi Island (Cvi), and C24. Asterisk (*) indicates that treated plants differ significantly from their respective control (P < 0.05). B, Changes in maximum rate of photosynthesis in Ws following a step increase in light from 100 to 400 μmol m⁻² s⁻¹ (black circles) compared to plants maintained at 100 μmol m⁻² s⁻¹ (white circles). C, Net CO₂ assimilation of Ws as a function of irradiance, in plants grown at 100 μmol m⁻² s⁻¹ (white circles) or transferred to 400 μmol m⁻² s⁻¹ (black circles) for 9 d. All data represent the mean (±se) of at least three replicates.

Figure 2.

GPT2 expression in photosynthetic acclimation. A, GPT2 expression in Ws following transition from 100 to 400 μmol m⁻² s⁻¹ light. Expression was quantified using real-time RT-PCR and normalized to ACT2 (At3g18780). B, Expression of GPT2 transcript estimated using RT-PCR, in plants grown for 8 weeks at 100 μmol m⁻² s⁻¹ light and then transferred to 400 μmol m⁻² s⁻¹ for 4 h. Wt, Ws wild type; gpt2−, plants from line FLAG_326E03 with a homozygous insertion in the gene At1g61800; gpt2+, plants from the same seed stock, characterized as lacking a T-DNA insertion in the GPT2 gene. C, Acclimation in plants from line FLAG_326E03 characterized as homozygote wild type (circles) or carrying a homozygote insertion in the GPT2 gene (triangles) and either maintained at 100 μmol m⁻² s⁻¹ (white symbols) or transferred to 400 μmol m⁻² s⁻¹ for 9 d (black symbols). D, Photosynthetic capacity of plants grown for 8 weeks at 100 μmol m⁻² s⁻¹ (white bars), grown at 100 μmol m⁻² s⁻¹ and then transferred to 400 μmol m⁻² s⁻¹ (hatched bars) or grown from seed at 400 μmol m⁻² s⁻¹ (gray bars) in plants of Ws wild type, gpt2− homozygote mutant, and in the mutant complemented with the wild-type GPT2 gene (comp). Quantitative data show the mean (±se) of at least three replicates. [See online article for color version of this figure.]

Figure 3.

Plant fitness in controlled and variable growth environments. A, Seed output per plant, estimated as the product of silique number and mean number of seeds per silique of plants of Ws (white bars), Ws gpt2− (hatched bars), Col (Col0; cross-hatched bars), and of the Ws gpt2− complemented mutant (Comp; black bars) grown under laboratory conditions (Lab) or in the greenhouse during the winters 2007 to 2008 and 2008 to 2009. B, Changes in total aboveground biomass of Ws (white symbols) and gpt2− (black symbols) during growth in the greenhouse in the winter of 2007 to 2008. C, Time to flowering in Ws, gpt2−, Col, and the complemented mutant grown under laboratory conditions and in the greenhouse in 2007 to 2008 and 2008 to 2009 (bar shading as in A). D, Germination of seeds of Ws and gpt2− originating from plants grown under laboratory conditions or in the greenhouse during the winter 2007 to 2008 or 2008 to 2009 (bar shading as in A). All data show the mean (±se) of at least 15 plants.