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Natural variation in stomatal responses to environmental changes among Arabidopsis thaliana ecotypes.

Takahashi S, Monda K, Negi J, Konishi F, Ishikawa S, Hashimoto-Sugimoto M, Goto N, Iba K - PLoS ONE (2015)

Bottom Line: The stomatal responses to light were also reduced in the three selected ecotypes when compared with Col-0.This study demonstrates that the stomatal responses to CO2 and light share closely associated signaling mechanisms that are not generally correlated with humidity signaling pathways in these ecotypes.The results might reflect differences between ecotypes in intrinsic response mechanisms to environmental signals.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Faculty of Sciences, Kyushu University, Fukuoka, Japan.

ABSTRACT
Stomata are small pores surrounded by guard cells that regulate gas exchange between plants and the atmosphere. Guard cells integrate multiple environmental signals and control the aperture width to ensure appropriate stomatal function for plant survival. Leaf temperature can be used as an indirect indicator of stomatal conductance to environmental signals. In this study, leaf thermal imaging of 374 Arabidopsis ecotypes was performed to assess their stomatal responses to changes in environmental CO2 concentrations. We identified three ecotypes, Köln (Kl-4), Gabelstein (Ga-0), and Chisdra (Chi-1), that have particularly low responsiveness to changes in CO2 concentrations. We next investigated stomatal responses to other environmental signals in these selected ecotypes, with Col-0 as the reference. The stomatal responses to light were also reduced in the three selected ecotypes when compared with Col-0. In contrast, their stomatal responses to changes in humidity were similar to those of Col-0. Of note, the responses to abscisic acid, a plant hormone involved in the adaptation of plants to reduced water availability, were not entirely consistent with the responses to humidity. This study demonstrates that the stomatal responses to CO2 and light share closely associated signaling mechanisms that are not generally correlated with humidity signaling pathways in these ecotypes. The results might reflect differences between ecotypes in intrinsic response mechanisms to environmental signals.

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The phenotype of Kl-4, Ga-0, and Chi-1, which exhibit low CO2 responsiveness.(A) Thermal imaging of the three selected ecotypes Kl-4, Ga-0, Chi-1, and the commonly used ecotype Col-0. Plants were subjected to 0 ppm CO2 for 2 h and then 1,000 ppm CO2 for 1 h at 40% RH. The subtractive image on the right shows that the largest temperature changes were exhibited by Col-0. (B) Time courses of stomatal conductance (gs) in response to changes in CO2 concentration in Kl-4, Ga-0, Chi-1, and Col-0. Col-0 is more responsive to changes in CO2 concentration than Kl-4, Ga-0, Chi-1. (C) Sizes of stomatal apertures at low and high CO2 concentrations. Plants were subjected to 0 ppm CO2 for 2 h and then transferred to 700 ppm CO2 for 1 h at 40% RH with 150 μmol m-2 s-1 photosynthetically active radiation. (D) The relative changes in stomatal aperture (relative stomatal aperture) were calculated as (stomatal aperture in 0 ppm CO2)/(stomatal aperture in 700 ppm CO2). Large values represent small responses. Data presented are means ± SE (n = 60) of five independent experiments. Significant differences from Col-0 at p < 0.05 (Student’s t test) are indicated by asterisks.
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pone.0117449.g002: The phenotype of Kl-4, Ga-0, and Chi-1, which exhibit low CO2 responsiveness.(A) Thermal imaging of the three selected ecotypes Kl-4, Ga-0, Chi-1, and the commonly used ecotype Col-0. Plants were subjected to 0 ppm CO2 for 2 h and then 1,000 ppm CO2 for 1 h at 40% RH. The subtractive image on the right shows that the largest temperature changes were exhibited by Col-0. (B) Time courses of stomatal conductance (gs) in response to changes in CO2 concentration in Kl-4, Ga-0, Chi-1, and Col-0. Col-0 is more responsive to changes in CO2 concentration than Kl-4, Ga-0, Chi-1. (C) Sizes of stomatal apertures at low and high CO2 concentrations. Plants were subjected to 0 ppm CO2 for 2 h and then transferred to 700 ppm CO2 for 1 h at 40% RH with 150 μmol m-2 s-1 photosynthetically active radiation. (D) The relative changes in stomatal aperture (relative stomatal aperture) were calculated as (stomatal aperture in 0 ppm CO2)/(stomatal aperture in 700 ppm CO2). Large values represent small responses. Data presented are means ± SE (n = 60) of five independent experiments. Significant differences from Col-0 at p < 0.05 (Student’s t test) are indicated by asterisks.

Mentions: We compared the three selected ecotypes and Col-0 in their temperature responses to changes in CO2 concentrations. The three selected ecotypes showed relatively small temperature differences, indicating the comparatively low CO2 responsiveness of the stomata (Fig. 2A). Next, we measured stomatal conductance in four ecotypes at various CO2 concentrations ranging from 0 to 1,000 ppm. The stomatal conductance levels of the three selected ecotypes were lower than those of Col-0 at low CO2 concentrations, however, they exhibited similar but slightly higher stomatal conductance levels when compared with Col-0 at high CO2 concentrations (Fig. 2B). This indicated that, when compared with Col-0, the three selected ecotypes showed lower responsiveness to CO2 in stomatal conductance as well as in leaf temperature. Stomatal conductance is determined predominantly by stomatal size, density, and aperture [23]. We found no differences in stomatal size, index, or density among the four ecotypes (Fig. 3A, B, C). On the other hand, the three selected ecotypes showed significantly smaller changes in stomatal aperture with an increase of CO2 concentration from 0 ppm to 700 ppm, when compared with Col-0 (Fig. 2C). This result was consistent with the thermography and stomatal conductance data. The least responsive of the three ecotypes was Chi-1, followed by Ga-0 and Kl-4 (Fig. 2D).


Natural variation in stomatal responses to environmental changes among Arabidopsis thaliana ecotypes.

Takahashi S, Monda K, Negi J, Konishi F, Ishikawa S, Hashimoto-Sugimoto M, Goto N, Iba K - PLoS ONE (2015)

The phenotype of Kl-4, Ga-0, and Chi-1, which exhibit low CO2 responsiveness.(A) Thermal imaging of the three selected ecotypes Kl-4, Ga-0, Chi-1, and the commonly used ecotype Col-0. Plants were subjected to 0 ppm CO2 for 2 h and then 1,000 ppm CO2 for 1 h at 40% RH. The subtractive image on the right shows that the largest temperature changes were exhibited by Col-0. (B) Time courses of stomatal conductance (gs) in response to changes in CO2 concentration in Kl-4, Ga-0, Chi-1, and Col-0. Col-0 is more responsive to changes in CO2 concentration than Kl-4, Ga-0, Chi-1. (C) Sizes of stomatal apertures at low and high CO2 concentrations. Plants were subjected to 0 ppm CO2 for 2 h and then transferred to 700 ppm CO2 for 1 h at 40% RH with 150 μmol m-2 s-1 photosynthetically active radiation. (D) The relative changes in stomatal aperture (relative stomatal aperture) were calculated as (stomatal aperture in 0 ppm CO2)/(stomatal aperture in 700 ppm CO2). Large values represent small responses. Data presented are means ± SE (n = 60) of five independent experiments. Significant differences from Col-0 at p < 0.05 (Student’s t test) are indicated by asterisks.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4338149&req=5

pone.0117449.g002: The phenotype of Kl-4, Ga-0, and Chi-1, which exhibit low CO2 responsiveness.(A) Thermal imaging of the three selected ecotypes Kl-4, Ga-0, Chi-1, and the commonly used ecotype Col-0. Plants were subjected to 0 ppm CO2 for 2 h and then 1,000 ppm CO2 for 1 h at 40% RH. The subtractive image on the right shows that the largest temperature changes were exhibited by Col-0. (B) Time courses of stomatal conductance (gs) in response to changes in CO2 concentration in Kl-4, Ga-0, Chi-1, and Col-0. Col-0 is more responsive to changes in CO2 concentration than Kl-4, Ga-0, Chi-1. (C) Sizes of stomatal apertures at low and high CO2 concentrations. Plants were subjected to 0 ppm CO2 for 2 h and then transferred to 700 ppm CO2 for 1 h at 40% RH with 150 μmol m-2 s-1 photosynthetically active radiation. (D) The relative changes in stomatal aperture (relative stomatal aperture) were calculated as (stomatal aperture in 0 ppm CO2)/(stomatal aperture in 700 ppm CO2). Large values represent small responses. Data presented are means ± SE (n = 60) of five independent experiments. Significant differences from Col-0 at p < 0.05 (Student’s t test) are indicated by asterisks.
Mentions: We compared the three selected ecotypes and Col-0 in their temperature responses to changes in CO2 concentrations. The three selected ecotypes showed relatively small temperature differences, indicating the comparatively low CO2 responsiveness of the stomata (Fig. 2A). Next, we measured stomatal conductance in four ecotypes at various CO2 concentrations ranging from 0 to 1,000 ppm. The stomatal conductance levels of the three selected ecotypes were lower than those of Col-0 at low CO2 concentrations, however, they exhibited similar but slightly higher stomatal conductance levels when compared with Col-0 at high CO2 concentrations (Fig. 2B). This indicated that, when compared with Col-0, the three selected ecotypes showed lower responsiveness to CO2 in stomatal conductance as well as in leaf temperature. Stomatal conductance is determined predominantly by stomatal size, density, and aperture [23]. We found no differences in stomatal size, index, or density among the four ecotypes (Fig. 3A, B, C). On the other hand, the three selected ecotypes showed significantly smaller changes in stomatal aperture with an increase of CO2 concentration from 0 ppm to 700 ppm, when compared with Col-0 (Fig. 2C). This result was consistent with the thermography and stomatal conductance data. The least responsive of the three ecotypes was Chi-1, followed by Ga-0 and Kl-4 (Fig. 2D).

Bottom Line: The stomatal responses to light were also reduced in the three selected ecotypes when compared with Col-0.This study demonstrates that the stomatal responses to CO2 and light share closely associated signaling mechanisms that are not generally correlated with humidity signaling pathways in these ecotypes.The results might reflect differences between ecotypes in intrinsic response mechanisms to environmental signals.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Faculty of Sciences, Kyushu University, Fukuoka, Japan.

ABSTRACT
Stomata are small pores surrounded by guard cells that regulate gas exchange between plants and the atmosphere. Guard cells integrate multiple environmental signals and control the aperture width to ensure appropriate stomatal function for plant survival. Leaf temperature can be used as an indirect indicator of stomatal conductance to environmental signals. In this study, leaf thermal imaging of 374 Arabidopsis ecotypes was performed to assess their stomatal responses to changes in environmental CO2 concentrations. We identified three ecotypes, Köln (Kl-4), Gabelstein (Ga-0), and Chisdra (Chi-1), that have particularly low responsiveness to changes in CO2 concentrations. We next investigated stomatal responses to other environmental signals in these selected ecotypes, with Col-0 as the reference. The stomatal responses to light were also reduced in the three selected ecotypes when compared with Col-0. In contrast, their stomatal responses to changes in humidity were similar to those of Col-0. Of note, the responses to abscisic acid, a plant hormone involved in the adaptation of plants to reduced water availability, were not entirely consistent with the responses to humidity. This study demonstrates that the stomatal responses to CO2 and light share closely associated signaling mechanisms that are not generally correlated with humidity signaling pathways in these ecotypes. The results might reflect differences between ecotypes in intrinsic response mechanisms to environmental signals.

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