The role of ethylene perception in the control of photosynthesis

Abstract

The process of photosynthesis is under the control by several internal factors. Apart from the effect of abscisic acid on stomatal conductance, little is known about the interaction between hormonal signals and photosynthesis in fully-developed, nonsenescing leaves. Recently, we found that the ethylene transduction pathway is involved in the regulation of photosynthesis. Using an ethylene-insensitive tobacco genotype we showed that the absence of a functional ethylene receptor leads to a reduction in Rubisco content and photosynthetic capacity. In this addendum, we present some additional data indicating that photosynthetic capacity is also reduced in ethylene-insensitive Arabidopsis mutants.

One of the mechanisms that affect photosynthetic activity and gene expression is feedback regulation by carbohydrate end-products of the Calvin cycle.¹ Long term growth at elevated CO₂ concentrations generally increases soluble sugar concentrations in the leaves. The increased sugar concentrations are correlated with a decrease in Rubisco transcript levels and a lower photosynthetic capacity.^2–4 By exploiting the fact that seedling development is hampered by high glucose concentrations, Zhou et al⁵ have elegantly shown that ethylene plays a role in sugar signaling.

In a previous paper, we showed that whole-plant photosynthesis per unit leaf area is 12% lower in ethylene-insensitive Arabidopsis and tobacco genotypes.⁶ Based on these findings, we set out to analyze the effects of ethylene-insensitivity on the composition of the photosynthetic machinery in more detail, and to test whether hormonal signals are involved in the feedback regulation of photosynthesis.⁷

First, we tested whether Rubisco expression of transgenic, ethylene-insensitive tobacco is more sensitive to externally applied glucose. We found that when ethylene-insensitive plants were grown in the presence of glucose, the Rubisco content was 30% lower, whereas wild-type plants only showed a 16% reduction. Pretreatment of the plants with the ABA-production inhibitor fluridone completely nullified this interaction, and resulted in similar levels of Rubisco in wild-type and ethylene-insensitive plants. In addition, we found that the ABA concentration in ethylene-insensitive plants was much higher compared to the wild type. These finding are consistent with previous studies in Arabidopsis showing that ethylene-insensitive genotypes are hypersensitive to externally applied glucose, and that this effect is most likely mediated by ABA.^5,8 However, until now, it was not clear whether this relation between ethylene and sugar sensitivity was physiologically relevant in plants that were not exposed to large amounts of externally applied glucose. To induce high internal glucose levels, we grew plants at elevated CO₂ concentrations. We subsequently tested whether internal glucose concentrations were correlated with Rubisco transcript expression. As expected, there was a negative correlation between the measured glucose concentration and Rubisco mRNA expression. In addition, consistent with our hypothesis, Rubisco expression was more strongly inhibited by high glucose levels in the ethylene-insensitive tobacco plants.

Analysis of the composition of the photosynthetic machinery showed that the absence of a functional ethylene receptor resulted in plants with comparable fractions of nitrogen invested in light harvesting, but lower amounts in electron transport and Rubisco. Gas-exchange measurements revealed that photosynthetic capacity of the ethylene-insensitive tobacco was clearly lower compared to the wild type. Here, we show a similar decrease in photosynthetic capacity between wild type and ethylene-insensitive Arabidopsis etr1-1 mutants (Fig. 1). However, tobacco and Arabidopsis differed considerably in the response of transpiration rate and stomatal conductance to ethylene-insensitivity, suggesting that this reaction is species specific. At saturating light conditions, stomatal conductance in the ethylene-insensitive tobacco genotype was 18% higher compared to the wild type. However, stomatal conductance in ethylene-insensitive Arabidopsis mutants was 44% lower compared to the wild type (Fig. 1). As a result of this, intercellular CO₂ concentration of the Arabidopsis etr1 mutant was not higher like in the ethylene-insensitive tobacco plants, but 4% lower (p < 0.05). In support of these findings, Tanaka et al⁹ showed that the stomatal aperture in etr1 Arabidopsis mutants is smaller compared to the wild type. Interestingly, the difference between Arabidopsis and tobacco parallels the responses of stomata to ethylene treatment, which is also found to vary between species.^10–14

Figure 1.

Comparison of carboxylation capacity (V_cmax), electron transport capacity (J_max) and stomatal conductance (g_s) in wild-type and ethylenesensitive tobacco and Arabidopsis. Capacity parameters were calculated using the biochemical model of photosynthesis as described by Farquhar & Von Caemmerer (1982). Mean values ± SE are shown (n = 6–8). *p < 0.05; **p < 0.01; ***p < 0.001.

How can these results be placed in perspective? Based on our result that plants with a dysfunctional ethylene-receptor have a lower photosynthetic capacity, we expect ethylene treatment to stimulate photosynthesis. However, the opposite is often observed.^12,15 The inhibition of photosynthesis by ethylene can be explained by several mechanisms: The first is that ethylene induces senescence, which results in the breakdown of the photosynthetic machinery. As demonstrated by Grbic & Bleecker,¹⁶ ethylene-insensitive mutant plants have a delayed senescence, resulting in a higher carboxylation activity in older leaves. However, in line with our results, they found younger (non-senescing) leaves of ethylene-insensitive plants to have a lower carboxylation activity.¹⁶ A second explanation for the inhibition of photosynthesis is a negative effect of ethylene on stomatal conductance;^11,12 which lowers the intercellular CO₂ concentration. However, recently it was shown by Khan¹⁴ that ethylene can have a stimulating effect on photosynthesis, independent of its effect on stomatal conductance.

Interestingly, endogenous glucose concentrations are often positively correlated with ethylene production in rice, and external sugar application in this species significantly stimulates ethylene production:¹⁷ In sunflower, ethylene production is stimulated in response to high CO₂ concentrations;¹⁸ but only in the light. It may well be that increased ethylene production plays an important role in maintaining growth under circumstances where leaf glucose concentrations are high, such as in plants growing in elevated atmospheric CO₂ levels.¹⁹

Our work shows that the absence of a functional ethylene perception pathway results in a decreased photosynthetic capacity in both tobacco and Arabidopsis. However, the effect on stomatal conductance differs strongly between the two species.

Addendum to: Ethylene insensitivity results in down-regulation of Rubisco expression and photosynthetic capacity in tobacco. Tholen D, Pons TL, Voesenek LACJ, Poorter H. Plant Physiol. 2007;144:1305–1315.