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First published online April 2, 2004; 10.1104/pp.103.034389 Plant Physiology 134:1803-1812 (2004) © 2004 American Society of Plant Biologists Ethylene Insensitivity Does Not Increase Leaf Area or Relative Growth Rate in Arabidopsis, Nicotiana tabacum, and Petunia x hybrida1Plant Ecophysiology, Utrecht University, 3584 CA Utrecht, The Netherlands
The plant hormone ethylene plays a role in various growth related processes. In this detailed study of the vegetative growth of Arabidopsis, Nicotiana tabacum, and Petunia x hybrida plants, we show that ethylene insensitivity does not result in an increased total leaf area or relative growth rate (RGR) under optimal growth conditions. When grown in semiclosed containers, leaf area of ethylene-insensitive plants was larger compared to the wild type. This effect was caused by a buildup of ethylene inside these containers, which inhibited the growth of wild-type plants. Ethylene-insensitive Arabidopsis and N. tabacum plants had a lower biomass, which was mainly the result of a smaller seed mass. RGR of vegetative plants was not affected by ethylene insensitivity, but the underlying components of RGR differed; specific leaf area (leaf area per unit leaf mass) was higher, and unit leaf rate (growth rate per unit leaf area) was lower. The latter was a result of a slower rate of photosynthesis per unit leaf area in the ethylene-insensitive plants.
Auxins, cytokinins, gibberellic acid, and abscisic acid play a role in the regulation of growth and can affect the rate of photosynthesis (Mansfield and McAinsh, 1995  ; Brenner and Cheikh, 1995) as well as plant morphology (Reid and Howel, 1995). The gas ethylene is also highly active morphogenetically, and its effects have been extensively studied in a range of species, including Arabidopsis seedlings (e.g. Bleecker et al., 1988; Guzman and Ecker, 1990; Smalle et al., 1997; Hall et al., 1999). Thickening of the hypocotyl, reduction in hypocotyl and root elongation, and a diageotropic orientation are typical effects of exogenously applied ethylene (Abeles et al., 1992). Although in many (semi)aquatic plants ethylene stimulates leaf and petiole extension (Voesenek et al., 2003), in terrestrial plants ethylene generally inhibits leaf expansion (Abeles et al., 1992). In support of this view are observations of larger rosette leaves in ethylene-insensitive Arabidopsis mutants (Guzman and Ecker, 1990; Ecker, 1995). More specifically, total leaf area of rosette leaves of ethylene-insensitive Arabidopsis genotypes (etr1-1 and ers1) was reported to be 25% to 50% larger than that of wild-type plants (Bleecker et al., 1988; Hua et al., 1995). The increase in leaf area was attributed to an increased cell expansion in ethylene-insensitive plants (Hua et al., 1995). A greater leaf area in ethylene-insensitive plants suggests that the low endogenous ethylene concentrations in the wild type have an inhibiting effect on leaf expansion. However, it could be that leaf expansion of wild-type plants was inhibited because ethylene accumulated in semiclosed tissue-culture containers used in some of this work (Kieber et al., 1993).
Leaf area is not necessarily a good descriptor of growth. A way to achieve a better understanding of the underlying growth processes is a growth analysis as described in, for example, Poorter (2002)
To our knowledge, no growth analysis has ever been made of ethylene-insensitive plants, but a small number of previous studies describe the effects of ethylene insensitivity on photosynthetic processes. Zhou et al. (1998) Given that the current knowledge about the role of ethylene in vegetative plant growth is largely incomplete, we aim to improve the understanding of whole-plant growth and allocation in ethylene-insensitive genotypes. To evaluate possible species-specific effects of ethylene insensitivity on plant growth parameters, three different species were examined. A growth analysis was performed on hydroponics as well as on soil to make the results more broadly applicable. First, we tested the sensitivity of ethylene-sensitive and -insensitive Arabidopsis, Nicotiana tabacum, and Petunia x hybrida genotypes to ethylene. Second, we determined the total leaf area of Arabidopsis grown on petri dishes with or without an ethylene absorbing compound. These results were compared with the total leaf area of plants growing in a well-ventilated climate room. Third, we studied the RGR and its components in ethylene-sensitive and -insensitive genotypes of the three species. Last, we analyzed whether the lower amount of active Rubisco per area reported for Arabidopsis etr1-1 mutants is reflected in a lower nitrogen content and photosynthesis per unit leaf area in all three ethylene-insensitive genotypes. We conclude that leaf area of ethylene-sensitive Arabidopsis was reduced when the plants were grown for 2 weeks in semiclosed containers. There was no difference in total leaf area or RGR between ethylene-sensitive and -insensitive plants under optimal conditions. However, the components underlying RGR were different: The ethylene-insensitive plants were found to have a higher SLA but a lower ULR than the ethylene-sensitive controls. The lower ULR was shown to be the outcome of a lower rate of photosynthesis in ethylene-insensitive plants.
Ethylene Sensitivity To confirm the ethylene insensitivity of the mutant and transgenic lines, their response capacity to 10 µL L–1 applied ethylene was assessed in terms of extension growth of seedling roots, seedling hypocotyls, adult roots, and chlorophyll content of full-grown leaves (Table I). All mutant and transgenic lines showed an impaired response to the applied ethylene. Overall, P. hybrida Atetr1-1 showed the most residual responsiveness and N. tabacum Atetr1-1 the least.
Ethylene Accumulation and Total Leaf Area
After 2 weeks of growth in petri dishes, wild-type Arabidopsis plants enriched the enclosed gas space with more than 0.08 µL L–1 ethylene. This concentration was 8 times larger than the ambient concentration in the growth room. The concentration of ethylene in petri dishes in which the etr1-1 mutants were growing was almost an order of magnitude greater (0.70 µL L–1), a likely outcome of larger plant size and a constitutive higher ethylene production rate (Guzman and Ecker, 1990
Growth Analysis
There are several factors that determine total plant biomass at any given time. First, differences in seed mass can have a large effect on the size of the adult plants to which they give rise (Leishman et al., 2000
Growth in ethylene-sensitive and -insensitive plants was examined in greater detail, through analysis of RGR and its underlying components (as described in "Materials and Methods"). On hydroponics, all three species had high growth rates (above 250 mg g–1 d–1), and the RGR of ethylene-sensitive genotypes was statistically indistinguishable from that of the corresponding ethylene-sensitive plants of the same species (Fig. 4 ). For plants grown on soil, the growth rates were lower compared to hydroponics culture, but again no differences between ethylene-sensitive and -insensitive plants were observed (Table II).
Growth parameters determining RGR are known to vary depending on the species and the developmental stage of the plants. To overcome this complication when making comparisons between different lines, all growth parameters were plotted against total plant dry mass. Since leaf number is a common measure for the developmental stage of Arabidopsis, we also examined the relationship between the total dry mass and leaf number for all three species. Figure 5 shows that there were no significant differences in leaf number between ethylene-sensitive and -insensitive plants of the same mass over the time period of our experiments.
When examining components that determine relative growth rate, it was found that the leaf area per leaf mass (SLA) was significantly greater in all three ethylene-insensitive genotypes (Fig. 6A ; Table II). A higher SLA can be the outcome of thinner leaves or leaves with a lower density. Ethylene-insensitive leaves indeed had a lower density than ethylene-sensitive plants, but this was not due to an increase in leaf porosity (25% air volume per total volume for N. tabacum and P. hybrida, 19% for Arabidopsis). The biomass allocation to the leaves, expressed as leaf mass fraction (LMF), was somewhat higher (5%, P < 0.05) in both ethylene-insensitive Arabidopsis and N. tabacum as compared to ethylene-sensitive controls (Fig. 6B). In ethylene-insensitive P. hybrida and N. tabacum, a significantly higher LMF was observed when the plants were grown on soil (Table II). Allocation of biomass to the roots, expressed as root mass fraction (RMF), was lower for ethylene-insensitive P. hybrida plants during the early stages of growth on hydroponics; in all other cases, we found no significant differences (Fig. 6C). The growth rate per unit leaf area (ULR) of ethylene-insensitive Arabidopsis and N. tabacum was almost 15% lower compared to controls, but in P. hybrida the effect was not statistically significant (Fig. 7A ) unless the plants were grown on soil (Table II). We conclude that, in ethylene-insensitive genotypes, a lower ULR (–15%) antagonizes the effect of a slightly higher SLA (10%) and LMF (5%), leading to a RGR similar to that of ethylene-sensitive plants.
Photosynthesis, Respiration, and Nitrogen Content The growth parameter ULR can also be calculated from physiological parameters using Equation 5 (see "Materials and Methods"). The resulting differences in ULR between ethylene-sensitive and -insensitive plants were found to be similar to the differences in ULR calculated from biomass and area measurements (Eq. 4) as described above (Fig. 7A). Figure 7B shows that the lower ULR in ethylene-insensitive plants is predominantly due to a slower rate of photosynthesis per unit area (PSA; Table III) and not a consequence of the fraction of photosynthetically fixed carbon that is incorporated into biomass instead of respired (FCI) or of differences in the carbon content ([C]). Only in ethylene-insensitive P. hybrida plants we found no significant decrease in net PSA (Fig. 7B). In the ethylene-insensitive genotypes with a slower rate of photosynthesis per area, we also found a lower organic nitrogen content per unit leaf area (Fig. 8A ). There was no significant difference in photosynthetic nitrogen use efficiency (rate of photosynthesis per mol of nitrogen) between ethylene-sensitive and -insensitive plants (data not shown).
The impact of insensitivity to ethylene on growth was assessed using plants containing the mutated ethylene receptor gene etr1-1 from Arabidopsis. No stimulating effect of ethylene insensitivity on total leaf area was found when using plants growing in well-ventilated conditions using soil or hydroponics. In separate experiments, similar results were obtained with ethylene-insensitive Arabidopsis ein2 and ein4 mutants (data not shown). When growing plants in (semi)closed tissue-culture containers, leaf growth of wild-type plants was inhibited. We have shown that this was a result of ethylene accumulation inside the containers (Fig. 1), as was suggested previously by Kieber et al. (1993) . Similar effects of enclosure have been reported before in studies of leaf abscission and ethylene-mediated auxin effects (Chadwick and Burg, 1970) and can be overcome by ethylene absorption (Jackson and Osborne, 1970) or ventilation of the containers (Zobayed et al., 2001). Accordingly, in our work a leaf growth inhibiting effect of accumulated ethylene was revealed by the promotive influence of an ethylene absorbent.
The absence of a stimulating effect of ethylene insensitivity on total leaf area seems to contrast with previously reported results (Bleecker et al., 1988
Taken together, our data show that ethylene-insensitive plants do not have a larger leaf area compared to ethylene-sensitive plants during their vegetative growth stage. In this view, the low, endogenous ethylene concentrations normally present in the wild type have no negative impact on vegetative growth. In fact, it could well be that very low concentrations (<0.05 µL L–1) of ethylene can stimulate leaf expansion, both in dicots (Lee and Reid, 1997
Previous work on ethylene perception mutants focused on the differences in leaf area as a parameter of plant growth. In this work the differences in total plant dry mass were also examined. We observed a reduced biomass in the ethylene-insensitive Arabidopsis and N. tabacum. This could be caused by a smaller seed mass, delayed germination, or a reduced RGR. It has been reported that the ethylene-insensitive Arabidopsis mutant displays enhanced seed dormancy (Bleecker et al., 1988
Defects in ethylene perception can result in abnormal development of tomato (Lycopersicon esculentum) and P. hybrida roots, especially in response to mechanical impedance (Clark et al., 1999
A lower chlorophyll and active Rubisco content per unit leaf area was shown by Grbi
Interestingly, there are some similarities between ethylene-insensitive plants and plants grown at low irradiances. We observed a higher SLA and lower nitrogen content per area in the ethylene-insensitive plants. Growing plants at low light also results in a higher SLA and a lower nitrogen content per unit leaf area (Evans and Poorter, 2001
Ethylene can alter cell wall synthesis and composition (Abeles et al., 1992 In contrast to Arabidopsis and N. tabacum, SLA was the only growth parameter of P. hybrida grown on hydroponics that was significantly affected by ethylene insensitivity, although ULR and LMF differed in soil-grown P. hybrida plants. A possible explanation is that P. hybrida Atetr1-1 plants are less insensitive to ethylene compared to the other ethylene-insensitive genotypes (Table I), possibly reducing the differences in growth parameters between P. hybrida Atetr1-1 and the nontransformed controls.
For at least the three species examined in this work, ethylene insensitivity had little effect on vegetative growth and development under optimal conditions. These results make the view that ethylene, in contrast to other hormones, is not essential for normal development more broadly applicable. This is also clearly apparent in the aquatic monocot Potamogeton pectinatus, a species that lacks ethylene production and yet develops completely and reproduces both sexually and asexually (Summers et al., 1996
When plants are grown in semiclosed containers, accumulation of ethylene results in a smaller leaf area of ethylene-sensitive Arabidopsis compared to ethylene-insensitive plants. However, when grown in well-ventilated conditions, no increased total leaf area was found during the vegetative growth phase in the ethylene-insensitive genotypes of three different species. Growth rates were similar for ethylene-sensitive and -insensitive plants, but a lower seed mass in Arabidopsis etr1-1 and N. tabacum Atetr1-1 resulted in smaller adult plants. Ethylene-insensitive plants had a larger leaf area per leaf mass, which generally promotes growth. However, this effect was counteracted by a slower rate of photosynthesis per unit leaf area. Overall, these findings indicate little impact of endogenous levels of ethylene on the growth of nonstressed plants.
Plant Material
Arabidopsis Columbia wild-type and etr1-1 (Bleecker et al., 1988
Seedlings of all six genotypes where grown in open petri dishes placed in closed 11-L dessicators in the absence or presence of a saturating ethylene concentration (10 µL L–1; Hoek Loos, Amsterdam). The glass dessicators contained a butyl-rubber septum for taking gas samples with a 1-mL syringe. The petri dishes contained 20 wild-type or etr1-1 Arabidopsis seeds on a half-strength Murashige and Skoog medium (Murashige and Skoog, 1962
The ethylene response capacity of the roots of 3-week-old plants was measured by growing six plants of each genotype on 6-L buckets filled with a modified Hoagland solution, described in Poorter and Remkes (1990)
The ethylene response capacity of full-grown leaves of 3-week-old plants was measured in terms of change in chlorophyll concentration. Parts of full-grown leaves were placed in a small volume of tap water inside 22-L dessicators in the absence or presence of 10 µL L–1 ethylene gas. For 5 d, the leaves were incubated and then removed from the containers, after which small discs were cut from the tissue. The leaf discs were quickly transferred to a vial containing N,N-dimethylformamide and stored for 5 d at 4°C in darkness. After 1 week of incubation in N,N-dimethylformamide, chlorophyll absorption was measured spectrophotometrically (Inskeep and Bloom, 1985
The ethylene response capacity (ERC) of the genotypes was calculated as follows:
To test the effect of ethylene accumulation, 40 wild-type or etr1-1 Arabidopsis seeds were germinated in 32 glass petri dishes (ø = 10 cm) on the previously described Murashige and Skoog medium with 1% (w/v) sucrose. The petri dishes contained a butyl-rubber septum for taking gas samples and were sealed with one layer of parafilm. Note that the parafilm is gas permeable and allows ethylene to slowly diffuse out of the petri dishes. For each of the two genotypes, one gram Ethysorb, an ethylene absorbing compound (Stay Fresh, London), was placed in a small plastic container inside half of the petri dishes. The petri dishes were kept in a growth room under the same conditions as described above. After 14 d, gas samples were taken from the petri dishes with a syringe, and ethylene concentrations were determined. Thereafter, five seedlings per petri dish were harvested and total leaf area per seedling was determined.
Prior to each experiment, seed mass (dried at 70°C for 48 h) was determined. A separate batch of seeds was germinated on sand in trays covered with a glass plate and watered with a modified Hoagland solution with a nitrate concentration of 2 mM (Poorter and Remkes, 1990
The leaf porosity (% air spaces) of full-grown leaves was measured by determining leaf buoyancy before and after vacuum infiltration of the gas spaces (Raskin, 1983 The growth analysis was repeated by growing the plants in soil, under the same light levels and daylength as previously described. N. tabacum and P. hybrida were grown in 500-mL pots, each containing a mixture of potting soil and perlite (1/1, v/v) including 3 g L–1 osmocote, 2 g L–1 MgO/CaO, and 2.5 mM KH2PO4. For Arabidopsis, 70-mL pots were used containing a mixture of potting soil and perlite (1/2, v/v) including 2 g L–1 osmocote and 2 g L–1 MgO/CaO. At the start, Arabidopsis plants were watered with a half-strength Hoagland nutrient solution. The pots were then transferred to irrigation mats (Maasmond-Westland, Utrecht, The Netherlands), which were automatically watered twice a day to saturation with tap water and the excess water drained.
After 7 (Arabidopsis) or 14 d (N. tabacum and P. hybrida) of growth on hydroponics, eight plants were used to measure whole-plant gas exchange (Poorter et al., 1990
On two time points, leaf number, leaf area, and the dry and fresh mass of roots, stem and leaves of each plant were measured. From these measurements, the following growth parameters can be calculated. The net dry biomass increase per unit dry mass per day is the RGR (mg g–1 d–1). RGR was calculated using the classical approach (Hunt, 1982
). The first component is the leaf area per leaf dry mass or SLA (m2 kg–1). The second is the fraction of total biomass allocated to the leaves or LMF (g g–1). The third is the increase of biomass per unit leaf area per day or ULR (g m–2 d–1). The formula for RGR then becomes:
The SLA is calculated as the leaf area divided by the leaf mass. The SLA is also the reciprocal of the product of leaf thickness (m) and leaf density (kg m–3). Leaf density is dependent on the amount of air space inside the leaf tissue (leaf porosity) and the amount of water per dry mass (leaf water content). LMF is calculated as the leaf mass divided by the plant mass. ULR can be calculated from plant mass and leaf area on two time points:
ULR can also be calculated from measurements of gas exchange and carbon concentration. The ULR depends on (1) photosynthesis per unit leaf area (PSA; mol C fixed m–2 leaf area d–1); (2) fraction of daily fixed carbon that is not respired but incorporated into the biomass of a plant (FCI; mol C incorporated mol–1 C fixed); and (3) the amount of biomass that can be formed with 1 mol carbon, referred to by the carbon concentration ([C]; mol C g–1 dry mass). This can be represented as (Poorter, 2002
The results were analyzed using the SPSS statistical package (release 8.0; SPSS, Chicago). Differences between growth parameters were tested using a Student's t test on the normalized averages. Differences in leaf area of seedlings grown in Petri dishes were tested using an ANOVA.
We thank Rob Welschen, Ankie Ammerlaan, Yvonne de Jong-van Berkel, and Petra Burger for technical assistance. Prof. M.B. Jackson and Fabio Fiorani made many helpful comments on the manuscript. We thank Prof. M. Koornneef and Prof. G. Angenent for providing the tobacco and petunia seeds used in this study. In addition, we thank Prof. L.C. van Loon for his advice and support as coordinator of the research program of the Earth and Life Sciences Foundation. Received October 6, 2003; returned for revision January 14, 2004; accepted January 14, 2004.
1 This work was supported by the Earth and Life Sciences Foundation, which is subsidized by the Netherlands Organization for Scientific Research (NWO; grant no. 805.33.463) and by the NWO (PIONIER grant no. 800.84.470 to L.A.C.J.V.).  Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.103.034389. * Corresponding author; e-mail h.poorter{at}bio.uu.nl; fax 31–30–2518366.
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and Bleecker (1995)
