Ethylene_a regulator of root architectural responses to soil phosphorus availability

Ethylene_a regulator of root architectural responses to soil phosphorus availability

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Unformatted text preview: Plant, Cell and Environment (1999) 22, 425–431 ORIGINAL ARTICLE OA 220 EN Ethylene: a regulator of root architectural responses to soil phosphorus availability K . BORCH, 1 T. J. BOUMA, 2* J. P. LYNCH 2 & K. M. BROWN 2 Danish Institute of Agricultural Sciences, 5792 Aarslev, Denmark, 2Department of Horticulture, Penn State University, University Park, PA 16802, USA 1 A BSTRACT The involvement of ethylene in root architectural responses to phosphorus availability was investigated in common bean (Phaseolus vulgaris L.) plants grown with sufficient and deficient phosphorus. Although phosphorus deficiency reduced root mass and lateral root number, main root length was unchanged by phosphorus treatment. This resulted in decreased lateral root density in phosphorusdeficient plants. The possible involvement of ethylene in growth responses to phosphorus deficiency was investigated by inhibiting endogenous ethylene production with aminoethoxyvinylglycine (AVG) and aerating the root system with various concentrations of ethylene. Phosphorus deficiency doubled the root-to-shoot ratio, an effect which was suppressed by AVG and partially restored by exogenous ethylene. AVG increased lateral root density in phosphorusdeficient plants but reduced it in phosphorus-sufficient plants. These responses could be reversed by exogenous ethylene, suggesting ethylene involvement in the regulation of main root extension and lateral root spacing. Phosphorus-deficient roots produced twice as much ethylene per g dry matter as phosphorus-sufficient roots. Enhanced ethylene production and altered ethylene sensitivity in phosphorus-deficient plants may be responsible for root responses to phosphorus deficiency. Key-words: Phaseolus vulgaris L.; Leguminosae; common bean; ethylene; phosphorus nutrition; root architecture. INTRODUCTION The rate of phosphorus diffusion in soil solutions is generally slower than the absorption rate needed to sustain maximum growth rate (Nye & Tinker 1977). Hence, the ability of the roots to explore the growth media efficiently in time and space is very important for phosphorus uptake in low phosphorus soils. Factors believed to directly influence phosphorus uptake by roots are root diameter (Eissenstat 1992), root topology (Fitter 1991), root extension rate (Barber 1995), root length and density (Baldwin 1975), Correspondence: K. Brown. Fax: 814-863-6139; E-mail: [email protected] *Present address: Netherlands Institute of Ecology, Center for Estuarine and Coastal Ecology, 4400 AC Yerseke, The Netherlands. © 1999 Blackwell Science Ltd root hairs (Jungk 1987), and the presence of mycorrhiza (Koide 1991). Little is known about how root growth responses to phosphorus deficiency are mediated. However, the plant hormone ethylene is known to be involved in elongation of roots, lateral and adventitious rooting, root extension, radial expansion and aerenchyma formation [reviewed by Jackson (1991) and Dolan (1997)]. There is evidence for ethylene involvement in stress-related and adaptive root responses to chemical toxicity, water stress, interactions with symbionts, and nutrient deficiency (Lynch & Brown 1997). Such responses may involve changes in ethylene synthesis and/or responsiveness. For example, although phosphorus or nitrogen starvation reduced ethylene production in maize roots, ethylene responsiveness, measured as aerenchyma formation, increased (Drew, He & Morgan 1989; He, Morgan & Drew 1992). On the other hand, wheat seedling roots grown under nitrogen deficiency and low pH displayed increased ethylene production and reduced root elongation (Tari & Szén 1995). Ethylene at high concentrations has been reported to inhibit root growth and root gravitropic responses (Ycas & Zobel 1983). The objective of our study was to test the hypothesis that ethylene is involved in the growth responses of intact bean root systems to phosphorus deficiency. Our approach was to measure ethylene production and responsiveness in bean plants grown in sand amended with a solid-phase phosphorus buffer providing sufficient or deficient phosphorus. A range of ethylene concentrations was achieved by aerating the root zone for 4 weeks with various amounts of ethylene while inhibiting endogenous ethylene production with amino-ethoxyvinylglycine (AVG). MATERIALS AND METHODS Plant material Seeds of common bean (Phaseolus vulgaris L. CIAT breeding line DOR364) were obtained from CIAT in Cali, Colombia. The seeds were surface sterilized in 7 mol m–3 NaOCl and 0·1% Triton X-100 (Sigma Chemical Co., St. Louis, MO, USA) for 10 min, and germinated in 0·5 mol m–3 CaSO4 for 36 h at 25 °C. Seedlings were then planted at a depth of 3 cm into 1400 cm3 containers. All plants were grown in a greenhouse in University Park, PA, USA (40°85' N, 77°83' W). The temperature ranged from a 425 426 K. Borch et al. maximum of 26 °C (day) to a minimum of 19 °C (night). Natural light was supplemented from 0900 to 1700 h with 110 ± 10 µmol m–2 s–1 from 400 W metal-halide bulbs (Energy Technics, York, PA, USA). Maximum midday photosynthetically active photon flux densities reached 1400 µmol m–2 s–1 on clear days and 500 µmol m–2 s–1 on days with heavy cloud cover. Phosphorus treatments Plants were grown in silica sand containing solid-phase phosphorus buffer (alumina) as described by Lynch et al. (1990) with two different desorption concentrations allowing precise management of phosphorus concentrations. Once a day, pots were irrigated with nutrient solution containing (in mol m–3) 3·1 NO3, 1·8 K, 1·2 Ca, 1·4 SO4, 1·0 NH4, 0·825 Mg, 0·05 Cl, 0·005 Fe-EDTA, 0·002 B, 0·0015 Mn, 0·0015 Zn, 0·000143 Mo, and 0·0005 Cu. Sufficient and deficient phosphorus treatments contained 50 mmol m–3 and 1 mmol m–3 KH2PO4, respectively, in the nutrient solution, in addition to the phosphorus desorbed from the alumina phosphorus buffer. Leachate sampled from the pots was analysed using the phosphomolybdenum blue method (Murphy & Riley 1962) giving phosphorus concentrations in the soil solution of 8·6 (± 0·9) mmol m–3 for sufficient and 1·1 (± 0·03) mmol m–3 for deficient treatments. Ethylene and AVG treatments In a preliminary experiment, common bean plants were irrigated with a phosphorus-sufficient nutrient solution mixed with a range of AVG concentrations (Fig. 1) to determine the lowest AVG concentration which would inhibit ethylene production from the roots without affecting growth. After visual evaluation of root size and mass, roots were excised from 3-week-old plants, cut into 1 cm pieces and placed in a 150 cm3 flask containing the same AVG concentration as used for irrigation during growth. There were six plants per treatment in each of two replications. The flask was sealed with a rubber stopper and held for 5 h in darkness at 20 °C. A 1 cm3 sample was then collected from the head space for ethylene analysis by gas chromatography (GC). The GC (Hewlett-Packard 6890, Palo Alto, CA, USA) was fitted with a flame ionization detector and a column of activated alumina. The detection limit was 0·013 cm3 m–3. To examine the effect of ethylene on root development, bean plants were grown under sufficient (50 mmol m–3) and deficient (1 mmol m–3) phosphorus in the presence of AVG plus one of four ethylene concentrations (0, 0·02, 0·1, 1 cm3 m–3). Control plants were grown without AVG or ethylene. The roots were exposed to different ethylene concentrations without affecting the shoot atmosphere by growing each bean plant in the apparatus shown in Fig. 2 (Bouma et al. 1997). Different ethylene concentrations were obtained by mixing ethylene (from 1 dm3 m–3 or 0·04 dm3 m–3 gas bottles) into a stream of ambient air, using a mass flow controller (Brooks 5800 series, Brooks Instrument B.V., Veenendaal, The Netherlands) for the two low concentrations and rotameters for the high concentration. Each container was provided with a flow of 500 cm3 min–1 except for the control (no AVG) and AVG + 0 [C2H4] treatment. Measuring ethylene concentrations in the root zone The ethylene concentrations in the root zone were measured to determine the effectiveness of our ethylene perfusion treatments, and to determine ethylene production rates by intact root systems in the absence of AVG. To allow gas sampling, small tubes were inserted through the sides of the containers at 14 cm depth before planting (Fig. 2). These were open to the root zone on the inside and sealed with a serum stopper on the outside so that the gas space inside would be in equilibrium with the gas space in the root zone. Ethylene samples (1 cm3) were withdrawn from this space and analysed by GC when the plants were 5 weeks old. There was no observable diurnal fluctuation in ethylene production, based on sampling every 4–6 h. Root growth and development Figure 1. Ethylene production rate by excised roots irrigated with different concentrations of amino-ethoxyvinylglycine (AVG), an ethylene biosynthesis inhibitor. Bars indicate standard error of the mean. Plants grown with the two different phosphorus availabilities were harvested after 4 weeks of ethylene exposure (just before anthesis). Leaf area, root length and biomass of the leaves, stem and roots were determined. The roots were excavated by rinsing the sand with deionized water. A subsample of the root (including two whole basal roots) was collected randomly from each plant and stained for 1 h prior to scanning to create optimal contrast (0·16 kg m–3 neutral red dye, Sigma Chemical Co., St. Louis, MO, USA). The leaves and the root subsamples were scanned using a flat bed scanner (HP ScanJet II, © 1999 Blackwell Science Ltd, Plant, Cell and Environment, 22, 425–431 Ethylene mediates phosphorus availability responses 427 Statistical analysis Data were analysed using the PC-statistical package JMP® (SAS Institute, Cary, NC). Data with one variable were analysed using Student’s t-test for each pair at P < 0·05. Data with more variables were analysed with ANOVA (randomized block design) and mean separations were performed by contrast for each parameter by t-test and F-test for all parameters tested jointly. When data were not normally distributed, they were log transformed before conducting the ANOVA. RESULTS Effect of phosphorus deficiency on root and shoot growth Figure 2. Apparatus used to expose roots to different gas mixtures. Air with a known ethylene concentration was pumped into the bottom of a container filled with sand. The incoming air was bubbled through water, which prevented desiccation of the root zone and provided a check on the flow into each pot. Equal flow rates in each pot were obtained by using 0·5 mm ID tubing from the main gas source to the Erlenmeyer flask. Irrigation solution could drain freely through the water lock. The air outlet was on the side of the pots, above the sand surface. Shoots were kept at ambient gas composition by sealing the top of each pot and pumping air from the head space out of the greenhouse. A flexible sealant (Terostat) was used to create a gas tight seal around the stem. Gas-sampling chambers were placed at 14 cm depth. resolution = 140 dots mm–2, Hewlett Packard). Leaf area, root length, and root diameter distribution were estimated using image analysis software (DELTA-T SCAN, Delta-T Devices Ltd, Cambridge, UK). The total root length was estimated by multiplying the subsample length by the dry weight (DW) ratio of the scanned subsample and the total DW of the root. The average lateral root length and density were determined from the scanned subsample. The main root length was estimated from the ratio between the lateral root length and the basal root length in the scanned subsample. Specific root length was calculated by dividing the total root length by the root DW. Plant material was dried at 70 °C for 48 h prior to dry matter determinations. © 1999 Blackwell Science Ltd, Plant, Cell and Environment, 22, 425–431 Phosphorus deficiency reduced total root length (main plus lateral roots) by more than one third (Fig. 3). The total lateral root length (the product of the mean lateral root length and the number of lateral roots) was significantly reduced by phosphorus deficiency (Fig. 3). This was a result of the reduction in lateral root number (Fig. 3), as mean lateral root length was unaffected by phosphorus treatment (Table 1). Lateral root density (the number of laterals per cm of main root) was significantly reduced in phosphorus-deficient roots compared with phosphorus-sufficient roots (Fig. 4). Phosphorus deficiency reduced the DW of roots by about one third (Table 2), but there was a proportionately greater reduction in shoot DW, nearly doubling the root-toshoot ratio (Fig. 4). There was no difference between the sufficient and deficient phosphorus treatments in ethylene concentrations in the root zones. However, ethylene production per g DW was significantly higher in phosphorus-deficient roots compared with phosphorus-sufficient roots (Table 2). Manipulation of ethylene with AVG and ethylene perfusion A preliminary dose–response experiment was used to determine the effect of AVG on growth and ethylene production by roots of bean plants grown with sufficient phosphorus. Ethylene production by excised roots was reduced to 10% of that of control roots when the plants were irrigated with at least 1·28 mmol m–3 AVG (Fig. 1). Figure 3. Effect of sufficient (+P) and deficient (–P) phosphorus concentrations in the growth media on total root length, total lateral root length, and lateral root number (data pooled across ethylene treatments). Bars indicate standard error of the mean. 428 K. Borch et al. Variable Statistic C2H4 Phosphorus Phosphorus × C2H4 Shoot dry weight (g) d.f. F P d.f. F1 P d.f. F1 P d.f. F1 P d.f. F1 P d.f. F1 P d.f. F1 P d.f. F1 P 4 4·6 0·01 4 5·8 0·01 4 6·2 0·01 4 1·3 ns 4 6·8 0·01 4 0·6 ns 4 2·2 ns 4 2·6 0·05 1 238 0·05 1 132 0·01 1 49·7 0·01 1 19·8 0·01 1 49·1 0·01 1 13·3 0·01 1 4·2 0·05 1 0·4 ns 4 2·2 ns 4 3·4 0·01 4 1·3 ns 4 2·5 0·05 4 0·5 ns 4 0·4 ns 4 3·5 0·01 4 0·3 ns Root-to-shoot ratio Total root length Main root length Total lateral root length Number of lateral roots Lateral root density Mean lateral root length 1 Error Table 1. Figs 3–5 ANOVA for data presented in 90 90 90 75 90 73 86 72 Data log transformed for statistical analysis. ns, no significant difference at P < 0·05. Consequently 1·3 mmol m–3 AVG was used in our experiments, resulting in ethylene concentrations below detection levels (< 0·013 cm3 m–3 ethylene) in pots irrigated with AVG and without ethylene perfusion (Table 3). Ethylene treatments to the root zones of AVG-treated plants resulted in stable ethylene concentrations bracketing the physiological range (Table 3). There were no significant differences between phosphorus-sufficient and -deficient plants in ethylene concentrations in the root zones. Interactions between phosphorus and ethylene AVG and AVG + ethylene treatments resulted in a small but significant increase in shoot DW (Fig. 4). The small increase in shoot DW (from 0·49 to 0·54 g, Fig. 4) combined with a decrease in root DW (0·23 to 0·19 g) resulted in a significant reduction in the root-to-shoot ratio when phosphorus-deficient plants were treated with AVG (Fig. 4). There was a significant phosphorus–ethylene interaction for the root-to-shoot ratio (Table 1). The total root length (all main and lateral roots) was reduced by phosphorus deficiency and by ≥ 0·1 cm3 m–3 ethylene (Figs 3 & 5), but there was no significant interaction between phosphorus and ethylene for this variable (Table 1). AVG treatment increased the main root length of phosphorus-sufficient plants, an effect which was reversed by added ethylene (Fig. 4). The ethylene-modifying treatments had opposite, although smaller, effects on phosphorus-deficient plants (Fig. 4). Unlike the effects on total root length, high ethylene concentrations did not significantly reduce the length of the main roots compared with controls (no AVG, no ethylene) (Fig. 4). The effects of AVG and ethylene on total lateral root length resembled their effect on total root length, with no significant interaction between phosphorus and ethylene (Fig. 5 & Table 1). The reduction in main root length caused by AVG in phosphorus-deficient plants (Fig. 4) was not accompanied by a significant change in lateral root number (Table 1), resulting in an increase in lateral root density (Fig. 4). The AVG effect was reversed by low ethylene concentrations. AVG had the opposite effect on phosphorus-sufficient roots: it reduced lateral root density, probably by increasing main root elongation (Fig. 4). AVG and ethylene reduced the mean lateral root length regardless of phosphorus treatment (Fig. 5 & Table 1). Although root diameter was unaffected by phosphorus treatment, the high ethylene treatment increased root diameter and reduced specific root length (cm mg DW–1) (data not shown). DISCUSSION Effect of phosphorus deficiency on root architecture The changes in root architecture observed under phosphorus deficiency suggest that resources are redistributed to the roots to allow continued exploration for phosphorus. Phosphorus deficiency resulted in the inhibition of both © 1999 Blackwell Science Ltd, Plant, Cell and Environment, 22, 425–431 Ethylene mediates phosphorus availability responses 429 affected by phosphorus deficiency (Table 1). The maintenance of growth of these roots would be expected to maximize the soil volume colonized by roots, and, therefore, access to phosphorus resources. In real soils, phosphorus availability is non-uniform. From an economic perspective (Bloom, Chapin & Mooney 1985; Fitter 1991), an efficient root system would explore the soil extensively in order to locate phosphorus-rich patches or microsites, but once such a patch is found, should intensively exploit that patch. This strategy could be implemented if roots responded differently to the phosphorus availability in their immediate soil environment, such that branching was more intense where phosphorus was most concentrated, whereas extension of main root axes was accentuated when phosphorus was limiting. In previous research on plants grown with heterogeneous phosphorus distribution, roots growing in a low phosphorus patch elongate but do not proliferate (develop quantities of fine roots), while in a high phosphorus patch, the reverse occurs: main root elongation is reduced, but proliferation is enhanced (Drew & Saker 1978; Snapp, Koide & Lynch 1995). In this study, we found a similar response to phosphorus availability in a homogeneous substrate, as has also been reported for Chrysanthemum (Hansen & Lynch 1998) and some families of Pinus radiata (Theodorou & Bowen 1993). The ability of plants to sense and respond to local phosphorus availability suggests the presence of a signalling mechanism to regulate changes in plant growth. Does ethylene mediate root architectural responses to nutrient stress? In non-AVG-treated plants, phosphorus-deficient roots produced twice as much ethylene per g as phosphorus-sufficient roots, resulting in similar root zone ethylene concentrations despite reduced root biomass in phosphorus-deficient plants (Table 2). Ethylene concentrations in the root tissues would be higher in phosphorusdeficient roots than in phosphorus-sufficient roots, because the production rate is higher. Increased internal ethylene could mediate some of the observed growth and development responses to phosphorus deficiency. When endogenous ethylene production was greatly reduced by AVG, there was a significant interaction between phosphorus availability and ethylene treatment, indicating that phosphorus deficiency changes tissue responsiveness to ethylene. Ethylene could, therefore, Figure 4. Effect of amino-ethoxyvinylglycine (AVG) and ethylene treatments on shoot dry weight, root-to-shoot ratio, main root length and lateral root density of phosphorus-sufficient or deficient plants. Bars indicate standard error of the mean. root and shoot growth, but the disproportionate reduction in shoot growth relative to root growth led to a higher rootto-shoot ratio (Fig. 3). The main root length (Figs 3 & 4) and the average lateral root length were not significantly Phosphorus treatment Root DW (g) Root zone [C2H4] (cm3 m–3) C2 H 4 (cm3 m–3 g DW–1 root) Sufficient Deficient 0·35 ± 0·02a 0·25 ± 0·02b 0·027 ± 0·002a 0·025 ± 0·002a 0·078 ± 0·007a 0·124 ± 0·018b © 1999 Blackwell Science Ltd, Plant, Cell and Environment, 22, 425–431 Table 2. Root dry weight (DW), ethylene concentration in the root zone, and ethylene concentration per g DW root in 5-week-old bean plants grown with sufficient or deficient phosphorus nutrition and no aminoethoxyvinylglycine (AVG). Values shown are means of 10 plants ± standard error of the mean. Values within columns followed by different letters indicate significant differences in a Student’s t-test at P < 0·05 430 K. Borch et al. Ethylene in perfused air (cm3 m–3) Phosphorus (mmol m–3) AVG (mmol m–3) Ethylene (cm3 m–3) n 0 0 0 0·02 0·1 1 Sufficient (50) Deficient (1) 50 + 1 50 + 1 50 + 1 50 + 1 0 0 1 1 1 1 0·027 ± 0·002 0·025 ± 0·002 Not detectable 0·026 ± 0·009 0·12 ± 0·036 1·12 ± 0·31 10 10 20 20 20 20 Figure 5. Effect of amino-ethoxyvinylglycine (AVG) and various ethylene concentrations in the root zone on total root length (main plus lateral roots), total lateral root length, and average lateral root length (data pooled across phosphorus treatments). Bars indicate standard error of the mean. Table 3. Ethylene concentration in the root zone of ethylene- and aminoethoxyvinylglycine (AVG)-treated plants. Plants without AVG were not perfused with either ethylene or air in the root zone. Ethylene data are pooled for sufficient and deficient phosphorus plants irrigated with AVG because there were no significant differences between phosphorus treatments. Values shown are the means ± the standard error of the mean for six plants in each of two replications mediate changes in root morphology via both changes in synthesis and changes in tissue responsiveness. Low endogenous ethylene has been shown to promote root extension in seedling roots for some species, although higher concentrations generally inhibit root growth (Smith & Robertson 1971; Konings & Jackson 1979; Jackson 1985, 1991; Abeles, Morgan & Saltveit 1992). We show here that the effect of ethylene on root length depends on the root type (main or lateral root) and on phosphorus nutrition. In phosphorus-sufficient plants, the main root length was increased by AVG treatment (Fig. 4), indicating that endogenous ethylene production limits main root growth. In phosphorus-deficient plants, AVG inhibited main root growth and exogenous ethylene reversed this effect (Fig. 4), indicating that ethylene promotes root extension under phosphorus deficiency. This is consistent with the hypothesis that ethylene action makes possible the maintenance of root extension under phosphorus-deficient conditions, despite an overall reduction in root growth. Ethylene appears to be important for the reduction in lateral root density observed in phosphorus-deficient plants. AVG reduced lateral root density in phosphorus-sufficient plants but increased it in phosphorus-deficient plants; both effects were reversible with exogenous ethylene. Because the lateral root number was unaffected in both phosphorus treatments (Fig. 3), the observed AVG effect on lateral root density (Fig. 5) is probably a result of the opposite effects of AVG on main root length (Fig. 4). Previous research on the effect of ethylene on root growth utilized plants supplied with sufficient or surplus phosphorus. The present study shows that the response of roots to ethylene depends on phosphorus availability. By irrigating with low, non-toxic AVG concentrations and flushing the root zone with ethylene, we succeeded in exposing the roots to ethylene concentrations in the physiologically relevant range. This method allowed us to show that ethylene permits continued root extension, even under phosphorus deficiency. Moreover, ethylene seems to be involved in the reduction of lateral root density that occurs in low phosphorus-deficient soils, which may be advantageous for efficient soil exploration. These findings support the hypothesis that ethylene may be a global regulator of root responses to soil nutrient availability (Lynch & Brown 1997). © 1999 Blackwell Science Ltd, Plant, Cell and Environment, 22, 425–431 Ethylene mediates phosphorus availability responses A CKNOWLEDGMENTS This research was partially supported by USDA-NRI grants 94-37100-0311 and 97-35100-4456. REFERENCES Abeles F.B., Morgan P.W. & Saltveit M.E. (1992) Ethylene in Plant Biology, pp. 113–114. Academic Press, San Diego. 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