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(American Journal of Botany. 1998;85:1586-1591.)
© 1998 Botanical Society of America, Inc.

The induction of soluble peroxidase activity in bean leaves by wind-induced mechanical perturbation1

Donald F. Cipollini Jr.2,a

a Department of Entomology, Pesticide Research Laboratory, The Pennsylvania State University, University Park, Pennsylvania 16802


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
The induction of defense-related peroxidase (POD) activity in plants occurs in response to many biotic and abiotic stimuli. This controlled greenhouse study was an attempt to provide insight into the nature of the induction of soluble POD activity by noninjurious wind-induced mechanical perturbation (MP). In a time course study, exposure of common bean (Phaseolus vulgaris) seedlings to daily periods of fan-produced wind induced a significant and sustained increase in soluble POD activity in primary leaves of 7–9-d-old seedlings. In a wind-gradient study, wind-induced MP led to increases in soluble POD activity in leaves that were proportionally related to the wind speed experienced by individual seedlings. Wind-induced MP enhanced soluble POD activity to a degree similar to treatment with 5 mmol/L HgCl2, a potent oxidizing elicitor of POD activity in plants. However, no further increases in POD activity were induced by HgCl2 on plants that were preconditioned with wind-induced MP. Finally, short periods of brushing-induced MP enhanced soluble POD activity to the same degree as longer periods of wind-induced MS, suggesting a greater sensitivity to thigmic stimuli than to seismic stimuli in leaves of bean seedlings. This study illustrates the potential importance of wind and other mechanical stimuli as inducers of POD activity and interacting factors in the elicitation of POD activity by other environmental stimuli.

Key Words: bean • brushing • Fabaceae • mechanical perturbation • mercuric chloride • peroxidase • Phaseolus vulgaris • wind


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
The induction of peroxidase (POD) activity in plants occurs in response to numerous biotic and abiotic stimuli, including exposure to pathogens or elicitor preparations, chemical oxidizing agents, red light, and mechanical stimuli (Hammerschmidt, Nuckles, and Kuc, 1982; DeJaegher, Boyer, and Gaspar, 1985; Casal, et al., 1994). The generality of this response is probably related to the multiple forms and overlapping functions of POD in normal plant development and following induction by abiotic and biotic elicitors (see Lagrimini and Rothstein, 1987). For example, POD is believed to play roles in auxin catabolism, the oxidation of phenolics to form lignin, the cross-linking of hydroxyproline-rich glycoproteins in plant cell walls, and the production and breakdown of hydrogen peroxide and other reactive oxygen species (Fry, 1988; Legendre et al., 1993; Klotz and Lagrimini, 1996). The roles that POD can play in cell wall toughening and in the production of toxic secondary metabolites and its simultaneous oxidant and anti-oxidant capabilities can make it an important factor in the integrated defense response of plants to a variety of stresses (Hammerschmidt, Nuckles, and Kuc, 1982; DeJaegher, Boyer, and Gaspar, 1985; Felton et al., 1989; Lorenzini et al., 1994).

In a previous study, I demonstrated the induction of soluble POD activity, soluble cinnamyl alcohol dehydrogenase activity, and lignification in leaves of 7-d-old bean seedlings by short daily periods of noninjurious wind-induced mechanical perturbation (MP) (Cipollini, 1997). Likewise, soluble and cell-wall-bound POD activity and lignification are also induced by brief mechanical rubbing episodes in internodes of Bryonia dioica, the only other plant in which the induction of POD activity by mechanical perturbation has been examined (Boyer, Gaspar, and Lamond, 1979; DeJaegher, Boyer, and Gaspar, 1985). MP-induced biochemical changes in plants are usually accompanied by decreased extension growth, increased radial growth, and reduced leaf area, a phenomenon known as "thigmomorphogenesis" (Jaffe, 1973). Because mechanical stimuli have been shown to immediately induce the production of such reactive oxygen species as H2O2 (the "oxidative burst") in cultured soybean cells (Legendre et al., 1993; Yahraus et al., 1995), POD activity induced by MP may serve an anti-oxidant function to rid cells of reactive oxygen species. In turn, MP-induced POD activity may contribute to such cell-wall toughening events as phenolic cross-linking and lignification, which can strengthen leaf and stem tissues against potential damage caused by MP and lead to a hardened and stunted phenotype. For example, Jaffe, Telewski, and Cooke (1984) have shown that stems of mechanically perturbed bean plants are more resistant to breakage than stems of unperturbed plants.

Regardless of the role that induced POD activity plays in a mechanically stimulated plant, its induction by wind and other forms of MP has not been studied in detail outside of the few studies cited above. Because enhanced POD activity is part of a generalized defense response to many environmental stimuli, its induction by wind-induced MP in the field may precondition the response of plants to other interacting biotic and abiotic stimuli (including drought, frost, and pests) with potentially wide-ranging ecological consequences (see Jaffe and Forbes, 1993; Cipollini, 1997). Thus, in an effort to provide more insight into the induction of soluble POD activity by noninjurious wind-induced MP in leaves of bean plants, I conducted a series of time-course, wind-gradient, and comparative studies to address the following questions: (1) Does the induction of POD activity by wind change through time? (2) Does a quantitative relationship exist between the induction of POD activity and the intensity of the MP? (3) Can wind-induced MP interact with another abiotic elicitor of POD activity? (4) How does the induction of POD activity by wind compare to its induction by another source of MP?


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 REFERENCES
 
Plant growth and mechanical perturbation treatment
Seeds of a bush variety of Phaseolus vulgaris L. (cv. OSU 4091-G) were sown in 0.5-L pots (two seeds per pot) in moistened vermiculite under natural light in a greenhouse. Maximum mid-day light levels ranged between 800 and 1200 µmol photons ·m ·s (photosynthetically active radiation). Greenhouse temperatures ranged from 25° to 30°C. Plants were thinned to one uniform seedling per pot upon emergence and watered with a 100-mL solution of Peter's 20–20–20 N-P-K soluble fertilizer (Grace-Sierra, Milipitas, California, USA) containing 0.0025% N, 0.0025% P2O5, 0.0025% K2O, and Mg, B, Cu, Fe, Mn, Mo, and Zn in minor amounts. Thereafter, plants were watered daily to maintain soil moisture levels near field capacity.

MP was administered by exposing plants to fan-produced wind for the duration of each experiment described below. Eight 60-cm electric box fans were placed along one edge of a greenhouse bench and blew laterally across the seedlings, producing considerable stem and leaf shaking. Fans did not interfere with the irradiation of seedlings. Treatments began when seedlings emerged and the primary leaves had just begun to expand. Wind treatment consisted of two 1-h periods of wind per day (at 0700 and 1600) at the wind speeds designated in each experiment. Wind speeds were measured at the center of each greenhouse bench with a hand-held wind speed indicator (Davis Instruments, Hayward, California, USA). Plants were randomly moved within each treatment daily to ensure that all seedlings experienced the same microenvironment over each treatment period. Wind-exposed plants and the entire fan setup were moved among benches at least once during each treatment period. Wind-treated plants were kept well watered to avoid possible desiccation caused by wind. No wind-induced leaf damage was observed using wind speeds up to 3 m/s. Above this wind speed, however, leaf damage occurred in greater frequency in the form of dried lesions or leaf tearing. Thus, because the emphasis of this research was on the inductive effects of noninjurious MP, wind speeds above 3 m/s were not included in this study. In all cases, unperturbed control plants were grown in a similar randomized fashion in the same greenhouse room as MP-treated plants, but were left unperturbed by wind or other sources of MP.

Time course
Newly emerged seedlings were either placed in wind at 3 m/s or left unperturbed. The identical wind speed was shown to maximally induce POD and lignification in leaves of 7-d-old been seedlings without inducing leaf damage (Cipollini, 1997). Primary leaves were collected from four MS-treated and four control seedlings on days 7, 8, and 9 of treatment, flash frozen in liquid nitrogen, and stored at -20°C until analysis of soluble POD activity.

Wind gradient
Newly emerged seedlings were placed into the following four wind treatments: no wind (control), and wind at 1, 2, and 3 m/s. Wind treatments produced considerable stem and leaf shaking that increased in intensity with increasing wind speed. Preliminary studies indicated that POD was not significantly induced in plants exposed to wind at 1 m/s for two 10-min periods/d (D. Cipollini, unpublished data). Thus, because wind at 1 m/s was thought to be near the lower threshold required for induction, wind speeds below 1 m/s were not included in this study. After 7 d of treatment, primary leaves were collected from four plants from each treatment, flash frozen in liquid nitrogen, and stored as above until analysis for soluble POD activity.

Interaction of wind and HgCl2
Newly emerged seedlings were placed into one of the following four treatments: unperturbed control, treatment with 5 mmol/L HgCl2, wind-induced MP (at 3 m/s), or wind-induced MP (at 3 m/s) plus treatment with 5 mmol/L HgCl2. MP was administered with fan-produced wind as above and began when seedlings were initially placed into the treatments. HgCl2 was dissolved in distilled water and administered by spraying 5-d-old plants with the aqueous solution until runoff as in Kim and Huang (1994). Thus, plants in the MP plus HgCl2 treatment had been conditioned with wind-induced MP for 5 d prior to the application of HgCl2. Primary leaves of six 7-d-old plants from each treatment were collected and stored as above until analysis for soluble POD activity.

Wind vs. brushing
Newly emerged seedlings were either exposed to wind (at 3 m/s) or brushed with a horizontally held bamboo rod across the upper portion of each seedling. Wind treatments consisted of two 1-h periods of wind per day (at 0700 and 1600) as above. Brushing treatments were administered at the same time, each consisting of 60 strokes back and forth across each seedling at a rate of one stroke/s. Each stroke produced a stem deflection of ~25–30% from the vertical, similar to the deflection angle caused by wind at 3 m/s. No leaf damage was caused by this treatment. However, the incidence of leaf damage (e.g., tearing) increased with brushing periods longer than 1 min and with greater brushing frequencies. Again, because the focus of this research was on the inductive effects of noninjurious MP, the wind speed and brushing regimes compared in this experiment were chosen in order to maximize their inductive effect without causing damage. Primary leaves of six 7-d-old plants from each treatment were collected and stored as above until analysis for soluble POD activity.

Soluble POD activity determinations
Leaves were ground using a chilled mortar and pestle in ice-cold 100mmol/L sodium phosphate buffer pH 7.0 using a ratio of 5 mL buffer/g leaf fresh mass. Leaf homogenates were centrifuged at 11 600 x g for 15 min at 4°C, and the cleared supernatant was used immediately as the enzyme source. Soluble POD activity was analyzed by following the formation of tetraguaiacol in a Beckman DU 7400 spectrophotometer (Beckman Instruments, Inc., Fullerton, California, USA) (modified from Hammerschmidt, Nuckles, and Kuc, 1982). Each reaction mixture (1 mL) consisted of 10 µL enzyme extract and 990 µL guaiacol solution containing 0.25% guaiacol (v/v) in 10 mmol/L sodium phosphate buffer pH 6.0 and 0.125% H2O2 (v/v). POD activity in the extracts was measured as an increase in absorbance at 470 nm·min·g fresh mass. The reaction was linear with time and followed for 1 min. Alternatively, some samples were analyzed using ferulic acid as the substrate in the same reaction mixture. Protein content of extracts was determined after Bradford (1976) using the Bio-Rad dye reagent (Bio-Rad, Hercules, California, USA) with bovine serum albumin as the standard. Because soluble protein contents did not differ between MP and control plants in any experiment POD activity is expressed per gram fresh mass. All chemicals were purchased from the Sigma Chemical Co., St. Louis, Missouri, USA.

Means presented in figures and used in statistical analyses represent at least three independent trials per main experiment run concurrently. However, main experiments were done over a 2-mo period during which greenhouse temperatures and particularly ambient light levels steadily rose. Thus, emphasis has been placed on interpreting variation found within each experiment. Data were analyzed for each experiment with Analysis of Variance using the General Linear Models procedure on SAS (SAS Institute, Cary, North Carolina, USA).


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
REFERENCES
 
The results presented here are an attempt to partially characterize the induction of soluble POD activity by wind-induced mechanical perturbation, a little investigated inducer of POD activity with potentially important ecological consequences.

Time course of soluble POD activity
Wind-induced MP at 3 m/s induced a significant and sustained increase in soluble POD activity in primary leaves of 7–9-d-old seedlings (Fig. 1), a period of time during which the primary leaves had just stopped expanding. POD activity of MP plants did not differ over this time course. However, POD activity in MP plants relative to controls ranged from ~17% higher on day 7 to 35% higher on day 8, primarily because of a decline in control levels. While it is not known how long this induction persists, Lagrimini and Rothstein (1987) have shown that POD activity induced in tobacco leaves by tobacco mosaic virus infection is sustained for at least 14 d after elicitation. Thus, POD activity in wind-treated bean plants would likely remain enhanced for some period of time beyond that measured in this experiment even after relaxation of the stimulus.



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  		Fig. 1. Soluble peroxidase activity (±1 SE) in primary leaves of 7–9-d-old mechanically perturbed (MP) and control plants. For each day, bars with different letters are significantly different at {alpha} = 0.05. N = 4.

 
Relationship of POD induction to the intensity of wind
No induction of POD activity over the control level was detected in leaves of plants treated with wind at 1 m/s (Fig. 2). This level of wind may represent the lower threshold for the significant induction of POD. However, POD activity in unperturbed control plants varied among experiments and was fairly high in this one. It is possible that background sources of MP (e.g., gravity, greenhouse exhaust fans, etc.) may have induced POD activity to a degree not distinguishable from wind at 1 m/s, obscuring any indication of induction, although no wind movement was detectable over control benches. If this were the case, differences should appear with a reduction in background POD induction if wind at 1 m/s is indeed sufficient to induce POD activity over control levels. Results of an independent preliminary study indicated that exposure to wind at 1 m/s for 10 min twice per day was not sufficient to induce POD activity over control levels in 7–10-d-old plants (D. Cipollini, unpublished data), supporting the notion that wind at 1 m/s is near the lower threshold for significant induction. Detecting the actual lower threshold for significant induction would require greater control of background noise and finer scale increments in wind speed.



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  		Fig. 2. Relationship of soluble peroxidase activity (±1 SE) in primary leaves of 7–d-old bean plants to wind speed from 0 to 3 m/s. Bars with different letters are significantly different at {alpha} = 0.05. N = 4.

 
Above this threshold level of wind, POD activity increased ~20% with each 1 m/sincrease in wind speed. Rapid and transient induction of the oxidative burst, protein kinase activity, and movement of putative secondary messengers like calcium occur immediately in response to touch, wind, or other mechanical stimuli (Knight, Smith, and Trewavas, 1992; Trewavas and Knight, 1994; Yahraus et al., 1995; Bogre et al., 1996). Likewise, a number of genes responsive to mechanical stress (TCH [TOUCH] genes) that encode calmodulin and calmodulin-related proteins are induced within several minutes by touch (Braam and Davis, 1990; Braam et al., 1996; Oh et al., 1996). Because the magnitude of the induction of such MP-signaling events and MP-induced gene expression is related to the intensity of the MP, wind may have increased the strength of the signal required to induce POD activity in a quantitative fashion with increasing wind speed.

Botella, Arteca, and Frangos (1995) have demonstrated the presence of a MP-inducible ACC-synthase gene in leaves of mung bean, which encodes the key regulatory enzyme in the ethylene biosynthetic pathway. Increased ethylene evolution occurs in response to MP in many plants, an effect shown to mediate their subsequent growth response (Jaffe et al., 1985; Jaffe and Forbes, 1993). Ethylene has also been implicated in the regulation of POD activity and other defense-related proteins in plants (Abeles, Morgan, and Saltveit, 1992). Thus, ethylene evolution may have increased with increasing wind intensity and upregulated the activity of POD accordingly, in response to, or in concert with other signaling events.

These results suggest that POD activity is probably induced in plants to some degree at all times in the field due to the ubiquitous nature of such sources of MP as wind, rain, and the effect of gravity on plant tissues. However, the level of POD induction is likely to vary with the degree of exposure of plants to such MP as chronic winds of varying intensity.

Interaction of wind and HgCl2
The induction of POD activity by wind and HgCl2, a known oxidizing elicitor of defense-related proteins in plants (Kim and Huang, 1994), was investigated to compare the effectiveness of these two abiotic elicitors at inducing POD activity and to examine their interactive effects. POD activity in MP-treated plants was ~78% higher than in controls in this experiment, a much greater induction than that found in other experiments, partly because control levels were very low in this experiment. Treatment of plants with wind at 3 m/s induced leaf POD activity to a significantly higher level than spraying plants with 5 mmol/L HgCl2 (Fig. 3). However, 5 mmol/L HgCl2 treatment of plants that had been conditioned for 5 d with wind-induced MP (at 3 m/s) induced leaf POD activity to a level that did not differ from either wind or HgCl2 alone, and no statistical interaction between these two stimuli was observed.



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  		Fig. 3. Effect of mechanical perturbation (M), HgCl2 (H), and their interaction on soluble peroxidase activity (±1 SE) in primary leaves of 10-d-old bean plants. Bars with different letters are significantly different at {alpha} = 0.05. N = 6.

 
Mercuric chloride caused the appearance of numerous necrotic flecks on the leaves of bean plants, likely due to oxidative damage to plant cells. Induced POD activity detected in these plants probably serves either an anti-oxidant or wound-healing function (Fry, 1988). However, HgCl2 treatment of plants preconditioned with wind-induced MP induced no further increases in POD activity than wind or HgCl2 alone. It is possible that the POD response was already induced maximally by MP, so that HgCl2 could induce no further increases. It is also possible that plants preconditioned with wind were more resistant to damage caused by HgCl2, thus no further elicitation of POD activity occurred. However, the appearance of necrotic flecks due to HgCl2 treatment on plants preconditioned with MP was similar to that on plants treated with HgCl2 alone, suggesting that this was not the case. Although MP and HgCl2 may induce POD through different mechanisms, the reduced induction of POD by HgCl2 on wind-treated plants indicates that conditioning of plants with wind-induced MP can alter their responsiveness to other abiotic elicitors of POD activity.

Effectiveness of wind vs. brushing
The induction of POD activity by wind and brushing was investigated to compare the effectiveness of these two distinct forms of MP at inducing POD activity in leaves of bean plants. POD activity in leaves of 7-d-old plants was induced by twice daily 1-min periods of brushing with a bamboo rod to a similar degree as twice daily 1-h periods of wind at 3 m/s (Fig. 4). In this experiment, POD activity in MP-treated plants was ~45–50% higher than in controls. Wind-induced MP was primarily in the form of stem and leaf shaking (seismic stimulation). Brushing, on the other hand, not only produced some seismic stimulation as plants were bent and returned to vertical after each brush stroke, but also caused actual touching (thigmic stimulation) to occur as the bamboo rod contacted stem and leaf surfaces with each stroke. Because two short periods of brushing per day induced POD activity to the same degree as two longer periods of wind per day, it is possible that plants are more responsive to thigmic stimulation imposed by brushing than to seismic stimulation alone. A study of the regulation of soybean and eggplant growth by shaking and rubbing or flexing illustrated that these plants were more responsive in such growth parameters as stem length and leaf area to thigmic stimulation than to seismic stimulation (Latimer, Pappas, and Mitchell, 1986). It is also possible that the induction of POD activity plateaus for some physical or biochemical reason at the level found in plants treated with wind at 3 m/s. In any case, these results indicate that the strength of the induction of POD activity by MP in plants may depend on the type of the MP imposed. These results also further support the notion that induced POD activity in wind-treated plants is indeed due to the mechanical component of the wind and not due to a secondary effect (such as drying) produced by the wind.



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  		Fig. 4. Effect of wind-induced mechanical perturbation (W) and brushing-induced mechanical perturbation (B) on soluble peroxidase activity (±1 SE) in primary leaves of 10-d-old bean plants. Bars with different letters are significantly different at {alpha} = 0.05. N = 6.

 
SDS-PAGE separation of soluble proteins from 7–9-d-old wind-treated and control bean leaves, followed by POD activity staining, indicated that three identical isozymes of POD were present in both wind-treated and control plants based on band migration (D. Cipollini, unpublished data). DeJaegher, Boyer, and Gaspar (1985) found that rubbed and nonrubbed internodes of Bryonia dioica also contained three identical major isozymes of POD in the soluble fraction. However, a fourth weak isozyme was detected in rubbed internodes that appeared much later in nonrubbed internodes. The lack of data on band size prevents the direct comparison of these isozymes with those found in my study, although it is possible that the isozymes detected in both studies were similar. Because no novel isozymes of POD were induced in bean leaves by wind in my study, increases in total POD activity were apparently due to either increased synthesis of constitutively present isozymes or through their upregulation by such processes as induced alterations in enzyme solubility (Ingemarsson, 1995). In a subset of samples from the wind-gradient study, POD activity toward ferulic acid was proportional to that toward guaiacol (D. Cipollini, unpublished data). Because ferulic acid is a natural substrate of POD in plant cells (Fry, 1988), this finding suggests that POD activity induced by MP has the ability to contribute to the cross-linking of phenolics and other compounds that contribute to cell wall structure and enhanced leaf toughness.

Another pattern that can be detected in the data is the steadily increasing ability of wind to induce POD from experiment to experiment. Wind at 3 m/s was used in all experiments. The absolute induction of POD by this wind speed in the last experiment (Fig. 4) was 4–5 times higher than in the first experiment (Fig. 1). Experiments were done in chronological order, as presented in the methods, from late April to late June. While greenhouse temperatures were well regulated over this period, ambient light levels steadily increased. This observation, while untested, suggests that the ability of wind to induce POD may depend on the light environment experienced by the seedlings. Specifically, it appears that higher light levels may support higher levels of induction.

Conclusions
The results from this study illustrate that wind (and MP in general) can be an effective inducer of POD activity in plants, the induction of which is related to the intensity of the MP, can be sustained and is comparable to the effect of other known elicitors of POD activity. The effect of wind is also sufficient to alter the response of plants to the subsequent exposure to other elicitors of POD activity in plants. In the field, enhancement of leaf POD activity by conditioning of plants with wind or rain may alter the interaction of those plants with other environmental stimuli, including light, moisture, pests, and abiotic pollutants, in which POD activity can play a defensive role. For example, MP in plants has been shown to increase stem-bending tolerance (Jaffe, Telewski, and Cooke, 1984), drought tolerance (Suge, 1980), chilling tolerance (Keller and Steffen, 1995), and pest resistance (Cipollini, 1997). Many of these effects may be due, in part, to the enhanced activity of POD induced by MP playing a protective role against this diverse array of environmental stimuli.


   FOOTNOTES
 
1 The author thanks Jack Schultz, Patrick Moran, and Kendra Lentz for their contributions to this work. Suggestions by M. Jaffe and S. Gilroy greatly improved this manuscript. Funding for this work was provided by the Department of Entomology, Penn State University, and National Science Foundation grants DEB-318073 and DEB-9420013 to Jack Schultz. Back

2 Current address: Department of Ecology and Evolution, University of Chicago, 1101 East 57th Street, Chicago, Illinois 60637. Back


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 RESULTS AND DISCUSSION
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