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1,000 ppm CCC plus SLW and 100 ppm GA, plus 1,000 ppm CCC were added to the treatments in Experiment 3 (spring 1996). CCC,. GA3, or CCC plus GA3 ...
J Plant Growth Regul (1997) 16:245–251

© 1997 Springer-Verlag New York Inc.

Possible Involvement of Altered Gibberellin Metabolism in the Induction of Tomato Irregular Ripening in Dwarf Cherry Tomato by Silverleaf Whitefly S. Hanif-Khan,1 R. C. Bullock,1 P. J. Stoffella,1,* C. A. Powell,1 J. K. Brecht,2 H. J. McAuslane,3 and R. K. Yokomi4 1

Indian River Research and Education Center, IFAS, University of Florida, Fort Pierce, FL 34945-3138; the 2Horticultural Sciences Department, and the 3Entomology and Nematology Department, IFAS, University of Florida, Gainesville, FL 32611-0630, and the 4USDA-Agricultural Research Station, Orlando, FL 32803, USA Received May 27, 1997; accepted September 26, 1997

Abstract. External and internal tomato irregular ripening (TIR) symptoms were associated with the feeding of silverleaf whitefly (SLW), Bemisia argentifolii Bellows and Perring. Four experiments consisting of various soil drench applications of GA3 (100 ppm) and cycocel (CCC, an inhibitor of GA biosynthesis; 1,000 and 2,000 ppm) were applied to dwarf cherry tomato cv. Florida Petite in the presence and absence of SLW in an attempt to mimic the disorders induced by the SLW. The application of GA3 induced external and internal TIR symptoms similar to the SLW-induced disorder. Minimal TIRlike symptoms also occurred in the control and CCC treatments. Internal TIR symptoms in GA3, GA3 plus SLW, and GA3 plus CCC treatments ranged from 66% to 97% throughout the experiments. The incidence of external TIR symptoms was highest in the GA3 plus SLW treatment compared with the other treatments. CCC reduced the incidence of external TIR symptoms induced by GA3 or GA3 plus SLW treatments. However, CCCtreated plants also attracted more oviposition and higher populations of SLW and consequently induced a greater incidence of TIR symptoms than SLW treatment alone. Furthermore, although low SLW populations may be associated with low external TIR symptoms, internal TIR symptoms almost always remained high in infested plants. The results suggest that the TIR disorder in dwarf cherry tomato which is induced by the SLW may be a gibberellin-regulated disorder.

Abbreviations: TIR, tomato irregular ripening; SLW, silverleaf whitefly; SSL, squash silverleaf; CCC, (2-chloroethyl trimethylammonium chloride; GA, gibberellic acid; K, kinetin; PG, polygalacturonase; PGR, plant growth regulator; ANOVA, analysis of variance; ABA, abscisic acid. *Author for correspondence: Indian River Research and Education Center, IFAS, University of Florida, 2199 South Rock Road, Fort Pierce, FL 34945-3138.

Key Words. Cherry tomato—Gibberellic acid— Cycocel—Silverleaf whitefly—Tomato irregular ripening Tomato irregular ripening (TIR) has been associated with the feeding of immature and/or adult silverleaf whitefly (SLW), Bemisia argentifolii Bellows and Perring (Homoptera: Aleyrodidae) (Maynard and Cantliffe 1989, Schuster et al. 1989). TIR is a fruit disorder without foliar symptoms (Schuster et al. 1990) characterized by uneven color development during ripening in tomato (Lycopersicon esculentum Mill.) fruit. Fruit from SLWinfested tomato plants develop longitudinal red streaks visible externally over the septa and blotches of yellow, red, or green in the locule area. In addition, fruit exhibit white or yellow tissues internally (Maynard and Cantliffe 1989, Schuster et al. 1990). Jimenez et al. (1994) reported that the TIR is a host-specific disorder induced by the SLW, but the mechanism(s) of symptom development has not been specifically identified. Yokomi et al. (1995) reported that the squash silverleaf (SSL) disorder induced by the feeding of SLW on Curcubita pepo L. results from an alteration of normal plant hormone production. In their study, foliar and soil drench application of CCC (2-chloroethyl trimethylammonium chloride), a GA biosynthesis inhibitor, induced leaf silvering symptoms in Senator and Dixie squash similar to those induced by SLW. CCC-induced silvering initially appeared in the major veins and spread laterally but did not extend over more than 80% of the leaf surface. Some of the cultivars treated with CCC had shorter stem internodes, higher chlorophyll content, and increased root and stem weight compared with untreated plants. GA3 applied after CCC on SLW-infested or uninfested plants decreased leaf silvering symptoms. More oviposition and nymphs of SLW occurred on CCC-

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treated plants than the untreated controls. Yokomi et al. (1995) reported that both CCC and SLW induced similar silvering symptoms in certain squash and that the leaf discoloration induced by CCC and SLW may be caused by the regulation of endogenous plant hormone synthesis. GA3 is known to retard ripening of tomatoes. AbdelKadar et al. (1966) reported that tomato ripening was retarded and the fruit ripened over a longer period of time when treated with kinetin (K) or K-GA at the maturegreen stage. Mature-green tomatoes treated with 1,000 ppm K-GA3 exhibited uneven color development or blotchy ripening. Dostal and Leopold (1967) treated intact fruit and pieces of fruit in tissue culture with 10−7 M GA3 and reported marked retardation of ripening and color development and prevention of ethylene-induced ripening but not ethylene-stimulated respiration. Mignani et al. (1995) reported inhibition of ripening in tomato pericarp discs by GA3 and calcium, which altered the pattern of pectin solubility changes. GA3 at 10 mM was also reported to delay tomato ripening significantly (Ben-Arie 1995) and reduce the amount of polygalacturonase (PG) activity, whereas GA3 at 100 and 1,000 mM almost eliminated PG activity. The purpose of this study was to evaluate dwarf cherry tomato fruit for external and internal TIR symptoms after continuous drench application of CCC and GA3 to plants in the presence or absence of SLW to evaluate the possibility that TIR symptoms are related to altered GA levels.

Materials and Methods Plant Establishment Dwarf cherry tomato cv. Florida Petite (seeds donated by Dr. M. Schon, The Land, Epcot Center, Walt Disney World, Orlando, FL) were sown in trays (72 cells/tray; 4 × 4 × 6 cm) filled with Vergrow Transplant Mix A (V-J Growers Supply, Apopka, FL) containing Canadian sphagnum peat moss, coarse grade vermiculite, starter nutrients, and a wetting agent. The media in the trays were kept moist at all times. Seeds were germinated in a growth chamber with fluorescent light (14-h light and 10-h dark at 27°C). About 2 weeks after sowing, the germinated seedlings were transplanted into plastic pots (16 × 16 cm) filled with Vergrow Container Mix A (V-J Growers Supply), which contained Canadian sphagnum peat moss, coarse grade vermiculite, perlite, starter nutrients with major and minor essential elements, and a wetting agent. Seedlings were grown in a whitefly-free condition in a growth chamber. Temperatures in the chamber ranged from 24 to 37°C and relative humidity from 55 to 100%. Manual watering was scheduled daily, and the plants were fertilized with 20N-16P-8K (2.5 g/liter) once a week.

Plant Growth Regulators (PGRs) in the Absence of SLW Experiment 1. The experiment was conducted during summer 1996 in a glass greenhouse with 50% shade (Environmental Horticulture De-

S. Hanif-Khan et al. partment, University of Florida, Gainesville). Plants were moved from the growth chamber and placed into the greenhouse about 2 weeks after transplanting. Plants were watered manually each day and were fertilized as described above. Temperatures ranged from 24 to 34°C and relative humidity from 50 to 76%. Treatments consisted of an untreated control, drench applications of 2,000 ppm CCC (8.3 ml/liter) (Cycocel 11.8%, American Cyanamid, Wayne, NJ), 100 ppm GA3 (2.5 mL/liter) (Gib Gro 4%, Agtrol Chemical Products, Houston, TX) and CCC plus GA3. Each PGR solution contained 0.01% Tween 20 surfactant. Each pot was treated with 50 mL of the respective PGR solution once a week for 8 weeks beginning at the reproductive stage (3 or more weeks after transplanting) (eight total applications). The control plants were treated with 50 mL of water. The experimental design was a randomized complete block design with treatments replicated six times. Experiment 2. During fall 1996, Experiment 1 was repeated in a shaded (50%) plastic-roofed greenhouse (USDA-ARS, Plymouth Laboratory, Apopka, FL). Seedlings were moved from the growth chamber and placed into the greenhouse about 2 weeks after transplanting. Drip irrigation was scheduled for 5 min daily and later reduced to every other day when the PGR treatments were initiated. Fertilization was scheduled as described previously. Temperatures ranged from 10 to 27°C, and relative humidity ranged from 45 to 100%. The CCC treatment was reduced to 1,000 ppm because of severe stunting observed at 2,000 ppm, and the PGR solutions were applied without the surfactant. Each pot was treated with 50 mL of the respective PGR solutions once a week for 8 weeks during early fruit set (5 weeks after transplanting). Control plants were treated with 50 mL of water. The tomato plants were sprayed with Benlate to control fungal infection and with imidacloprid (0.04 g ai/plant) (Admire 2F, Bayer, Kansas City, MO) in 25 mL of water/plant as a soil drench, and a second treatment was applied a month later to maintain a whitefly-free environment. A randomized complete block experimental design was used with treatments replicated eight times. Fruit Harvest and TIR Evaluation (Experiments 1 and 2). Tomato fruit were harvested at the breaker to pink stages and stored at 20°C. At the full-red stage, the incidence of external TIR symptoms was evaluated, the fruit sliced in half, and the incidence of internal white tissue evaluated. In Experiment 1, external TIR symptoms were evaluated as with (blotches and streaks) and without TIR symptoms, and internal TIR symptoms were evaluated as with (white endocarp) or without TIR symptoms. In Experiment 2, external TIR symptoms were evaluated as with (blotches and streaks) and without TIR symptoms, and internal TIR symptoms were graded as 0 (no symptoms), 1 (pink endocarp), and 2 (white endocarp). The total fruit yield reported for each treatment represented all of the fruit harvested until the last day of the experiment (Experiment 2). The number of fruit reported consisted only of fruit that were evaluated for TIR symptoms (Experiments 1 and 2).

PGRs in the Presence and Absence of SLW Experiment 3. The experiment was conducted during spring 1996 in a glass greenhouse with 50% shade (Environmental Horticulture Department, University of Florida, Gainesville). Two weeks after transplanting, four plants were placed into each of 15 screened cages (61 × 61 × 91 cm). The cages were made of 1.3-cm-diameter PVC frame, covered with a 70 mesh off-white nylon chiffon fabric (BioQuip Products, Gardena, CA). Drip irrigation was scheduled to water for 3 min daily. Fertilization was scheduled as described for Experiments 1 and 2. Temperatures ranged from 15 to 46°C, and relative humidity ranged from 30 to 75%. Treatments consisted of an untreated control, SLW-infested, drench

Whitefly-induced GA3 Metabolism Changes applications of 100 ppm GA3 or 2,000 ppm CCC, and SLW plus 100 ppm GA3. Three weeks after transplanting, 50 mL of CCC or GA3 solution was applied as a soil drench into the appropriate cages three times a week (18 total applications). The experimental design was a randomized complete block with treatments replicated three times. SLW-infested treatments were initiated 3 weeks after transplanting by releasing 150 pairs of adult SLW twice, a week apart, into the appropriate cages. Adult SLW were obtained from colonies maintained on tomato in a greenhouse. Control plants in whitefly-free cages were treated with imidacloprid (0.04 g ai/plant) in 25 mL of water/plant as soil drench. Tomato fruit were harvested at the breaker to pink stages and stored at 20°C. At the full-red stage, external TIR symptoms were evaluated, the fruit sliced in half, and the internal white tissue symptoms evaluated. External and internal TIR symptoms were evaluated as described previously for Experiment 1. The total fruit yield and number of fruit were reported as described previously for Experiment 2. Experiment 4. During summer 1996, Experiment 3 was repeated in an open shade (50%) house (Environmental Horticulture Department, University of Florida, Gainesville). Two weeks after transplanting, four potted plants were placed in each of 21 screened cages as described previously for Experiment 3. Manual watering was scheduled daily, except for rainy days. Fertilization was applied as described previously. CCC was applied at 1,000 ppm and two additional treatments of 1,000 ppm CCC plus SLW and 100 ppm GA, plus 1,000 ppm CCC were added to the treatments in Experiment 3 (spring 1996). CCC, GA3, or CCC plus GA3 was applied (50 mL/pot) as a soil drench into the appropriate cages three times a week (24 total applications). SLW infestation was also reduced to 50 pairs of adult SLW released twice, a week apart, into the appropriate cages. Adult SLW were obtained from a laboratory SLW colony maintained on cotton (Gossypium hirsutum) and collard (Brassica oleracea) plants (Entomology and Nematology Department, University of Florida, Gainesville). The experimental design was a randomized complete block with treatments replicated three times. Tomato fruit were harvested at the breaker to pink stages and stored at 20°C. At the full-red stage, external TIR symptoms were evaluated, the fruit sliced in half, and the incidence of internal white tissue symptoms evaluated. Total fruit yield, number of fruit, and external and internal TIR symptoms were measured as described previously for Experiment 2.

Insect Count About 5 weeks after transplanting (before the first harvest), three to four leaflets were collected from each plant in each experiment, except for Experiment 3, for egg, nymph, red-eyed nymph, and exuviae counts. Counts were made under 15× magnification on one 2-cm2 disk cut from the center of each leaflet. Initial leaf sampling revealed no eggs, nymphs, or exuviae in either Experiment 1 or 2. However, during fruit development stage, plants were infested with SLW in Experiment 2.

247 Table 1. Effect of PGRs on TIR symptoms of dwarf cherry tomato (Experiment 1). TIR symptoms (%)a Treatment Control CCCc GA3c GA4 + CCC

Fruit quantity 270 137 315 120

External 1b 7b 20 a 14 a

b

Internal 14 b 12 b 76 a 66 a

a

Values were subjected to arcsin(sqrt((% fruit + 0.1)/100)) transformation. b Mean separation by Waller/Duncan multiple range test at the p < 0.05 level. c Concentration of CCC 4 2,000 ppm and GA3 4 100 ppm.

were separated by the Waller/Duncan multiple k-ratio comparison at the 5% level.

Results PGRs in the Absence of SLW

Experiments 1 and 2. Application of GA3 in the presence and absence of CCC consistently resulted in a higher incidence of external and internal TIR symptoms than CCC alone or the untreated control in Experiments 1 and 2 (Tables 1 and 2) (Figs. 1 and 2). The percent of fruit with TIR symptoms was similar between the control and CCC treatments in both experiments. Internal TIR grade 1 symptoms (pink endocarp) were higher in the control and CCC treatments, whereas grade 2 symptoms (white endocarp) were higher in the GA3 and GA3 plus CCC treatments (Experiment 2; Table 2). The lower nutritional status of the plants attributed to overwatering and a late SLW infestation may have contributed to the high (59 and 63%) internal TIR symptoms in the untreated control and CCC treatments, respectively (Experiment 2; Table 2). Overwatering during early plant growth (Experiment 2) may have leached the nutrients from the pots, particularly K, resulting in internal white tissue associated with the blotchy ripening disorder as reported by Picha and Hall (1981). However, fruit yield did not differ among the treatments (Experiment 2; Table 2).

PGRs in the Presence and Absence of SLW Statistical Analyses The percentage of fruit with external and internal TIR symptoms was calculated and data arcsine square root transformed before conducting analysis of variance (ANOVA). The number of eggs, nymphs, and exuviae/cm2 were also calculated and data transformed by square roots before conducting ANOVA. All of the measured variables were subjected to ANOVA using SAS (SAS Institute 1990). Treatment means

Experiment 3. Fruit from plants treated with GA3 plus SLW exhibited the highest incidence of external TIR symptoms (56%) among the treatments in Experiment 3 (Table 3 and Fig. 3). The incidence of external TIR symptoms in the fruit was very low in the control, CCC,

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Table 2. Effect of PGRs on TIR symptoms of dwarf cherry tomato (Experiment 2). TIR symptoms (%)a Internal graded Treatment Control CCCf GA3f CCC + GA3

Fruit quantity 422 495 450 478

Externalb e

6b 7b 44 a 42 a

Internalc

1

2

Fruit yield (g/plant)

59 b 63 b 84 a 84 a

36 a 32 a 13 b 11 b

24 b 31 b 72 a 73 a

90.3 97.8 92.3 99.3g

a

Values were subjected to arcsin(sqrt((% fruit + 0.1)/100)) transformation. b External TIR symptoms were rated as with or without symptoms. c Combined grade 1 and 2 internal TIR symptoms. d Internal white tissue rating scale: 0 (no symptoms), 1 (pink endocarp), and 2 (white endocarp). e Mean separation by Waller/Duncan multiple range test at the p < 0.05 level. f Concentration of CCC 4 1,000 ppm and GA3 4 100 ppm. g No significant difference.

Fig. 3. External TIR symptoms induced by drench application of GA3 plus SLW-infested fruit in dwarf cherry tomatoes.

Fig. 4. Internal TIR symptoms induced by drench application of GA3 plus SLW-infested fruit in dwarf cherry tomatoes. Fig. 1. External TIR symptoms induced by drench application of GA3 in dwarf cherry tomatoes.

Fig. 2. Internal TIR symptoms induced by drench application of GA3 in dwarf cherry tomatoes.

Fig. 5. Internal TIR symptoms induced by drench application of GA3 and symptomless untreated control fruit in dwarf cherry tomatoes.

Whitefly-induced GA3 Metabolism Changes

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Table 3. Effects of PGRs and SLW on TIR symptoms of dwarf cherry tomato (Experiment 3). TIR symptoms (%)a Treatment

Fruit quantity

External

Internal

Fruit yield (g/plant)

Control CCCc SLWd GA3c GA3 + SLW

95 58 90 111 77

3 bb 0b 7b 10 b 56 a

9c 5c 47 b 97 a 96 a

11.5 b 3.1 b 8.3 b 32.3 a 5.1 b

a

Values were subjected to arcsin (sqrt((% fruit + 0.1)/100)) transformation. b Mean separation by Waller/Duncan multiple range test at the p < 0.05 level. c Concentration of CCC 4 2,000 ppm and GA3 4 100 ppm. d About 300 pairs of adult SLW.

SLW, and GA3 treatments. However, SLW infestation caused a high (47%) incidence of internal TIR symptoms. GA3 treatment, in the presence (96% (Fig. 4) and absence of SLW (97%) (Fig. 5), induced a higher incidence of internal TIR symptoms than the control (Table 3). The incidence of internal TIR symptoms was low and did not differ between the control and CCC treatments. GA3-treated plants had the highest total fruit yield in Experiment 3 (Table 3). The low incidence of external TIR symptoms in SLW-infested plants may have resulted from low SLW population, but internal TIR symptoms were high, suggesting that internal TIR symptoms were induced more easily by SLW feeding than external TIR symptoms. Plants treated with CCC were severely stunted with dark green leaves and fewer flowers than the control plants. SLW-infested plants also were stunted, and leaves exhibited chlorotic and necrotic spots during later stages of the experiment.

Experiment 4. Plants treated with GA3 in the presence or absence of SLW exhibited a significantly higher incidence of both external and internal TIR fruit symptoms than the untreated control (Table 4). Fruit from GA3 plus CCC-treated plants (23%) exhibited fewer external TIR symptoms than GA3-treated plants (45%). Internal TIR development was high at 83%, 81%, and 86% in the GA3, GA3 plus CCC, and GA3 plus SLW treatments, respectively, compared with the control (15%). However, internal TIR incidence did not differ between the GA3 plus CCC and CCC plus SLW treatments. Grade 1 internal TIR symptoms were observed in all of the treatments (14–32%). The light pink endocarp (grade 1 symptom) may have been induced by other factors such as nutrition and environmental conditions. All GA3 treatments, however, induced a higher percent-

Table 4. Effects of PGRs and SLW on TIR symptoms of dwarf cherry tomato (Experiment 4). TIR symptoms (%)a Internal graded Treatment Control CCCf SLWg CCC + SLW GA3f GA3 + CCC GA3 + SLW

Fruit quantity 231 148 128 104 282 257 240

Externalb Internalc 1 e

4c 9 bc 3c 21 b 45 a 23 b 47 a

15 d 17 d 53 c 70 b 83 a 81 ab 86 a

14 13 23 28 27 26 32h

2

Fruit yield (g/plant)

1c 4c 30 b 42 ab 56 a 55 a 54 a

39.8 a 16.3 b 20.1 b 18.3 b 50.4 a 45.5 a 49.2 a

a

Values were subjected to arcsin(sqrt((% fruit + 0.1/100)) transformation. b External TIR symptom was rated as with and without symptoms. c Combined grade 1 and 2 internal TIR symptom. d Internal white tissue rating scale: 0 (no symptom), 1 (pink endocarp), and 2 (white endocarp). e Mean separation by Waller/Duncan multiple range test at the p < 0.05 level. f Concentration of CCC 4 1,000 ppm and GA3 4 1,000. g About 100 pairs of adult SLW/cage. h No significant difference.

age of fruit with grade 2 (white endocarp) internal TIR symptoms than the other treatments. The GA3, GA3 plus CCC, SLW, and the control treatments had significantly higher yields than CCC in the presence or absence of SLW (Table 4). CCC plus GA3-treated (23 and 81%) or SLW-infested (21 and 70%) plants had significantly less fruit with external and internal TIR symptoms, respectively, than GA3 or GA3 plus SLW treatments. However, the incidence of internal TIR fruit symptoms from the GA3 plus CCC treatment did not differ from the GA3 or GA3 plus SLW treatment. Furthermore, CCC plus SLW plants had significantly higher incidences of external and internal TIR symptoms than SLW-infested plants. Therefore, the application of CCC reduced only the external TIR symptoms, but not internal TIR symptom expression in the presence or absence of SLW or GA3 (Table 4). Among the SLW-infested treatments, the highest incidences of external and internal TIR symptoms were observed in the GA3 plus SLW treatment, followed by the CCC plus SLW treatment, whereas the lowest incidence occurred in the SLW treatment. GA3 plus SLWtreated plants produced about a 2.5-fold higher yield than CCC plus SLW- or SLW-treated plants (Table 4). Application of CCC in the presence of SLW did not reduce the expression of external and internal TIR symptoms more than the SLW treatment alone (Table 4) because of the high SLW population in the CCC plus SLW treatment (Table 5). Leaf samples of SLW plus CCC plants

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Table 5. Population of SLW in the presence and absence of PGR in dwarf cherry tomato in Experiment 4. Results are no./cm2 leaflet, where no./cm2 4 total upper and lower 10–12 leaflets/4 cm2 (total area of upper and lower leaflets). Values were subjected to [square root (no./cm2 + 0.1)] transformation; mean separation by Waller/Duncan multiple range test at p < 0.05 level. Treatment

Eggs

Nymphs

Redeye

Exuviae

Control CCCd SLWe CCC + SLW GA3d GA3 + CCC GA3 + SLW

0 cc 0 c 9.1 b 27.9 a 0 c 0 c 9.6 b

1.1 bf 0 b 4.7 b 21.0 a 0 b 0 b 5.1 b

0.8 abf 0 b 0.7 ab 2.1 a 0 b 0 b 1.1 ab

0 b 0 b 0.2 ab 08. a 0 b 0 b 0.3 ab

had significantly more eggs and nymphs than other treatments (Table 5). The low levels of external and internal TIR symptoms in the SLW treatment may be associated with the low SLW population on those plants compared with the CCC plus SLW treatment (Tables 3 and 4). Control, CCC-, and SLW-infested plants had a similar percentage of fruit with external TIR symptom expression. The lowest incidences of fruit with internal TIR symptoms were in the control and CCC-treated plants. SLW-infested plants exhibited higher internal TIR (white endocarp) than the control or CCC treatments. Internal TIR grade 1 symptom expression was similar among all the treatments. However, each treatment exhibited more than 30% fruit with internal TIR grade 2 symptoms than the control (1%) or CCC (4%) treatments (Table 4). Perhaps the internal TIR (15%) expression in the control was caused by the nutritional status of the plants.

Discussion Soil drench application of GA3 resulted in external and internal TIR symptom expression similar to the SLWinduced disorder in dwarf cherry tomato. Generally, GA3 application consistently inhibited ripening or induced high incidence of external and internal TIR symptoms (Experiments 1–4; Tables 1–4). The inhibition of tomato ripening by GA3 is in agreement with reports by AbdelKader et al. (1996), Dostal and Leopold (1967), BenAire et al. (1995), and Mignani et al. (1995). GA3-treated plants also exhibited blotchiness and streakiness in the fruit, especially in combination with CCC, which are distinct symptoms expressed by SLW-infested tomato fruit (data not included). The GA3-induced TIR symptoms were intensified further by the SLW infestation in each of the experiments, especially in Experiment 3 (Table 3). The SLW population density and/or GA3 con-

centration may have had an influence on the severity of the TIR symptom expression, particularly for external fruit symptoms. GA3 is known to inhibit lycopene synthesis and delay chlorophyll degradation in tomato (Dostal and Leopold 1967; Khudairi 1972). Khudairi (1972) also reported that the levels of GA3 decline in tomato fruit just before the mature-green stage, followed by an increase in levels of ABA. In these experiments, the abnormally high levels of GA3 may have inhibited ABA synthesis and consequently inhibited or delayed lycopene production and fruit ripening. CCC treatment reduced the external TIR symptoms induced by GA3 treatment. The high SLW population in the presence of CCC observed in Experiment 4 (Table 5) was similar to results reported by Yokomi et al. (1990) that oviposition and nymphs of SLW increased on squash after the application of CCC. The application of CCC was observed to cause severe stunting, thicker and darker green leaves, and rosette leaf formation in the tomato plants (data not included). The control and CCC treatments generally had low incidences of TIR-like symptoms. The expression of these symptoms in the control and CCC treatments may have been induced by other factors. Picha and Hall (1981) reported that K deficiency and certain environmental conditions have been associated with the development of external blotchy and internal white tissue in fresh-market tomato. Results from Experiments 3 and 4 suggest that the development of external and internal TIR symptoms induced by SLW feeding in dwarf cherry tomato may be partially caused by the alteration of normal plant hormone levels, especially GA3. Furthermore, SLW may secrete a type of toxin, possibly produced by the symbiotic microorganisms in or on the whitefly to facilitate the feeding or probing process. Perhaps the plant may respond to the SLW feeding and/or toxin by producing proteins or phytoalexins as a defense mechanism, and as a consequence, these factor(s) may induce the plant to synthesize abnormal levels of GA which result in abnormal ripening patterns in the fruit.

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Whitefly-induced GA3 Metabolism Changes sion of dsRNA in the sweetpotato whitefly. Entomol Exp Appl 70:143–152 Maynard DN, Cantliffe DJ (1989) Squash silverleaf and tomato irregular ripening: New vegetable disorder in Florida. Fla Coop Ext Serv IFAS VC-37 Mignani I, Greve LC, Ben-Arie R, Stotz HU, Li C, Shackel KA, Labavitch JM (1995) The effect of GA3 and divalent cations on aspects of pectin metabolism and tissue softening in ripening tomato pericarp. Physiol Plant 93:108–115

251 Schuster DJ, Muller TF, Kring JB, Price JF (1990) Relationship of the sweetpotato whitefly to a new tomato fruit disorder in Florida. HortScience 25:1618–1620 Schuster DJ, Price JF, Kring JB, Everett PH (1989) Integrated management of the sweetpotato whitefly on commercial tomato. Citrus Veg Grower 52:11–75 Yokomi RK, Jimenez DR, Osborne LS, Shapiro JP (1995) Comparison of silverleaf whitefly-induced and chlormequat chloride-induced leaf silvering in Cucurbita pepo. Plant Dis 79:950–955