PHYSIOLOGIA PLANTARUM 109: 291297.

2000
Printed in Ireland all rights reser6ed

Copyright Physiologia Plantarum 2000 ISSN 0031-9317

Silverleaf whitey stress impairs sugar export from cotton source leaves
Tong-Bao Lin, Shmuel Wolf, Amnon Schwartz and Yehoshua Saranga*
Faculty of Agricultural, Food and En6ironmental Quality Sciences, The Hebrew Uni6ersity of Jerusalem, P.O. Box 12, Reho6ot 76100, Israel *Corresponding author, e-mail: saranga@agri.huji.ac.il Received 2 November 1999; revised 21 February 2000

Silverleaf whitey (SLW), Bemisia argentifolii Bellows and Perring, is one of the most noxious pests of numerous eld and vegetable crops, causing billions of dollars worth of damage throughout the world. SLW is a phloem feeder whose feeding is likely to interfere with phloem transport. The aim of this study was to test the hypothesis that SLW infestation impairs carbohydrate export from source leaves, and consequently increases their carbohydrate content. The youngest fully expanded leaves of cotton (Gossypium hirsutum L., cv. Sivon), grown under SLW-infested and noninfested conditions, were characterized for their diurnal changes in carbohydrate content and photoassimilate export. SLW infestation induced a considerable reduction in net photosynthetic rate (Pn), coupled with increased sucrose, glu-

cose and fructose and decreased starch concentrations. Export rate was determined after 14CO2 pulse-labeling both by in situ monitoring of leaf radioactivity and by analyzing the content and radioactivity of the major carbon metabolites. Radioactive counting indicated a lower rate of 14C efux for the infested plants. A similar trend was found for the specic activities of sucrose and the three soluble sugars combined (sucrose, glucose and fructose). A single exponential decay function with asymptote was tted to the above efux curves. All the calculated exponential coefcients demonstrated lower export rates after SLW injury. These results indicate that SLW impairs photoassimilate export, suggesting possible down-regulation of Pn due to increased foliar soluble sugar contents.

Introduction
Insect pests have long been recognized as a signicant threat to agriculture. It is estimated that 16 and 23% of crop yield potential is lost due to insect injury under insect-controlled and noncontrolled cropping systems, respectively (Oerke et al. 1994). The silverleaf whitey (SLW), Bemisia argentifolii Bellows and Perring, is one of the most noxious pests of many eld and vegetable crops, causing billions of dollars worth of damage through direct sap feeding and massive deposition of honeydew (Byrne et al. 1990, Perring et al. 1993, Brown et al. 1995). As with other insect injuries, a large reduction in plant dry matter and nal yield is commonly reported after SLW infestation (Chu et al. 1994, Riley and Palumbo 1995, Lin et al. 1999a), which may be partly ascribed to the reduced net photosynthetic rate (Pn) documented in different plant species (Buntin et al. 1993, Yee et al. 1996, Lin et al. 1999a,b). In tomato (Lycopersicon esculentum Mill.), the reduced Pn induced by SLW infestation was associated with decreases in chlorophyll content, photosynthetic capacity and stomatal conductance (Buntin et al. 1993). In our previous work on cotton (Gossypium hirsutum L., cv. Sivon), the SLW-induced reduction in Pn in the youngest fully expanded leaves was not accompanied by a decline in chlorophyll content (Lin et al. 1999a). Diffusional limitation analysis indicated that nonstomatal factors are mainly responsible for the depression in Pn, which was validated by 14CO2 autoradiographs demonstrating a homogeneous distribution of radioactive photosynthates on those leaves (Lin et al. 1999b). Photochemical analysis indicated an impaired photochemical reaction (Lin et al. 1999a,b), while CO2 response curves suggested possible limited endproduct synthesis and/or carbohydrate export (Lin et al. 1999b). Numerous physiological and biochemical studies have suggested that plant photosynthesis is feedback-regulated by the accumulation of carbohydrates in source leaves (Neales and Incoll 1968, Herold 1980, Sawada et al. 1986, Foyer

Abbre6iations Pn, net photosynthetic rate; PPFD, photosynthetic photon ux density; SLW, silverleaf whitey.
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1988, Goldschmidt and Huber 1992, Baxter and Farrar 1999). A similar phenomenon has also been reported for Pima cotton (G. barbadense L.) under ozone stress (Grantz and Yang 1996, Grantz and Farrar 1999). Veen (1985) documented that the export rate of radio-labeled assimilates from potato (Solanum tuberosum L.) leaves infested with potato aphids (Macrosiphum euphorbiae Thomas) was lower relative to noninfested leaves, thus resulting in the accumulation of carbohydrates in the leaf and the subsequent end-product inhibition of photosynthesis. To our knowledge, no research is available, to date, characterizing the effects of SLW on the export of newly xed carbon and diurnal changes in carbohydrate levels in source leaves. SLW is a phloem feeder (Cohen et al. 1996), whose feeding habit includes frequent insertion of its stylet into vascular tissues to suck plant sap. This feeding activity is highly likely to interfere with phloem transport. The aim of this study was to test the hypothesis that SLW infestation impairs sugar export from cotton source leaves, and consequently increases their carbohydrate content. Such an effect may result in down-regulation of photosynthesis in SLW-infested leaves.

ter, ltered through a 0.45-mm membrane (Whatman, Clifton, NJ, USA), and separated with an analytical HPLC system (Kontron 325, Zurich, Switzerland), tted with a Sugar-Pak I column (6.5 300 mm; Waters) using a refractive-index detector. Starch content of the sugar-extracted discs was determined spectrophotometrically (Uvikon 930, Kontron Instruments) as glucose equivalents after amyloglucosidase conversion using the Sigma (HK) quantitative glucose determination kit. Gas exchange and
14

CO2-labeling

Materials and methods

Plant material Cotton (Gossypium hirsutum L., cv. Sivon) was sown in 5-l pots containing a mixture of peat (30%), compost (20%), styrofoam (25%) and volcanic stone (25%) in a greenhouse in Rehovot, Israel (3154%N, 3448%E). When plants reached the square initiation period, they were transferred to an insect-proof screenhouse (0.270.78 mm pore size) divided into two compartments. One compartment was heavily infested with SLW adults and nymphs being fed on cotton plants which were already inside, while the other was free of SLW. Forty pots (with two plants each) were arranged in 4 rows (referred to as replicates) in each screenhouse compartment. Four representative plants were selected from each replicate after a 1-month treatment and subjected to the various measurements. Water and nutrients were supplied via a drip irrigation system as recommended for commercial cotton. Temperatures in the screenhouse varied from 37 to 42C for the daily maximum and from 16 to 23C for the daily minimum. Photosynthetic photon ux density (PPFD) at midday was usually about 1200 mmol m 2 s 1.

On the day on which leaf discs were sampled for carbohydrate determination, 8 pots (one from each replicate) were transferred to a temperature-controlled (30 92/1692C, day/night) greenhouse for gas exchange measurements and 14 CO2 pulse-labeling. One day after the pots relocation, daily gas exchange curves were established under natural light. The same youngest fully expanded leaves were measured in rotation throughout the day, using a portable closed photosynthesis system (LI-6200, Li-Cor, Lincoln, NE, USA) equipped with a 1-l chamber. Radioactive 14CO2 was applied, using a pulse-labeling system, on the following day between 1000 and 1200 h under a PPFD of about 600 mmol m 2 s 1. An attached youngest fully expanded leaf was sealed in a 4-l chamber. A volume of 60 ml of 14CO2 was then released into the chamber for 40 s to give a specic activity of 200 kBq mg 1 carbon. After 10 min of ushing the system with air, the leaf was released from the chamber and used for analysis of 14C-photoassimilate export.
14

C-carbon export

Sugar and starch contents Three plants from each replicate were used to determine the diurnal uctuations in carbohydrate content. Pre-assigned youngest fully expanded leaves (third to fourth from the apex) were rinsed before sampling to remove any possible honeydew deposits. Six leaf discs (8 mm diameter) were taken from a replicate (two discs from each plant) 8 times during a 24-h period. Sugar and starch contents were determined as described by Lucas et al. (1993). In brief, soluble sugars were extracted in 80% ethanol, and the supernatant was evaporated to dryness. Sugars were redissolved in wa292

A time-course reduction in 14C radioactivity in the fed leaves was determined using two different methods for 6 h after labeling. A portable Geiger-Muller tube (RAM-DA, Rotem Industries, Beer Sheva, Israel) containing a circled i-counter (Model GM-10) was placed on the adaxial surface of the mid-tip of the labeled leaf for 100 s during each measurement, to record leaf radioactivity. In addition, leaf discs were punched from the side-tips of the fed leaf for determinations of sugar and starch contents and their individual 14C radioactivities. Sugars and starch were analyzed as described earlier for the nonlabeled samples. Sugars (sucrose, glucose and fructose) were fractionated by HPLC and collected based on the retention times of standard samples. The radioactivity of sugars after fractionation and starch after enzymatic conversion into glucose residues was measured by liquid scintillation counter (1600 TR, Packard, Meriden, CT, USA). Data analysis Export rate of newly incorporated 14C, expressed both as percentage of the original radioactivity and as specic activity per mg of sucrose or of the three soluble sugars combined (sucrose+ glucose+fructose), was determined by tting a single exponential curve with asymptote y = ae bx + c
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Results
Photosynthetic performance SLW-infested plants exhibited a signicantly lower Pn throughout the day, with smaller daily uctuations than their noninfested counterparts (Fig. 1). A similar trend of diurnal Pn changes has been obtained previously in our screenhouse experiments (Lin et al. 1999b), albeit with higher Pn values and greater SLW effects relative to the greenhouse measurements recorded here. Carbohydrate content Diurnal carbohydrate contents of the screenhouse-sampled, youngest fully expanded leaves revealed a typical accumulation of sucrose and starch during the morning hours with maximal values in the early afternoon (Fig. 2A,D). From mid-afternoon, both sucrose and starch decreased until midnight, at which time sucrose reached its minimal level, whereas starch continued to decrease at a faster rate until the next morning. Glucose and fructose concentrations remained relatively stable throughout the day (Fig. 2B,C). Whitey infestation resulted in a markedly higher level of soluble sugar contents. By contrast, starch content was greatly reduced due to SLW infestation, by about 50% on average. Furthermore, slower rates of starch accumulation and decrease were found for the infested plants during the main accumulation and decreasing periods, respectively. Carbon export Carbohydrate content, determined for the pulse-labeled leaves in the greenhouse, exhibited SLW effects similar to those in the screenhouse (Table 1). Sucrose content in labeled leaves (sampled between 1030 and 1800 h) was comparable to the values obtained in the screenhouse during

Fig. 1. Net photosynthetic rate (Pn) of the youngest fully expanded leaves of SLW (Bemisia argentifolii )-infested ( + SLW) and noninfested (SLW) cotton (Gossypium hirsutum) plants. Data points are means of four individual plant measurements 9 SE.

where x is time after labeling (h) and the calculated parameters are: a, the proportion of xed 14C that can be exported during the coming chase period; b, the exponential coefcient; and c, an asymptote representing the nonexportable portion. This model is similar to the one-compartment model proposed by Evans et al. (1963), and analogous to the more complex multicompartment models (Moorby and Jarman 1975, Owera et al. 1983, Baxter and Farrar 1999). JMP software (Sall and Lehman 1996) was used for statistical analyses. A randomized one-way model was employed for the analyses of variance based on individual measured or calculated plant values. Treatments were contrasted using F-test. A nonlinear t was used to obtain the tted curves and the corresponding estimated parameters.

Fig. 2. Diurnal changes in sucrose (A), glucose (B), fructose (C) and starch (D) contents of youngest fully expanded cotton (Gossypium hirsutum) leaves under SLW (Bemisia argentifolii )-infested ( +SLW) and noninfested ( SLW) conditions. Leaf samples were taken in a screenhouse (midday PPFD 1200 mmol m 2 s 1). Data points are means of four individual plant measurements 9 SE.
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Table 1. Carbohydrate contents (mg cm2) of youngest fully expanded leaves of SLW (Bemisia argentifolii )-infested (+SLW) and noninfested (SLW) cotton (Gossypium hirsutum) plants. Leaf samples were taken in a greenhouse (midday PPFD 600 mmol m2 s1). Data points are means from four individual plant replicates, contrasted using F-test; * and ** indicate signicant effects of whitey at P = 0.05 and 0.01, respectively. Time (h) SLW 11:00 13:00 15:00 17:00 23.8 46.0 35.2 32.9 Sucrose +SLW 45.2* 60.4** 57.2* 52.8* SLW 50.5 58.2 53.2 42.7 Glucose +SLW 67.3 72.3 78.3** 69.4* SLW 37.2 34.6 30.3 28.4 Fructose +SLW 51.3** 59.1* 55.2* 48.6* SLW 933 952 1011 1046 Starch +SLW 373* 457* 538* 497**

the light period for both treatments, whereas starch content was reduced by about 20%. Glucose and fructose contents were markedly lower in the greenhouse relative to the screenhouse, with a more pronounced decrease in the infested treatment, which resulted in smaller differences between treatments. The decline in total radioactivity of 14CO2-labeled source leaves was greater for noninfested plants than for SLW-infested ones (Fig. 3). The radioactivity of sucrose alone as well as of the three soluble sugars combined (sucrose+ glucose + fructose) exhibited a steeper decrease in the control plants relative to their infested counterparts (Fig. 4A,C). Moreover, expression of the changes in leaf radioactivity in terms of sugars specic activity also indicated faster decay rates in the noninfested plants (Fig. 4B,D). Starch radioactivity revealed lower and stable values for the control plants during all of the chase periods (Fig. 5), indicating that the faster reduction in radio-labeled sugar in the noninfested leaves cannot be attributed to their conversion into starch. The radioactivity data obtained after labeling (within the photoperiod) revealed a highly signicant t for both treatments (r2 ]0.988) to the single exponential plus asymptote function. This one-compartment model assumes that, immediately after photosynthetic incorporation of 14CO2, labeled sucrose or soluble sugars will be produced and instantaneously enter into a mixing compartment containing unlabeled sucrose or soluble sugars (Evans et al. 1963). The labeled sucrose or soluble sugars leave the mixing compartment and enter the heterotrophic tissues at an exponential rate (b) because of the export and continuous dilution by the newly formed unlabeled sugars. The part that cannot be exported to the import-dependent organs is presented as an asymptote, which may be associated with structural and temporarily stored carbohydrates. SLW infestation signicantly reduced the exponential coefcient, by 37.5%, for the time-course changes in radioactivity of the fed leaves (Table 2). The exponential coefcients for the radioactivities of sucrose and the three soluble sugars combined (sucrose, glucose and fructose) were also reduced (by 19.5 and 57.8%, respectively) by SLW injury. In addition, a smaller exportable portion (a) and a larger nonexportable portion (c) of sucrose were also observed in the infested treatment (Table 2). Similar trends were also found in terms of specic radioactivity: both sucrose and the three soluble sugars combined revealed considerably lower levels of exponential coefcient and exportable portion (a), accompanied by a larger nonexportable portion (c) in SLW-infested plants. The reduced 294

exponential coefcients of 14C efux for the fed leaf and its major carbon metabolites indicated a slower export of the labeled photoassimilates to the heterotrophic tissues after SLW injury.

Discussion
The accumulation of soluble sugars in source leaves is usually ascribed to the sinks limited ability to utilize carbohydrates or to the reduced source leaves capacity to export carbohydrates (Hibberd et al. 1996). To minimize the possible sink effects, cotton plants were studied at the onset of owering, before reproductive organs became a considerable sink. Total radioactivity data revealed that SLW infestation reduced the export coefcient of newly xed carbon (Table 2). This reduction (37.5%) was greater than the Pn depression (28% at midday), which could account for the rapid accumulation of soluble sugars in the source leaves of infested plants. Sucrose and its derivatives represent the major forms of photosynthetically assimilated carbon in plants (Lalonde et al. 1999). Assuming that newly synthesized 14C sugars were able to mix in one pool with their unlabeled counterparts,

Fig. 3. Time-course decreases in 14C radioactivity of pulse-labeled youngest fully expanded leaves of SLW (Bemisia argentifolii )-infested ( +SLW) and noninfested ( SLW) cotton (Gossypium hirsutum) plants. Radioactivity was assayed nondestructively with a Geiger-Muller i-counter. Data points are means of four individual plant measurements9 SE. The lines are tted single exponential curves (see text for equations).
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Fig. 4. Time-course changes in 14C radioactivity in sucrose (A and B) and three soluble sugars (sucrose+glucose +fructose) (C and D) in pulse-labeled leaves of SLW (Bemisia argentifolii )-infested ( + SLW) and noninfested ( SLW) cotton (Gossypium hirsutum) plants. Radioactivity was assayed destructively, and expressed as both percentage of the original activity (A and C) and specic activity of sucrose and three soluble sugars. Data points are means of four individual plant measurements 9 SE. The lines are tted single exponential curves (see text for equations).

the changes in their specic activities provide direct information on their turnover. The faster reduction in soluble sugars radioactivity (both in terms of percentage of original activity and specic activity) for the control plants (Fig. 4 and Table 2) suggested that more labeled carbons were either translocated to sinks or converted into starch. The latter possibility was excluded by the fact that noninfested leaves did not accumulate more labeled starch than their infested counterparts with chase time (Fig. 5). Therefore, these results conrmed that SLW infestation inhibited the export of newly xed carbon. A similar effect of insect injury has also been reported for a few other phloem feeders: Medler (1941) documented that disruption of phloem ow due to feeding by potato leaf hoppers (Empoasca fabae Harris) is the result of saliva-induced cell hypertrophy near the phloem, whereas Wood et al. (1985) found that pecan aphids (Melanocallis caryyaefoliae, M. pecanis, and M. caryella) can induce phloem clogging with callose and other substances in pecan leaves. SLW is a phloem feeder (Cohen et al. 1996), whose frequent penetration and release of saliva into the leaves are most likely to interfere with phloem transport. SLW stress affected the partitioning of photoassimilates into water-soluble and insoluble fractions in source leaves. Under noninfested conditions, the newly xed carbon was partitioned preferentially into starch rather than sucrose or other soluble sugars, whereas the infested treatment increased the sucrose and hexose concentrations and decreased the starch content (Fig. 2 and Table 1). A similar phenomenon has been reported in sunower (Helianthus annuus L.) under water stress (Kanechi et al. 1998), and it was suggested to be due to osmoregulation (Jones and Turner 1980) and inhibited sugar transport (Bunce 1982).
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Osmotic potential is not affected by SLW (Lin et al. 1999a), excluding the possibility of osmoregulation in our case. Sugar accumulation may inhibit the rate of photosynthesis (Neales and Incoll 1968, Herold 1980). In wheat, Azcon Bieto (1983) observed the rapid inhibition of photosynthesis in response to sugar accumulation in source leaves within a few hours of the extreme treatments of high CO2 partial pressure and leaf-base chilling. In potato, higher sugar concentrations were reported in leaves after aphid infestation, which was suggested to be responsible for the reduction in photosynthesis (Veen 1985). The mechanisms for sugar-induced feedback inhibition of photosynthesis have

Fig. 5. Time-course changes in starch 14C radioactivity of pulse-labeled leaves of SLW (Bemisia argentifolii )-infested ( + SLW) and noninfested ( SLW) cotton (Gossypium hirsutum) plants. Radioactivity was assayed destructively. Data points are means of four individual plant measurements 9 SE.

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Table 2. Source leaf export parameters of SLW (Bemisia argentifolii )-infested (+SLW) and noninfested (SLW) cotton (Gossypium hirsutum) plants. Parameters were calculated from a single exponential curve based on the one-compartment model, where a is the proportion of xed 14C that will be exported during the coming chase period, b is the exponential coefcient, and c is an asymptote representing the nonexportable part. Data points are means derived from four individual plant replicates, contrasted using F-test; *, ** and *** indicate signicant effects of whitey at P= 0.05, 0.01 and 0.001, respectively. Parameter SLW Total leaf radioactivity a (%) b (h1) c (%) Sucrose radioactivity a (% or dpm mg1) b (h1) c (% or dpm mg1) 39.8 0.56 60.2 91.1 0.41 8.9 Percentage of original activity +SLW 38.1 0.35** 61.9 63.1** 0.33* 36.9* 87.5 0.19*** 12.5 47.1 0.88 7.3 28.7 0.65 4.4 30.2* 0.75* 16.6* 17.8* 0.43* 8.5* SLW Specic radioactivity +SLW

Three soluble sugars radioactivity a (% or dpm mg1) 92.3 b (h1) 0.45 7.7 c (% or dpm mg1)

been proposed to be the result of increased hexose production and cytosolic phosphate (Pi) depletion (Foyer 1988, Goldschmidt and Huber 1992), or to the repression of the transcription of photosynthetic genes (Sheen 1990, Jang and Sheen 1994). More recently, several investigations have identied hexose as the active signal molecule in sugar-sensing among higher plants, and convincing evidence has been presented that substrate ux through hexokinase is a key step in transducing the sugar signal (Jang and Sheen 1994, Jang et al. 1997). In cases where genes respond to changes in sucrose level, hexose released by hydrolysis of such sucrose is responsible for the altered pattern of gene expression (Chiou and Bush 1998). In our experiment, SLW infestation induced considerably higher levels of sucrose and hexoses (glucose +fructose) during the photoperiod relative to the control (Fig. 2). A similar trend was observed for 14C-labeled leaves during the 6-h chase period (Table 1). As suggested above, the higher hexose and sucrose concentrations in infested source leaves might inhibit the expression of genes encoding photosynthetic enzymes such as Rubisco. This is further supported by an analysis of CO2 response curves, suggesting that Rubisco limitation could be one of the reasons for the SLW-induced reduction in Pn (Lin et al. 1999b). In conclusion, SLW infestation impairs photoassimilate export, suggesting a possible down-regulation of Pn associated with increased foliar soluble sugar contents.
Acknowledgments This study was supported by The Israel Cotton Production and Marketing Board.

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Edited by C. H. Foyer
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