PHYSIOLOGIA PLANTARUM 109: 291–297. 2000 Copyright © Physiologia Plantarum 2000ISSN 0031-9317Printed in Ireland—all rights reser6ed

Silverleaf whitefly 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 whitefly (SLW), Bemisia argentifolii Bellows and cose and fructose and decreased starch concentrations. Ex-Perring, is one of the most noxious pests of numerous field port rate was determined after 14CO2 pulse-labeling both by

in situ monitoring of leaf radioactivity and by analyzing theand vegetable crops, causing billions of dollars worth ofcontent and radioactivity of the major carbon metabolites.damage throughout the world. SLW is a phloem feederRadioactive counting indicated a lower rate of 14C efflux forwhose feeding is likely to interfere with phloem transport.the infested plants. A similar trend was found for the specificThe aim of this study was to test the hypothesis that SLWactivities of sucrose and the three soluble sugars combinedinfestation impairs carbohydrate export from source leaves,

and consequently increases their carbohydrate content. The (sucrose, glucose and fructose). A single exponential decayyoungest fully expanded leaves of cotton (Gossypium hirsu- function with asymptote was fitted to the above efflux curves.

All the calculated exponential coefficients demonstratedtum L., cv. Siv’on), grown under SLW-infested and nonin-fested conditions, were characterized for their diurnal lower export rates after SLW injury. These results indicatechanges in carbohydrate content and photoassimilate export. that SLW impairs photoassimilate export, suggesting possi-

ble down-regulation of Pn due to increased foliar solubleSLW infestation induced a considerable reduction in netsugar contents.photosynthetic rate (Pn), coupled with increased sucrose, glu-

photosynthetic capacity and stomatal conductance (Buntinet al. 1993). In our previous work on cotton (Gossypiumhirsutum L., cv. Siv’on), the SLW-induced reduction in Pn inthe youngest fully expanded leaves was not accompanied bya decline in chlorophyll content (Lin et al. 1999a). Diffu-sional limitation analysis indicated that nonstomatal factorsare mainly responsible for the depression in Pn, which wasvalidated by 14CO2 autoradiographs demonstrating a homo-geneous distribution of radioactive photosynthates on thoseleaves (Lin et al. 1999b). Photochemical analysis indicatedan impaired photochemical reaction (Lin et al. 1999a,b),while CO2 response curves suggested possible limited end-product synthesis and/or carbohydrate export (Lin et al.1999b).

Numerous physiological and biochemical studies havesuggested that plant photosynthesis is feedback-regulated bythe accumulation of carbohydrates in source leaves (Nealesand Incoll 1968, Herold 1980, Sawada et al. 1986, Foyer

Introduction

Insect pests have long been recognized as a significant threatto agriculture. It is estimated that 16 and 23% of crop yieldpotential is lost due to insect injury under insect-controlledand noncontrolled cropping systems, respectively (Oerke etal. 1994). The silverleaf whitefly (SLW), Bemisia argentifoliiBellows and Perring, is one of the most noxious pests ofmany field and vegetable crops, causing billions of dollarsworth of damage through direct sap feeding and massivedeposition of honeydew (Byrne et al. 1990, Perring et al.1993, Brown et al. 1995). As with other insect injuries, alarge reduction in plant dry matter and final yield is com-monly reported after SLW infestation (Chu et al. 1994,Riley and Palumbo 1995, Lin et al. 1999a), which may bepartly 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 (Lycopersiconesculentum Mill.), the reduced Pn induced by SLW infesta-tion was associated with decreases in chlorophyll content,

Abbre6iations – Pn, net photosynthetic rate; PPFD, photosynthetic photon flux density; SLW, silverleaf whitefly.

Physiol. Plant. 109, 2000 291

1988, Goldschmidt and Huber 1992, Baxter and Farrar1999). A similar phenomenon has also been reported forPima cotton (G. barbadense L.) under ozone stress (Grantzand Yang 1996, Grantz and Farrar 1999). Veen (1985)documented that the export rate of radio-labeled assimilatesfrom potato (Solanum tuberosum L.) leaves infested withpotato aphids (Macrosiphum euphorbiae Thomas) was lowerrelative to noninfested leaves, thus resulting in the accumu-lation of carbohydrates in the leaf and the subsequentend-product inhibition of photosynthesis. To our knowl-edge, no research is available, to date, characterizing theeffects of SLW on the export of newly fixed carbon anddiurnal changes in carbohydrate levels in source leaves.

SLW is a phloem feeder (Cohen et al. 1996), whosefeeding habit includes frequent insertion of its stylet intovascular tissues to suck plant sap. This feeding activity ishighly likely to interfere with phloem transport. The aim ofthis study was to test the hypothesis that SLW infestationimpairs sugar export from cotton source leaves, and conse-quently increases their carbohydrate content. Such an effectmay result in down-regulation of photosynthesis in SLW-in-fested leaves.

Materials and methods

Plant material

Cotton (Gossypium hirsutum L., cv. Siv’on) was sown in 5-lpots containing a mixture of peat (30%), compost (20%),styrofoam (25%) and volcanic stone (25%) in a greenhousein Rehovot, Israel (31°54%N, 34°48%E). When plants reachedthe square initiation period, they were transferred to aninsect-proof screenhouse (0.27×0.78 mm pore size) dividedinto two compartments. One compartment was heavily in-fested with SLW adults and nymphs being fed on cottonplants which were already inside, while the other was free ofSLW. Forty pots (with two plants each) were arranged in 4rows (referred to as replicates) in each screenhouse compart-ment. Four representative plants were selected from eachreplicate after a 1-month treatment and subjected to thevarious measurements. Water and nutrients were suppliedvia a drip irrigation system as recommended for commercialcotton. Temperatures in the screenhouse varied from 37 to42°C for the daily maximum and from 16 to 23°C for thedaily minimum. Photosynthetic photon flux density (PPFD)at midday was usually about 1200 mmol m−2 s−1.

Sugar and starch contents

Three plants from each replicate were used to determine thediurnal fluctuations in carbohydrate content. Pre-assignedyoungest fully expanded leaves (third to fourth from theapex) were rinsed before sampling to remove any possiblehoneydew deposits. Six leaf discs (8 mm diameter) weretaken from a replicate (two discs from each plant) 8 timesduring a 24-h period. Sugar and starch contents were deter-mined as described by Lucas et al. (1993). In brief, solublesugars were extracted in 80% ethanol, and the supernatantwas evaporated to dryness. Sugars were redissolved in wa-

ter, filtered through a 0.45-mm membrane (Whatman,Clifton, NJ, USA), and separated with an analytical HPLCsystem (Kontron 325, Zurich, Switzerland), fitted with aSugar-Pak I column (6.5× 300 mm; Waters) using a refrac-tive-index detector. Starch content of the sugar-extracteddiscs was determined spectrophotometrically (Uvikon 930,Kontron Instruments) as glucose equivalents after amyloglu-cosidase conversion using the Sigma (HK) quantitative glu-cose determination kit.

Gas exchange and 14CO2-labeling

On the day on which leaf discs were sampled for carbohy-drate determination, 8 pots (one from each replicate) weretransferred to a temperature-controlled (3092/1692°C,day/night) greenhouse for gas exchange measurements and14CO2 pulse-labeling. One day after the pots’ relocation,daily gas exchange curves were established under naturallight. The same youngest fully expanded leaves were mea-sured in rotation throughout the day, using a portableclosed 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 followingday between 1000 and 1200 h under a PPFD of about 600mmol m−2 s−1. An attached youngest fully expanded leafwas 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 specificactivity of 200 kBq mg−1 carbon. After 10 min of flushingthe system with air, the leaf was released from the chamberand used for analysis of 14C-photoassimilate export.

14C-carbon export

A time-course reduction in 14C radioactivity in the fed leaveswas determined using two different methods for 6 h afterlabeling. A portable Geiger-Muller tube (RAM-DA, RotemIndustries, Be’er Sheva, Israel) containing a circled b-coun-ter (Model GM-10) was placed on the adaxial surface of themid-tip of the labeled leaf for 100 s during each measure-ment, to record leaf radioactivity. In addition, leaf discswere punched from the side-tips of the fed leaf for determi-nations of sugar and starch contents and their individual 14Cradioactivities. Sugars and starch were analyzed as describedearlier for the nonlabeled samples. Sugars (sucrose, glucoseand fructose) were fractionated by HPLC and collectedbased on the retention times of standard samples. Theradioactivity of sugars after fractionation and starch afterenzymatic conversion into glucose residues was measured byliquid scintillation counter (1600 TR, Packard, Meriden,CT, USA).

Data analysis

Export rate of newly incorporated 14C, expressed both aspercentage of the original radioactivity and as specific activ-ity per mg of sucrose or of the three soluble sugars combined(sucrose+glucose+ fructose), was determined by fitting asingle exponential curve with asymptote

y=ae−bx+c

Physiol. Plant. 109, 2000292

Fig. 1. Net photosynthetic rate (Pn) of the youngest fully expandedleaves of SLW (Bemisia argentifolii )-infested (+SLW) and nonin-fested (−SLW) cotton (Gossypium hirsutum) plants. Data pointsare means of four individual plant measurements9SE.

Results

Photosynthetic performance

SLW-infested plants exhibited a significantly lower Pn

throughout the day, with smaller daily fluctuations thantheir noninfested counterparts (Fig. 1). A similar trend ofdiurnal Pn changes has been obtained previously in ourscreenhouse experiments (Lin et al. 1999b), albeit withhigher Pn values and greater SLW effects relative to thegreenhouse measurements recorded here.

Carbohydrate content

Diurnal carbohydrate contents of the screenhouse-sampled,youngest fully expanded leaves revealed a typical accumula-tion of sucrose and starch during the morning hours withmaximal values in the early afternoon (Fig. 2A,D). Frommid-afternoon, both sucrose and starch decreased until mid-night, at which time sucrose reached its minimal level,whereas starch continued to decrease at a faster rate untilthe next morning. Glucose and fructose concentrations re-mained relatively stable throughout the day (Fig. 2B,C).Whitefly infestation resulted in a markedly higher level ofsoluble sugar contents. By contrast, starch content wasgreatly reduced due to SLW infestation, by about 50% onaverage. Furthermore, slower rates of starch accumulationand decrease were found for the infested plants during themain accumulation and decreasing periods, respectively.

Carbon export

Carbohydrate content, determined for the pulse-labeledleaves in the greenhouse, exhibited SLW effects similar tothose in the screenhouse (Table 1). Sucrose content inlabeled leaves (sampled between 1030 and 1800 h) wascomparable to the values obtained in the screenhouse during

where x is time after labeling (h) and the calculated parame-ters are: a, the proportion of fixed 14C that can be exportedduring the coming chase period; b, the exponential coeffi-cient; and c, an asymptote representing the nonexportableportion. This model is similar to the one-compartmentmodel proposed by Evans et al. (1963), and analogous to themore complex multicompartment models (Moorby and Jar-man 1975, Owera et al. 1983, Baxter and Farrar 1999).

JMP® software (Sall and Lehman 1996) was used forstatistical analyses. A randomized one-way model was em-ployed for the analyses of variance based on individualmeasured or calculated plant values. Treatments were con-trasted using F-test. A nonlinear fit was used to obtain thefitted curves and the corresponding estimated parameters.

Fig. 2. Diurnal changes in sucrose (A),glucose (B), fructose (C) and starch (D)contents of youngest fully expandedcotton (Gossypium hirsutum) leavesunder SLW (Bemisiaargentifolii )-infested (+SLW) andnoninfested (−SLW) conditions. Leafsamples were taken in a screenhouse(midday PPFD 1200 mmol m−2 s−1).Data points are means of fourindividual plant measurements9SE.

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Table 1. Carbohydrate contents (mg cm−2) of youngest fully expanded leaves of SLW (Bemisia argentifolii )-infested (+SLW) andnoninfested (−SLW) cotton (Gossypium hirsutum) plants. Leaf samples were taken in a greenhouse (midday PPFD 600 mmol m−2 s−1).Data points are means from four individual plant replicates, contrasted using F-test; * and ** indicate significant effects of whitefly atP=0.05 and 0.01, respectively.

StarchTime (h) Sucrose Glucose Fructose

−SLW +SLW −SLW +SLW −SLW +SLW −SLW +SLW

11:00 23.8 45.2* 50.5 373*67.3 37.2 51.3** 93313:00 46.0 60.4** 457*58.2 72.3 34.6 59.1* 95215:00 35.2 57.2* 53.2 538*78.3** 30.3 55.2* 101117:00 32.9 52.8* 42.7 497**69.4* 28.4 48.6* 1046

the light period for both treatments, whereas starch contentwas reduced by about 20%. Glucose and fructose contentswere markedly lower in the greenhouse relative to thescreenhouse, with a more pronounced decrease in the in-fested treatment, which resulted in smaller differences be-tween treatments.

The decline in total radioactivity of 14CO2-labeled sourceleaves was greater for noninfested plants than for SLW-in-fested ones (Fig. 3). The radioactivity of sucrose alone aswell as of the three soluble sugars combined (sucrose+glu-cose+ fructose) exhibited a steeper decrease in the controlplants relative to their infested counterparts (Fig. 4A,C).Moreover, expression of the changes in leaf radioactivity interms of sugars specific activity also indicated faster decayrates in the noninfested plants (Fig. 4B,D). Starch radioac-tivity revealed lower and stable values for the control plantsduring all of the chase periods (Fig. 5), indicating that thefaster reduction in radio-labeled sugar in the noninfestedleaves cannot be attributed to their conversion into starch.

The radioactivity data obtained after labeling (within thephotoperiod) revealed a highly significant fit for both treat-ments (r2]0.988) to the single exponential plus asymptotefunction. This one-compartment model assumes that, imme-diately after photosynthetic incorporation of 14CO2, labeledsucrose or soluble sugars will be produced and instanta-neously enter into a mixing compartment containing unla-beled sucrose or soluble sugars (Evans et al. 1963). Thelabeled sucrose or soluble sugars leave the mixing compart-ment and enter the heterotrophic tissues at an exponentialrate (b) because of the export and continuous dilution bythe newly formed unlabeled sugars. The part that cannot beexported to the import-dependent organs is presented as anasymptote, which may be associated with structural andtemporarily stored carbohydrates.

SLW infestation significantly reduced the exponential co-efficient, by 37.5%, for the time-course changes in radioac-tivity of the fed leaves (Table 2). The exponentialcoefficients for the radioactivities of sucrose and the threesoluble sugars combined (sucrose, glucose and fructose)were also reduced (by 19.5 and 57.8%, respectively) by SLWinjury. In addition, a smaller exportable portion (a) and alarger nonexportable portion (c) of sucrose were also ob-served in the infested treatment (Table 2). Similar trendswere also found in terms of specific radioactivity: bothsucrose and the three soluble sugars combined revealedconsiderably lower levels of exponential coefficient and ex-portable portion (a), accompanied by a larger nonex-portable portion (c) in SLW-infested plants. The reduced

exponential coefficients of 14C efflux for the fed leaf and itsmajor carbon metabolites indicated a slower export of thelabeled photoassimilates to the heterotrophic tissues afterSLW injury.

Discussion

The accumulation of soluble sugars in source leaves isusually ascribed to the sinks’ limited ability to utilize carbo-hydrates or to the reduced source leaves’ capacity to exportcarbohydrates (Hibberd et al. 1996). To minimize the possi-ble sink effects, cotton plants were studied at the onset offlowering, before reproductive organs became a considerablesink. Total radioactivity data revealed that SLW infestationreduced the export coefficient of newly fixed carbon (Table2). This reduction (37.5%) was greater than the Pn depres-sion (28% at midday), which could account for the rapidaccumulation of soluble sugars in the source leaves ofinfested plants.

Sucrose and its derivatives represent the major forms ofphotosynthetically assimilated carbon in plants (Lalonde etal. 1999). Assuming that newly synthesized 14C sugars wereable to mix in one pool with their unlabeled counterparts,

Fig. 3. Time-course decreases in 14C radioactivity of pulse-labeledyoungest fully expanded leaves of SLW (Bemisia argentifolii )-in-fested (+SLW) and noninfested (−SLW) cotton (Gossypium hirsu-tum) plants. Radioactivity was assayed nondestructively with aGeiger-Muller b-counter. Data points are means of four individualplant measurements9SE. The lines are fitted single exponentialcurves (see text for equations).

Physiol. Plant. 109, 2000294

Fig. 4. Time-course changes in 14Cradioactivity in sucrose (A and B) andthree soluble sugars(sucrose+glucose+ fructose) (C and D)in pulse-labeled leaves of SLW (Bemisiaargentifolii )-infested (+SLW) andnoninfested (−SLW) cotton (Gossypiumhirsutum) plants. Radioactivity wasassayed destructively, and expressed asboth percentage of the original activity(A and C) and specific activity ofsucrose and three soluble sugars. Datapoints are means of four individualplant measurements9SE. The lines arefitted single exponential curves (see textfor equations).

the changes in their specific activities provide direct informa-tion on their turnover. The faster reduction in soluble sugarsradioactivity (both in terms of percentage of original activityand specific activity) for the control plants (Fig. 4 and Table2) suggested that more labeled carbons were either translo-cated to sinks or converted into starch. The latter possibilitywas excluded by the fact that noninfested leaves did notaccumulate more labeled starch than their infested counter-parts with chase time (Fig. 5). Therefore, these resultsconfirmed that SLW infestation inhibited the export ofnewly fixed carbon. A similar effect of insect injury has alsobeen reported for a few other phloem feeders: Medler (1941)documented that disruption of phloem flow due to feedingby potato leaf hoppers (Empoasca fabae Harris) is the resultof saliva-induced cell hypertrophy near the phloem, whereasWood et al. (1985) found that pecan aphids (Melanocalliscaryyaefoliae, M. pecanis, and M. caryella) can inducephloem clogging with callose and other substances in pecanleaves. SLW is a phloem feeder (Cohen et al. 1996), whosefrequent penetration and release of saliva into the leaves aremost likely to interfere with phloem transport.

SLW stress affected the partitioning of photoassimilatesinto water-soluble and insoluble fractions in source leaves.Under noninfested conditions, the newly fixed carbon waspartitioned preferentially into starch rather than sucrose orother soluble sugars, whereas the infested treatment in-creased the sucrose and hexose concentrations and de-creased the starch content (Fig. 2 and Table 1). A similarphenomenon has been reported in sunflower (Helianthusannuus L.) under water stress (Kanechi et al. 1998), and itwas suggested to be due to osmoregulation (Jones andTurner 1980) and inhibited sugar transport (Bunce 1982).

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 photosynthe-sis (Neales and Incoll 1968, Herold 1980). In wheat, Azcon-Bieto (1983) observed the rapid inhibition of photosynthesisin response to sugar accumulation in source leaves within afew hours of the extreme treatments of high CO2 partialpressure and leaf-base chilling. In potato, higher sugarconcentrations were reported in leaves after aphid infesta-tion, which was suggested to be responsible for the reduc-tion in photosynthesis (Veen 1985). The mechanisms forsugar-induced feedback inhibition of photosynthesis have

Fig. 5. Time-course changes in starch 14C radioactivity of pulse-la-beled leaves of SLW (Bemisia argentifolii )-infested (+SLW) andnoninfested (−SLW) cotton (Gossypium hirsutum) plants. Radioac-tivity was assayed destructively. Data points are means of fourindividual plant measurements9SE.

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Table 2. Source leaf export parameters of SLW (Bemisia argentifolii )-infested (+SLW) and noninfested (−SLW) cotton (Gossypiumhirsutum) plants. Parameters were calculated from a single exponential curve based on the one-compartment model, where a is theproportion of fixed 14C that will be exported during the coming chase period, b is the exponential coefficient, and c is an asymptoterepresenting the nonexportable part. Data points are means derived from four individual plant replicates, contrasted using F-test; *, ** and*** indicate significant effects of whitefly at P=0.05, 0.01 and 0.001, respectively.

Parameter Percentage of original activity Specific radioactivity

+SLW−SLW +SLW −SLW

Total leaf radioactivitya (%) 39.8 38.1b (h−1) 0.56 0.35**c (%) 60.2 61.9

Sucrose radioactivitya (% or dpm mg−1) 91.1 30.2*63.1** 47.1b (h−1) 0.41 0.33* 0.88 0.75*c (% or dpm mg−1) 8.9 16.6*36.9* 7.3

Three soluble sugars’ radioactivitya (% or dpm mg−1) 17.8*92.3 87.5 28.7b (h−1) 0.45 0.43*0.19*** 0.65c (% or dpm mg−1) 7.7 12.5 8.5*4.4

been proposed to be the result of increased hexose produc-tion and cytosolic phosphate (Pi) depletion (Foyer 1988,Goldschmidt and Huber 1992), or to the repression of thetranscription of photosynthetic genes (Sheen 1990, Jang andSheen 1994). More recently, several investigations have iden-tified hexose as the active signal molecule in sugar-sensingamong higher plants, and convincing evidence has beenpresented that substrate flux through hexokinase is a keystep in transducing the sugar signal (Jang and Sheen 1994,Jang et al. 1997). In cases where genes respond to changes insucrose level, hexose released by hydrolysis of such sucroseis responsible for the altered pattern of gene expression(Chiou and Bush 1998). In our experiment, SLW infestationinduced considerably higher levels of sucrose and hexoses(glucose+ fructose) during the photoperiod relative to thecontrol (Fig. 2). A similar trend was observed for 14C-la-beled leaves during the 6-h chase period (Table 1). Assuggested above, the higher hexose and sucrose concentra-tions in infested source leaves might inhibit the expression ofgenes encoding photosynthetic enzymes such as Rubisco.This is further supported by an analysis of CO2 responsecurves, suggesting that Rubisco limitation could be one ofthe reasons for the SLW-induced reduction in Pn (Lin et al.1999b).

In conclusion, SLW infestation impairs photoassimilateexport, suggesting a possible down-regulation of Pn associ-ated with increased foliar soluble sugar contents.

Acknowledgments – This study was supported by The Israel CottonProduction and Marketing Board.

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Edited by C. H. Foyer

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