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Copyright © Physiologia Plantarum 2000 ISSN 0031-9317

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: Received 2 November 1999; revised 21 February 2000

Silverleaf whitefly (SLW), Bemisia argentifolii Bellows and Perring, is one of the most noxious pests of numerous field 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. Siv’on), 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 efflux for the infested plants. A similar trend was found for the specific activities of sucrose and the three soluble sugars combined (sucrose, glucose and fructose). A single exponential decay function with asymptote was fitted to the above efflux curves. All the calculated exponential coefficients 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.

Insect pests have long been recognized as a significant 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 whitefly (SLW), Bemisia argentifolii Bellows and Perring, is one of the most noxious pests of many field 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 final 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. Siv’on), 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 flux density; SLW, silverleaf whitefly.
Physiol. Plant. 109, 2000


Grantz and Farrar 1999). Data analysis Export rate of newly incorporated 14C. filtered through a 0.78 mm pore size) divided into two compartments. using a portable closed photosynthesis system (LI-6200. fitted with a Sugar-Pak I column (6. 1996). Radioactive 14CO2 was applied. Such an effect may result in down-regulation of photosynthesis in SLW-infested leaves. A volume of 60 ml of 14CO2 was then released into the chamber for 40 s to give a specific activity of 200 kBq mg − 1 carbon. To our knowledge. Lincoln. day/night) greenhouse for gas exchange measurements and 14 CO2 pulse-labeling.) under ozone stress (Grantz and Yang 1996. Gas exchange and 14 CO2-labeling Materials and methods Plant material Cotton (Gossypium hirsutum L. Veen (1985) documented that the export rate of radio-labeled assimilates from potato (Solanum tuberosum L. Four representative plants were selected from each replicate after a 1-month treatment and subjected to the various measurements. no research is available. Goldschmidt and Huber 1992. the leaf was released from the chamber and used for analysis of 14C-photoassimilate export. Sugar and starch contents were determined as described by Lucas et al. Israel (31°54%N. 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. Six leaf discs (8 mm diameter) were taken from a replicate (two discs from each plant) 8 times during a 24-h period. Temperatures in the screenhouse varied from 37 to 42°C for the daily maximum and from 16 to 23°C for the daily minimum.45-mm membrane (Whatman. Plant. The aim of this study was to test the hypothesis that SLW infestation impairs sugar export from cotton source leaves. Pre-assigned youngest fully expanded leaves (third to fourth from the apex) were rinsed before sampling to remove any possible honeydew deposits. 2000 . Sugars (sucrose. 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. When plants reached the square initiation period. and the supernatant was evaporated to dryness. styrofoam (25%) and volcanic stone (25%) in a greenhouse in Rehovot. Clifton. ter. 34°48%E). Zurich. soluble sugars were extracted in 80% ethanol. using a pulse-labeling system. One compartment was heavily infested with SLW adults and nymphs being fed on cotton plants which were already inside. Kontron Instruments) as glucose equivalents after amyloglucosidase conversion using the Sigma (HK) quantitative glucose determination kit. This feeding activity is highly likely to interfere with phloem transport. Forty pots (with two plants each) were arranged in 4 rows (referred to as replicates) in each screenhouse compartment. Starch content of the sugar-extracted discs was determined spectrophotometrically (Uvikon 930. A similar phenomenon has also been reported for Pima cotton (G. on the following day between 1000 and 1200 h under a PPFD of about 600 mmol m − 2 s − 1. 8 pots (one from each replicate) were transferred to a temperature-controlled (30 92/1692°C. Siv’on) was sown in 5-l pots containing a mixture of peat (30%). Waters) using a refractive-index detector. 14 C-carbon export Sugar and starch contents Three plants from each replicate were used to determine the diurnal fluctuations in carbohydrate content. cv. Sugars and starch were analyzed as described earlier for the nonlabeled samples. Be’er Sheva. The radioactivity of sugars after fractionation and starch after enzymatic conversion into glucose residues was measured by liquid scintillation counter (1600 TR. Water and nutrients were supplied via a drip irrigation system as recommended for commercial cotton. compost (20%). NE. Photosynthetic photon flux density (PPFD) at midday was usually about 1200 mmol m − 2 s − 1. (1993). A portable Geiger-Muller tube (RAM-DA. characterizing the effects of SLW on the export of newly fixed carbon and diurnal changes in carbohydrate levels in source leaves.1988. In addition. barbadense L. On the day on which leaf discs were sampled for carbohydrate determination. whose feeding habit includes frequent insertion of its stylet into vascular tissues to suck plant sap. and separated with an analytical HPLC system (Kontron 325. was determined by fitting a single exponential curve with asymptote y = ae − bx + c Physiol. Packard.. After 10 min of flushing the system with air. An attached youngest fully expanded leaf was sealed in a 4-l chamber. Rotem ¨ Industries. to record leaf radioactivity. USA). The same youngest fully expanded leaves were measured in rotation throughout the day. Li-Cor. CT. 109. while the other was free of SLW. thus resulting in the accumulation of carbohydrates in the leaf and the subsequent end-product inhibition of photosynthesis. and consequently increases their carbohydrate content. USA). to date. Switzerland). glucose and fructose) were fractionated by HPLC and collected based on the retention times of standard samples.5 × 300 mm. leaf discs were punched from the side-tips of the fed leaf for determinations of sugar and starch contents and their individual 14C radioactivities. expressed both as percentage of the original radioactivity and as specific activity per mg of sucrose or of the three soluble sugars combined (sucrose+ glucose+fructose). In brief. they were transferred to an insect-proof screenhouse (0. One day after the pots’ relocation.27×0. NJ. SLW is a phloem feeder (Cohen et al. daily gas exchange curves were established under natural light.) leaves infested with potato aphids (Macrosiphum euphorbiae Thomas) was lower relative to noninfested leaves. USA) equipped with a 1-l chamber. Meriden. Baxter and Farrar 1999).

From mid-afternoon. 1. 1983. Data points are means of four individual plant measurements 9 SE. slower rates of starch accumulation and decrease were found for the infested plants during the main accumulation and decreasing periods. This model is similar to the one-compartment model proposed by Evans et al. By contrast. youngest fully expanded leaves revealed a typical accumulation of sucrose and starch during the morning hours with maximal values in the early afternoon (Fig. determined for the pulse-labeled leaves in the greenhouse. an asymptote representing the nonexportable portion. JMP® software (Sall and Lehman 1996) was used for statistical analyses. with smaller daily fluctuations than their noninfested counterparts (Fig. fructose (C) and starch (D) contents of youngest fully expanded cotton (Gossypium hirsutum) leaves under SLW (Bemisia argentifolii )-infested ( +SLW) and noninfested ( − SLW) conditions. Fig. Whitefly infestation resulted in a markedly higher level of soluble sugar contents. Owera et al. where x is time after labeling (h) and the calculated parameters are: a. A randomized one-way model was employed for the analyses of variance based on individual measured or calculated plant values. Carbon export Carbohydrate content. Furthermore. Net photosynthetic rate (Pn) of the youngest fully expanded leaves of SLW (Bemisia argentifolii )-infested ( + SLW) and noninfested (−SLW) cotton (Gossypium hirsutum) plants. A similar trend of diurnal Pn changes has been obtained previously in our screenhouse experiments (Lin et al. 1). by about 50% on average. the proportion of fixed 14C that can be exported during the coming chase period. b. Plant.Results Photosynthetic performance SLW-infested plants exhibited a significantly lower Pn throughout the day. (1963). A nonlinear fit was used to obtain the fitted curves and the corresponding estimated parameters. 2000 293 . 2B. both sucrose and starch decreased until midnight.C). and analogous to the more complex multicompartment models (Moorby and Jarman 1975. 2. respectively. 109. exhibited SLW effects similar to those in the screenhouse (Table 1). at which time sucrose reached its minimal level. 2A. the exponential coefficient. Baxter and Farrar 1999). Glucose and fructose concentrations remained relatively stable throughout the day (Fig. Carbohydrate content Diurnal carbohydrate contents of the screenhouse-sampled. whereas starch continued to decrease at a faster rate until the next morning.D). albeit with higher Pn values and greater SLW effects relative to the greenhouse measurements recorded here. 1999b). Physiol. starch content was greatly reduced due to SLW infestation. Sucrose content in labeled leaves (sampled between 1030 and 1800 h) was comparable to the values obtained in the screenhouse during Fig. glucose (B). 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. Diurnal changes in sucrose (A). and c. Treatments were contrasted using F-test.

which resulted in smaller differences between treatments. 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.2 34. before reproductive organs became a considerable sink.7 Glucose +SLW 67.3** 59. The exponential coefficients for the radioactivities of sucrose and the three soluble sugars combined (sucrose. Glucose and fructose contents were markedly lower in the greenhouse relative to the screenhouse. respectively. 5).4 Fructose +SLW 51. This reduction (37. The decline in total radioactivity of 14CO2-labeled source leaves was greater for noninfested plants than for SLW-infested ones (Fig. The reduced 294 exponential coefficients of 14C efflux for the fed leaf and its major carbon metabolites indicated a slower export of the labeled photoassimilates to the heterotrophic tissues after SLW injury.3 78. contrasted using F-test. * and ** indicate significant effects of whitefly at P = 0. Assuming that newly synthesized 14C sugars were able to mix in one pool with their unlabeled counterparts. which could account for the rapid accumulation of soluble sugars in the source leaves of infested plants. which may be associated with structural and temporarily stored carbohydrates.5%. glucose and fructose) were also reduced (by 19. Plant. Starch radioactivity revealed lower and stable values for the control plants during all of the chase periods (Fig.8 46. 4A. 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.1* 55. 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. The radioactivity data obtained after labeling (within the photoperiod) revealed a highly significant fit for both treatments (r2 ]0.05 and 0.Table 1. respectively) by SLW injury. The lines are fitted single exponential curves (see text for equations).3 72. SLW infestation significantly reduced the exponential coefficient. 1999).8* −SLW 50. 2000 .988) to the single exponential plus asymptote function. Data points are means of four individual ¨ plant measurements9 SE. by 37. 3).D). 1996).6* −SLW 933 952 1011 1046 Starch +SLW 373* 457* 538* 497** the light period for both treatments. 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. The part that cannot be exported to the import-dependent organs is presented as an asymptote. Similar trends were also found in terms of specific radioactivity: both sucrose and the three soluble sugars combined revealed considerably lower levels of exponential coefficient and exportable portion (a).6 30.3** 69.2* 52.4* −SLW 37. Leaf samples were taken in a greenhouse (midday PPFD 600 mmol m−2 s−1). Carbohydrate contents (mg cm−2) of youngest fully expanded leaves of SLW (Bemisia argentifolii )-infested (+SLW) and noninfested (−SLW) cotton (Gossypium hirsutum) plants.5 and 57.5 58.0 35.9 Sucrose +SLW 45. for the time-course changes in radioactivity of the fed leaves (Table 2).5%) was greater than the Pn depression (28% at midday).4** 57. 109.2* 60. Total radioactivity data revealed that SLW infestation reduced the export coefficient of newly fixed carbon (Table 2). Data points are means from four individual plant replicates.2 42. accompanied by a larger nonexportable portion (c) in SLW-infested plants. 3.3 28. cotton plants were studied at the onset of flowering. expression of the changes in leaf radioactivity in terms of sugars specific activity also indicated faster decay rates in the noninfested plants (Fig. indicating that the faster reduction in radio-labeled sugar in the noninfested leaves cannot be attributed to their conversion into starch. To minimize the possible sink effects.01.2 53. 1963). Time (h) −SLW 11:00 13:00 15:00 17:00 23.2* 48. Fig. Moreover.2 32.C). Sucrose and its derivatives represent the major forms of photosynthetically assimilated carbon in plants (Lalonde et al.8%. This one-compartment model assumes that. 4B. In addition. with a more pronounced decrease in the infested treatment. whereas starch content was reduced by about 20%. Physiol. 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. a smaller exportable portion (a) and a larger nonexportable portion (c) of sucrose were also observed in the infested treatment (Table 2). Radioactivity was assayed nondestructively with a Geiger-Muller i-counter.

2 and Table 1). and it was suggested to be due to osmoregulation (Jones and Turner 1980) and inhibited sugar transport (Bunce 1982). 4 and Table 2) suggested that more labeled carbons were either translocated to sinks or converted into starch. A similar effect of insect injury has also been reported for a few other phloem feeders: Medler (1941) documented that disruption of phloem flow due to feeding by potato leaf hoppers (Empoasca fabae Harris) is the result of saliva-induced cell hypertrophy near the phloem. whereas the infested treatment increased the sucrose and hexose concentrations and decreased the starch content (Fig. Herold 1980). In wheat. 5). Data points are means of four individual plant measurements 9 SE. 109. Therefore. 1998). caryella) can induce phloem clogging with callose and other substances in pecan leaves. The mechanisms for sugar-induced feedback inhibition of photosynthesis have Fig. Time-course changes in starch 14C radioactivity of pulse-labeled leaves of SLW (Bemisia argentifolii )-infested ( + SLW) and noninfested ( −SLW) cotton (Gossypium hirsutum) plants. pecanis. whereas Wood et al. the changes in their specific activities provide direct information on their turnover. 295 . 2000 Osmotic potential is not affected by SLW (Lin et al. Physiol. Sugar accumulation may inhibit the rate of photosynthesis (Neales and Incoll 1968. 1999a). M.Fig. and M. higher sugar concentrations were reported in leaves after aphid infestation. The lines are fitted single exponential curves (see text for equations). In potato.) under water stress (Kanechi et al. these results confirmed that SLW infestation inhibited the export of newly fixed carbon. the newly fixed carbon was partitioned preferentially into starch rather than sucrose or other soluble sugars. 1996). SLW stress affected the partitioning of photoassimilates into water-soluble and insoluble fractions in source leaves. Radioactivity was assayed destructively. 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. 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. Data points are means of four individual plant measurements 9 SE. and expressed as both percentage of the original activity (A and C) and specific activity of sucrose and three soluble sugars. Radioactivity was assayed destructively. (1985) found that pecan aphids (Melanocallis caryyaefoliae. whose frequent penetration and release of saliva into the leaves are most likely to interfere with phloem transport. Under noninfested conditions. 5. 4. SLW is a phloem feeder (Cohen et al. which was suggested to be responsible for the reduction in photosynthesis (Veen 1985). 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. Plant. The faster reduction in soluble sugars radioactivity (both in terms of percentage of original activity and specific activity) for the control plants (Fig. excluding the possibility of osmoregulation in our case. A similar phenomenon has been reported in sunflower (Helianthus annuus L.

suggesting that Rubisco limitation could be one of the reasons for the SLW-induced reduction in Pn (Lin et al. Goldschmidt and Huber 1992). b is the exponential coefficient. SLW infestation impairs photoassimilate export. Intercept. Rosell RC (1995) The sweet potato or silverleaf whiteflies: Biotypes of Bemisia tabaci or a species complex? Annu Rev Entomol 40: 511–534 Bunce JA (1982) Effects of water stress on photosynthesis in relation to diurnal accumulation of carbohydrates in source leaves.2* 0. A similar trend was observed for 14C-labeled leaves during the 6-h chase period (Table 1). Proc Natl Acad Sci USA 95: 4784–4788 Chu CC. Frohlich DR. Maekawa S (1998) Non-stomatal inhibition of photosynthesis associated with partitioning of the recent assimilates into starch and sucrose in sunflower leaves under water stress. at elevated CO2 and two nutrient regimes.6* 17.Table 2. and convincing evidence has been presented that substrate flux through hexokinase is a key step in transducing the sugar signal (Jang and Sheen 1994.35** 61. In our experiment. Henneberry TJ. pp 227 – 261. Inagaki N. 0. Gilbertz DA. Aust J Plant Physiol 7: 181 – 192 Kanechi M.1 0. several investigations have identified hexose as the active signal molecule in sugar-sensing among higher plants. *.41 8. sucrose. Oetting RD (1993) Chlorophyll loss and gas exchange in tomato leaves after feeding injury by Bemisia tabaci (Homoptera: Aleyrodidae). Andover. Chu CC (1996) Geometric relationships between whitefly feeding behavior and vascular bundle arrangements. or to the repression of the transcription of photosynthetic genes (Sheen 1990. Plant Cell 9: 5 – 19 Jones MM. Turner NC (1980) Osmotic adjustment in expanding and fully expanded leaves of sunflower in response to water deficits. TN.05.2 91.4 30. Memphis.65 4. 109. where a is the proportion of fixed 14C that will be exported during the coming chase period.9* 87. Parameter −SLW Total leaf radioactivity a (%) b (h−1) c (%) Sucrose radioactivity a (% or dpm mg−1) b (h−1) c (% or dpm mg−1) 39.8 0. Farrar JF (1999) Export of carbon from leaf blades of Poa alpina L.19*** 12.7 0. Acknowledgments – This study was supported by The Israel Cotton Production and Marketing Board. Akey DH. the higher hexose and sucrose concentrations in infested source leaves might inhibit the expression of genes encoding photosynthetic enzymes such as Rubisco. Yamada J.7 c (% or dpm mg−1) been proposed to be the result of increased hexose production and cytosolic phosphate (Pi) depletion (Foyer 1988. Ebert M.001. Plant Physiol 99: 1443–1448 Grantz DA.3 28. New Phytol 133: 659– 671 Jang JC. Whitbread R. Pest Status and Management. hexose released by hydrolysis of such sucrose is responsible for the altered pattern of gene expression (Chiou and Bush 1998). Yang S (1996) Effect of O3 on hydraulic architecture in Pima cotton: Biomass allocation and water transport capacity of roots and shoots. 1997). Plant Physiol Biochem 26: 483 – 492 Goldschmidt EE. National Cotton Council of America. In conclusion.43* 8. Sheen J (1997) Hexokinase as a sugar ´ sensor in higher plants. As suggested above. Parameters were calculated from a single exponential curve based on the one-compartment model. SLW infestation induced considerably higher levels of sucrose and hexoses (glucose +fructose) during the photoperiod relative to the control (Fig. Jang et al.01 and 0. 2). suggesting a possible down-regulation of Pn associated with increased foliar soluble sugar contents. Can J Bot 60: 195 – 200 Buntin GD. Farrar JF (1999) Acute exposure to ozone inhibits rapid carbon translocation from source leaves of Pima cotton. Leon P.3 b (h−1) 0. ** and *** indicate significant effects of whitefly at P= 0.45 7.75* 16. More recently. Plant. Parrella MP (1990) Whiteflies in agricultural systems. Plant Physiol 112: 1649 – 1657 Grantz DA.9 Percentage of original activity +SLW 38. J Exp Bot 50: 1215–1221 Brown JK. ISBN 0-946707-16-2 Chiou TJ. 2000 296 . Bellows TS Jr. J Exp Bot 50: 1253 – 1262 Herold A (1980) Regulation of photosynthesis by sink activity: The missing link. J Jpn Soc Hortic Sci 67: 190 –197 Physiol.5 47. respectively. Henneberry TJ. Sheen J (1994) Sugar sensing in higher plants.8* 0. Hants. and hexose sugars. References Azcon-Bieto J (1983) Inhibition of photosynthesis by carbohydrates ´ in wheat leaves. Jang and Sheen 1994). 1999b). Plant Physiol 73: 681–686 Baxter R. contrasted using F-test.1** 0.5* −SLW Specific radioactivity +SLW Three soluble sugars’ radioactivity a (% or dpm mg−1) 92. In cases where genes respond to changes in sucrose level.56 60. New Phytol 86: 131 – 144 Hibberd JM. Farrar JF (1996) Carbohydrate metabolism in source leaves of barley grown in 700 mmol mol − 1 CO2 and infected with powdery mildew. pp 1239– 1241 Cohen AC. Prabhaker N. Plant Cell 6: 1665 – 1679 Jang JC.33* 36.1 0. Source leaf export parameters of SLW (Bemisia argentifolii )-infested (+SLW) and noninfested (−SLW) cotton (Gossypium hirsutum) plants. Zhou L. This is further supported by an analysis of CO2 response curves.88 7.5 0. In: Gerling D (ed) Whiteflies: Their Bionomics. Moorby J (1963) A model for the translocation of photosynthate in soybean. Huber SC (1992) Regulation of photosynthesis by end-product accumulation in leaves of plants storing starch.1 0. Entomol Exp Appl 78: 135 – 142 Evans NT. Bush DR (1998) Sucrose is a signal molecule in assimilate partitioning. J Exp Bot 14: 221–231 Foyer CH (1988) Feedback inhibition of photosynthesis through source-sink regulation in leaves. Data points are means derived from four individual plant replicates. J Econ Entomol 86: 517–522 Byrne DN.9 63. Perkins HH (1994) A study on control threshold for Bemisia tabaci (Gennadius) on cotton. and c is an asymptote representing the nonexportable part. In: Proceedings Beltwide Cotton Conferences.

Weber A. Crop Sci 39: 174 – 184 Lin T-B. Foyer Physiol. Jarman PD (1975) The use of compartmental analysis in the study of the movement of carbon through leaves. Memphis. NC. pp 742 – 770. Plant Cell 2: 1027 – 1083 Veen BW (1985) Photosynthesis and assimilate transport in potato with top-roll disorder caused by the aphid Macrosiphum euphoribae. Saranga Y (1999b) Non-stomatal factors limit cotton photosynthesis under silverleaf whitefly stress. H. Toscano NC. Planta 190: 88 – 96 Medler JT (1941) The nature of injury to alfalfa caused by Empoasca fabae (Harris). pp 1011 – 1015 Edited by C. Planta 122: 155 – 168 Neales TF. 2000 297 . Ann Entomol Soc Am 34: 439–450 Moorby J. Dehne HW. Dehne HW. Chu CC. Physiol Plant 107: 303–311 Lucas WJ. Incoll LD (1968) The control of leaf photosynthesis by the level of assimilate in the leaf. Cary. Farrar CA. New Phytol 94: 111 – 123 Perring TM. Thompson JM (1985) Feeding influence of three pecan aphid species on carbon exchange and phloem integrity of seedling pecan foliage. Nicholas RL (1996) Photosynthesis and stomatal conductance of cotton infested by different whitefly threshold levels. In: Oerke EC. Schwartz A. In: Proceedings Beltwide Cotton Conference. ISBN 0-444-82095-7 Owera SAP. Farrar JF. Schwartz A. Barker L. Deom CM. J Am Soc Hortic Sci 110: 393 – 397 Yee WL. Bellows TS Jr (1993) Identification of a whitefly species by genomic and behavioral studies. Boles E. Ward JM (1999) The dual function of sugar carriers: Transport and sugar sensing. SAS Institute. ISBN 0-534-26565-0 Sawada S. Palumbo JC (1995) Interaction of silverleaf whitefly (Homoptera: Aleyrodidae) with cantaloupe yield.Lalonde S. Wolf S (1993) Influence of the tobacco mosaic virus 30-kDa movement protein on carbon metabolism and photosynthate partitioning in transgenic tobacco plants. Hellmann H. Haudenshield JS. Cooper AD. Schonbeck F. J Econ Entomol 88: 1726 – 1732 Sall J. Elsevier. National Cotton Council of America. Olesinski A. Bot Rev 34: 431 – 454 Oerke EC. Plant. 109. Hull RJ. Science 259: 74 – 77 Riley DG. Kasai M (1986) Influence of carbohydrates on photosynthesis in single. Tedder WL. rooted soybean leaves used as a source-sink model. Beachy RN. Patrick JW. Schonbeck F (1994) Conclusions and perspectives. Frommer WB. Fukushi K. Whitbread R (1983) Translocation from leaves of barley infested with brown rust. Ann Appl Biol 107: 319 – 323 Wood BW. Amsterdam. Hayakawa T. Plant Cell 11: 707 – 726 Lin T-B. Hennerberry TJ. Saranga Y (1999a) Photosynthesis and productivity of cotton under silverleaf whitefly stress. Plant Cell Physiol 27: 591 – 600 Sheen J (1990) Metabolic repression of transcription in higher plants. Weber A (eds) Crop Production and Crop Protection: Estimated Losses in Major Food and Cash Crops. Lehman A (1996) JMP® Start Statistics. Rodriguez RJ. TN.

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