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This article in AJ

  1. Vol. 103 No. 6, p. 1849-1861
    unlockOPEN ACCESS
     
    Received: Feb 7, 2011


    * Corresponding author(s): maria.sena@ufv.br
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doi:10.2134/agronj2011.0049

Resistance of Tomato Subsamples to Bemisia tabaci Biotype B (Genn.) (Hemiptera: Aleyrodidae)

  1. Maria Elisa de Sena Fernandes *a,
  2. Derly José Henriques da Silvaa,
  3. Marcelo Coutinho Picançob,
  4. Flávio Lemes Fernandesc,
  5. Gulab Newandran Jhamd and
  6. Pedro Crescêncio Souza Carneiroe
  1. a UFV, Dep. de Fitotecnia, Genética e Melhoramento de Plantas, Cep 36570-000 Viçosa, MG, Brazil
    b UFV, Dep. de Biologia Animal, Campus Universitário, Cep 36570-000 Viçosa, MG, Brazil
    c Instituto de Ciências Agrárias, Campus de Rio Paranaíba, UFV, 38810-000 Rio Paranaíba, MG, Brazil
    d Dep. de Química, UFV, 36570-000 Viçosa, MG, Brazil
    e Dep. de Biologia Geral, UFV, 36570-000 Viçosa, MG, Brazil

Abstract

Whitefly (Bemisia tabaci) causes damage to tomato (Solanum lycopersicum L.) and is controlled by insecticides harmful to man and the environment. Development of resistant cultivars is ideal for whitefly management, with alternate genetic sources being indispensable. Germplasm banks are potentially good sources of resistant cultivars. Agronomic characteristics of the tomato subsamples from the Horticultural Germplasm Bank (HGB) at Universidade Federal de Viçosa (UFV) have been typified but little is known about their insect resistance. Thus, the objective of this study was to assess the resistance of 103 HGB-UFV tomato subsamples to B. tabaci as well evaluate the resistance mechanism. The characteristics of the subsamples evaluated were the number of nymphs and eggs per plant and the resistance index compared with the susceptible cultivar Santa Clara, arbitrarily chosen as the susceptible standard. The trichome number per 0.04 cm2 of the leaf blades and 15 leaf hydrocarbon concentrations were also determined. Resistant subsamples were submitted to antibiosis test and the mortality (%) and life cycle of the B. tabaci were evaluated. The difference in the number of eggs per plant, nymphs per plant, and nymph/egg ratio in the tomato subsamples was evaluated. A positive correlation was observed between the hydrocarbons undecane and tridecane with B. tabaci nymphs. Significant and positive differences in the trichome per 0.04-cm2 density were found between the trichome density and the number of eggs per plant. The subsamples HGB-225, -327, -630, -813, -985, -2029, -2030, -2055, -2057, -2060, -2062, and -2068 were resistant to B. tabaci biotype B through antixenosis and antibiosis resistance mechanisms.


Abbreviations

    HGB, Horticultural Germplasm Bank; UFV, Universidade Federal de Viçosa

Insect pests and plant diseases are the main factors that reduce the productivity of the commercial tomato, with the whitefly Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) causing significant damage (Lima et al., 2000). Bemisia tabaci has an incomplete metamorphosis, with egg, nymph (first, second, third, and fourth instars), and adult phases (Bellows et al., 1994). Losses caused by the nymphs and adults can be either direct or indirect. Direct losses constitute sap sucking and toxin injection, affecting plant development and hence the quantity and quality of the final product (Toscano et al., 2004). Indirect loss is due to the transmission of the geminivirus (tomato yellow vein streak virus) disease, as well as sooty mold (Capnodium sp.), which reduce chlorophyll protein concentrations and the rate of photosynthesis (Hunter et al., 1998)

Whitefly of the Bemisia genus has become more important due to the introduction and dispersion of the biotype B, also referred to as Bemisia argentifolii, in North and South America and Europe. This biotype differs from the biotype A by its higher fecundity, higher number of hosts, resistance to several insecticides, and ability to induce more physiological abnormalities, such as silverleaf in cucurbits and irregular ripening of tomato fruits (Brown et al., 2000).

The main method for B. tabaci biotype B control is insecticides; however, they are often inefficient, pollute the environment, reduce natural enemies, and sort resistant biotypes (Bacci et al., 2007). Resistant tomato cultivars are considered to be ideal for B. tabaci management (Russell, 1978; Smith, 1989). Alternate genetic sources are indispensable in developing resistant cultivars, with germplasm banks being potentially important sources. Besides resistance, agronomic characteristics are highly desirable in breeding programs. Agronomic characteristics of the tomato subsamples from the HGB at UFV have been typified (Abreu et al., 2006) but little is known about their insect resistance (Oliveira et al., 2009). Despite the importance of breeding insect-resistant tomato cultivars, only a few such studies involving a few subsamples have been conducted (Suinaga et al., 2003, 2004). In addition, possible resistance mechanisms have not been investigated. Hence, the objective of this study was to evaluate the resistance of 103 HGB-UFV tomato subsamples to B. tabaci as well as to assess the resistance mechanism.


MATERIALS AND METHODS

Rearing of Bemisia tabaci

Adult whiteflies were collected from a commercial tomato plantation in Viçosa, MG, Brazil, and mailed for identification to Dr. Judith K. Brown, Department of Plant Science, University of Arizona, Tucson. After identification, the insects were reared in a greenhouse at UFV on cabbage (Brassica oleracea var. acephala DC.) cultivars and serralha-lisa (Sonchus oleraceus L.) (Panda and Khush, 1995), with weekly additions of cabbage, not infected with whitefly or other insects. The soil in the pots was irrigated twice a day. The average temperature in the greenhouse was 27 ± 7°C and the relative humidity was 65 ± 5%.

Resistance Mechanism of Tomato to Bemisia tabaci

Experiments were conducted in a greenhouse (6-m length by 5-m width by 3.5-m height at UFV). One hundred and three HGB-UFV tomato subsamples along with the cultivar Santa Clara (susceptibility standard to the whitefly) were used (Table 1).


View Full Table | Close Full ViewTable 1.

Origin and collection year of the tomato subsamples from the Horticultural Germplasm Bank (HGB) at the Universidade Federal de Viçosa (source: www.ufv.br/bgh; verified 8 Aug. 2011).

 
Subsample Origin Year
HGB-24 Teóphyllo Otoni, MG, Brazil 1966
HGB-83 Feira de Santana, BA, Brazil 1966
HGB-121 Salvador, BA, Brazil 1966
HGB-161 Muribeca, BA, Brazil 1966
HGB-168 Maceió, AL, Brazil 1966
HGB-186 Vitória do Santo Antão, PE, Brazil 1966
HGB-216 Vitória do Santo Antão, PE, Brazil 1966
HGB-224 Alagoinha, BA, Brazil 1966
HGB-225 Alagoinha, BA, Brazil 1966
HGB-279 Goiás, GO, Brazil 1966
HGB-327 Estiva, GO, Brazil 1966
HGB-349 Estiva, GO, Brazil 1966
HGB-351 Jussara, GO, Brazil 1966
HGB-378 Itapirapuan, GO, Brazil 1966
HGB-468 Goiás, GO, Brazil 1966
HGB-603 Barbacena, MG, Brazil 1966
HGB-606 Barbacena, MG, Brazil 1966
HGB-630 São João Del Rei, MG, Brazil 1966
HGB-700 Cuiabá, MT, Brazil 1966
HGB-773 Porto Simão, MT, Brazil 1967
HGB-813 Cuiabá, MT, Brazil 1967
HGB-970 Campinas, SP, Brazil 1966
HGB-971 Campinas, SP, Brazil 1966
HGB-978 Campinas, SP, Brazil 1966
HGB-981 Campinas, SP, Brazil 1966
HGB-984 Campinas, SP, Brazil 1966
HGB-985 Campinas, SP, Brazil 1966
HGB-987 Campinas, SP, Brazil 1966
HGB-988 Campinas, SP, Brazil 1966
HGB-989 Campinas, SP, Brazil 1966
HGB-991 Campinas, SP, Brazil 1966
HGB-992 Campinas, SP, Brazil 1966
HGB-993 Campinas, SP, Brazil 1966
HGB-994 Campinas, SP, Brazil 1966
HGB-996 Campinas, SP, Brazil 1966
HGB-1019 Belo Horizonte, MG, Brazil 1967
HGB-1254 Goiânia, GO, Brazil 1969
HGB-1258 São Gonçalo, MT, Brazil 1969
HGB-1287 Londrina, PR, Brazil 1969
HGB-1490 São Paulo, SP, Brazil 1967
HGB-1497 São Paulo, SP, Brazil 1967
HGB-1498 São Paulo, SP, Brazil 1967
HGB-1532 Belo Horizonte, MG, Brazil 1967
HGB-1706 São Paulo, SP, Brazil 1967
HGB-1985 Purdue Univ., West Lafayette, IN 1966
HGB-1989 Purdue Univ., West Lafayette, IN 1966
HGB-1991 Purdue Univ., West Lafayette, IN 1966
HGB-2004 Purdue Univ., West Lafayette, IN 1966
HGB-2008 Purdue Univ., West Lafayette, IN 1966
HGB-2009 Purdue Univ., West Lafayette, IN 1966
HGB-2010 Purdue Univ., West Lafayette, IN 1966
HGB-2011 Purdue Univ., West Lafayette, IN 1966
HGB-2013 Purdue Univ., West Lafayette, IN 1966
HGB-2014 Purdue Univ., West Lafayette, IN 1966
HGB-2017 Purdue Univ., West Lafayette, IN 1966
HGB-2018 Purdue Univ., West Lafayette, IN 1966
HGB-2020 Purdue Univ., West Lafayette, IN 1966
HGB-2021 Purdue Univ., West Lafayette, IN 1966
HGB-2025 Purdue Univ., West Lafayette, IN 1966
HGB-2027 Purdue Univ., West Lafayette, IN 1966
HGB-2029 Purdue Univ., West Lafayette, IN 1966
HGB-2030 Purdue Univ., West Lafayette, IN 1966
HGB-2032 Purdue Univ., West Lafayette, IN 1966
HGB-2034 Purdue Univ., West Lafayette, IN 1966
HGB-2035 Purdue Univ., West Lafayette, IN 1966
HGB-2038 Purdue Univ., West Lafayette, IN 1966
HGB-2039 Purdue Univ., West Lafayette, IN 1966
HGB-2040 Purdue Univ., West Lafayette, IN 1966
HGB-2041 Purdue Univ., West Lafayette, IN 1966
HGB-2048 Purdue Univ., West Lafayette, IN 1966
HGB-2049 Purdue Univ., West Lafayette, IN 1966
HGB-2054 Purdue Univ., West Lafayette, IN 1966
HGB-2055 Purdue Univ., West Lafayette, IN 1966
HGB-2057 Purdue Univ., West Lafayette, IN 1966
HGB-2060 Purdue Univ., West Lafayette, IN 1966
HGB-2062 Purdue Univ., West Lafayette, IN 1966
HGB-2064 Purdue Univ., West Lafayette, IN 1966
HGB-2065 Purdue Univ., West Lafayette, IN 1966
HGB-2068 Purdue Univ., West Lafayette, IN 1966
HGB-2071 Purdue Univ., West Lafayette, IN 1966
HGB-2073 Purdue Univ., West Lafayette, IN 1966
HGB-2075 Purdue Univ., West Lafayette, IN 1966
HGB-2083 Purdue Univ., West Lafayette, IN 1966
HGB-2088 Purdue Univ., West Lafayette, IN 1966
HGB-2089 Purdue Univ., West Lafayette, IN 1966
HGB-2095 Purdue Univ., West Lafayette, IN 1966
HGB-2096 Purdue Univ., West Lafayette, IN 1966
HGB-2097 Purdue Univ., West Lafayette, IN 1966
HGB-2098 Purdue Univ., West Lafayette, IN 1966
HGB-2100 Purdue Univ., West Lafayette, IN 1966
HGB-2112 Purdue Univ., West Lafayette, IN 1966
HGB-2113 Purdue Univ., West Lafayette, IN 1966
HGB-2116 Purdue Univ., West Lafayette, IN 1966
HGB-2117 Purdue Univ., West Lafayette, IN 1966
HGB-2119 Purdue Univ., West Lafayette, IN 1966
HGB-2121 Purdue Univ., West Lafayette, IN 1966
HGB-2122 Purdue Univ., West Lafayette, IN 1966
HGB-2123 Purdue Univ., West Lafayette, IN 1966
HGB-2124 Purdue Univ., West Lafayette, IN 1966
HGB-2127 Purdue Univ., West Lafayette, IN 1966
HGB-2128 Purdue Univ., West Lafayette, IN 1966
HGB-2129 Purdue Univ., West Lafayette, IN 1966
HGB-2130 Purdue Univ., West Lafayette, IN 1966

Seeds were sown in polystyrene trays (68 by 34 cm) with 128 cells. Pine bark with vermiculite (Bioplant, Nova Ponte, MG, Brazil) was used as the substrate. Three to four tomato seeds were added to each cell. Seedlings were transplanted to 500-mL plastic containers containing dirt and tanned cow manure. The cultivation techniques used were described by Silva et al. (2008).

The experimental block design was entirely randomized with 104 treatments (103 subsamples plus Santa Clara) with three replicates. Each experimental plot consisted of a plastic vase with one tomato plant with six fully expanded leaves (about 20 d after transplant) placed on wooden benches (4-m length by 1.20-m width by 1.30-m height) in a greenhouse. At the beginning of the experiment, about 3600 adult whiteflies from insect colonies were released in the central part of the greenhouse.

Eggs from all parts of the plants were counted using a magnifying glass (20× magnification) after 6 d of infestation with adult insects. The nymph/egg ratio was calculated asThe resistance index (RI) of the 103 tomato subsamples relative to Santa Clara was calculated. This procedure was used for all intensity characters (number of eggs and nymphs per plant and nymph/egg ratio) of B. tabaci attack using the following formula (Baldin et al., 2000):where X is number of eggs and nymphs per plant and nymph/egg ratio; RIX is the resistance index for the characteristic X; XS is the characteristic X for the HSB tomato subsample; and XP is the characteristic X for the susceptible standard (Santa Clara).

The confidence interval for the RI for Santa Clara was calculated for each characteristic evaluated and used as the standard to compare all the subsamples. The subsamples were classified as resistant, susceptible, or highly susceptible if the RI was lower, within, or higher than that of the Santa Clara confidence interval. This classification was based on the degree of resistance to insects (Lara, 1991).

The subsamples selected were submitted to antibiosis tests by removing one leaf from the median region and immersing its petiole in a plastic container with 100 mL of water to maintain leaf turgor. The container openings were sealed with hydrophobic cotton to avoid the death of B. tabaci adults by drowning. Each container containing one leaf of a subsample was placed in a plastic container (3 L), using a screen with a covered side opening to prevent insect attack. In the inner part of each bottle, 30 adult whiteflies were released and removed after 2 d. Eggs were counted with the help of a magnifying glass (20× magnification). Every 3 d, the number of nymphs and adults was counted. From these data, nymph and adult densities in each phase and the mortality percentage in each life cycle phase were calculated for all the subsamples.

Resistance Factors of Tomato to Bemisia tabaci

Trichome Density

The first fully expanded leaf from the plant apex was collected from each experimental plot and the number of trichomes on the first leaflet (0.04-cm2 area) in the left region, without overlapping the nerve region, was evaluated. The trichome number was counted using a stereoscopic microscope (SMZ-140 Series, Motic, Xiamen, China) with 40× magnification.

Chemical Analysis

Leaves were removed from the plants and immediately cut with a pair of scissors into small pieces (approximately 1 cm in length) and 10 g of each subsample was placed in an Erlenmeyer flask and extracted with 250 mL of double-distilled hexane for 24 h. The hexane was evaporated to dryness at 45°C and the residue was stored in sealed glass vials (8 mL) in a freezer. For analysis, the residue was allowed to thaw to room temperature, diluted with hexane (1 mL), and analyzed by gas chromatography–mass spectrometry (GC–MS).

All data were obtained on a Shimadzu gas chromatograph–mass spectrometer (Model QP 5000, Shimadzu Corp., Kyoto, Japan) with the software program Class-5000, Version 1.2, an autosampler, a mass spectral database with 160,000 entries, and a DB-5 fused-silica capillary column (30 m by 0.25 mm, 0.25-μm μlm thickness) (Supelco, Bellefonte, PA). The oven temperature was increased from 20 to 80°C at 20°C/min and from 80 to 250°C at 8°C/min. Injector and transfer line temperatures were maintained at 280 and 300°C, respectively. The split ratio was 1:1 with He as the carrier gas at a flow rate of 1.2 mL/min (linear flow of 39.5 cm/s). Electron impact ionization mass spectra (70 eV) were recorded by scanning the mass spectrometer from m/z 29 to 320. To obtain representative data, the mass spectra of each GC peak (∼50 scans) of interest was grouped and subtracted from the grouped mass spectra of the region closest (before or after) where no compound eluted.

The peaks were first identified by the GC–MS library system based on similarity indices. Final confirmation was made by comparing retention times with authentic hydrocarbon standards. Quantification was performed using the external standard method.

Statistical Analysis

Eggs per plant, nymphs per plant, nymph/egg ratio, and trichome density per 0.04 cm2 data were submitted to Cochran and Lilliefors tests to verify if the data obeyed presuppositions of homogeneity variance and error normality (Cochran, 1947). Data were then submitted to variance analysis and their means were compared using the Scott–Knott test to group means (P < 0.05) (Scott and Knott, 1974).

Pearson correlations between B. tabaci attack and the hydrocarbon concentrations in the hexane leaf extract of the subsamples were conducted. Regression analysis of the number of eggs as a function of trichome density was also performed.


RESULTS

Bemisia tabaci Egg Density

Significant differences were noted in the number of B. tabaci eggs and adult insects per plant [F(103,208) = 3.64; P < 0.0001] among the subsamples. Fifty-three subsamples showed significantly fewer eggs than Santa Clara (Table 2). Based on the resistance index for the number of eggs per plant, subsamples HGB-225, -327, -468, -606, -630, -984, -985, -1019, 1287, -1991, -2009, -2010, -2030, -2034, -2041, -2048, -2060, -2062, -2073, -2075, and 2097 were classified as resistant to whitefly; subsamples HGB-981, -1254, -1497, and -2098 were classified as highly susceptible, while the remaining 79 subsamples were classified as highly susceptible (Fig. 1A).


View Full Table | Close Full ViewTable 2.

Number (average ± standard error) of eggs per plant of the Bemisia tabaci biotype B (Hemiptera: Aleyrodidae) in the subsamples from the Horticultural Germplasm Bank (HGB) at the Universidade Federal de Viçosa.

 
Subsample Eggs per plant†
HGB-981 100.00 ± 45.61 a
HGB-2098 63.33 ± 2.19 b
HGB-1254 57.67 ± 12.77 b
HGB-1497 55.00 ± 4.73 b
HGB-2121 43.33 ± 19.92 b
HGB-1989 42.67 ± 16.46 b
HGB-2011 41.00 ± 10.69 b
HGB-2095 32.33 ± 3.18 c
HGB-1258 30.00 ± 4.62 c
HGB-2088 28.67 ± 15.76 c
HGB-2021 26.67 ± 8.57 c
HGB-2008 26.67 ± 6.39 c
HGB-2096 26.33 ± 1.45 c
HGB-121 26.33 ± 3.76 c
HGB-2083 24.67 ± 6.64 c
HGB-1490 24.33 ± 2.91 c
HGB-2100 23.67 ± 8.41 c
HGB-378 22.67 ± 2.40 c
HGB-2089 22.33 ± 1.20 c
HGB-700 21.67 ± 3.53 c
HGB-993 20.67 ± 9.49 c
HGB-971 20.33 ± 3.76 c
HGB-2014 20.33 ± 7.22 c
HGB-1532 20.00 ± 1.15 c
HGB-2039 19.67 ± 2.60 c
HGB-1985 18.67 ± 7.75 c
HGB-83 18.33 ± 3.18 c
HGB-2040 18.33 ± 2.03 c
HGB-2054 18.33 ± 11.67 c
HGB-978 18.33 ± 16.37 c
HGB-2049 18.00 ± 4.62 c
HGB-989 18.00 ± 9.87 c
HGB-2004 16.67 ± 4.33 c
HGB-2123 16.67 ± 7.80 c
HGB-2130 16.33 ± 13.45 c
HGB-2017 16.33 ± 0.67 c
HGB-2122 16.00 ± 2.31 c
HGB-2027 15.67 ± 6.12 c
HGB-603 15.00 ± 10.07 c
HGB-970 15.00 ± 7.55 c
HGB-1498 15.00 ± 1.73 c
HGB-994 15.00 ± 1.73 c
HGB-2020 14.67 ± 5.49 c
HGB-2035 14.33 ± 4.91 c
HGB-2117 14.00 ± 2.31 c
HGB-1706 13.67 ± 8.09 c
HGB-2129 13.67 ± 3.18 c
HGB-988 13.33 ± 9.35 c
HGB-2112 13.00 ± 1.53 d
HGB-186 12.33 ± 12.33 d
HGB-2025 12.00 ± 2.08 d
HGB-2119 12.00 ± 1.73 d
HGB-216 11.33 ± 5.93 d
HGB-349 10.67 ± 4.70 d
HGB-992 10.33 ± 4.18 d
HGB-996 10.33 ± 10.33 d
HGB-2057 9.00 ± 6.66 d
HGB-991 8.67 ± 0.33 d
HGB-24 8.67 ± 0.33 d
HGB-2068 8.33 ± 2.60 d
HGB-2064 8.33 ± 2.73 d
HGB-2029 8.33 ± 8.33 d
HGB-2071 8.00 ± 8.00 d
HGB-2018 8.00 ± 1.15 d
HGB-2038 7.67 ± 7.67 d
HGB-224 7.67 ± 3.28 d
HGB-168 7.33 ± 7.33 d
HGB-2128 7.33 ± 4.33 d
HGB-2116 7.33 ± 3.18 d
HGB-2055 7.33 ± 2.19 d
HGB-2032 7.00 ± 0.58 d
HGB-2065 7.00 ± 0.58 d
HGB-161 7.00 ± 0.58 d
HGB-351 6.67 ± 3.18 d
HGB-773 6.33 ± 3.33 d
HGB-2113 6.33 ± 6.33 d
HGB-987 6.33 ± 2.91 d
HGB-813 6.33 ± 5.36 d
HGB-2127 6.00 ± 1.73 d
HGB-2013 5.33 ± 1.20 d
HGB-279 5.33 ± 4.37 d
HGB-2124 5.00 ± 2.89 d
HGB-2075 4.33 ± 4.33 d
HGB-2048 4.33 ± 4.33 d
HGB-2097 4.33 ± 4.33 d
HGB-1019 4.33 ± 4.33 d
HGB-225 4.33 ± 2.19 d
HGB-985 4.33 ± 2.60 d
HGB-630 4.33 ± 2.33 d
HGB-2034 4.00 ± 4.00 d
HGB-606 4.00 ± 1.15 d
HGB-2010 3.67 ± 2.03 d
HGB-468 3.33 ± 1.76 d
HGB-2060 3.33 ± 2.40 d
HGB-1991 3.33 ± 3.33 d
HGB-2073 3.00 ± 1.53 d
HGB-2030 3.00 ± 3.00 d
HGB-2041 2.67 ± 2.67 d
HGB-984 2.67 ± 2.19 d
HGB-2009 1.67 ± 0.88 d
HGB-1287 1.00 ± 0.58 d
HGB-327 1.00 ± 1.00 d
HGB-2062 0.00 ± 0.00 d
Santa Clara 16.33 ± 3.18 c
Averages followed by the same letter in a column belong to the same group according to the Scott–Knott test at P < 0.05.
Fig. 1.
Fig. 1.

Resistance index (RI) of the tomato subsamples from the Horticultural Germplasm Bank at Universidade Federal de Vicosa to Bemisia tabaci biotype B for (A) eggs per plant (RIEg/Pl), (B) nymphs per plant (RINy/Pl) and (C) nymph/egg ratio (RINy/Eg). Discontinuous horizontal lines delineate regions of the graph containing highly susceptible, susceptible, and resistant subsamples.

 

Bemisia tabaci Nymph Density

Significant differences were observed in the number of B. tabaci nymphs perplant [F(103,208) = 6.00; P < 0.0001] and B. tabaci nymph/egg ratio [F(103,208) = 3.48; P < 0.0001] among the subsamples. Thirty-eight subsamples showed significantly fewer nymphs than Santa Clara (Table 3). Based on the resistance index for the number of nymphs per plant, the subsamples HGB-225, -327, -606, -2009, -2029, and -2060 were resistant to whitefly, while the remaining 97 subsamples were classified as susceptible (Fig. 1B).


View Full Table | Close Full ViewTable 3.

Number (average ± standard error) of nymph/plant of Bemisia tabaci biotype B (Hemiptera: Aleyrodidae) in the subsamples from the Horticultural Germplasm Bank (HGB) at the Universidade Federal de Viçosa.

 
Subsample Nymphs per plant†
HGB-1287 105.33 ± 0.88 a
HGB-2034 101.67 ± 0.88 a
HGB-1497 96.00 ± 22.54a
HGB-996 89.00 ± 0.58 a
HGB-1532 88.00 ± 16.74a
HGB-700 84.00 ± 15.04a
HGB-2098 83.00 ± 25.70a
HGB-2123 75.00 ± 20.21a
HGB-2121 73.67 ± 9.84 a
HGB-2096 71.33 ± 6.06 a
HGB-2048 71.00 ± 1.53 a
HGB-2088 67.67 ± 21.88a
HGB-2038 65.33 ± 0.88 b
HGB-1989 60.67 ± 1.76 b
HGB-1258 60.00 ± 9.81 b
HGB-2021 59.33 ± 9.84 b
HGB-2011 55.67 ± 8.37 b
HGB-2049 55.00 ± 5.20 b
HGB-83 54.33 ± 4.33 b
HGB-2112 53.67 ± 1.86 b
HGB-2128 53.67 ± 19.95b
HGB-2100 52.33 ± 16.05b
HGB-981 50.67 ± 9.94 b
HGB-2130 49.33 ± 30.33b
HGB-121 48.33 ± 18.10b
HGB-971 47.00 ± 4.36 b
HGB-2039 46.67 ± 2.60 b
HGB-2008 46.67 ± 13.02b
HGB-2071 45.67 ± 1.20 b
HGB-2004 45.67 ± 20.79b
HGB-2124 45.67 ± 5.49 b
HGB-378 44.33 ± 4.84 b
HGB-168 42.33 ± 1.45 c
HGB-2127 42.00 ± 8.39 c
HGB-2032 40.67 ± 15.30c
HGB-2073 40.33 ± 0.88 c
HGB-2089 39.33 ± 2.40 c
HGB-186 38.33 ± 0.88 c
HGB-1706 38.00 ± 13.58 c
HGB-992 36.67 ± 11.78 c
HGB-2122 36.67 ± 6.64 c
HGB-2113 35.67 ± 1.20 c
HGB-1019 35.00 ± 1.53 c
HGB-1254 34.00 ± 13.28 c
HGB-2020 34.00 ± 8.50 c
HGB-1498 33.33 ± 0.88 c
HGB-994 33.33 ± 17.61 c
HGB-2013 32.33 ± 3.18 c
HGB-2075 32.00 ± 0.58 c
HGB-2017 30.33 ± 5.49 c
HGB-988 30.00 ± 12.10 c
HGB-984 29.33 ± 11.89 c
HGB-978 28.67 ± 11.32 c
HGB-991 28.00 ± 5.69 c
HGB-2040 26.67 ± 3.76 c
HGB-2014 26.67 ± 7.22 c
HGB-2035 26.33 ± 0.33 c
HGB-2129 26.00 ± 9.07 c
HGB-2054 25.67 ± 6.36 c
HGB-1985 25.33 ± 5.78 c
HGB-1991 25.00 ± 0.58 c
HGB-2083 24.67 ± 1.45 c
HGB-2018 24.67 ± 0.88 c
HGB-2097 24.33 ± 0.88 c
HGB-224 24.33 ± 5.24 c
HGB-2117 23.67 ± 0.33 d
HGB-2116 23.33 ± 2.60 d
HGB-1490 23.00 ± 0.58 d
HGB-2064 23.00 ± 9.45 d
HGB-2068 22.33 ± 2.60 d
HGB-2119 21.33 ± 6.64 d
HGB-993 21.00 ± 7.21 d
HGB-468 20.33 ± 6.06 d
HGB-351 20.00 ± 5.20 d
HGB-2055 20.00 ± 8.96 d
HGB-773 19.33 ± 7.88 d
HGB-349 19.00 ± 6.11 d
HGB-813 18.67 ± 15.68 d
HGB-2065 18.33 ± 2.33 d
HGB-216 17.67 ± 1.86 d
HGB-2057 17.00 ± 3.79 d
HGB-24 16.67 ± 7.06 d
HGB-970 16.67 ± 7.80 d
HGB-279 16.00 ± 5.03 d
HGB-2030 15.33 ± 9.87 d
HGB-630 15.33 ± 7.88 d
HGB-2041 15.00 ± 0.58 d
HGB-2027 15.00 ± 4.04 d
HGB-2095 14.00 ± 5.20 d
HGB-2062 13.33 ± 4.48 d
HGB-985 13.00 ± 5.86 d
HGB-2025 12.67 ± 3.71 d
HGB-603 12.00 ± 5.77 d
HGB-2010 11.67 ± 1.20 d
HGB-989 11.33 ± 2.03 d
HGB-987 10.67 ± 1.76 d
HGB-161 10.33 ± 4.91 d
HGB-2029 10.00 ± 4.73 d
HGB-225 9.00 ± 2.65 d
HGB-606 8.00 ± 3.00 d
HGB-2060 7.67 ± 1.86 d
HGB-2009 6.00 ± 0.58 d
HGB-327 4.67 ± 1.20 d
Santa Clara 37.33 ± 8.09 c
Averages followed by the same letter in a column belong to the same group according to the Scott–Knott test at P < 0.05.

Twenty-five subsamples showed significantly more nymphs than Santa Clara (Table 4). Based on the resistance index for the nymph/egg ratio, all the subsamples studied were classified as susceptible to B. tabaci attack (Fig. 1C).


View Full Table | Close Full ViewTable 4.

Nymph/egg ratios (average ± standard error) of Bemisia tabaci biotype B (Hemiptera: Aleyrodidae) in the subsamples from the Horticultural Germplasm Bank (HGB) at the Universidade Federal de Viçosa.

 
Subsample nymph/egg ratio†
HGB-1287 78.25 ± 21.02 a
HGB-2073 22.00 ± 9.29 b
HGB-2123 14.14 ± 11.30 b
HGB-992 11.02 ± 9.25 c
HGB-2034 8.58 ± 0.00 c
HGB-988 7.68 ± 5.17 c
HGB-2127 7.46 ± 0.82 c
HGB-2124 7.35 ± 1.51 c
HGB-279 6.86 ± 5.02 d
HGB-2013 6.59 ± 1.21 d
HGB-2032 6.26 ± 2.73 d
HGB-984 6.21 ± 0.17 d
HGB-978 5.95 ± 4.73 d
HGB-351 5.60 ± 2.79 e
HGB-773 5.59 ± 3.21 e
HGB-2048 5.54 ± 0.00 e
HGB-2116 4.98 ± 2.28 e
HGB-2128 4.60 ± 2.78 e
HGB-1532 4.48 ± 1.05 e
HGB-700 4.31 ± 1.49 e
HGB-2112 4.22 ± 0.39 e
HGB-224 4.21 ± 1.29 e
HGB-987 4.14 ± 2.93 e
HGB-2030 3.89 ± 0.00 e
HGB-2049 3.69 ± 1.36 e
HGB-2018 3.25 ± 0.59 f
HGB-2020 3.21 ± 1.20 f
HGB-991 3.20 ± 0.57 f
HGB-2068 3.11 ± 0.72 f
HGB-83 3.10 ± 0.43 f
HGB-2121 3.04 ± 1.60 f
HGB-2088 3.01 ± 0.86 f
HGB-1706 2.95 ± 0.98 f
HGB-468 2.92 ± 0.34 f
HGB-2060 2.88 ± 1.33 f
HGB-996 2.84 ± 0.00 f
HGB-2038 2.78 ± 0.00 f
HGB-2064 2.77 ± 0.45 f
HGB-2021 2.72 ± 0.79 f
HGB-2096 2.71 ± 0.22 f
HGB-2100 2.70 ± 0.98 f
HGB-2009 2.67 ± 0.27 f
HGB-2065 2.62 ± 0.26 f
HGB-1019 2.62 ± 0.00 f
HGB-606 2.61 ± 1.49 f
HGB-1991 2.60 ± 0.00 f
HGB-2057 2.53 ± 1.69 f
HGB-2122 2.52 ± 0.80 f
HGB-2039 2.48 ± 0.40 f
HGB-813 2.47 ± 0.38 f
HGB-2010 2.46 ± 0.85 f
HGB-2035 2.45 ± 0.96 f
HGB-603 2.40 ± 1.20 f
HGB-971 2.40 ± 0.24 f
HGB-2004 2.39 ± 0.68 f
HGB-2055 2.39 ± 0.63 f
HGB-2075 2.38 ± 0.00 f
HGB-2129 2.36 ± 1.03 f
HGB-327 2.33 ± 0.00 f
HGB-1498 2.28 ± 0.24 f
HGB-1258 2.21 ± 0.69 f
HGB-1989 2.16 ± 1.01 f
HGB-2130 2.10 ± 0.35 f
HGB-378 2.06 ± 0.47 f
HGB-2119 2.03 ± 0.88 f
HGB-349 2.01 ± 0.64 f
HGB-994 2.00 ± 0.96 f
HGB-2113 2.00 ± 0.00 f
HGB-970 1.97 ± 1.52 f
HGB-24 1.92 ± 0.77 f
HGB-2041 1.88 ± 0.00 f
HGB-2017 1.86 ± 0.33 f
HGB-2097 1.85 ± 0.00 f
HGB-2071 1.83 ± 0.00 f
HGB-168 1.82 ± 0.00 f
HGB-993 1.79 ± 0.86 f
HGB-121 1.79 ± 0.49 f
HGB-2117 1.78 ± 0.28 f
HGB-2089 1.77 ± 0.10 f
HGB-2008 1.72 ± 0.09 f
HGB-1497 1.70 ± 0.28 f
HGB-1985 1.65 ± 0.49 f
HGB-161 1.59 ± 0.87 f
HGB-2040 1.54 ± 0.37 f
HGB-2054 1.49 ± 0.58 f
HGB-985 1.47 ± 0.79 f
HGB-2011 1.45 ± 0.18 f
HGB-2014 1.43 ± 0.17 f
HGB-981 1.43 ± 1.01 f
HGB-2098 1.34 ± 0.45 f
HGB-225 1.26 ± 0.49 f
HGB-2083 1.16 ± 0.29 f
HGB-630 1.11 ± 0.42 f
HGB-2027 1.09 ± 0.22 f
HGB-2025 1.03 ± 0.16 f
HGB-216 1.03 ± 0.27 f
HGB-186 1.00 ± 0.00 f
HGB-1490 0.98 ± 0.15 f
HGB-2029 0.68 ± 0.00 f
HGB-1254 0.54 ± 0.12 f
HGB-2095 0.43 ± 0.14 f
HGB-989 0.42 ± 0.02 f
HGB-2062 0.00 ± 0.00 f
Santa Clara 2.75 ± 1.20 f
Averages followed by the same letter in a column belong to the same group according to the Scott–Knott test at P < 0.05.

In the antibiosis test, the mortality in the adult-egg phase for the subsamples HGB-2029, -2055, -985, and -327 was 89.75, 84.00, 83.95, and 67.11%, respectively. These mortalities were significantly higher than that recorded for Santa Clara (27.96%). The whitefly egg-to-adult life cycle was longer for the subsamples HGB-813 (36 d), -985 and -2029 (34 d), -2062, -2055, -327, and -2057 (approximately 33 d) than for Santa Clara (28 d) (Table 5).


View Full Table | Close Full ViewTable 5.

Number (average ± standard error) of eggs and adults per plant, mortality, and life cycle length of Bemisia tabaci biotype B (Hemiptera: Aleyrodidae) in the selected tomato subsamples with possible resistance factors (at 25 ± 2°C, 70 ± 5% relative humidity).

 
Subsample Eggs per plant Adults per plant Mortality Life cycle
% d
HGB-225 32.00 ± 3.00 20.00 ± 2.50 37.00 ± 1.75 29.00 ± 4.00
HGB-327 76.00 ± 2.00 25.00 ± 1.50 67.11 ± 0.95 33.00 ± 2.00
HGB-813 58.50 ± 2.86 37.50 ± 2.86 36.03 ± 1.76 36.00 ± 1.00
HGB-985 81.00 ± 1.50 13.00 ± 2.20 83.95 ± 2.00 34.00 ± 2.08
HGB-2029 45.50 ± 20.82 6.00 ± 4.08 89.75 ± 4.28 34.00 ± 2.08
HGB-2030 44.00 ± 4.90 13.00 ± 3.05 69.89 ± 3.35 29.00 ± 4.93
HGB-2055 25.00 ± 1.00 4.00 ± 2.80 84.00 ± 2.07 33.00 ± 4.00
HGB-2057 30.00 ± 2.00 14.00 ± 1.25 53.33 ± 1.58 33.00 ± 4.00
HGB-2060 80.00 ± 1.00 63.00 ± 2.55 21.25 ± 2.75 27.50 ± 2.04
HGB-2062 48.00 ± 12.25 28.50 ± 2.86 31.67 ± 23.39 33.33 ± 1.66
HGB-2068 48.50 ± 20.00 42.00 ± 21.23 20.09 ± 10.81 29.00 ± 3.05
Santa Clara 93.00 ± 1.50 67.00 ± 2.43 27.96 ± 1.45 28.33 ± 1.66

Causes of Resistance to Bemisia tabaci

Morphological Causes

Significant differences among the subsamples were detected in the number of trichomes per 0.04 cm2 [F(103,208) = 6.08; P < 0.0001]. High trichome density was observed in the subsamples HGB-630, -1490, -2004, -2009, -2011, -2013, -2017, -2020, -2098, -2100, -2121, -2122, and -2130. A low trichome density was observed in the subsamples HGB-349, -773, -2029, and -2060 (Table 6). A positive and significant correlation was found between the trichome density in the subsamples and the number of eggs per plant (Y = –0.88 + 0.09X; R2 = 0.23; F = 85.75; P < 0.001), suggesting that the subsamples with higher trichome density received greater oviposition of adult B. tabaci.


View Full Table | Close Full ViewTable 6.

Number (average ± standard error) of trichomes per 0.04 cm2 of leaf blade of the tomato subsamples from the Horticultural Germplasm Bank (HGB) at the Universidade Federal de Viçosa.

 
Subsample Trichomes per 0.04 cm2
HGB-2011 365.67 ± 55.14 a
HGB-1490 364.00 ± 98.73 a
HGB-2121 337.67 ± 11.26 a
HGB-2098 320.00 ± 11.02 a
HGB-2009 316.67 ± 21.07 a
HGB-2020 303.00 ± 6.93 a
HGB-2004 303.00 ± 59.47 a
HGB-2122 296.33 ± 62.96 a
HGB-2100 288.33 ± 10.93 a
HGB-630 286.00 ± 12.49 a
HGB-2013 283.67 ± 19.92 a
HGB-2130 280.00 ± 90.84 a
HGB-2017 275.67 ± 53.98 a
HGB-1497 264.67 ± 1.20 b
HGB-2127 255.00 ± 33.49 b
HGB-2021 252.00 ± 45.90 b
HGB-1985 250.67 ± 35.51 b
HGB-2008 249.67 ± 25.69 b
HGB-1706 242.33 ± 65.89 b
HGB-1498 235.83 ± 57.53 b
HGB-978 226.67 ± 8.82 b
HGB-2116 224.50 ± 21.98 b
HGB-186 223.00 ± 0.00 b
HGB-2054 220.67 ± 26.19 b
HGB-2083 217.67 ± 36.66 b
HGB-2128 217.67 ± 14.72 b
HGB-994 210.00 ± 0.58 b
HGB-2129 201.67 ± 42.46 b
HGB-2018 200.67 ± 2.33 b
HGB-2010 200.00 ± 50.81 b
HGB-2057 196.67 ± 38.27 c
HGB-2014 193.00 ± 23.09 c
HGB-1254 189.00 ± 39.84 c
HGB-992 187.00 ± 1.53 c
HGB-468 180.67 ± 36.66 c
HGB-993 176.33 ± 16.22 c
HGB-2025 175.67 ± 2.33 c
HGB-2119 171.67 ± 37.24 c
HGB-2124 169.33 ± 0.67 c
HGB-327 168.00 ± 46.19 c
HGB-606 161.67 ± 37.82 c
HGB-603 161.33 ± 29.45 c
HGB-989 160.67 ± 47.05 c
HGB-1019 160.00 ± 0.58 c
HGB-2068 157.67 ± 36.38 c
HGB-2034 157.67 ± 0.33 c
HGB-2035 157.00 ± 0.58 c
HGB-351 156.33 ± 35.80 c
HGB-2027 153.33 ± 7.26 c
HGB-225 152.67 ± 34.35 c
HGB-984 152.00 ± 25.40 c
HGB-2071 149.67 ± 0.33 c
HGB-2039 146.00 ± 0.58 c
HGB-2089 145.33 ± 2.91 c
HGB-2096 144.00 ± 0.58 c
HGB-1287 142.33 ± 1.45 c
HGB-2032 141.33 ± 10.68 c
HGB-2073 138.67 ± 0.88 c
HGB-996 138.00 ± 0.58 c
HGB-1532 137.67 ± 40.19 c
HGB-2097 137.00 ± 0.58 c
HGB-2038 134.00 ± 0.58 d
HGB-2112 134.00 ± 40.45 d
HGB-1989 133.67 ± 40.70 d
HGB-2088 133.00 ± 40.82 d
HGB-1991 133.00 ± 40.82 d
HGB-2065 131.33 ± 23.17 d
HGB-279 130.00 ± 23.67 d
HGB-970 128.33 ± 24.55 d
HGB-2030 127.33 ± 10.97 d
HGB-83 126.67 ± 0.67 d
HGB-216 124.00 ± 13.00 d
HGB-971 124.00 ± 0.58 d
HGB-2123 124.00 ± 0.58 d
HGB-224 122.00 ± 18.48 d
HGB-168 121.33 ± 0.67 d
HGB-813 120.00 ± 25.12 d
HGB-2040 120.00 ± 0.58 d
HGB-985 119.33 ± 8.57 d
HGB-981 117.67 ± 1.45 d
HGB-2062 117.67 ± 12.99 d
HGB-378 116.00 ± 6.08 d
HGB-2048 115.00 ± 0.58 d
HGB-161 113.33 ± 10.40 d
HGB-700 113.00 ± 13.00 d
HGB-121 110.00 ± 0.58 d
HGB-2113 109.00 ± 0.58 d
HGB-991 105.67 ± 0.67 e
HGB-987 103.67 ± 11.57 e
HGB-2064 101.33 ± 3.28 e
HGB-24 99.33 ± 6.64 e
HGB-1258 98.67 ± 0.33 e
HGB-2117 98.00 ± 0.58 e
HGB-2055 96.33 ± 5.93 e
HGB-2075 94.00 ± 0.58 e
HGB-2049 91.00 ± 0.58 e
HGB-2041 91.00 ± 0.58 e
HGB-2095 87.00 ± 0.58 e
HGB-988 86.00 ± 3.06 e
HGB-773 81.67 ± 5.21 f
HGB-349 75.67 ± 2.03 f
HGB-2060 74.00 ± 6.66 f
HGB-2029 57.33 ± 8.25 g
Santa Clara 168.67 ± 30.85 c
Averages followed by the same letter in a column belong to the same group according to the Scott–Knott test at P < 0.05.

Chemical Causes

Fifteen hydrocarbons (C9, nonane; C10, decane; C11, undecane; C12, dodecane; C13, tridecane; C14, tetradecane; C15, tetradecane; C16, hexadecane; C17, heptadecane; C18, octadecane; C19, nonadecane; C20, eicosane; C21, henecosane; C22, docosane; and C24, tetracosane) were quantified in the leaf extracts of 98 subsamples. No hydrocarbons were observed in the subsamples HGB-121, -186, -349, -1287, -2049, and -2097 (Table 7). Of the 15 hydrocarbons, only C11 and C13 were significantly correlated (P < 0.05) with the number of nymphs (r = 0.24 and 0.23, respectively).


View Full Table | Close Full ViewTable 7.

Concentrations of 15 hydrocarbons in the hexane leaf extracts of 103 tomato subsamples from the Horticultural Germplasm Bank (HGB) at the Universidade Federal de Viçosa and the cultivar Santa Clara (SC).

 
Concentration†
Subsample C9 C10 C11 C12 C13 C14 C15 C16 C17 C18 C19 C20 C21 C22 C24
g/kg of leaves based on fresh weight
SC 67.3 6 8.5
HGB-24 21
HGB-83 74.8 17.3 23.2 56.3 9
HGB-161 3757.4 36
HGB-168 8 3.4 3.3 10 0.5
HGB-216 6 6 3
HGB-224 1 40
HGB-225 10 7 33
HGB-279 39.45 25.1 15
HGB-327 3.7
HGB-351 1 4.6
HGB-378 4.5 15
HGB-468 5.3 9.5 16
HGB-603 3 1.5 12.6
HGB-606 4.2 7
HGB-630 8.5
HGB-700 5 73
HGB-773 31.7 24
HGB-813 121 5.4
HGB-970 809 5.5 18 341
HGB-971 3.4 34 11
HGB-978 10.5 13
HGB-981 3 4
HGB-984 1.6
HGB-985 6 333
HGB-987 6.3 7 20 7 54
HGB-988 2924
HGB-991 2.5
HGB-992 7.2 388
HGB-993 9
HGB-994 151.5 69
HGB-996 4.1
HGB-1019 131.8 195 18.1 21.5 6.3 7 7 62 16 79
HGB-1254 3 13
HGB-1258 7 5.5
HGB-1490 5
HGB-1497 2.3 3.3 48
HGB-1498 6.5 15.6 1.7 138
HGB-1532 13.3 14.5 6 11 33 1 97
HGB-1706 6 2.6 173
HGB-1985 1.2 85.5 427
HGB-1991 14
HGB-1999 121 540
HGB-2004 9.4 9.0 4.7 3.5 35
HGB-2008 13 103
HGB-2009 5 4.5 4.7 5 48
HGB-2010 4.6 4 3.3 3.7 3 6 0.5 132
HGB-2011 4.4 9
HGB-2013 9 6.2 5.5 2 18
HGB-2014 4.5 15.7 10.3 8.5 9 24
HGB-2017 5 5.4 6.2 4.5 7 11 8
HGB-2018 37
HGB-2020 16
HGB-2021 6 6 8 197
HGB-2025 3.3
HGB-2027 4.6 3.5 7.3
HGB-2029 1.5 4
HGB-2030 1.5
HGB-2032 13.7 11 14.1 25 9 10 7 11 17.7
HGB-2034 5
HGB-2035 9 6 2.2 2.7 3 24
HGB-2038 12 10.8 13.8 5 6.2 6 36 1
HGB-2039 51.3 17.7 6 30 6.5 50
HGB-2040 6.5 3 4 3.5 7 27 3
HGB-2041 15.0 10.2 3 44 30
HGB-2048 6
HGB-2054 31 6 67.7
HGB-2055 47.2
HGB-2057 1.5 6
HGB-2060 24 34
HGB-2062 4 30
HGB-2064 7.8 77
HGB-2065 2.2 145
HGB-2067 63
HGB-2068 7 5
HGB-2072 4.4 85
HGB-2075 9 15.2 5.2 1.5 33 1.3
HGB-2083 15 43 12 473
HGB-2088 66.7
HGB-2089 61.3
HGB-2095 3 5 5 33 1.2
HGB-2096 14, 6 5
HGB-2098 3.20 3.7 4 1 92.2
HGB-2100 4.4
HGB-2112 4.1 6 2.5 6 70
HGB-2113 17.7 7
HGB-2116 11 192
HGB-2119 34 290
HGB-2121 18 11 24 13 487
HGB-2122 5.4 9 7 29 15.6 27 215
HGB-2123 31.7 14.2 26 17.5 31
HGB-2124 44 28 19.4 35 501
HGB-2127 20 14 3
HGB-2128 1.5 2 3 29
HGB-2129 4
HGB-2130 2.2 43
C9, nonane; C10, decane; C11, undecane; C12, dodecane; C13, tridecane; C14, tetradecane; C15, tetradecane; C16, hexadecane; C17, heptadecane; C18, octadecane; C19, nonadecano; C20, eicosane; C21, henecosane; C22, docosane; C24, tetracosane. No hydrocarbons were detected in the subsamples HGB-121, -186, -349, -1287, -2049, and -2097.


DISCUSSION

Of the 103 subsamples, 55 had a low egg density per plant; 38 had lower nymph density per plant, and 79 subsamples had a lower nymph density per egg. The subsamples HGB-225, -327, -630, -813, -985, -2029, -2055, -2057, -2060, -2062, and -2068 were less attacked by B. tabaci for all traits evaluated in this study.

Few studies have investigated sources of resistance to B. tabaci in S. lycopersicum species (Oliveira et al., 2009). Most studies have been conducted with Lycopersicon hirsutum Donal, L. hirsutum Dunal forma glabratum C. H. Müll., L. peruvianum (L.) Mill., L. pennellii (Correll) D'Arcy, and L. pimpinellifolium (L.) Mill. (Fancelli and Vendramim, 2002; Toscano et al., 2002). Toscano et al. (2002) reported B. tabaci ovipostion of 2.3 ± 0.7 and 3.16 ± 2 in the subsamples PI-134417 of L. hirsutum f. glabratum and of LA 716 (L. pennellii), respectively, compared with 17.6 ± 7.8 in the susceptible Santa Clara. Based on lower oviposition, these subsamples were considered to be sources of resistance to this insect. Of the seven subsamples evaluated in preference tests by Fancelli and Vendramim (2002), only the subsamples LA 1739 of L. hirsutum and PI-134417 of L. hirsutum f. glabratum were less oviposited by B. tabaci than Santa Clara.

Other studies have reported differences in adult and nymph populations in different tomato subsamples. For example, Baldin et al. (2005) studied nine subsamples of Lycopersicon sp. and reported a lower number of adult B. tabaci in the subsample PI-134417 of L. hirsutum f. glabratum than IAC-Santa Clara. On the other hand, of the eight subsamples, only LA 716 of L. pennellii was less attacked than Santa Clara (Fancelli et al., 2005).

Low insect densities of eggs per plant and nymphs per plant of the subsamples HGB-225, -327, -813, -985, -2029, -2030, -2055, -2057, -2060, -2062, and -2068 could be associated with the antixenosis mechanism. Antixenosis is a resistance mechanism where insects exhibit a lower preference for oviposition, feeding, or shelter due to chemical stimulus or morphological or physical barriers (Panda and Khush, 1995). Antixenosis studies in arthropods have been conducted in tomato (S. lycopersicum) (Kennedy, 2003; Resende et al., 2006). Channarayappa et al. (1992) observed that the subsample LA 1777 of L. hirsutum f. typicum Humb. & Bonpl. expressed antixenosis resistance to the whitefly B. tabaci.

Another associated resistance mechanism is antibiosis, characterized by a negative effect on insect biology (Jindal et al., 2008). Morillo and Marcano (1997) and Pai and Shih (2003) reported that oviposition duration, nymph, and life cycle of the whitefly differed significantly in tomato subsamples. This mechanism has also been reported in cotton (Gossypium hirsutum L.), bean (Phaseolus vulgaris L.), and cucurbits (Soria et al., 1999; Jindal et al., 2008).

The antibiosis mechanism in our subsamples was apparently associated with a lower nymph/egg ratio in 73 out of the 103 subsamples studied. This low ratio demonstrated that these subsamples interfered with eclosion or caused nymph mortality (Panda and Khush, 1995). Antibiosis can also be related to adult mortality and insect life cycle duration (Panda and Khush, 1995). Tsai and Wang (1996) showed that host plants have a significant effect on the longevity and female oviposition of B. tabaci B biotype. Life cycles longer than 25 d were reported by Villas Bôas et al. (2002), in agreement with the results found in some subsamples.

Higher trichome density in the subsamples HGB-1490, -2004, -2011, -2017, -2020, -2098, -2100, -2121, -2122, and -2130, associated with a higher number of whitefly eggs, apparently furnished a favorable microclimate for eggs (Butter and Vir, 1989). The female whitefly deposits eggs more frequently at the base of leaf trichomes (Vendramim et al., 2009). Such conditions provide enough relative humidity for the physiological processes to occur during the embryonic phase as well as protection against predators (Bernays and Graham, 1988). Trichomes also allow better nymph protection (Butter and Vir, 1989). Several studies have reported that high trichome density was positively correlated to B. tabaci oviposition in tomato, cotton, and soybean [Glycine max (L.) Merr.] (McAuslane, 1996; Chu et al., 2001; Toscano et al., 2002). Because offspring performance is determined by the choice of the adult insect for oviposition, a low trichome density in tomato leaves can be extremely important for the subsamples to be less visited by B. tabaci adults. This fact can be considered in breeding programs to select genes that express fewer numbers of trichomes. Some subsamples presented an unexpected response for the trichome × egg interaction. The subsamples HGB-630, -2009, and -2013 presented low egg densities of B. tabaci and high numbers of trichomes. On the other hand, the subsample HGB-981 presented a higher number of eggs and a low density of leaf trichomes.

Besides morphological factors, the presence of certain organic compounds, such as terpenes, phenols, and methyl ketones, among others (Suinaga et al., 1999; Kennedy, 2003; van Tol et al., 2007; Thompson, 1988; Resende et al., 2008) can affect insect behavior. These compounds can influence changes in feeding habits, oviposition, body weight, life cycle, and mortality through different mechanisms (Panda and Krush, 1995; Resende et al., 2008). No studies have associated these compounds with whitefly nymphs. The role of hydrocarbons in whitefly behavior has been little investigated (Hull-Sanders et al., 2007; Oliveira et al., 2009; Nerio et al., 2010; Nawrot et al., 2010).

Among the 15 hydrocarbons identified in this study, only undecane and tridecane concentrations resulted in positive correlations with nymphs per plant. Thus, compounds identified in the HGB subsamples could be associated with higher susceptibility to B. tabaci nymphs. The subsample HGB-2029 stood out because it caused high whitefly mortality; however, undecane and tridecane were not detected. The cultivar Santa Clara was the extreme opposite, being very susceptible to whitefly with high undecane and tridecane concentrations. Higher undecane and tridecane concentrations in Santa Clara, as opposed to their absence in subsample HGB-2029, could have attracted whitefly adults, encouraging higher oviposition and thus a higher number of nymphs. This is in agreement with Walling (2000) and Martinez de Ilarduya et al. (2003), who reported that tomato releases volatile compounds that attract Macrosiphum euforbiae (Hemiptera: Aphididae). Oliveira et al. (2009), investigating HGB subsamples, reported susceptibility to Tuta absoluta (Lepidoptera: Gelechiidae) in some tomato subsamples with these hydrocarbons. In addition to S. lycopersicum, other studies have reported hydrocarbon changes in insect feeding, oviposition, survival, and other traits (Hull-Sanders et al., 2007; Nerio et al., 2010; Nawrot et al., 2010). Thus, breeding programs should consider developing cultivars with low concentrations of volatile compounds and emphasize other compounds used against whiteflies.

The subsamples HGB-225, -327, -813, -985, -2029, -2030, -2055, -2057, -2060, -2062, and -2068 were resistant to B. tabaci biotype B through the antixenosis and antibiosis resistance mechanisms. Trichome density and some hydrocarbons explain the resistance of some subsamples. The subsample HGB-2029 appears to be the most promising because it influenced most significantly the biology of B. tabaci and should be further studied in breeding programs.

Acknowledgments

We thank CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) and CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) for the scholarships and Mark Berhow of the USDA, Peoria, IL, for revising the manuscript.

 

References

Footnotes


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