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Induced systemic resistance to anthracnose in cucumber as influenced by the location of the inducer inoculation with Colletotrichum lagenarium and the onset of flowering and fruiting
Physio&icai
Plant Patkolugy
(1980)
17,229-233
SHORT COMMUNICATION Induced systemic resistance to anthracnose in cucumber as influenced by the location of the inducer inoculation with Colletotrichum lagenarium and the onset of flowering and fruiting M. E. M. Dejartment
GUEDES~,
S. RICHMOND:
of Plant Pathology,
(Accepedforpublication
Uaiucrsity
AND of Kentucky,
J. Ku6 Lexington,
Kentucky,
40546,
U.S.A.
Ati.11980)
Infection of the second true leaf (leaf 2) of cucumber with Colletotricha lagemhm systemically protected the tlrst true leaf (leaf 1) and leaf 3 from subsequent disease caused by the fungus. Protection of leaf 3 was consistently better than leaf 1. Excising the stem below the petiole of leaf 3 at the time leaf 2 was inoculated did not affect protection of leaf 1. When the petiole of inducer leaf 2 was girdled with cotton and hot water prior to inoculation with C. &sgenurianr, resistance was not induced in leaves 1 or 3. Similarly, when the petiole of inducer leaf 1 was girdled prior to inoculation with C. hsgerzarium, resistance was not induced in leaf2. Resistance was not induced in leaf 2 if its petiole was girdled prior to the inoculation of inducer leaf 1. Inoculating leaf 5 with the fungus induced resistance in leaves 1 to 4 and 6 to 10, but protection was greater in leaves 9 and 10. Resistance was not induced in cucumber plants once they set fruit, and was markedly reduced when induced at the time of flowering.
INTRODUCTION
Systemic resistance against disease caused by C. lagenarium, CLados~oriumcucumerinum Pseudomonaslachrymans and tobacco necrosis virus was induced by inoculation with any one of the pathogens [1-Q. In all of the reports, the cotyledons or first true leaves were inoculated with the pathogen and the tissue above was systemically protected against disease. It was not evident whether protection could be elicited below the leaf receiving the inducing inoculation. Though resistance induced in the seedling stage persisted through the period of fruiting [7] it was not evident that it could be induced in flowering and fkuiting plants. The purpose of this research was to determine whether resistance to anthracnose is systemically induced above and below the site of the inducing inoculation with the fungus and whether it can be induced in flowering and fruiting plants. MATERIALS
AND
METHODS
Colk!otrichum lagenarium (Pass.) Ell. & Halst race 1 and cucumber cultivar SMR-58, which is susceptible to anthracnose, were used in all studies. The growth and t On leave from the Coffee Rust Research 1 Present address: P. 0. Box 159, Cadwell, 0048-4059/80/050229+05
802.00/O
Centre, Oeiras, Georgia 31699
Portugal
@ 1980 Academic
Press Inc.
(London)
Limited
230
M. E. M. Guedes
et al.
inoculation of plants and culture of fimgus were described earlier [7J. The inducing and challenge inoculations were with spore suspensions containing 5 x lo6 and lo5 spores ml-l, respectively. The method described by Solel, Schooley and Edgington [IO] was used to girdle petioles. Girdled plants and their appropriate controls were partially shaded in the greenhouse after removal from moist chambers. Lesions were counted 6 to 7 days after the challenge inoculations. RESULTS
Systemic resistance to anthracnose was induced above and below the site of the inducing infection; however, protection was consistently better above the site (Tables 1 to 3). This difference was most evident on plants with 3 to 4 expanded leaves. TABLE
1
The effect of infecting leaf 2 of caxarnber SMR-58 with Colletotrichum lagenarium on the number of lesions resultingfrom a subsequent challenge with the fw on leaf I and 3 (fist 1) or challenge of leaf I when the stem was excised below the petiole of leaf 3 (Test 2)
Test
Number of lesions per challenged leafp Infected leaf 2 Water on leaf 2 Leaf 1 Leaf 3 Leaf 1 Leaf 3 24Ab 22A
:
8B -
36c 35c
35c -
a Forty 5 l.tl drops of a spore suspension of C. kagenurium (5 x 10s ml-l) or water were applied to the second true leaf (leaf2). 6 to 7 days later the first true leaf (leaf 1) and the third true leaf (leaf 3) (Test 1) or leaf 1 (Test 2) were challenged with 40 5 ul drops of a spore suspension of the fungus (1 x 10s ml-l). In Test 2, the stem was excised below the petiole of leaf 3 at the time of inoculating leaf 2. Symptoms were recorded 6 to 7 days after challenge and represent the means of a total of 35 plants per treatment in test 1 and 48 plants in Test 2 in 6 and 8 experiments, respectively. b Within and between tests the same letters following the number of lesions indicate no significant differences between treatments at the 0.05 level ofprobability. TABLE
2
The effect of kocukating the fifth true leaf of cucumber SMR-58 with Colletotrichum on the number of lesions resultingfrom a subsequent challenge of leaves below andabove
Treatment
ofleaf
5
1
Lower 2
Number
of lesions
after
3
4
6
leaves
lagenarium with the+
challenge of le& Upper leaves 7 8
9
a Forty 5 ul drops of a spore suspension ofC. kzgenarium (5 x 10s ml-i) or water were applied to the fifth true leaf (leaf5). 7 days later, leaves below (1 to 4) and above (6 to 10) were challenged with the fungus (106 spores ml-r). Lesions were counted 7 days after the second inoculation, and results are the means of 7 plants per treatment in one experiment. The differences between corresponding leaves of plants inoculated on leaf 5 and the water controls are significant at the O-05 level of probability. Figures in parentheses are the y. protection based on the number of lesions on corresponding control leaves.
10
Resistance to anthracnose in cucumber
231 TABLE
3
2% effict of girdling thepstioles of cwmnber SMR-58 kaoesprior to infection with Colletotrichum lager&urn MI sys&mic induced resistanceto diseasecaused69 subsequent&Uenge with thefwrgus
Induced 1
Treatments Petiole Petiole Petiole Petiole Petiole Petiole
girdled b on inducer leaf 2 intact girdle& on inducer leaf 1 intact girdled on challenge leaf 2 d intact on leaves 2, 3
Number of lesions resistance 2 3
30Ae 21B
per challenged 1
33A 8C 33A 13D 35A 1OC
le# Control 2
31A 35A
32A 35A 34A 33A 34A 32A
6C 8C
’ Forty 5 p1 drops of a spore suspension ofC. lugenurium (5 x lo6 ml-r) (Induced resistance) or water (Control) were applied to leaf2 or leaf 1. 6 to 7 days later leaves 1 and 3, leaf 2, or leaves 2 and 3, were challenged with 40 5 pl drops of spore suspension of the fungus ( IO5 spores ml-r). Symptoms were recorded 6 to 7 days after challenge and data represent a total of 23 plants per treatment in four experiments. b Petioles of inducer leaf2 girdled with cotton and hot water prior to inoculation. c Petioles of inducer leaf 1 girdled with cotton and hot water prior to inoculation. d Petioles of leaf2 girdled with cotton and hot water prior to inoculation of inducer leaf 1. e The same letters following the number of lesions indicate nosignificant differences between treatments at the 0.05 level of probability.
TABLE
4
Theeffectof inoculating thefourth leaf of a?melo+icucumberoineswith Colletotrichumlagenarium on systemicprotection elicited by thefungus Average number per leafper Maturity of plant
Experiment number
One wee-k before
flowering
Flowering but not pollinated Pollinated flowers with developing fruit
Control
b
of lesions plants Protected
17 27 34 21 36 34 16 17 ;;
(9-22)” (6-w (32-48) (8-29) (25-40) (12-q (3-30) (9-28) y{
3 8 8 12 29 25 11 15 17
22
F-3
232
3
b
a An average of 6 plants were used per experiment. All leaves above the leaf receiving the inducing inoculation were challenged with 40 drops of inoculum per leaf on plants teated one week before flowering. Every other leaf above the leafreceiving the inducing inoculation was challenged on plants tested after flowering. b Protected: leaf four inoculated with 5 x IO6 spores ml-’ 1 week prior to challenge of upper leaves with c. &rgeaufiWn. Control: water was applied to leaf four. 5 Figures in parentheses are the range in the number oflesions.
38A 36A
232
M. E. M. Guedes et al.
Excising the stem below the petiole of leaf 3 at the time leaf 2 was inoculated did not enhance protection of leaf 1 (Table 1). Induced systemic resistance was not observed above or below the inducer leaf when the petiole of the inducer leaf was girdled with cotton and hot water before the leaf was inoculated (Table 3). The girdled leaf remained turgid and green throughout the experiment if supported on a plastic-coated wire support. Similarly, resistance was not induced in leaf 2 if its petiole was girdled prior to inoculation of inducer leaf 1. Resistance was not induced in plants which had set fruit and was markedly reduced when induced at the time of flowering [Table 4). DISCUSSION Systemic induced resistance is not limited to tissue above the site of induction. This observation may have practial significance in studies where the inducing inoculation or substance with inducer activity is applied to plants growing in the field. The difference in the magnitude of protection above and below the site of induction may be due to the generally increased susceptibility of fully expanded as opposed to expanding leaves and/or to a “sink” effect at the growing point. The design of experiments in the past, in which cotyledons or leaf 1 served as the site of induction, suggested the possibility that induction occurred only with leaves at the growing point. Data in this paper do not support this suggestion. The “postulated resistanceinducing substance” was reported by Ross to move equally well up or down in large tobacco plants infected with TMV [9]. Data from experiments with petiole girdling support the possibility that a signal for resistance is transported from the inducer leaf to leaves above and below. The inability of petiole girdling itself to induce resistance is further evidence that the induction is not caused by a response to instantaneous injury. Plants inoculated at the two leaf stage, and given a booster inoculation 3 to 4 weeks after the inducer inoculations, were protected through the period of fruiting [7]. The inability to elicit resistance in cucumber once the plants had set fruit, suggests that either the chemical signal for resistance is not produced by the plants or cells are not in an appropriate physiological state to respond to the signal. A change in hormonal balance at the time of flowering and fruiting might be implicated in the phenomenon. It is unlikely that the inability to induce resistance is due to a dilution of signal since plants induced in the seedling stage remained resistant through the fruiting period, and resistance was readily induced 1 week before flowering. Journal paper number 80-l l-18 of the Kentucky Agricultural Experiment Station, Lexington, Kentucky 40546. This research was supported in part by a grant from the Ciba-Ceigy Corporation. REFERENCES 1. CARUSO,F. L. & Ku& J. (1977). Protection of watermelon and muskmelon against Collctotih~m ZagenariumbyCoU&ot&hwn kapankm. Phe0 67,128~1289. 2. t&wso, F. L. & Ku6, J. (1979). Induced rqktancc of cucumber to anthracnose and angular leaf spot by Pmdmwnas kdwymam and cOl&totricAum lagewium. Physiological Plot Pathokgy 14, 191-201. 3. HAMMERSCHMIDT,R., ACIW, S. & Ku& J. (1976). Protection of cucumber against ColIetot&hum Lzgenarkm and Cl~sspmium ixcwthw. Phytopathology66,790-793.
Resistance to anthracnose in cucumber
233
4. JENNS, A. E. & Ku&J. (1977). Localized infection with tobacco necrosis virus protects cucumber against Colletotriehum lagenarium. Physiological Plant Pathology 11,207-2 12. 5. JENM), A., CARUSO, F. L. & Kud, J. (1980). Non-specific resistance to pathogens induced systemically by local infection of cucumber with tobacco necrosis virus, Colletottichum lagenarium or Psednnonas la&mans. Phytopathologia Mediterranea. (In Press). 6. Kud, J., SHOCKLEY, G. & KEARNEY, K. (1975). Protection of cucumber against Colletotrichum lagemarium by Colletotrizhum lagenarium. Physiological Plant Pathology 7, 195-l 99. 7. KuC, J. & RICHMOND, S. (1977). Aspects of the protection of cucumber against Colletotrichum lagenarium by Collctotrichum lagenarium. Phyt@athologp 67,533-536. 8. RICHMOND, S., Ku6, J. & ELLISTON, J. E. (1979). Penetration of cucumber leaves by Colletotrichum lagenarium is reduced in plants systemically protected by previous infection with the pathogen. Physiological Plant Pathology 14,329-338. 9. Ross, A. F. (1966). Systemic effects of local lesion formation. In Viruses of Plants, Ed. by A. B. R. Beemster and J. Dijkstra, pp. 127-150. North Holland, Amsterdam. 10. SOLEL, L., SCHOOLEY, J. M. & EDGINGTON, L. V. (1973). Uptake and translocation of benomyl and carbendazim (Methyl benzimidozol-2-yl carbamate) in the symplast. PestkideScience4,713-718.
Plant Patkolugy
(1980)
17,229-233
SHORT COMMUNICATION Induced systemic resistance to anthracnose in cucumber as influenced by the location of the inducer inoculation with Colletotrichum lagenarium and the onset of flowering and fruiting M. E. M. Dejartment
GUEDES~,
S. RICHMOND:
of Plant Pathology,
(Accepedforpublication
Uaiucrsity
AND of Kentucky,
J. Ku6 Lexington,
Kentucky,
40546,
U.S.A.
Ati.11980)
Infection of the second true leaf (leaf 2) of cucumber with Colletotricha lagemhm systemically protected the tlrst true leaf (leaf 1) and leaf 3 from subsequent disease caused by the fungus. Protection of leaf 3 was consistently better than leaf 1. Excising the stem below the petiole of leaf 3 at the time leaf 2 was inoculated did not affect protection of leaf 1. When the petiole of inducer leaf 2 was girdled with cotton and hot water prior to inoculation with C. &sgenurianr, resistance was not induced in leaves 1 or 3. Similarly, when the petiole of inducer leaf 1 was girdled prior to inoculation with C. hsgerzarium, resistance was not induced in leaf2. Resistance was not induced in leaf 2 if its petiole was girdled prior to the inoculation of inducer leaf 1. Inoculating leaf 5 with the fungus induced resistance in leaves 1 to 4 and 6 to 10, but protection was greater in leaves 9 and 10. Resistance was not induced in cucumber plants once they set fruit, and was markedly reduced when induced at the time of flowering.
INTRODUCTION
Systemic resistance against disease caused by C. lagenarium, CLados~oriumcucumerinum Pseudomonaslachrymans and tobacco necrosis virus was induced by inoculation with any one of the pathogens [1-Q. In all of the reports, the cotyledons or first true leaves were inoculated with the pathogen and the tissue above was systemically protected against disease. It was not evident whether protection could be elicited below the leaf receiving the inducing inoculation. Though resistance induced in the seedling stage persisted through the period of fruiting [7] it was not evident that it could be induced in flowering and fkuiting plants. The purpose of this research was to determine whether resistance to anthracnose is systemically induced above and below the site of the inducing inoculation with the fungus and whether it can be induced in flowering and fruiting plants. MATERIALS
AND
METHODS
Colk!otrichum lagenarium (Pass.) Ell. & Halst race 1 and cucumber cultivar SMR-58, which is susceptible to anthracnose, were used in all studies. The growth and t On leave from the Coffee Rust Research 1 Present address: P. 0. Box 159, Cadwell, 0048-4059/80/050229+05
802.00/O
Centre, Oeiras, Georgia 31699
Portugal
@ 1980 Academic
Press Inc.
(London)
Limited
230
M. E. M. Guedes
et al.
inoculation of plants and culture of fimgus were described earlier [7J. The inducing and challenge inoculations were with spore suspensions containing 5 x lo6 and lo5 spores ml-l, respectively. The method described by Solel, Schooley and Edgington [IO] was used to girdle petioles. Girdled plants and their appropriate controls were partially shaded in the greenhouse after removal from moist chambers. Lesions were counted 6 to 7 days after the challenge inoculations. RESULTS
Systemic resistance to anthracnose was induced above and below the site of the inducing infection; however, protection was consistently better above the site (Tables 1 to 3). This difference was most evident on plants with 3 to 4 expanded leaves. TABLE
1
The effect of infecting leaf 2 of caxarnber SMR-58 with Colletotrichum lagenarium on the number of lesions resultingfrom a subsequent challenge with the fw on leaf I and 3 (fist 1) or challenge of leaf I when the stem was excised below the petiole of leaf 3 (Test 2)
Test
Number of lesions per challenged leafp Infected leaf 2 Water on leaf 2 Leaf 1 Leaf 3 Leaf 1 Leaf 3 24Ab 22A
:
8B -
36c 35c
35c -
a Forty 5 l.tl drops of a spore suspension of C. kagenurium (5 x 10s ml-l) or water were applied to the second true leaf (leaf2). 6 to 7 days later the first true leaf (leaf 1) and the third true leaf (leaf 3) (Test 1) or leaf 1 (Test 2) were challenged with 40 5 ul drops of a spore suspension of the fungus (1 x 10s ml-l). In Test 2, the stem was excised below the petiole of leaf 3 at the time of inoculating leaf 2. Symptoms were recorded 6 to 7 days after challenge and represent the means of a total of 35 plants per treatment in test 1 and 48 plants in Test 2 in 6 and 8 experiments, respectively. b Within and between tests the same letters following the number of lesions indicate no significant differences between treatments at the 0.05 level ofprobability. TABLE
2
The effect of kocukating the fifth true leaf of cucumber SMR-58 with Colletotrichum on the number of lesions resultingfrom a subsequent challenge of leaves below andabove
Treatment
ofleaf
5
1
Lower 2
Number
of lesions
after
3
4
6
leaves
lagenarium with the+
challenge of le& Upper leaves 7 8
9
a Forty 5 ul drops of a spore suspension ofC. kzgenarium (5 x 10s ml-i) or water were applied to the fifth true leaf (leaf5). 7 days later, leaves below (1 to 4) and above (6 to 10) were challenged with the fungus (106 spores ml-r). Lesions were counted 7 days after the second inoculation, and results are the means of 7 plants per treatment in one experiment. The differences between corresponding leaves of plants inoculated on leaf 5 and the water controls are significant at the O-05 level of probability. Figures in parentheses are the y. protection based on the number of lesions on corresponding control leaves.
10
Resistance to anthracnose in cucumber
231 TABLE
3
2% effict of girdling thepstioles of cwmnber SMR-58 kaoesprior to infection with Colletotrichum lager&urn MI sys&mic induced resistanceto diseasecaused69 subsequent&Uenge with thefwrgus
Induced 1
Treatments Petiole Petiole Petiole Petiole Petiole Petiole
girdled b on inducer leaf 2 intact girdle& on inducer leaf 1 intact girdled on challenge leaf 2 d intact on leaves 2, 3
Number of lesions resistance 2 3
30Ae 21B
per challenged 1
33A 8C 33A 13D 35A 1OC
le# Control 2
31A 35A
32A 35A 34A 33A 34A 32A
6C 8C
’ Forty 5 p1 drops of a spore suspension ofC. lugenurium (5 x lo6 ml-r) (Induced resistance) or water (Control) were applied to leaf2 or leaf 1. 6 to 7 days later leaves 1 and 3, leaf 2, or leaves 2 and 3, were challenged with 40 5 pl drops of spore suspension of the fungus ( IO5 spores ml-r). Symptoms were recorded 6 to 7 days after challenge and data represent a total of 23 plants per treatment in four experiments. b Petioles of inducer leaf2 girdled with cotton and hot water prior to inoculation. c Petioles of inducer leaf 1 girdled with cotton and hot water prior to inoculation. d Petioles of leaf2 girdled with cotton and hot water prior to inoculation of inducer leaf 1. e The same letters following the number of lesions indicate nosignificant differences between treatments at the 0.05 level of probability.
TABLE
4
Theeffectof inoculating thefourth leaf of a?melo+icucumberoineswith Colletotrichumlagenarium on systemicprotection elicited by thefungus Average number per leafper Maturity of plant
Experiment number
One wee-k before
flowering
Flowering but not pollinated Pollinated flowers with developing fruit
Control
b
of lesions plants Protected
17 27 34 21 36 34 16 17 ;;
(9-22)” (6-w (32-48) (8-29) (25-40) (12-q (3-30) (9-28) y{
3 8 8 12 29 25 11 15 17
22
F-3
232
3
b
a An average of 6 plants were used per experiment. All leaves above the leaf receiving the inducing inoculation were challenged with 40 drops of inoculum per leaf on plants teated one week before flowering. Every other leaf above the leafreceiving the inducing inoculation was challenged on plants tested after flowering. b Protected: leaf four inoculated with 5 x IO6 spores ml-’ 1 week prior to challenge of upper leaves with c. &rgeaufiWn. Control: water was applied to leaf four. 5 Figures in parentheses are the range in the number oflesions.
38A 36A
232
M. E. M. Guedes et al.
Excising the stem below the petiole of leaf 3 at the time leaf 2 was inoculated did not enhance protection of leaf 1 (Table 1). Induced systemic resistance was not observed above or below the inducer leaf when the petiole of the inducer leaf was girdled with cotton and hot water before the leaf was inoculated (Table 3). The girdled leaf remained turgid and green throughout the experiment if supported on a plastic-coated wire support. Similarly, resistance was not induced in leaf 2 if its petiole was girdled prior to inoculation of inducer leaf 1. Resistance was not induced in plants which had set fruit and was markedly reduced when induced at the time of flowering [Table 4). DISCUSSION Systemic induced resistance is not limited to tissue above the site of induction. This observation may have practial significance in studies where the inducing inoculation or substance with inducer activity is applied to plants growing in the field. The difference in the magnitude of protection above and below the site of induction may be due to the generally increased susceptibility of fully expanded as opposed to expanding leaves and/or to a “sink” effect at the growing point. The design of experiments in the past, in which cotyledons or leaf 1 served as the site of induction, suggested the possibility that induction occurred only with leaves at the growing point. Data in this paper do not support this suggestion. The “postulated resistanceinducing substance” was reported by Ross to move equally well up or down in large tobacco plants infected with TMV [9]. Data from experiments with petiole girdling support the possibility that a signal for resistance is transported from the inducer leaf to leaves above and below. The inability of petiole girdling itself to induce resistance is further evidence that the induction is not caused by a response to instantaneous injury. Plants inoculated at the two leaf stage, and given a booster inoculation 3 to 4 weeks after the inducer inoculations, were protected through the period of fruiting [7]. The inability to elicit resistance in cucumber once the plants had set fruit, suggests that either the chemical signal for resistance is not produced by the plants or cells are not in an appropriate physiological state to respond to the signal. A change in hormonal balance at the time of flowering and fruiting might be implicated in the phenomenon. It is unlikely that the inability to induce resistance is due to a dilution of signal since plants induced in the seedling stage remained resistant through the fruiting period, and resistance was readily induced 1 week before flowering. Journal paper number 80-l l-18 of the Kentucky Agricultural Experiment Station, Lexington, Kentucky 40546. This research was supported in part by a grant from the Ciba-Ceigy Corporation. REFERENCES 1. CARUSO,F. L. & Ku& J. (1977). Protection of watermelon and muskmelon against Collctotih~m ZagenariumbyCoU&ot&hwn kapankm. Phe0 67,128~1289. 2. t&wso, F. L. & Ku6, J. (1979). Induced rqktancc of cucumber to anthracnose and angular leaf spot by Pmdmwnas kdwymam and cOl&totricAum lagewium. Physiological Plot Pathokgy 14, 191-201. 3. HAMMERSCHMIDT,R., ACIW, S. & Ku& J. (1976). Protection of cucumber against ColIetot&hum Lzgenarkm and Cl~sspmium ixcwthw. Phytopathology66,790-793.
Resistance to anthracnose in cucumber
233
4. JENNS, A. E. & Ku&J. (1977). Localized infection with tobacco necrosis virus protects cucumber against Colletotriehum lagenarium. Physiological Plant Pathology 11,207-2 12. 5. JENM), A., CARUSO, F. L. & Kud, J. (1980). Non-specific resistance to pathogens induced systemically by local infection of cucumber with tobacco necrosis virus, Colletottichum lagenarium or Psednnonas la&mans. Phytopathologia Mediterranea. (In Press). 6. Kud, J., SHOCKLEY, G. & KEARNEY, K. (1975). Protection of cucumber against Colletotrichum lagemarium by Colletotrizhum lagenarium. Physiological Plant Pathology 7, 195-l 99. 7. KuC, J. & RICHMOND, S. (1977). Aspects of the protection of cucumber against Colletotrichum lagenarium by Collctotrichum lagenarium. Phyt@athologp 67,533-536. 8. RICHMOND, S., Ku6, J. & ELLISTON, J. E. (1979). Penetration of cucumber leaves by Colletotrichum lagenarium is reduced in plants systemically protected by previous infection with the pathogen. Physiological Plant Pathology 14,329-338. 9. Ross, A. F. (1966). Systemic effects of local lesion formation. In Viruses of Plants, Ed. by A. B. R. Beemster and J. Dijkstra, pp. 127-150. North Holland, Amsterdam. 10. SOLEL, L., SCHOOLEY, J. M. & EDGINGTON, L. V. (1973). Uptake and translocation of benomyl and carbendazim (Methyl benzimidozol-2-yl carbamate) in the symplast. PestkideScience4,713-718.