Field study of the interaction between Orobanche crenata Forsk. and some new lines of Vicia faba L. in Egypt

FiLeld study of the interaction between Orobanche crenata Forsk. and some new lines of Vicia faba L. in Egypt S.J. ter Borg *t, A. Willemsen t, S.A. Khalil*, H.A. Saber ~, J. A. C. Verkleij ~ and A . H . Piel:erse" tDepartment of Terrestrial Ecology and Nature Conservation, Agricultural University, Bornsesteeg 69, 6708 PD Wageningen, The Netherlands; ~Field Crops Research Institute, Agricultural Research Centre, Giza, Egypt; aDepartment of Ecology and Ecotoxicology, Free University, de Boelelaan 1087, 1081 HV Amsterdam, The Netherlands; and "Royal Tropical Institute, Department of Agriculture and Enterprise Development, Mauritskade 63, 1092 AD Amsterdam, The Net~erlands

In Egypt, some newly derived lines of faba bean (Vicia faba L.) as well as Giza 402, all of which had shown a certain resistance against the parasitic weed Orobanche crenata Forsk., were tested in the field. For reasons of comparison, the susceptible cultivars Giza 3 and Reina Blanca were included in this test. Faba bean plants and Orobanche attachments were regularly harvested and examined. The susceptible cultwars completely collapsed before the end of the growing season, whereas others, particularly line 402/294, remained alive until pod formation was completed. It appeared that fewer Orobanche spikes emerged on the new lines and Giza 402. Evidence is given that this was not due to avoidance mechanisms, such as smaller root mass, a deeper root system or lack of germination stimulants. Numbers of Orobanche attachments per unit of lateral root length were found to be low. Hence, it could be concluded that these lines are partially resistant; this resistance must be due to some defence mechanism in their roots. The few Orobanche plants attached grew very fast so that final Orobanche dry weight was similar in resistant and susceptible host plants. Further experiments, including broomrape-free controls, are required to study whether some tolerance mechanism might be involved.

Keywords: host root system; Orobanche crenata; Vicia faba A major strategy for tackling the Orobanche problem in cool-season food legumes is breeding for resistance. More than 30 years ago, breeding programmes for faba bean (Viciafaba L.) were started, followed by those for lentil (Lens culinaris Medik.), chickpea ( Cicer arietinum L.), common vetch (Vicia sativa L.) and field pea (Pisum sativum L.) (Cubero et al., 1988, 1993; Cubero, 1991; Linke, 19cP2; Sauerborn, 1992). In the 1970s a faba bean cultivar, Giza 402, with low numbers of Orobanche spikes, had already been selected in Egypt; it produced a relatively high yield in spite of a certain degree of broomrape infestation (Nassib, Ibrahim and Saber, 1978; Nassib, Ibrahim and Khalil, 1982). However, the resistance was not always apparent and it seemed that eventually it had disappeared from material[ released to the farmers, probably owing to crossing with susceptible plants. Subsequently, new breeding programmes were started in Egypt, Morocco and Spain ( I C A R D A , 1990; Khalil et al., 1990). In Egypt this resulted in new productive lines, derived from Giza 402 (Khalil et al., 1990). There was a striking difference between these new lines and susceptible cultivars: in heavily infested fields, susceptible plants collapsed owing to severe Orobanche attack, whereas plants of newly derived lines, although *To whom correspondence should be addressed

also parasitized, remained green and healthy for a relatively long period, and produced seeds (H. A. Saber and A. H. Pieterse, unpublished observations, 1991). On the basis of unpublished observations in field and pot experiments Nassib et al. (1978, 1982) concluded that the effects in Giza 402 were due to avoidance and a certain degree of resistance. With respect to avoidance they mentioned the formation of fewer lateral roots, a more compact root mass and reduced production of germination stimulants. In a greenhouse experiment, A. H. Pieterse (unpublished data, 1982) observed that roots of Giza 402 grew deeper than those of the susceptible cultivars ILB and CRS, and that formation of lateral roots mainly occurred in deeper soil layers. More recently, ter Borg and van Ast (1991a) also reported a relatively deep growth of Giza 402 roots compared with Giza 2. Khalaf and El-Bastawesy (1989) suggested that a smaller root mass was a key factor, since the susceptible faba bean variety 'Aquadulce' produced more roots than Giza 402. On the other hand, ter Borg and van Ast (1991a) found root masses of Giza 402 and the susceptible cultivar Giza 2 to be similar. Khalaf and E1-Bastawesy (1989) found no major differences between the activity of germination stimulants in partly purified root extracts of Giza 402 and Aquadulce. Moreover, S. J. ter Borg and A. van

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Interaction between Orobanche and Vicia faba: S.J. ter Borg et al.

Ast (unpublished data) observed no relevant differences when the activities of root exudates of a wide range of faba bean accessions were compared; the activity of Giza 402 root exudates appeared to be relatively strong. Hence, it seems unlikely that an avoidance mechanism, either root mass, architecture of the root system or low production of germination stimulant(s), is a major defence mechanism in this cultivar. Nassib et al. (1978, 1982) hypothesized that mechanical and physiological barriers in the roots cause a certain form of resistance in Giza 402. This was supported when ter Borg and van Ast (1991a and unpublished data) found that fewer Orobanche attachments developed per unit of lateral root length on Giza 402 than on the susceptible cultivar Giza 2. Details of morphological and anatomical differences between resistant and susceptible culfivars were presented by Zaitoun, AI-Menoufi and Weber (!991), who observed defence reactions in the cortex of Giza 402, and by Attia (1991) who reported differences in rupturing of the endodermis. Attia (1991) compared some of the newly derived faba bean lines with Giza 402 and the susceptible Giza 2 in a pot experiment. She observed significantly fewer Orobanche spikes and lower total dry weights of Orobanche on line 674/155/85 and on Giza 402, than on Giza 2. This paper reports the results of a study of parasite development on a range of newly derived faba bean lines under field conditions. For reasons of comparison, Giza 402 as well as two susceptible cultivars were included. Special attention was given to the host root system and early attachments of Orobanche.

Materials and methods

sieve.

Subsequently,

the

developmental

stage

of

Orobanche attachments was recorded, using a 1-7 scale (1, small tubercle 1-3 mm; 2, crown roots start to develop; 3, bud ~<1 cm; 4, first development of spike below ground surface; 5, emergence of spike; 6, flowering; 7, setting of seeds). After removing the Orobanche attachments the lateral roots were cut off and the length of the tap root was measured. Total length of the lateral roots was then measured using a modified line intercept method (Tennant, 1975). The various samples were oven-dried and weighed. At the third harvest the root system of plants of each cultivar or line from two hills was dug up to examine the vertical distribution of both faba bean roots and Orobanche attachments. Two weeks after the fourth harvest (14 March), the general condition and pod formation of the faba bean lines and cultivars were estimated. Data were processed using the SPSS statistical programme (Norusis, 1986); differences were tested with the A N O V A and X2 test. The relative growth rate ( R G R ) was calculated according to Poorter and Lewis (1986).

Results

The winter of 1991/1992 was exceptionally cold in Egypt and also rather wet, resulting in a sub-optimal growth of faba bean. Moreover, the infestation level of Orobanche appeared to be very high in the experimental field. As a result, most plants of the susceptible cultivars Giza 3 and Reina Blanca had died by midMarch. However, in the newly derived tolerant lines, as well as in Giza 402, a relatively large number of plants were still green. Some pods were produced in 402/294, 674/155 (block 3 only) and in one plant of 674/154

(Table 1). Trials with the various faba bean cultivars were conducted in the experimental fields of the Agricultural Research Centre in Giza, Egypt, in the 1991/1992 growing season. Faba bean plants were sown in hills 5-10 cm high (distance between hills 5-25 cm) on ridges 10-15 cm high; these were 6 m long, and the distance between them was 65 cm. Three seeds were sown per hill. After germination the plots were thinned; only those hills with two plants were sampled. There were three blocks with 15 ridges each - seven ridges planted with one of the cultivars or lines to be tested, alternating with buffer ridges planted with the susceptible cultivar Giza 2. The ridges with test material were randomized within each block. Faba bean plants were sown on 3 and 4 November. The plots were regularly hand-weeded, and irrigated at 4-6-week intervals. The test concerned four new lines, all resulting from breeding programmes based on Giza 402: 402/294, 674/ 154(85), 561/2077, 674/155(85), as well as Giza 402 (breeder's material); the susceptible varieties Giza 3 and Reina Blanca were included for reasons of comparison. From mid-December to mid-March, faba bean plants as well as Orobanche attachments of each cultivar were harvested at monthly intervals from four to six hills, i.e. one or two per block. The above-ground parts of the faba bean plants were cut off and divided into leaves, stems, flowers and pods. After the roots had been dug up, they were cleaned with water over a

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The first Orobanche attachments were found around 15 December. The first spikes emerged around 15 February, except in Reina Blanca, where they emerged later. Numbers of Orobanche varied markedly between lines (Figure 1), with most attachments on the susceptible cultivars Giza 3 and Reina Blanca and lowest numbers on 402/294. The differences were highly significant (p <~ 0.001 for harvest 2 and p ~< 0.01 for harvests 3 and 4; one-way A N O V A ) . A similar pattern was found for numbers of Orobanche attachments per metre of host root (Figure2;p <<,0.05 for harvests 2 and 3, p ~< 0.001 in harvest 4, one-way A N O V A after logtransformation). At the first harvest the proportion of attachments in different stages did not differ between cultivars. However, at the second harvest 402/294 and Giza 402 had proportionally more attachments in stage 1, pointing to later development of Orobanche (Figure 3; X2: p ~< 0.01, if 402/294 and Giza 402 were taken together and tested against the five others). In spite of the differences in number of attachments, no relevant overall difference was found in the final Orobanche dry weights on the different cultivars and lines (Figure 4). When broomrapes developed later they appeared to be able to catch up with the others and became large, due to a high growth rate per plant

(Table 2). As there were few, if any pods at the time of the fourth harvest (mid-March), host production could

Interaction between Orobanche and Vicia faba: S.J. ter Borg et aL Table 1. Visual assessment of the condition of Vicia faba host plants in the presence of Orobanche crenata at the end of the observation period (14 March 11992)

Block Host plants

1

2

3

402/294 674/154 Giza 402

Pods Green, one with pods Green

Green, one with pods Green to dead Green, leaves dehiscing

Pods, some green Green Green to dead

561/2077 674/155

Dead Dead

Green Dead

Green to dead Green to pods

Giza 3 Reina Blanca

Dead Dead

Dead Dead

Green to dead Dead

10

160

140

120

100

80

60 40

20

402 /294

674 Giza /154 402

561 /2077

674 Giza 3 R.BI /155

402 /294

674 /154

Giza 402

561 /2077

674 Giza 3 R.BI /155

Figure 1. Numbers of O. cronata attachments on the various faba bean lines and varieties tested, per hill with two faba bean plants, at three consecutive harvests (e harvest 2, mid-January; • harvest 3, mid-February; I i harvest 4, early March). Different letters within a harvest indicate that values are significantly different at p < 0.05 (one-way ANOVA). Vertical axis, no. of Orobanche attachments per hill; R. BI, Reina Blanca

Figure 2. Numbers of Orobanche per metre of lateral host root at three consecutive harvests (~ harvest 2, mid-January; • harvest 3, mid-February; n harvest 4, early March). Different letters within a harvest indicate that values are significantly different at p < 0.05 (one-way ANOVA after log-transformation). Vertical axis, no. of Orobanche plants m-1 host root; R. BI, Reina Blanca

only be expressed as tot~tl dry weight (Figure 5). D r y weights differed at the first harvest, mainly due to the larger seed size in Reina Blanca. No relevant variation was observed at the second and the third harvests. Between harvests 3 and 4, host growth had continued in 402/294, 674/154, Giza 402 and 674/155, but it was impeded in 561/2077 as well as in the susceptible cultivars Reina Blanca and Giza 3 (Table 2). At harvest 4 dry weight of 402/294 was significantly higher than that of all others (p = 0.1)015). The proportion of Orobanche dry weight to total dry weight of host and parasite together gradually increased with time, latest in 402/294 and Giza 402 (Figure 6). A t the last harvest, in March, it was approximately 5 0 60%, except in 402/294 where it was only 25%. Figure 7 shows a positive correlation between Orobanche dry

weights and dry weights of individual host plants. The relation was significant (p ~< 0.001), if 402/294 was excluded. R o o t weights as well as root lengths a p p e a r e d to be similar in all cultivars and lines tested, except at the first and second harvests when roots were slightly longer in the susceptible cultivars Giza 3 and Reina Blanca. Almost all Orobanche attachments appeared to be situated in the u p p e r 20 cm of the soil. The few data on root distribution in the soil suggest that roots of 402/ 294,674/155 and Giza 402 were concentrated in the 1020 cm layer, whereas the roots of the other cultivars and lines were mainly situated in the u p p e r 10 cm. The numbers of Orobanche attachments per metre of root did not differ between layers. Comparison of the secondary haustoria, connecting

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Interaction between Orobanche and Vicia faba: S.J. ter Borg et al. Table 2. Dry weight production and allocation between the third and fourth harvest of faba bean plants in the presence of Orobanche crenata

100%

75%

Host plants 402/294 674/154 Giza 402 561/2077 674/155 Giza 3 Reina Blanca

50%

= ~,iIliili;lii/ii/ii~

6 7 4 Giza /154 4 0 2

561 /2077

6 7 4 Giza 3 /155

32 66 64 74

0.047 0.060 0.052 0.048 0.032 0.030 0.007

100

77 125

100

= | 402 /294

0.025 0.016 0.023 0.009 0.000 0.007 --0.003

RGRa broomrape

~RGR, relative growth rate (g g-i day t); bproportion of biomass produced that is attributable to O. c r e n a t a

25%

0%

Broomrape biomass (%)b

RGR" faba bean

R.BI

Figure 3. Proportion of various stages of development of O. crenata (in each column, from top to bottom: [] stage 1; ~;~;stage 2; lU stage 3; [] stage 4) on various faba bean lines and varieties, recorded at the second harvest. X2 test: p < 0.01 if (402/294 + Gisa 402) were tested against the other five taken together. Vertical axis: percentage of Orobanche attachments; R. BI, Reina Blanca 50

80

o

60

|

,0! I

Qbb

b

40

r ob

ab

b

b --

b

O

C

0

30

402 /294

674 /154

Giza 561 402 /2077

674 Giza 3 R.BI /155

Figure 5. Dry weights of faba bean plants infested with O. crenata; data are values per hill, i.e. per two faba bean plants: [] harvest 1; ~ harvest 2; • harvest 3; • harvest 4. Different letters within a harvest indicate that values are significantly different at p < 0.05 (one-way ANOVA). Vertical axis, host dry weight (g per hill); Ft. BI, Reina Blanca

20

10 Discussion

402 /294

674 /154

Giza 5 6 1 402 /2077

674 Giza 3 R.BI /155

Figure 4. O. crenata dry weights on the different faba bean lines and varieties tested at three consecutive harvests (~'! harvest 2, mid-January; • harvest 3, mid-February; • harvest 4, early March). The dry weights are averages per hill (i.e. per two faba bean plants). Different letters within a harvest indicate that values are significantly different at p < 0.05 (one-way ANOVA). Vertical axis, Orobanche dry weight (g per hill); R. BI, Reina Blanca

the thick broomrape crown roots to the host-plant roots, showed that roots of the susceptible Reina Blanca were less swollen at the point of attachment than those of the new line, 402/294. In the latter a wartlike structure was formed, and few secondary haustoria developed successfully.

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Results indicate that, unlike the susceptible cultivars Giza 3 and Reina Blanca, one or more defence mechanisms are operative in the new lines, line 402/294 in particular, as well as in Giza 402. Most obvious was the lower number of attachments per metre of lateral root. As far as Giza 402 is concerned, this is in accordance with the low numbers of attachments per metre of root reported by ter Borg and van Ast (1991a), or per unit root dry weight as follows from the data presented by Khalaf and Bastawesy (1989) and Zaitoun et al. (1991). Lack of root exudates does not seem to be the reason for this p h e n o m e n o n (Khalaf and EI-Bastawesy, 1989; S. J. ter Borg and A. van Ast, unpublished data). It may be assumed, therefore, in line with Nassib et al. (1978, 1982), that some defence mechanism in the roots of the new lines and Giza 402 hampers attachment. Attia (1991) reported an early rupture of the endodermis in susceptible material due

Interaction between Orobanche and Vicia faba: S.J. ter Borg et al.

a

b

402 /294

674 /154

G i ~ 2 561 674 Giza 3 R~I /2077 /154

402 /294

c

674 /154

Giza 561 674 Giza 3 RBI 402 /2077 /155

674 /154

G~za 561 674 Giza 3 RBI 402 /2077 /155

d

402 /294

674 /154

G~za 561 674 Giza 3 RI31 402 / 2 0 7 7 /155

402 /294

Figure 6. Distribution of dry weight over host (• Vicia faba) and parasite ( • Orobanche crenata) at four consecutive harvests (a, harvest 1, mid-December; b, harvest 2, mid-January; c, harvest 3, mid-February; d, harvest 4, early March). Vertical axes, percentage of total dry weight; R. BI, Reina Blanca 100

80

60

~-X []

40

60

×

Lx ×+~ 20 "D

0

o I

0

20

~ I

I

I

40 60 80 Host dry wt. (g / hill)

I

100

120

Figure 7. Relation between host plant (Vicia faba: *, 402/294; +, 674/154; x, Giza 402; E3, 561/2077; A, 674/155; ~ , Giza 3; • Reina Blanca) and O. crenat~ dry weights at the fourth harvest. Each point represents a :separate hill. The correlation is significant if 402/294 is excluded (p < 0.001). Vertical axis, Orobanche dry weight (g per HII)

to secondary growth of vascular tissue, irrespective of Orobanche attachment. According to Zaitoun et al. (1991), a corky tissue and cavities in the vascular cylinder develop in resistant material after Orobanche penetration. They found narrow, pin-shaped intrusive organs on Giza 402 redLucing parasite-host contact, when compared with the massive cylindrical intrusion

on the susceptible cultivar Reina Blanca. We observed that very few secondary haustoria developed between Orobanche crown roots and host roots of 402/294, and that the roots of 402/294 became more swollen at the point of attachment, compared with those of Reina Blanca. This suggests that formation of primary and secondary haustoria is hampered by similar mechanisms. As root masses and rooting depth of the new lines as well as Giza 402 were similar to those of the susceptible cultivars, this could not be the reason for the low numbers of Orobanche spikes in this experiment. However, a relatively solid soil layer at 20-30 cm depth may have hampered free development of the root system here. As previous data (A. H. Pieterse, unpublished; ter Borg and van Ast, 1991a) indicate that differences between lines might exist, a definite conclusion regarding this point with respect to the new lines cannot be drawn as yet. In spite of a lower number of attachments in the new lines, total dry weights of Orobanche on susceptible and resistant faba bean plants at the end of the growing season were similar. The late-developing Orobanche spikes on the resistant plants appeared to have a high growth rate and could reach similar or even larger sizes than those on the susceptible hosts. This high growth rate may have been brought about by the healthy condition of the host, as there appeared to be a positive relation between sizes of host and parasite. It should be noted that this positive relation between host and parasite concerned total dry weights, rather than final yields. The latter could not be established, as most host plants died at an earlier stage. However, comparison of the data in Figure 5 and Table 1 indicates that an overall negative relation was to be expected between Orobanche numbers and faba bean seed yield. In this experiment the effects of Orobanche on the host could not be studied in detail, owing to a lack of controls. Orobanche growth rate was remarkably high in 402/294 between the third and fourth harvest. This might result from the vigorous host, but it might also be attributable to some tolerance mechanism, or to both factors. True tolerance, i.e. unhampered growth of the host in spite of a significant number of Orobanche attachments, so far has not been reported for V. faba, although data on 'line 241' reported by Radwan et al. (1988) suggest that it might be present to some extent. The stimulating effect of the parasite on host dry weight production reported in Giza 402 by ter Borg and van Ast (1991b) could imply that some compensating mechanism exists, as it does in hosts of Striga hermonthica (Graves et al., 1990; Cechin and Press, 1993). Finally, it should be stated in this context that Harloff (1991) reported an inhibiting effect of Giza 402 on mannitol and proline synthesis in Orobanche, disrupting its osmoregulation mechanism. Clearly, a more extensive analysis is required to test and integrate these preliminary, and sometimes contradictory, observations on the physiological aspects of the hostparasite interaction. All new lines included in our study were in some way or other derived from Giza 402. Their performance differed to some extent from that in previous experiments (Attia, 1991; H. A. Saber, unpublished). This may be due to the genetic heterogeneity that one may

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Interaction between Orobanche and Vicia faba: S.J. ter Borg et al.

expect in new lines under development, but it may also point once again to the sensitivity of all mechanisms discussed to environmental conditions (ter Borg, 1986). However, it is evident that partial resistance is present in the original Giza 402 as well as in the new lines; anatomical and physiological details as well as their genetic basis need further study. Possible effects of avoidance by variation in root mass or rooting depth require further work under conditions of free development of the host root system. Conclusions with respect to tolerance require studies allowing a comparison of infested and uninfested material. However, it is evident that one or more defence mechanisms are present in faba bean germplasm. Additional breeding will be required to produce commercially useful cultivars, which may then be included in integrated control programmes (Pieterse et al., 1993).

ICARDA (1990) Annual Report 1990, International Center for Agricultural Research in Dry Areas, Aleppo, Syria, 133 pp Khalaf, K. and EI-Bastawesy, F. I. (1989) Some studies of the basis of resistance of Vicia faba cultivar 'Giza 402' to Orobanche crenata parasitism. FABIS Newslett. 25, 5-9 Khalil, S. A., Saber, H. A., Amer, M. I., Dossoki, R. F., Omar, M. A., EI-Hady, M. M., Shendi, M., Omar, S. A. and EI-Sorady, A. A. (1990) Report on Back-up Research Faba Bean Breeding 1989/ 90. Nile Valley Regional Program on Cool-Season Food Legumes, Second Annual Regional Meeting, Giza, 23-27 September 1990, 14 PP Linke, K.-H. (1992) Biology and Control of Orobanche in Legume Crops. PLITS vol. 10 (2), Verlag J. Margraf, Weikesheim, Germany, 62 pp Nassib, A. M., Ibrahim, A. A. and Khalil, S. A. (1982) Breeding for resistance to Orobanche. In: Faba Bean Improvement (Ed. by G. Hawtin and C. Webb) pp. 199-206, Martinus Nijhoff, The Hague Nassib, A. M., Ibrahim, A. A. and Saber, H. A. (1978) Broomrape (Orobanche crenata) resistance in broad beans. In: Proc. ICARDA Workshop: "Seed Legumes", pp. 133-135, ICARDA, Aleppo, Syria

Acknowledgements

Norusis, M. J. (1986) SPSS/PC+: SPSS for the IBM PC/XT/AT. SPSS Inc., Chicago, Illinois, USA

This research was partly financed by the European C o m m u n i t y ( D G X I I , S T D I I ) in t h e f r a m e w o r k o f t h e project TS2-014-C(GDF). Research facilities were provided by the NVRP (Nile Valley Research Project). T h e a u t h o r s a r e g r a t e f u l to I C A R D A f o r a d m i n i s t r a t i v e support.

Pieterse, A. H., Garcia-Torres, L., AI-Menoufi, O. A., Linke, K. H. and ter Borg, S . J . (1993) Integrated control of the parasitic angiosperm Orobanche (broomrape). In: Expanding the Production and Use of Cool Season Food Legumes (Ed. by F. J. Muehlhauer and W. J. Kaiser), pp. 695-702, Kluwer, Dordrecht Poorter, H. and Lewis, C. (1986) Testing differences in relative growth rate: a method avoiding curve fitting and pairing. Physiologia PI. 67, 223-226

References

Radwan, M. S., Abdalla, M. M. F., Fischbeck, G., Metwally, A. A. and Darwish, D. S. (1988) Variation in reaction of faba bean lines to different accessions of Orobanche crenata Forsk. Plant Breed. 101, 208-216

Attia, S. M. (1991) Response of Some Faba Bean (Vicia faba L.) Varieties to Broomrape (Orobanche crenata Forsk.). MSc thesis, University of Cairo, Egypt, 73 pp

Sauerborn, J. (1992) Parasitic Flowering Plants: Ecology and Management. Verlag J. Margraf, Weikesheim, Germany, 127 pp

Ceehin, I. and Press, M . C . (1993) Nitrogen relations of the sorghum-Striga hermonthica association: growth and photosynthesis. Plant Cell Environ. 16, 237-247 Cubero, J. I. (1991) Breeding for resistance to Orobanche species: a review. In: Progress in Orobanche Research (Ed. by K. Wegmann and L . J . Musselman) pp. 257-277, Eberhard-Karls-Universit~it, Tiibingen, Germany Cubero, J. I., Pieterse, A. H., Saghir, A. R. and ter Borg, S . J . (1988) Parasitic weeds on cool season food legumes. In: World Crops: Cool Season Food Legumes. Proc. Int. Food Legume Res. Conf. on Pea, Lentil, Faba Bean and Chickpea, July 1986 (Ed. by R. J. Summerfield) pp. 549-563, Spokane, Washington, USA Cubero, J. I., Pieterse, A. H., Khalil, S. A. and Sauerborn, J. (1993) Sources of host crop resistance to parasitic angiosperms and techniques for screening. In: Expanding the Production and Use of Cool Season Food Legumes (Ed. by F. J. Muehlbauer and W. J. Kaiser) pp. 333-345, Kluwer, Dordrecht Graves, J. D., Wylde, A., Press, M. C. and Stewart, G. R. (1990) Growth and carbon allocation in Pennisetum typhoides infected with the parasitic angiosperm Striga hermonthica. Plant Cell Environ. 13, 367-373

Harloff, H. J. (1991 ) Die Bedeutung des Mannitsstoffwechsels fiir die osmotische Anpassung in Orobanche ramosa und Orobanche crenata. PhD thesis, Eberhard-Karls-Universit~it, Tiibingen, Germany, 274 pp

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Tennant, D. (1975) A test of a modified line intersect method of estimating root length. J. Ecol. 63,995-1001 ter Borg, S. J. (1986) Effects of environmental factors on Orobanchehost relationships; a review and some recent results. In: Biology and Control of Orobanche (Ed. by S. J. ter Borg) pp. 57-69, LH/VPO, Wageningen, The Netherlands ter Borg, S . J . and van Ast, A. (1991a) Soil moisture, root architecture and broomrape (Orobanche crenata) infestation in faba bean (Vicia faba). In: Progress in Orobanche Research (Ed. by K. Wegmann and L . J . Musselman) pp. 278-292, Eberhard-KarlsUniversit~it, Ttibingen, Germany ter Borg, S. J. and van Ast, A. (1991b) Parasitic plants as stimulants of host growth. In: Proc. 5th Int. Syrup. on Parasitic Weeds (Ed. by J. K. Ransom, L. J. Musselman, A. D. Worsham and C. Parker) pp. 442-446, CIMMYT, Nairobi, Kenya Zaitoun, F. M. F., AI-Menoufi, O . A . and Weber, H.-C. (1991) Mechanisms of tolerance and susceptibility of three Vicia faba varieties to the infection with Orobanche crenata. In: Proc. 5th Int. Syrup. on Parasitic Weeds (Ed. by J. K. Ransom, L. J. Musselman, A. D. Worsham and C. Parker) pp. 195-207, CIMMYT, Nairobi, Kenya

Received 8 May 1993 Revised 12 February 1994 Accepted 24 February 1994