Branched broomrape (Orobanche ramosa L.) control in tomato (Lycopersicon esculentum Mill.) by trap crops and other plant species in rotation

Crop Protection 120 (2019) 75–83

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Branched broomrape (Orobanche ramosa L.) control in tomato (Lycopersicon esculentum Mill.) by trap crops and other plant species in rotation Jamal R. Qasem Plant Protection Department, Faculty of Agriculture, University of Jordan, Amman, Jordan

A R T I C L E I N F O

A B S T R A C T

Keywords: Parasitic weed Branched broomrape Orobanche ramosa Tomato Traps species Catch species Control Rotation

Forty-four plant species of 13 families were tested as trap plants reducing Orobanche ramosa L. infestation on tomato under glasshouse conditions. Many species were parasitized but Orobanche shoot number and dry weight were varied. Petroselinum sativum Hoffm and Trifolium alexandrinum L. were the most infested and Origanum syriacum L. and Citrullus vulgaris Schard. the least. Tomato growth was reduced after many tested species and none prevented parasite infection. Parasite shoot number was the highest on tomato followed Anethum graveolens L., C. vulgaris, Cucumis melo var. flexuosus L., Pimpinella anisum L., Sesamum indicum L., Solanum elaeagnifolium Cav., Sorghum vulgare Pers., Spinacia oleracea L., and T. alexandrinum and the lowest after Brassica oleracea L. var. italica Plenck, Brassica rapa L. var. rapa, Capsicum annuum L., Capsicum frutescens L., Cicer arietinum L., Citrullus colocynthis (L.) Schrad., Cucurbita maxima Duch., Cuminum cyminum L., Hordeum vulgare L., Linum usitatissimum L., Spinacia oleracea L. cv. Epinard greant and Vigna sinensis (L.) Savi. Parasite dry weight per shoot was the lowest on tomato grown after C. arietinum, C. frutescens, Cucumis melo L., Hibiscus sabdariffa L., P. anisum and T. alexandrinum but the highest after Cichorium endivia L. var. crispum Lam., Peganum harmala L., S. oleracea cv. Epinard greant, and Zea mays L. Tomato shoot dry weight increased by 126% over parasite-free control following Ecballium elaterium (L.) A. Rich. and parasite infestation reduced by 56% of the Orobanche-infested control. Considering the average of two experiments, high tomato growth and best parasite control (73% reduction) were obtained after V. sinensis. H. sabdariffa, H. vulgare, and S. vulgare reduced both Orobanche infestation and tomato growth.

1. Introduction

selective control of Orobanche aegyptiaca Pers. by chlorsulfuron and triasulfuron (Ghannam et al., 2012) and O. ramosa by chlorsulfuron (Qasem, 1998) have been reported. However, persistence, toxicity and low selectivity of this group and imidazolinones herbicides associated with high cost and increase in public concern on synthetic agricultural pesticides and their effects on human health and environment, neces­ sitate further attention and search for alternatives in parasites man­ agement in different parts of the world. The ability of plant species to stimulate Orobanche seed germination, encouraged search on possible use of catch and/or trap species to reduce parasite infestation. Catch crop is a host that must be destroyed before parasite development or flowering. Trap species is a false host that stimulates the parasite seed germination without itself supporting parasitism. It is used in order to deplete the seed reserve, this is referred to as a suicidal germination at which both trap species or stimulatory natural chemicals (Yoneyama et al., 1998, Evidente et al., 2010; Daniel et al., 2011) may be incorporated in parasite management. A review of species reported as traps of different Orobanche spp. including O. ramosa

Broomrapes (Orobanche spp.) are among the most problematic and destructive parasitic species to agriculture in different parts of the world �ndez-Aparicio, 2012; Hab­ and difficult to control (Rubiales and Ferna imana et al., 2014; Fern� andez-Aparicio et al., 2016). They are holo-parasites attacking a large number of cultivated and wild grown species (Parker and Riches, 1993; Qasem, 2009) and can totally destroy crops under heavy infestation. Complete control methods are not yet available, although many are practiced worldwide including prevention, cultural, mechanical, biological and chemicals (Rubiales and Fern� an­ �ndez-Aparicio et al., dez-Aparicio, 2012; Disciglio et al., 2016; Ferna 2016). Some satisfactory chemicals have been reported as effective against Orobanche ramosa L. in celery (Americanos, 1991), tobacco (Lolas, 1986) and potato (Haidar et al., 2005) but none proved effective and/or selective to tomato plants (Foy et al., 1988). In the last two decades, sulfonylurea urea herbicides were intro­ duced in a struggle against these parasites in tomato and results on E-mail address: [email protected].

https://doi.org/10.1016/j.cropro.2019.02.021 Received 2 April 2018; Received in revised form 28 January 2019; Accepted 24 February 2019 Available online 28 February 2019 0261-2194/© 2019 Elsevier Ltd. All rights reserved.

J.R. Qasem

Crop Protection 120 (2019) 75–83

and other promising species is available (Qasem, 2006). Stimulants are mainly natural chemicals released through the host root system into the surroundings, received by parasite seeds and stimulate their germination. Some of the chemicals released with root exudates were identified as strigol (isolated from maize root exudates), sorgolactone, isolated from sorghum (Hauck et al., 1992), alectrol pro­ duced by cowpea and orobanchol, by red clover (Xie et al., 2008). In addition, some of these chemicals, such as coumarin-type compounds and other metabolites are allelochemicals (Qasem, 2006; Cimmino et al., 2015). Different species have been reported to show strong ability’ to stimulate seed germination of different Orobanche species by more than 90%, and extracts of hundreds plant species were tested for possible stimulating or inhibiting seed germination of different Orobanche spp. and many proved effective and may be considered as trap, cover, catch species or a source of natural germination stimulants for these parasites (Babaei et al., 2010; Ma et al., 2012). The objectives of this work were to investigate the ability of selected none host and reported trap species of different Orobanche spp. as actually not attacked by O. ramosa, evaluate their potential to stimulate parasite seed germination in a suicidal treatment without being them­ selves attacked, and finally measure the effectiveness of these species in reducing parasite infection to the following tomato crop in rotation.

at 80� C for 72 h, and their dry weight (DW) was determined. The same experiment with all species tested and same methodology was repeated on March 2nd, 2015 and harvested by 7th June, 2015, (average day/night temperature 26.3/14.6oC) and similar data on plant species tested and O. ramosa infestation were recorded. 2.3. Experiment 2. O. ramosa infestation on tomato plants grown after tested plant species The same soil previously grown by tested plant species, replicates and experimental design used in experiment 1 were used in this exper­ iment. Soil in each pot was refilled into relevant pot and all pots were sown with seeds of tomato (Lycopersicon esculentum Mill cv. Pomodoro ACE 55vF) on 28th February, 2014. Parasite-infested and parasite-free pots were included as positive and negative controls, respectively. Pots were irrigated as needed. Ten days after emergence, tomato seed­ lings were thinned into one seedling per pot. Orobanche shoot emergence dates were recorded started four weeks after tomato emergence and continued until harvest. Tomato was grown for 3 months, after which plants were harvested from the above soil level on 13th June, 2014 and parasite shoots emerged above the soil in each pot were counted and harvested. The soil in each pot was emptied onto a large metal sieve, searched first by hand for Orobanche attachments, and then sieved to collect any Orobanche shoots or haustoria, seperated from the root sys­ tem. Roots were gently washed using a hose with a rose attached and Orobanche attachments were collected and counted, tomato shoot fresh weight and shoots and roots dry weights of tomato and Orobanche were determined after oven- dried at 80� C for 72 h. The same experiment was repeated on 17th June, 2015 (day/night temperature of 28.6/ 19.3oC) and continued until 1st of September, 2015, similar methodology was used and data on tomato growth and parasite infestation were recorded.

2. Materials and methods 2.1. Seed collection of O. ramosa and other plant species Seeds of O. ramosa were collected from tomato fields in Deir Alla (35.62oE Longitude and 32.221oN Latitude) and Abu-El-Zeighan (35.637oE Longitude and 32.186oN Latitude) sites, located in the cen­ tral Jordan Valley at an elevation of 224 m b.s.l. Weed seeds were collected from cultivated vegetable (broad-leaved weeds) and cereal (narrow-leaved weeds) fields in different parts of the country and crop seeds were bought from local markets. Pots with test plants were placed on benches in unconditioned glasshouse at the Faculty of Agriculture, University of Jordan Campus, Al-Jubeiha (35 87o E Longitude and 32 02o N Latitude and an elevation of 980m a.s.l.), Amman hence experiments were carried out during spring/summer periods of 2014, 2015 and 2016. Average day/night temperatures were 24.8� /15.4� C for the first two experiments, and 28.8� /18.1� C for the third and fourth. The following experiments were carried out:

2.4. Experiment 3. O. ramosa infestation on selected trap species The same procedure as that mentioned in Experiment 1 was followed in this experiment except that 15 cm-diameter plastic pots were used and 34 plant species (most of which have been reported as traps for different Orobanche species) were tested (Table 3). Seeds of different species were sown on 3rd January, 2016 and the experiment was terminated on 15th April, 2016 and similar data on O. ramosa on each plant species were recorded. 2.5. Experiment 4. O. ramosa infestation on tomato plants grown after selected trap species

2.2. Experiment 1. O. ramosa infestation on different plant species used as parasite traps

The same method used in experiment 2 was also followed in this experiment. The soil used in experiment 3 was reused in this experiment, pots were re-filled each by its own soil mixture, tomato cultivar, repli­ cates and experimental design were all the same. Tomato seeds were sown on 24th April, 2016; tomato plants were grown for 3 months before harvested on 21st July, 2016. Orobanche shoots above and below soil parasite attachments were harvested, and similar data on tomato plants and Orobanche were obtained.

Plastic pots (20-cm diameter) were filled with a methyl bromidefumigated soil mixture [3:1:1 (v/v/v) clay: sand: peat] of pH 7.3. The soil in each pot was thoroughly mixed with a 100 mg (approx. 20,000) seeds of a population of O. ramosa. Each four pots (replicates) were sown with an excess number of seeds of a single plant species on 3rd December, 2013, and a total number of 30 species of different plant families were tested (Table 1), many of which are known as nonhost and others re­ ported as traps for different Orobanche spp. At 10 – 14 d after emergence, seedlings in all pots were thinned to the appropriate number per pot, based on their growth rate and vegetative biomass using higher density for species of small plant size. Plants were irrigated as required and grown for 3 months. At harvest on 26th February, 2014, plants growth stages were recorded and the emerged Orobanche shoots above the soil were counted and harvested. Shoots of the tested species were severed just above the soil surface and discarded. The soil in each pot was left to become relatively dry by stopping irrigation, emptied onto a plastic sheet, searched by hand for Orobanche attachments, and then sieved to collect any of the below soil Orobanche shoots or haustoria, attached to the root systems. Roots of tested species were also collected and removed from the soil. Orobanche attachments were counted, oven dried

2.6. Experimental design and statistical analysis In all experiments, treatments were laid out in a randomized com­ plete block design with four replicates. Experiments 1 and 2 were carried out twice in 2014 and 2015, data of each repeated experiment were combined and statistically analysed. Experiments 3 and 4 and since a large number of species tested in experiment 1 were re-tested in experiment 3 therefore, these experiments were regarded as another set of almost similar methods and not repeated. Data of all experiments were subjected to the analysis of variance (ANOVA) using SAS software SAS (r) version 9.1 (SAS Institute Inc., 2004). Treatments means were separated and compared using the least significant difference test (LSD) 76

J.R. Qasem

Crop Protection 120 (2019) 75–83

Table 1 Orobanche ramosa infestation levels on different plant species used as parasite traps and grown under glasshouse conditions. Plant species

Growth stage at harvest

No. of plants per pot

No. of emerged O. ramosa shoots per pot

No. of O. ramosa shoots below soil per pot

Total no. of O. ramosa shoots per pot

Shoot dry weight of emerged O. ramosa (g/ pot)

Shoot dry weight of O. ramosa below soil (g/ pot)

Total shoot dry weight of O. ramosa (g/ pot)

Dry weight of O. ramosa per shoot (g)

Anethum graveolens L Brassica rapa L. var. rapa Capsicum annuum L. Capsicum frutescens L. Cicer arietinum L. Citrullus colocynthis (L.) Schrad Citrullus vulgaris Schard. Coriandrum sativum L Cucumis melo L. Cucumis prophetarum L. Cucumis sativus L. Cucurbita maxima Duch. Cucurbita moschata Duch. Cuminum cyminum L. Ecballium elaterium (L.) A. Rich. Hibiscus sabdariffa L. Hordeum vulgare L. Linum usitatissimum L. Lupinus albus L. Origanum syriacum L. Petroselinum sativum Hoffm Phaseolus vulgaris L. Pimpinella anisum L. Sesamum indicum L. Solanum elaeagnifolium Cav. Sorghum vulgare Pers. Spinacia oleracea L. Trifolium alexandrinum L. Trigonella foenumgraecum L. Vigna sinensis (L.) Savi. LSD (p ≤ 0.05)

Seeding

7

2.50ab

3.50e-f

6.00c-f

0.2187ab

0.1057b

0.3244c

0.0541

Vegetative

29

1.75abc

4.25c-f

6.00c-e

0.1096b-d

0.1364b

0.2460c

0,0410

b

c

0.0106

c

Fruiting

25

e

0.00

e

f

0.50f

f

f

0.50

d

0.0000

d

0.0055

b

0.0053

Fruiting

7

0.25

0.25

0.50

0.0113

0.0000

0.0113

0.0226

Flowering Flowering

12 2

0.00e 0.00e

0.00f 0.00f

0.00f 0.00f

0.0000d 0.0000d

0.0000b 0.0000b

0.0000c 0.0000c

0.0000 0.0000

Flowering

6

0.00e

0.25f

0.25f

0.0000d

0.0038b

0.0380c

0.1520

Seeding

32

0.00e

0.00f

0.00f

0.0000d

0.0000b

0.0000c

0.0000

Flowering Vegetative

2 3

0.00e 0.00e

0.00f 0.00f

0.00f 0.00f

0.0000d 0.0000d

0.0000b 0.0000b

0.0000c 0.0000c

0.0000 0.0000

Flowering

1

0.00e

0.00f

0.00f

0.0000d

0.0000b

0.0000c

0.0000

Flowering

3

0.00e

0.00f

0.00f

0.0000d

0.0000b

0.0000c

0.0000

Flowering

6

0.50de

0.25f

0.75f

0.0122d

0.0135b

0.0256c

0.0333

Seeding

12

0.75c-e

1.25ef

2.00d-f

0.0331cd

0.0316b

0.0646c

0.0323

Flowering

10

0.00e

0.00f

0.00f

0.0000d

0.0000b

0.0000c

0.0000

Flowering

8

0.00e

0.00f

0.00f

0.0000d

0.0000b

0.0000c

0.0000

e

f

f

d

b

c

Heading

13

0.00

0.00

0.00

0.0000

0.0000

0.0000

0.0000

Flowering

20

0.00e

0.00f

0.00f

0.0000d

0.0000b

0.0000c

0.0000

Seeding Vegetative

17 3

0.00e 0.00e

0.00f 0.25f

0.00f 0.25f

0.0000d 0.0000d

0.0000b 0.0148b

0.0000c 0.0148c

0.0000 0.0592

Flowering

13

2.75a

9.50c

12.25c

0.2340a

0.8129a

1.0971a

0.0896

Fruiting

4

0.00e

0.00f

0.00f

0.0000d

0.0000b

0.0000c

0.0000

Flowering

6

1.50a-c

6.25c-e

7.75c-e

0.1567a-c

0.2553b

0.4120bc

0.0532

e

f

f

d

b

c

Flowering

80

0.00

0.00

0.00

0.0000

0.0000

0.0000

0.0000

Flowering

15

0.00e

8.25cd

8.25cd

0.0000d

0.1712b

0.1712c

0.0208

Preflowering Seeding

28

0.00e

0.00f

0.00f

0.0000d

0.0000b

0.0000c

0.0000

40

0.50

1.00

1.50

d

0.0126

b

0.0307

c

0.0427

0.0285

Flowering

60

0.00e

19.25b

19.25b

0.1475bc

1.1486a

1.2961a

0.0673

Fruiting

8

0.50de

5.00c-f

5.50d-f

0.0122d

0.1702b

0.1825c

0.0332

Fruiting

12

0.00e

0.00f

0.00f

0.0000d

0.0000b

0.0000c

0.0000

-

-

1.00

5.81

6.41

0.1321

0.4253

0.5010

-

de

ef

e-f

Mean values in the same column followed by the same lower-case letter are not significantly different according to Fisher’s LSD at P ¼ 0.05.

77

J.R. Qasem

Crop Protection 120 (2019) 75–83

at p � 0.05.

the least (0.25 shoot/pot). The lowest dry weight per shoot of O. ramosa was on C. annuum and the highest on C. vulgaris.

3. Results

3.2. Experiment 2. O. ramosa infestation on tomato plants grown after tested plant species

3.1. Experiment 1. O. ramosa infestation on different plant species used as parasite traps

3.2.1. Tomato growth Tomato growth was greatly varied when grown after different tested species. Tomato shoot fresh and dry weights after all tested plant species were significantly higher than those of the parasite-infested control (Table 2). Tomato grown after Ecballium elaterium (L.) A. Rich. and T. alexandrinum significantly produced higher shoot dry weight than that of the parasite-free control and tomato growth after C. maxima, C. moschata, C. sativum, Hibiscus sabdariffa L., Hordeum vulgare L., Linum usitatissimum L., Origanum syriacum L., Pe. sativum, P. vulgaris, S. indicum, S. elaeagnifolium, S. vulgare, T. foenum-graecum and Vigna sinensis (L.) Savi was not significantly different from that of the parasite-free control. Tomato root growth was also varied after different species. The highest root dry weight was obtained after E. elaterium and T. alexandrinum. Tomato grown after Coriandrum sativum L., C. maxima, O. syriacum, and T. foenum-graecum produced higher root dry weight than that of parasite-free control but differences were not significant.

Fourteen out of the 30 plant species tested were parasitized by O. ramosa (Table 1). Infested species were varied in susceptibility, some slightly attacked while others were heavily infested. Differences were found in number and dry weight of emerged shoots, below soil attach­ ments and in total number and dry weight of parasite on different spe­ cies. While few Orobanche shoots emerged on Anethum graveolens L., Brassica rapa L. var. rapa, Capsicum annuum L., Capsicum frutescens L., Cucumis sativus L., Cucurbita moschata Duch, Cucurbita maxima Duch., Cuminum cyminum L., Helianthus annuus L., Medicago sativa L., Petrose­ linum sativum Hoffm, Pimpinella anisum L., Solanum elaeagnifolium Cav., Spinacia oleracea L. and Trigonella foenum-graecum L., no parasite shoots emerged on other species infected. However, great variations were also found in number and dry weight of Orobanche attachments from the below soil level. It was the highest on Trifolium alexandrinum L., Pe. sativum, S. elaeagnifolium, P. anisum, and T. foenum-graecum with T. alexandrinum the most. Similar differences were also found in parasite shoot dry weight on different species. Overall, T. alexandrinum was most heavily infested (19.25 shoots/pot), while Citrullus vulgaris Schard. was

3.2.2. O. ramosa infection None of the species grown before tomato prevented parasite

Table 2 Orobanche ramosa infestation levels on tomato plants grown after tested plant species under glasshouse conditions. Plant species

Shoot fresh weight of tomato (g/pot)

Shoot dry weight of tomato (g/pot)

Root dry weight of tomato (g/pot)

No. of emerged O. ramosa shoots

No. of O. ramosa shoots below soil

Total no. of O. ramosa shoots per pot

Shoot dry weight of emerged O. ramosa (g/ pot)

Shoot dry weight of O. ramosa below soil (g/ pot)

Total shoot dry weight of O. ramosa (g/ pot)

Dry weight of O. ramosa per shoot (g)

A. graveolens B. rapa var. rapa C. annuum C. frutescens C. arietinum C. colocynthis C. vulgaris C. sativum C. melo C. prophetarum C. sativus C. maxima C. moschata C. cyminum E. elaterium H. sabdariffa H. vulgare L.usitatissimum L. albus O. syriacum Pe. sativum P. vulgaris P. anisum S. indicum S. elaeagnifolium S. vulgare S. oleracea . T. alexandrinum T. foenumgraecum V. sinensis Control (Orobancheinfestead) Control (Orobanchefree) LSD (p ≤ 0.05)

12.96d-h 9.69e-h 6.25g-h 13.96c-g 9.39e-h 12.86d-h 16.26b-e 21.36a-c 8.77e-h 15.21c-f 12.73d-h 13.67c-h 11.80d-h 12.31d-h 27.38a 23.58ab 7.83f-h 13.07d-h 8.83e-h 14.44c-f 11.49d-h 8.87e-h 11.81d-h 8.28e-h 15.81b-f 11.72d-h 8.51e-h 19.05b-d 14.11c-g

0.99d-i 0.77f-i 0.74f-i 0.96d-i 0.94e-i 0.81f-i 1.02d-i 1.46c-h 0.48i 1.04d-i 0.72f-i 1.89b-e 1.49c-h 0.99d-i 2.75ab 1.90d-e 1.28c-i 1.40c-i 0.63h-i 1.65c-g 1.28c-i 1.49c-h 0.57h-i 1.69c-f 1.27c-i 1.47c-h 0.95e-i 2.93a 1.42c-i

0.55d-f 0.53e-f 0.33f 0.62c-f 0.58c-f 0.53e-f 0.42f 0.84b-e 0.39f 0.57c-f 0.68c-f 0.83b-e 0.61c-f 0.43f 1.28a 0.92bc 0.59c-f 0.49e-f 0.54d-f 0.80c-e 0.67c-f 0.66c-f 0.41f 0.44f 0.64c-f 0.64c-f 0.56d-f 1.18ab 0.82c-e

1.25e-g 0.75e-g 0.25f-g 0.00g 0.00g 1.25e-g 4.00bc 3.75b 0.25f-g 2.50c-e 0.50e-g 0.00g 2.25c-f 1.00e-g 2.00c-g 0.00g 2.50c-e 0.00g 1.00e-g 2.25c-f 0.75e-g 1.75d-g 2.00c-g 2.25c-f 3.50b-d 4.75b 1.75d-g 0.75e-g 0.00g

3.00g-j 1.00j 1.00j 1.50j-i 2.00j-i 1.50j-i 10.75d-g 6.25e-i 3.75e-j 2.00j-i 2.75g-j 0.50j 10.50d-h 6.25g-j 5.00e-i 7.50e-j 5.25e.i 1.25j-i 3.25g-j 12.75a 5.25e-i 1.75j-i 9.75d-i 22.50bc 18.00cd 6.25e-i 13.00de 28.75b 1.50j-i

4.25h-l 1.75j-l 1.25k-l 1.50k-l 2.00j-l 2.75i-l 14.75e-g 10.00f-k 4.00h-l 4.50h-l 3.25i-l 0.50l 12.75e-h 7.25f-l 7.00f-l 7.50f-l 7.75f-l 1.25k-l 4.25h-l 15.00e-g 6.00g-l 3.50i-l 11.75f-i 24.75cd 21.50c-e 11.00f14.75e-g 29.50c 1.50k-l

0.483f-h 0.213gh 0.159h 0.000h 0.000h 0.383gh 1.585bc 0.301gh 0.065h 0.600e-h 0.133h 0.000h 1.060c-f 0.265gh 0.637e-h 0.000h 0.548e-h 0.000h 0.293gh 1.468b-d 0.170h 0.282gh 0.333gh 0.8475d-g 2.040ab 0.416f-h 0.358g-h 0.430f-h 0.000h

0.130cd 0.038cd 0.015cd 0.033cd 0.133cd 0.068cd 0.340cd 0.298cd 0.075cd 0.090cd 0.150cd 0.153cd 0.275cd 0.285cd 0.193cd 0.358cd 0.189cd 0.128cd 0.063cd 2.063b 0.325cd 0.055cd 0.273cd 2.960a 0.368cd 0.340cd 0.449cd 2.830a 0.040cd

0.620e-g 0.250g 0.174g 0.033g 0.133g 0.450e-g 1.925cd 0.601e-g 0.140g 0.690e-g 0.283g 0.153g 1.335df 0.548e-g 0.834e-g 0.358fg 0.737e-g 0.128g 0.358fg 3.531a 0.495e-g 0.337g 0.618e-g 3.775a 2.408bc 0.786e-g 0.806e-g 3.260ab 0.040g

0.1459 0.1486 0.1392 0.0220 0.0665 0.1636 0.1305 0.0601 0.0350 0.1533 0.0871 0.3060 0.1047 0.0731 0.1191 0.0477 0.0983 0.1024 0.0842 0.2354 0.0825 0.0963 0.0526 0.1525 0.1120 0.0715 0.0546 0.1105 0.0267

10.04e-h 5.95h

1.94b-d 0.68g-i

0.89b-d 0.49e-f

1.75d-g 3.75b-d

2.50g-j 12.25d-f

4.25h-l 16.00d-f

0.426f-h 1.188b-d

0.038cd 0.188cd

0.470e-g 1.394de

0.1106 0.0871

11.55d-h

1.22c-i

0.60c-f

0.00g

0.00j

0.00l

0.000h

0.000d

0.000g

0.0000

7.99

0.99

0.354

2.20

8.66

9.37

0.660

0.666

0.989

-

Mean values in the same column followed by the same lower-case letter are not significantly different according to Fisher’s LSD at P ¼ 0.05. 78

J.R. Qasem

Crop Protection 120 (2019) 75–83

Table 3 Orobanche ramosa infestation levels on different selected trap plant species grown under glasshouse conditions. Plant species

Growth stage at harvest

No. of plants per pot

No. of emerged O. ramosa shoots

No. of O. ramosa shoots below soil

Total no. of O. ramosa shoots per pot

DW of emerged O. ramosa shoots (g/pot)

DW of below soil O. ramosa shoots (g/pot)

Total O. ramosa DW (g/pot)

O. ramosa DW per shoot (g)

Anethum graveolens L. Beta vulgaris L. Brassica oleracea L. var. italica Plenck Brassica oleracea var. capitata L. F. rubra Brassica rapa L. var. rapa Capsicum annuum L. Cichorium endivia L. var. crispum Lam. Citrullus vulgaris Schard. Coriandrum sativum L. Cucumis melo var. flexuosus L. Cucumis sativus L. Cucurbita lagenaria L. Cucurbita maxima Duch. Cucurbita moschata Duch Cuminum cyminum L. Glycine max (L.) Merr. Helianthus annuus L. Linum usitatissimum L. Lupinus albus L. Medicago sativa L. Panicum miliaceum L. Peganum harmala L. Petroselinum sativum Hoffm Pimpinella anisum L. Pisum sativum L. Sesamum indicum L. Solanum elaeagnifolium Cav. Sorghum vulgare Pers. Spinacia oleracea L. cv. Epinard greant Spinacia oleracea L. Trifolium alexandrinum L. Trigonella foenumgraecum L. Vigna sinensis (L.) Savi. Zea mays L.

Seeding

10

2.50b

16.0a

18.5ab

0.995a

0.6580a-c

1.6530bc

0.0894

Vegetative Vegetative

5 8

0.00d 0.00d

0.0f 3.5de

0.0f 3.5d-f

0.000e 0.000e

0.0000e 0.5750a-d

0.0000e 0.5765de

0.0000 0.1647

Preflowering

5

0.00d

4.0c-e

4.0df

0.000e

0.2485b-e

0.2485de

0.0621

Vegetative

4

0.00d

1.0

1.0f

0.000e

0.0250e

0.0250e

0.0250

Fruiting

4

0.50cd

2.5d-f

3.0ef

0.060de

0.2050c-e

0.2650de

0.0883

LSD (p ≤ 0.05)

Preflowering

30

0.00

Flowering

3

Flowering

d

f

f

e

e

e

0.0

0.0

0.000

0.0000

0.0000

0.0000

0.00d

0.5f

0.5f

0.000e

0.0900e

0.0900e

0.1800

7

0.00d

0.0f

0.0f

0.000e

0.0000e

0.0000e

0.0000

Flowering

1

0.00

d

f

f

e

Flowering Flowering

3 4

Vegetative

c-e

de

0.5

0.5

0.000

0.1910

0.1910

0.3820

0.50cd 0.00d

0.5f 0.0f

1.0f 0.0f

0.211c-e 0.000e

0.0205e 0.0000e

0.2315d-e 0.0000e

0.2315 0.0000

2

1.00b-d

0.0f

1.0f

0.5206b

0.0500de

0.5755de

0.5755

Flowering

4

1.00

b-d

f

f

de

Seeding

7

Flowering Flowering

b-d

e

0.0

1.0

0.321

0.0000

0.3210

0.3210

0.00d

0.5f

0.5f

0.000e

0.0210e

0.0210de

0.0420

3

0.00d

0.5f

0.5f

0.000e

0.0000e

0.0000e

0.0000

3

2.50

b

a

a

d

Flowering

26

0.00

Seeding Flowering Preflowering Vegetative

4 23 30

cd

5.0

f

cd

7.5

f

1.159

e

0.8205

e

ab

0.2639

e

1.9795

0.0

0.0

0.000

0.0000

0.0000

0.0000

0.00d 2.00bc 0.00d

0.0f 2.0de 0.0f

0.0f 4.0df 0.0f

0.000e 0.406bc 0.000e

0.0000e 0.4795a-e 0.0000e

0.0000e 0.8855cd 0.0000e

0.0000 0.2214 0.0000

7

0.00d

2.5d-f

2.5ef

0.000e

0.0865de

0.0865de

0.0346

Flowering

8

3.50ab

12.0b

15.5b

0.032e

0.6621a-c

0.6936de

0.0448

Preflowering Fruiting Vegetative

2

1.50b-d

14.0ab

15.5b

0.016e

0.6920a-c

0.7080de

0.0457

1 45

0.00 0.00d

0.0 0.0f

0.0 0.0f

0.000 0.000e

0.0000 0.0000e

0.0000 0.0000e

0.0000 0.0000

Preflowering

5

0.50cd

3.5ef

4.0df

0.115de

0.2000c-e

0.3150de

0.2100

Vegetative

6

0.00d

0.0f

0.0f

0.000e

0.0000e

0.0000e

0.0000

Seeding

6

0.00

d

f

f

e

e

e

Seeding Flowering

5 28

Fruiting

15

d

f

f

e

e

e

0.0

0.0

0.000

0.0000

0.0000

0.0000

4.50a 0.50cd

6.0c 6.0c

10.5c 6.5ce

0.037e 0.088d-e

0.0678de 0.3220a-e

0.1043de 0.4095de

0.0099 0.0630

0.50cd

1.5ef

2.0f

0.038e

0.0645de

0.1245de

0.0622

f

e

Fruiting

5

0.00

Preflowering -

7 -

d

f

e

e

0.0

0.0

0.000

0.0000

0.0000

0.0000

0.00d

0.0f

0.0f

0.000e

0.0000e

0.0000e

0.0000

1.96

3.32

4.25

0.269

0.5390

0.8678

–

Mean values in the same column followed by the same lower-case letter are not significantly different according to Fisher’s LSD at P ¼ 0.05.

79

J.R. Qasem

Crop Protection 120 (2019) 75–83

infection to tomato plants (Table 2). However, number of above-soil emerged parasite shoots on tomato was varied, the highest on tomato grown after Sorghum vulgare Pers. and C. vulgaris. Great variation in Orobanche shoot number was also found in the below soil infestation. The highest number was on tomato grown after T. alexandrinum and Sesamum indicum L. which was significantly higher than that of parasiteinfested control. Differences in parasite infestation to tomato grown after S. elaeagnifolium, S. oleracea, O. syriacum, C. vulgaris and C. moschata were not significantly different from that of Orobancheinfested control. The highest total number (above and below soil level) of parasite shoots and haustoria was on tomato grown after T. alexandrinum, S. indicum, and S. elaeagnifolium with significantly higher total parasite shoot number on tomato grown after the first species than that of parasite-infested tomato control. Orobanche infes­ tation on tomato was extremely low (� 3 shoots per pot) after B. rapa var. rapa, C. annuum, C. frutescens, Cicer arietinum L., Citrullus colocynthis (L.) Schrad, C. maxima, L. usitatissimum and T. foenum-graecum. Oro­ banche shoot dry weight above and below soil level and total weight was

also varied on tomato grown after different plant species. The lowest dry weight per shoot of O. ramosa was found on tomato grown in the potted soils that C. frutescens, Cucumis melo L., T. foenum-graecum, H. sabdariffa and P. anisum were raised, while the highest was found from that O. syriacum and C. colocynthis were grown. 3.3. Experiment 3. O. ramosa infestation on selected trap species Out of 34 species tested for possible attack by O. ramosa, 14 species were found parasite-free while the other 20 species were infested (Table 3). A. graveolens, H. annuus, P. anisum, Pe. sativum, S. oleracea and T. alexandrinum showed the highest total number of parasite infestation. While S. oleracea showed the highest number of above-soil emerged Orobanche shoots but differences from that of Pe. sativum were not sig­ nificant. A. graveolens and P. anisum had the highest below soil parasite infestation. Infected species showed differences in shoot dry weight of Orobanche from the above and below soil level as well as in total shoots dry weight and dry weight per individual parasite shoot. The lowest dry

Table 4 Orobanche ramosa infestation levels on tomato plants grown after selected trap plant species grown under glasshouse conditions. Plant species

Shoot fresh weight of tomato (g/pot)

Shoot dry weight of tomato (g/pot)

Root dry weight of tomato (g/pot)

No. of emerged O. ramosa shoots

No. of O. ramosa shoots below soil

Total no. of O. ramosa shoots per pot

Shoot dry weight of emerged O. ramosa (g/ pot)

Shoot dry weight of O. ramosa below soil (g/ pot)

Total shoot dry weight of O. ramosa (g/ pot)

Dry weight of O. ramosa per shoot (g)

A. graveolens B. vulgaris B. oleracea L var italica B. oleracea var. capitata F. rubra B. rapa var. rapa C. annuum C. endivia L. var. crispum C. vulgaris C. sativum C. melo var. flexuosus. C. sativus C. lagenaria C. maxima C. moschata C. cyminum G. max H. annuus L.usitatissimum L. albus M. sativa P. miliaceum P. harmala Pe. sativum P. anisum P. sativum S. indicum S. elaeagnifolium S. vulgare S. oleracea cv. Epinard greant S. oleracea T. alexandrinum T. foenumgraecum V. sinensis Z. mays Control (Orobancheinfestead) Control (Orobanchefree) LSD (p ≤ 0.05)

15.70g-m 19.87l-p 9.14o-q

1.79g-l 1.03k-m 0.87lm

0.47i-k 0.74f-k 0.87f-k

2.00a-f 0.75d-f 1.25b-f

14.25b-d 4.25e-l 0.75j-l

16.25a-c 5.00e-j 2.00jk

2.7275a-e 1.0100f-j 1.9000b-i

3.0325a-e 2.8325b-e 1.3025g-j

5.760a-d 3.843d-g 1.203e-g

0.3545 0.7686 0.6015

10.26m-p

1.06k-m

2.14a

0.50ef

6.75e-k

7.25d-j

0.6070h-j

3.8525ab

4.460b-g

0.6152

16.03g-l 24.35a-c 9.17o-q

1.70h-l 3.63ab 0.85l-m

0.52i-k 1.12d-k 0.42j-k

1.00c-f 0.25ef 0.75d-f

2.00j-l 7.25e-j 3.25g-l

3.00h-k 7.50d-k 4.00h-k

1.3725d-j 0.7225h-j 2.0100a-i

1.3150h-i 2.2600d-g 2.6325b-f

2.680gh 2.983f-g 4.843a-f

0.8933 0.3849 1.2108

17.13e-k 11.10l-p 11.22k-p

2.24d-i 1.46i-m 2.14e-j

0.65h-k 0.67g-k 1.04d-k

0.75d-f 0.75d-f 2.00a-f

9.00c-i 5.00el 15.50bc

9.75c-h 5.75d-k 17.5ab

1.5025d-j 2.9050a-d 2.5175a-g

2.8625b-e 2.6100b-g 3.2000a-e

4.365b-g 5.515a-d 5.718a-d

0.4477 0.9591 0.3267

15.38g-n 9.62n-p 14.30g-o 14.82g-o 30.23a 17.64e-j 12.32i-p 14.11g-p 9.89m-p 17.42e-j 18.33d-h 21.23b-f 17.78f-g 12.03j-p 26.58ab 24.53a-c 22.35b-e 12.70h-p 8.25p-q

1.86f-l 1.49i-m 0.65m 1.76h-l 3.18b-d 2.30c-i 1.08k-m 1.56h-m 1.42i-m 2.17e-j 2.83b-f 2.55c-g 0.92k-m 1.22j-m 3.31a-c 2.72b-g 2.54c-h 1.10k-m 0.95k-m

0.77f-k 1.87a-d 0.65h-k 0.28k 1.23b-j 1.77a-e 0.83f-k 1.55a-f 0.33k 0.83f-k 1.01e-k 1.44a-h 0.82f-k 0.69g-k 1.97a-c 1.13d-k 1.27b-i 1.29b-i 1.19c-j

3.00a-c 0.00f 1.00c-f 1.00c-f 0.50ef 1.75a-f 0.50ef 0.75d-f 0.50ef 3.50a 3.00a-c 0.75d-f 1.50a-f 1.25b-f 2.25a-e 0.00f 3.25ab 2.25a-e 0.75d-f

9.50c-h 8.75e-i 5.00e-l 3.00h-l 2.75i-l 10.00b-f 6.50e-l 5.00e-l 4.25e-l 6.00e-l 3.75f-l 3.50f-l 4.25e-l 10.00b-f 7.00e-j 4.75e-l 5.50e-l 9.75c-g 2.50i-l

12.50b-d 8.75d-i 6.00d-k 4.00h-k 3.25h-k 11.75b-f 7.00d-k 5.75d-k 4.75f-k 9.50c-h 6.75d-k 4.25g-k 5.75d-k 11.25b-g 9.25c-h 4.75f-k 8.75d-i 12.0b-e 3.25h-k

3.2375a-c 0.0600j 1.4650d-j 1.8375b-i 0.6800h-j 2.6350a-f 0.5975h-j 2.1250a-h 0.9050g-j 3.6000a 2.8800a-e 1.3250d-j 3.3525ab 2.6275a-f 1.5650e-j 0.0000j 3.4925ab 2.1175a-h 1.6475c-j

3.1975a-e 3.6075a-c 2.7000b-f 1.9375e-h 2.0000e-h 2.3550c-g 3.0700a-e 2.9950a-e 2.8050b-e 3.0500a-e 1.4675f-h 2.9300a-e 3.0050a-e 2.9575a-e 2.3575c-g 3.1125a-e 3.1750a-e 3.0975a-e 2.4700c-g

6.435ab 3.668d-g 4.165d-g 3.775d-g 2.680gh 4.990a-f 3.168e-g 5.120a-e 3.710d-g 6.640a 4.348b-g 4.255c-g 6.358a-c 5.585a-d 3.923d-g 3.113e-g 6.668a 5.215a-e 4.118d-g

0.5148 0.4192 0.6942 0.9438 0.8246 0.4247 0.4526 0.8904 0.7811 0.7378 0.6441 1.0010 1.1057 0.4964 0.4241 0.6554 0.7621 0.4346 1.2670

13.33g-p 12.25i-p 12.72h-p

3.13b-e 1.83f-l 1.91f-k

1.50e-g 0.91f-k 0.92f-k

2.75a-d 1.50a-f 1.25b-f

5.75e-l 16.50ab 4.50e-l

8.50d-j 18.00ab 5.75d-k

2.7125a-e 1.3575d-j 2.2300a-h

2.4900c-g 3.3825a-d 2.1725d-g

5.203a-e 4.740a-g 4.403b-g

0.6121 0.2633 0.7657

11.90j-p 9.18o-q 3.28q

2.53c-h 1.06k-m 2.12e-j

0.95e-k 2.06ab 0.70g-k

1.25b-f 0.50ef 1.25b-f

0.25l 4.75e-l 10.50b-e

1.50jk 5.25e-j 11.75b-f

0.4080i-j 1.2325e-j 1.3675d-j

0.0700i-j 4.2025a 3.1225a-e

0.478i 5.435a-d 4.490b-g

0.3187 1.0352 0.3821

23.64b-c

4.20a

1.06d-k

0.00f

0.00l

0.00k

0.0000j

0.0000j

0.000i

0.0000

5.91

1.01

0.85

2.00

6.54

7.03

1.6647

1.3083

2.1195

-

Mean values in the same column followed by the same lower-case letter are not significantly different according to Fisher’s LSD at P ¼ 0.05. 80

J.R. Qasem

Crop Protection 120 (2019) 75–83

weight per Orobanche shoot was with Peganum harmala L. and the highest with C. maxima.

number of seeds of long dormancy period and high dispersal capacity is the ultimate goal of control measures. In the present work, many of the tested species were found infested although some were reported as traps for different Orobanche species (Schnell et al., 1994; Abebe et al., 2005; Ferna�ndez-Aparicio et al., 2008; Babaei et al., 2010). Infestation however, was low on most species and widely varied from extremely low (0.25 shoot/pot on O. syriacum) to relatively high in average (13.88 shoot/pot on Pe. sativum). T. alexan­ drinum and T. foenum graecum were reported as traps for Orobanche crenata Forsk (Schnell et al., 1994; Ferna�ndez-Aparicio et al., 2008) and C. cyminum and also M. sativa for Oobanche cernua Loefl (Krishnamurthy et al., 1977; Acharya, 2012). These were attacked in the present work and regarded as hosts for O. ramosa but may be traps for other Orobanche species. These species however, may be used in intercropping or crop rotation systems to reduce parasite infestation. T. alexandrinum, T. foe­ num graecum, Lupinus termis L., C. sativum and B. rapa were suggested for intercropping system with faba bean or tomato to reduce Orobanche �ndez-Aparicio et al., infection rate (AI-Menoufi and Adam, 1998; Ferna 2010). Differences between tested trap species were expected since differ in taxonomy, physiology, ability to produce germination stimu­ lants, chemical nature and mechanism of resistance (Parker and Riches, 1993; Qasem, 2006). A wide array of natural stimulants of different plant species for different parasites including Orobanche spp. have been reported (Sugimoto, 2000; Qasem, 2006; Samejima and Sugimoto, 2018) while allelochemicals may have a role at different stages from germination to growth and development of parasite life cycle (Qasem, 2006; Aksoya et al., 2016). In this study, number of emerged parasite shoots was generally limited and only found with few species. Many species may be regarded as true traps providing that the following host species in rotation are not attacked or low infested. C. sativum, C. lagenaria, H. sabdariffa, H. vulgare, L. albus, L. usitatissimum, P. miliaceum, Phaseolus vulgaris L., S. indicum, S. vulgare, Z. mays and V. sinensis were not parasitized by O. ramosa. Some of these have been reported as traps for different Orobanche species (Krishnamurthy et al., 1977; Linke et al., 1991). Other reported traps including C. annuum, C. arietinum, T. foenum-graecum, B. rapa var. rapa, and C. frutescens (Krishnamurthy et al., 1977; Labrada and Perez, 1988; AI-Menoufi and Adam, 1998) were slightly infected in the present work. These may be used in intercropping to affect Oro­ bonche-host interaction (Bouhatous and Jacquard, 1994). It has been reported that unsuitable host crops of O. cernua including C. annuum, S. vulgare, V. sinensis, Phaseolus aconitifolius Jacquin. and H. sabdariffa stimulated germination of the parasite at a high level, while S. indicum stimulated germination but without offering it any chance for further growth and development (Bouhatous and Jacquard, 1994). Root dif­ fusate of L. usitatissimum, C. annuum, S. indicum, T. alexandrinum and C. cyminum enhanced Orobanche seed germination, but the germinated seeds normally failed to attach to their root systems (Krishnamurthy et al., 1977; Ferna�ndez-Aparicio et al., 2008; Acharya, 2012). Our results were in conflict with some of these reports since C. annuum, C. cyminum and T. alexandrinum (highly infestead) were parasitized by O. ramosa. Other least infected species are hosts but since infestation is extremely low they may be regarded as a new category of unpreferable/tolerant species. However, both non- or low-infested spe­ cies could have stimulated parasite seed germination. Replacement of these species by tomato as a parasite preferable host resulted tomato infection after all and none of the species completely destroyed parasite seeds in the soil although infestation was varied. Tomato grown after T. alexandrinum, S. indicum and S. elaeagnifolium was heavily parasitized and more than parasite-infested control. T. alexandrinum and S. elaeagnifolium may be regarded as highly pref­ erable susceptibile hosts that highly attacked and also stimaulated more parasite seed germination and attachment on the following tomato plants. S. indicum is a nonhost but its root exudates in the soil stimulated more parasite infection on tomato plants grown after this crop. How­ ever, root exudates of these species may have lasted longer in the soil

3.4. Experiment 4. O. ramosa infestation on tomato plants grown after selected trap species 3.4.1. Tomato growth Growth of tomato plants grown after different plant species was greatly varied (Table 4). The highest tomato shoot dry weight was in parasite-free control and the lowest after C. maxima. Tomato grown after C. annuum and P. sativum, produced shoot dry weight not significantly different from that of parasite-free control. In contrast, tomato followed Beta vulgaris L., Brassica oleracea L. var. italica Plenck, Brassica oleracea var. capitata L. F. rubra, Cichorium endivia L. var. crispum Lam., C. maxima, H. annuus L., Pe. sativum, S. vulgare, Spinacia oleracea L. cv. Epinard greant and Zea mays L. was negatively affected and its shoot dry weight was significantly reduced below parasite-infested control. In addition, T. foenum-graecum, T. alexandrinum, P. anisum, L. usitatissimum, Lupinus albus L., C. moschata, Cucurbita lagenaria L., C. sativum, C. sativus, B. rapa var. rapa and A. graveolens lowered tomato shoot dry weight below that of the parasite-infested tomato control but differences were not significant. Tomato root dry weight was also varied after different plant species; highest after B. oleracea var. capitata F. rubra, Z. mays and P. sativum and significantly more than that of parasite-free control. The lowest root dry weight was in tomato that followed A. graveolens, B. rapa var. rapa, C. endivia var. crispum, C. moschata and L. albus with reduction in tomato root dry weight by > 50% of the parasite-infested tomato control after the last two species. 3.4.2. O. ramosa infection Tomato grown after all tested plant species was parasitized by O. ramosa but infestation was varied from the above and below soil levels and in total parasite shoot number and dry weight per pot (Table 4). Above soil emerged number of Orobanche shoot was highest on tomato followed S. elaeagnifolium, Panicum miliaceum L., M. sativa and C. sativus, while only tomato grown after C. lagenaria and S. indicum showed no emerged parasite shoot above soil level. The below soil infestation was quite varied on tomato grown after different species. The highest number of Orobanche below soil and total number per pot were on tomato grown after A. graveolens, Cucumis melo var. flexuosus L. and T. alexandrinum. Tomato followed other plant species had similar or lower O. ramosa infestation than tomato-infested control. The lowest total parasite infestation however, was on tomato grown after V. sinensis, B. oleracea var. italic, B. rapa var. rapa, S. oleracea cv. Epinard greant, and C. cyminum with >72% reduction of the parasite-infested control. Considering O. ramosa shoot dry weight, differences were also found in the above-soil emerged shoots, below-soil and in total parasite shoot dry weights. Similar differences were also found per single shoot dry weight of the parasite on tomato grown after different species. The highest total shoot dry weight of Orobanche per pot was on tomato fol­ lowed C. sativus, S. elaeagnifolium, M. sativa and Pe. sativum and higher than that of parasite-infested control. In contrast, tomato grown after V. sinensis showed the lowest total parasite shoot dry weight. The highest dry weight per shoot of the parasite was after S. oleracea cv. Epinard greant followed by C. endivia L. var. crispum and the lowest after T. alexandrinum followed by V. sinensis and C. melo var. flexuosus. 4. Discussion Control of Orobanche spp. is a challenge to farmers worldwide and their successful control method is not yet available. Techniques aiming at stimulating or preventing parasite seed germination, attachment, development and/or shoot emergence may play a major role in their control or eradication especially when integrated with other methods of control. Trap and catch species are important and may play a major role in this regard. Parasite main starategy through production of a huge 81

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Crop Protection 120 (2019) 75–83

and thus encouraged more parasite infection, or have different chemical nature and/ or concentration of germination stimulants. T. alexandrinum and S. elaeagnifolium may serve as catch species while S. indicum is a nonhost but its root exudates stimulated more parasite infection on to­ mato plants (Parker and Riches, 1993; Qasem, 2006). Our results were �nde­ compatible with results of other workers for some species (Ferna z-Aparicio et al., 2010) reported as traps reduce parasite infestation on the following host crops but in conflict with others’ (Kara�ci�c et al., 2010; Acharya, 2012) reported some of these as parasite traps. However, these are few in number while most species greatly reduced O. ramosa infes­ tation on tomato plants. The differences obtained in parasite shoot number above and/or below soil, total attachments, and dry weights on tomato may reflect differences in the effect of species root exudates on parasite germination, attachment and development or their persistence in the soil. Low parasite infestation on tomato grown after C. maxima, L. usitatissimum, C. arietinum, and C. colocynthis may prove these as true traps since were not parasitized and greatly reduced parasite infestation on the followed tomato crop. On the other hand, great variation was found in dry weight of Orobanche shoots on tomato grown after all species. Parasite dry weight per shoot was extremely low on tomato grown after certain species but high after others reflecting differences in the effect of their root exudates on parasite development. Some enhanced parasite growth and development while others inhibited both. Results obtained were valid and indicative on the ability of these species to kill parasite germinated seeds either before or after attachment since high variation were found in number and dry weight of the parasite on tomato grown after different species. These results were in agreement with the findings of other workers who reported L. usitatissimum and C. arietinum as able to stimulate parasite seed germination and reduce its infestation level on the following host plants (Abebe et al., 2005; Babaei et al., 2010; Acharya, 2012; Aksoy et al., 2016). Low infections on to­ mato roots may be explained by exhaustion of parasite seed bank by former grown species or small development of tomato roots that less encouraged parasite infection. However, many of these species also reduced tomato growth compared with parasite free-control and lower than in parasite-infested control. This indicates that chemicals released from roots of such species although stimulated parasite seed germina­ tion but also harmed tomato plants and allelopathy may be involved (Cimmino et al., 2015) or species have exhausted soil growth resources (mainly nutrients). The low parasite infestation on tomato roots after these species may be also due to their reduced root growth and thus parasite attachments. In average of repeated species in the two experiments, parasite infestation on all tested species ranged from 0 (many species) to 13.88 shoots per pot (Pe. sativum). Other highly parasitized species were T. alexandrinum (12.88 shoots), A. graveolens (12.25 shoots) and P. anisum (11.63). The high infestation on these crops may be due to their high density used per pot which might have stimulated more parasite seed germination than other attacked species of low density or are more susceptible or have different stimulatory chemical nature. Repeated testing of many screened species in experiment 1 showed similar results. In addition the new examined species in experiment 3 were infected although some are known as traps including B. oleracea var. capitata L. F. rubra, B. oleracea L. var. italic, C. melo var. flexuosus, H. annuus, M. sativa and P. harmala (Krishnamurthy et al., 1977; Labrada and Perez, 1988; Abbes et al., 2008). Variations in dry weight of parasite shoots on infected species indicate differences in parasite development and the potential of some of these to reduce infestation on the following hosts. Some of the species tested were wild grown or weeds of low or no economical value including E. elaterium, C. colocynthis, Cucumis proph­ etarum L. and S. elaeagnifolium. These were included to investigate their possible stimulation of Orobanche seed suicide since their control later is easier than the parasite. However, only S. elaeagnifolium was parasitized and showed relatively high infestation. Tomato grown after these

species showed significantly lower O. ramosa infestation except after S. elaeagnifolium where infestation was higher than in parasite-infested control. Considering tomato growth as an indicator on crop perfor­ mance after these species, highest growth produced after E. elaterium which was similar to the average (in two experiments) growth of tomato parasite-free control and reduced parasite infestation, therefore may be regarded as a trap species. Tomato growth after C. colocynthis and C. prophetarum was lower than the average growth in parasite-free control in two experiments although both reduced parasite infestation on the following tomato plants. These results confirm the value of using some wild species as parasite traps encouraged or not harmed tomato growth but reduced parasite infestation to the following hosts or in absence of host crop but in heavily infested soils. These may also serve as a source of natural stimulatory chemicals encourage crop growth and inhibit pasrasite infestation. Qasem (2002) reported many weed species as hosts for the same parasite while others were not infested and reduced para­ site infestation on tomato followed these species. It is to conclude that many of the previously reported Orobanche traps were found infestead in the present study but parasite shoot number and dry weight were varied. None of the examined species prevented parasite infection to the following tomato plants but infes­ tation was greatly varied. Considering total number of O ramosa shoots per pot and in all ex­ periments, species may be grouped into four categories. The first was parasite-free and included 20 species among which only C. arietinum, L. usitatissimum and V. sinensis reduced average parasite infestation level on the following tomato plants by 85.6, 74.9 and 79.3% of the parasiteinfested control and for the three species, respectively. These species may be regarded as strong true traps, while other species were less so. The second group included parasite-unsuitable/unpreferable species slightly infested (0.25-2 shoots per pot) and could be considered as suiting plant mixtures and possibly reduce parasite infestation on host crops in intercropping system. It included 9 species but only C. annuum, C. frutescens and C. maxima effectively reduced average parasite infes­ tation on the following tomato plants and by 68.5, 89.2 and 76.6% of the parasite–infested control for the three crops, respectively. The third group was moderately (2.5-8 shoot/pot) parasitized included 8 species but only tomato grown after B. rapa var. rapa, H. annuus, S. oleracea, and P. harmala showed moderate infestation (2.25-8 shoot/pot) and may be considered as catch species while S. elaeagnifolium resulted in similar parasite infestation on tomto to that of tomato-infested control. The fourth group was heavily (8-20 shoot per pot) attacked included 4 spe­ cies these were; A. graveolens, Pe. sativum, P. anisum and T. alexandrinum and tomato grown after all was most infested (8-30 shoot/pot). These could be considered as catch species highly preferable, may exude high amounts/concentration of germination stimulants or of different chemical nature enhanced their parasite infection and tomato plants. These must be destroyed with the parasite before emergence. In average of two experiments, tomato growth after T. alexandrinum, V. sinensis, S. indicum, E. elaterium and C. annuum was similar to that of the parasitefree control. High tomato growth and best parasite control were after V. sinensis followed by E. elaterium. Tomato grown after L. usitatissimum, H. sabdariffa, H. vulgare, T. foenum-graecum, C. annuum and C. cyminum showed lower growth than its average growth in parasite-free control but parasite infestation was significantly reduced compared with parasite-infested control. Tomato grown after other reported tarp spe­ cies showed relatively moderate growth compared with that in parasitefree control but parasite infestation was higher or similar to parasiteinfested control. These included A. graveolens, C. vulgaris, C. sativus, C. sativum, C. moschata, P. anisum, S. indicum, S. oleracea and S. vulgare. However, in such studies parasite-host specificity or preference must be taken into account. Trap species for certain parasite may be infected by other species of the same parasite. Conditions under the work was done is another factor must be also considered. Orobanche and plant species tested are not all of similar growth requirements at different growing periods. Overlapping in the effect of trap and certain unsuitable catch 82

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species in their effects on parasite infestation to host species grown after these is possible. Some catch species may affect the parasite better than traps and vice versa. However, there is a high level of contradiction in literature on species regarded as traps for different Orobanche species at which some were actually infected by the same or different parasite species although infestation level was generally low, while certain trap species may reduce parasite infestation and growth of host crop.

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