https://orcid.org/0000-0002-4707-0618
Figures
Abstract
Orobanche spp. are root parasitic plants that cause yield losses in faba bean (Vicia faba L.). In Tunisia, O. crenata and O. foetida are among the major problems limiting faba bean production and productivity. Breeding for resistance and development of resistant varieties remain the most efficient control strategy to combat these parasites. In our study, field trials were conducted over two consecutive cropping seasons. A set of 42 genotypes were used in this study; 39 advanced lines and three checks; Najeh and Baraca (resistant) and Badi (susceptible). The trials were conducted in highly infested O. foetida plot at Oued-Beja Research Station in Tunisia. Results showed that advanced lines XAR-VF00.13-1-2-1-2-1 and XBJ90.04-2-3-1-1-1-2A expressed high resistance level exceeding those recorded for resistance checks Najeh and Baraca. O. foetida significantly affected the biomass, grain yield, chlorophyll content index (CCI) and the maximum quantum efficiency (Fv/Fm ratio). No significant effect was observed on host plant water content (WC). CCI decreases varied from 46.4% for the susceptible check Badi and 4.2% and 9.3%, respectively, for Baraca and XBJ90.04-2-3-1-1-1-2A. Orobanche parasitism resulted in a slight decreases of Fv/Fm ratio for the advanced lines XBJ90.04-2-3-1-1-1-2A and XAR-VF00.13-1-2-1-2-1 against important decreases observed for Badi and Baraca. Correlation between resistance to O. foetida and CCI and Fv/Fm makes this, easy-to-measure, parameter very useful as a practical screening tool for early parasitism detection, diagnosis and identification and selection of high resistant plants against this parasite.
Citation: Amri M, Abbes Z, Trabelsi I, Ghanem ME, Mentag R, Kharrat M (2021) Chlorophyll content and fluorescence as physiological parameters for monitoring Orobanche foetida Poir. infection in faba bean. PLoS ONE 16(5): e0241527. https://doi.org/10.1371/journal.pone.0241527
Editor: Walid Elfalleh, Higher Institute of Applied Sciences and Technology of Gabes University of Gabes, TUNISIA
Received: October 14, 2020; Accepted: April 30, 2021; Published: May 25, 2021
Copyright: © 2021 Amri et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All the data are listed in this paper. The row data underlying the results presented in the study are the property of the National Institute of Agricultural Research of Tunisia (INRAT) - Field Crop Laboratory. These data are part of a another database (multiyear + multilocation data) that will be used in other publications under preparation. The data underlying this study are available upon request. Contact: National Institute for Agricultural Research of Tunisia (INRAT) Address: Rue Hédi Karray, CP : 1004 Menzah 1 - Tunisia Tel : +216 71 23 00 24 / 71 23 02 39 Fax : +216 71 71 65 37 E-mail: [email protected] website: http://www.inrat.agrinet.tn/index.php/fr/.
Funding: This work was supported by the Tunisian Ministry of Agriculture, Hydraulic Resources and Fishery and Ministry of Higher Education and Scientific Research.
Competing interests: The authors have declared that no competing interests exist.
Introduction
Broomrapes (Orobanche spp.) are holoparasitic plants completely dependent on the host for their nutritional requirements. In the Mediterranean region, where broomrapes are considered as a serious threat, they cause important damages and yield losses on many legume crops [1–3]. In Tunisia, O. foetida, O. crenata, O. cumana, and Phelipanche ramosa are parasitizing many crops such as faba bean, chickpea, lentil, grass pea and sunflower [4, 5]. While O. crenata was mentioned as a serious pest for decades, O. foetida has been presented as an emerging problem for many legume crops such as faba bean, chickpea, lentil, grass pea, medick, common and narbon vetch [4, 6, 7]. The Orobanche infested area in Tunisia is estimated to more than 80,000 ha mostly situated in the main grain legumes production area (unpublished data, authors’ own estimates). In high infested fields, farmers abandoned planting legumes especially faba bean and switched to non-host crops such as wheat leading to a strict wheat mono-cropping system. The devastating effect of Orobanche is associated with their multiplication rate and high seed viability (15–20 years) [8]. Many control methods were used to control Orobanche, including agricultural practices, chemical and biological methods [9, 11, 14]. The chemical method using especially synthetic strigolactones and herbicides were the most explored but resulted in a limited success due to their application complexity in the farmer’s field [8]. Till date, no single control method has shown successful with full control of the parasite. All control strategies resulted in an incomplete protection of the crop [9–11]. To date, the only effective method is through an integrated management strategy with genetic resistance as a main component. Farmers should use resistant varieties, avoid planting contaminated seeds and follow preventive practices to limit the spread of the parasite to new fields [12]. While avoidance of broomrape dispersal is virtually difficult, crop resistance and prevention measures could be the most effective and economical methods to reduce this root parasitic weed infestations. Genetic resistance coupled with other control methods resulted someway in good control of the parasite with significant decreases of the damages. At this level, research is needed for generating new technologies and developing new resistant varieties and effective screening tools. Many resistance mechanisms were studied focusing mainly on the physical and biochemical host-parasite interface such as low production of Orobanche seed germination stimulants and/or release of inhibitors by the host root system [2, 13, 14], the existence of a host plant roots physical barrier resulting in unsuccessful haustorial penetration and necrosis [15] and the development of a deep root system that escape Orobanche infestation [16, 17]. In addition, an integrated control strategy could be improved through early detection and monitoring of the underground infestation and the parasite development. Rousseau et al. [18], mentioned that plant infestation by root parasitic weeds has a systemic impact that could be observed on host leaves. In this regard, chlorophyll fluorescence, which is a non-destructive and rapid assessing tool of photochemical quantum yield and photoinhibition, could be used for early Orobanche infestation and estimate its impact on the host plant. It is widely used as a plant response indicator under biotic and abiotic constraints such as heat, drought, waterlogging, salt stress, nitrogen deficiency, pathogen infection and herbicide resistance [19–21]. However, only few studies were conducted on parasitism effect on host plant chlorophyll fluorescence [22–24]. As reported by Maxwell and Johnson [25], the photochemical processes alterations are usually the first signs in the stressed plant leaves that could be used to estimate photosynthetic performance under stress conditions. These photochemical processes alterations appear in the chlorophyll fluorescence kinetics and induce changes in the established fluorescence parameters and consequently PSII damages. Cameron et al. [26], reported that the parasitic plant Rhinanthus minor significantly reduced biomass production in Phleum bertolinii and demonstrated that such decrease was reflected by changes in photosynthetic activities and significant reductions in the quantum efficiency of PSII and chlorophyll concentration.
In this paper we aim to evaluate the performances of faba bean advanced lines collection under O. foetida infested conditions and assess the impact of the parasite on plant growth and seed yield in correlation with physiological behavior using chlorophyll content and chlorophyll fluorescence parameters.
Material and methods
Plant material and field trials
Genotypes evaluation and screening for resistance to O. foetida.
A set of 39 small-seeded faba bean advanced lines, developed from crosses performed in Tunisia (Table 1), were used for a first-year (2009/2010) screening and evaluation for resistance to O. foetida. Three checks were added to the list, two Tunisian varieties Badi and Najeh and a Spanish variety Baraca. Both varieties Najeh and Baraca, carrying partial resistance to O. foetida and O. crenata [1, 27] were used as resistance check while Badi was used as susceptible check. The screening was performed under high O. foetida infested sick plot at Oued-Beja Research Station—Tunisia (36°44’N; 9°13’E). The trial was conducted in a randomized complete block design with three replications. Each genotype was planted, at a density of 24 seeds per m2, in four rows of 4 m length and 50 cm inter-rows spacing. The planting was performed the last week of November. No fertilizer’s supply or herbicide treatments were applied after plant emergence, only hand weeding was carried out keeping only faba bean plants and emerged Orobanche shoots.
Confirmation of the resistance and assessment of the parasitism impact.
Out of the total tested collection, the two best resistant genotypes XAR-VF00.13-1-2-1-2-1 and XBJ90.04-2-3-1-1-1-2A were selected all with the three checks to conduct the second-year (2010/2011) evaluation and confirmation trials. These genotypes were selected not only based on the cropping season (2009/2010) but also from preliminary data and observations recorded during previous cropping seasons (data not shown). The five genotypes were planted the last week of November in both infested and free Orobanche fields. Both trials were conducted same as described in the first-year screening.
For both cropping seasons, monthly rainfall and average temperature distribution for the two cropping seasons collected from the iMETOS meteorological station (Pessl instruments) are presented in the Table 2.
Measurements
The field evaluation of the studied genotypes and assessment of their resistance level to O. foetida was evaluated through different parameters measured at different crop development stages.
During the first-year screening, data related to Parasitism Index (PI), number of emerged Orobanche shoots (EOS) per faba bean plant and seed yield (SY) (g.m-2) were recorded at harvesting time on the two central rows.
- OIN: Orobanche incidence or percentage of plants showing at least on Orobanche emerged shoot
- OSV: Orobanche severity (1–9 scale) or level of damage caused by Orobanche on the host plant development and seed production [28].
During the second-year evaluation, in addition to OIN, OSV, PI, EOS and SY mentioned above, the number of days to Orobanche emergence (NDOE) and total emerged Orobanche number per plant were also recorded. At pod-setting stage and from both infested and non-infested fields, five random faba bean plants from each plot were carefully dug-up with all Orobanche attachments. For each single plant the biomass and water content (WC) were recorded and Orobanche attachments (TON) were classified into emerged and non-emerged attachments.
Chlorophyll content index (CCI) and the maximum quantum efficiency (Fv/Fm ratio) measurements were recorded once a week between 10 am and 1 pm from 123 to 144 days after planting (DAP) in both infested and non-infested fields. The two parameters were recorded on leaves from the 11th main stem node of random faba bean plants. CCI was measured on five random faba bean plants per plot using an CL-01 Chlorophyll Content Meter (Hansatech Instruments Ltd, UK). For every measurement almost the same part of the leaf was placed between two clips and the CCI was determined in dual wavelength optical absorbance (620 and 940 nm). Fv/Fm ratio measurements were performed on two random faba bean plants from the two central rows using a Plant Efficiency Analyzer (Handy-PEA, Hansatech instruments Ltd, P02.002 v.). For each plant, almost the same part/point of the leaflet was delimited by measure clip and was maintained in dark during 16 min by closing the clip shutter. Dark adaptation time was required to obtain a steady state value of the ratio of variable to maximum fluorescence. After 16 min, chlorophyll fluorescence transients were induced by a red light of 1500 μmol.m-2.s-1 intensity.
Plant sampling, biomass, WC, CCI and the Fv/Fm ratio measurements were performed only during second cropping season (2010/2011).
Results
Field evaluation and identification of potential resistance genotypes to O. foetida
Results showed high variability in the resistance to O. foetida between the genotypes. Significant differences were observed for the EOS, PI and SY (Fig 1). Based on PI, almost 46% of the tested genotypes showed a resistance level higher than the resistant check Najeh. The two advanced lines XBJ90.04-2-3-1-1-1-2A and XAR-VF00.13-1-2-1-2-1 expressed a high resistance level to O. foetida with respective PI of 1.2 and 2.2. Both genotypes showed low Orobanche infestation level with only 0.9 and 1.4 EOS, respectively. Such resistance observed for these two genotypes was reflected by a high seed yield with 154.2 g.m-2 and 257 g.m-2 respectively. They produced almost two (1.8) and three (2.9) times more than the resistant check Najeh. High negative correlation between SY and both EOS (r = - 0.636, P ≤ 0.001) and PI (r = - 0.770, P ≤ 0.001) was observed.
Confirmation of the resistance under infested and non-infested field conditions
Results generated from the second-year evaluation showed high differences (P ≤ 0.01) between the five studied genotypes for OIN, OSV, DOE, TON, and EOS. High OIN was observed for the two cultivars Badi and Baraca with 81.7% and 85%, respectively (Table 3) against moderate to low OIN observed for Najeh (65%), XAR-VF00.13-1-2-1-2-1 (60%) and XBJ90.04-2-3-1-1-1-2A (40%). Maximum infestation was observed for the susceptible genotype Badi with 5 attachments per plant against only 1.2, 1.3 and 1.9 attachments observed for Najeh, XAR-VF00.13-1-2-1-2-1 and XBJ90.04-2-3-1-1-1-2A (Fig 2). At crop maturity (early June), EOS varied from 0.9 observed for XBJ90.04-2-3-1-1-1-2A to 2.7 recorded for Badi (Table 3). Only, 1.2, 1.4 and 2.6 shoots per plant were recorded respectively for Najeh, XAR-VF00.13-1-2-1-2-1 and Baraca. The NDOE varied from 133 days for the susceptible check cv. Badi to 145 days recorded for XBJ90.04-2-3-1-1-1-2A (Table 3). Compared to Badi, delay of 2.7, 4, 4.3 and 11.7 days were observed for NDOE for the genotypes XAR-VF00.13-1-2-1-2-1, Baraca, Najeh and XBJ90.04-2-3-1-1-1-2A, respectively. Orobanche severity varied from a minimum of 3 for XBJ90.04-2-3-1-1-1-2A to a maximum of 6.3 for Badi (Table 3). Such infestation levels resulted in a significant negative parasitism impact on plant growth and seed production for different tested genotypes.
Orobanche parasitism effect on biomass and seed yield.
Compared to non-infested field, results showed that O. foetida has significantly affected the host plant biomass (P ≤ 0.01) for all the genotypes (Table 4). A maximum decrease of biomass production (68.5%) was observed for the susceptible check Badi against only 15.6% recorded for Najeh. Respective decreases of 31%, 22.5% and 21.2% were recorded for Baraca, XAR-VF00.13-1-2-1-2-1 and XBJ90.04-2-3-1-1-1-2A (Table 4). For all tested genotypes, Orobanche parasitism has significantly affected the host plant biomass production but with no significant effect on the water content. No decreases in WC were observed between infected and non-infected plants (Table 4).
Orobanche parasitism effect on the host plant development resulted in significant seed yield losses for all the studied genotypes (Fig 3). Compared to free Orobanche plants, seed yield decreases varied from 3.9% recorded for XBJ90.04-2-3-1-1-1-2A to 93.9% observed for the susceptible check Badi. Respective decreases of 77.4%, 39.5% and 28.8% were observed for Baraca, Najeh and XAR-VF00.13-1-2-1-2-1. Among all the tested genotypes, XAR-VF00.13-1-2-1-2-1 was the most productive under O. foetida infested conditions with 228.4 g.m-2 representing 3 and 4 times the seed yield recorded for the resistant checks Najeh (78.3 g.m-2) and Baraca (53.8 g.m-2). For cv. Baraca which is reported to be resistant to O. crenata, SY varied from 237.8 g.m-2 to 53.8 g.m-2 (77.4% less) under free and Orobanche infested fields, respectively.
Chlorophyll content index and chlorophyll fluorescence.
Orobanche parasitism significantly affected (P ≤ 0.01) the host plant chlorophyll content index (CCI) and Fv/Fm ratio for all the studied genotypes (Figs 4 and 5). All genotypes showed significant difference between infected and non-infected plants before Orobanche emergence. Between 125 and 146 DAP, CCI decreases under O. foetida infestation varied from 23.6% for Baraca to 77.2% recorded for Badi. Respective decreases of 19.4% and 30.8% were recorded for the same genotypes under free Orobanche field. Clear differences were observed for the CCI between infected and free Orobanche plants. Such differences were more pronounced for the susceptible check Badi. Variation between 125 and 146 DAP, varied from 4.2% for Baraca to 46.4% observed for Badi.
Fv/Fm ratio was significantly affected by Orobanche parasitism (Fig 5). In infected plants Fv/Fm decreased by 58.8% (0.789 to 0.325) for the susceptible check Badi against only 9.9% (0.787 to 0.709) observed for free Orobanche plants. Decreases of 46.2%, 14.5%, 5.9% and 4.7% were recorded, respectively, for Baraca, Najeh, XAR-VF00.13-1-2-1-2-1 and XBJ90.04-2-3-1-1-1-2A. Except for the susceptible check Badi, all other genotypes showed significant differences in Fv/Fm between infected and free Orobanche plants before Orobanche emergence (Fig 5). High decreases of Fv/Fm ratio were observed for Badi and Baraca after 139 DAP against only slight decreases recorded for Najeh and both selected advanced lines XAR-VF00.13-1-2-1-2-1 and XBJ90.04-2-3-1-1-1-2A. At 146 DAP, comparison of Fv/Fm ratio between infected and free Orobanche plants showed differences of 54.2% (0.709 vs 0.325), 39.3% (0.702 vs 0.426) and 16.5% (0.802 vs 0.670) recorded for Badi, Baraca and Najeh, respectively, against only 6.4% (0.804 vs 0.753) for XBJ90.04-2-3-1-1-1-2A and 9.5% (0.781 vs 0.707) for XAR-VF00.13-1-2-1-2-1.
Discussion
Results from the first-year screening showed high variability for the resistance to O. foetida in the tested collection. Resistance to broomrapes is not only the capacity of the genotype to limit the parasite development and the damages that causes, but also the capacity of that same genotype to grow and produce grains under such parasitism attack. Two advanced lines, XBJ90.04-2-3-1-1-1-2A and XAR-VF00.13-1-2-1-2-1 were identified and selected for their high resistance level and good SY under high O. foetida infestion. Both genotypes showed a low infestation level compared to resistant and susceptible checks. Previous studies showed that Orobanche causes early wilting symptoms in parasitized plants and results in a shortening of the reproductive phase and affecting significantly the flowering, pod setting, plant biomass and seed production [13, 16, 28]. Such effects were highly pronounced for cv. Badi, for which O. foetida has severely restrained plant growth, and resulted in almost complete damage and yield losses. Moderate effect of the parasite on plant development and seed production was observed for both selected advanced lines XAR-VF00.13-1-2-1-2-1 and XBJ90.04-2-3-1-1-1-2A. Results also showed that despite the biomass decreases recorded for different studied genotypes, no significant effect of Orobanche parasitism was observed on the host plant’s WC. Indeed, due to the parasitic burden and resources sinking the host plant has limited its biomass and dry matter production and allocation in order to keep its physiological functioning through a normal and optimum water content. It was also reported that Orobanche parasitism effects on host plant growth and biomass production and allocation are directly associated with the infestation level [2, 9, 10]. Ennami et al., [29] reported a high negative correlation between both faba bean and lentil plant’s growth and O. crenata development attributing that to the competition between the host and the parasite for nutrients. Other previous studies reported that the detrimental effect of both O. foetida and O. crenata on faba bean grain yield can reach up to 90–100% depending on the infestation severity and the broomrape-crop association [30, 31]. In addition, our results showed significant differences in CCI between infected and noninfected plants for the five tested genotypes, even before Orobanche emergence. These results indicate that this parameter could be very useful for early detection of the underground Orobanche infestation. In fact, several studies reported the importance of the number of host leaves and their greenness in plant eco-physiological studies because they provide information about physiological responses of plants under stress conditions [32, 33]. Decreases in CCI that were observed in parasitized plants could be explained by the parasite nutritional requirements that limits the normal growth and functioning of the host plant. Similar results were reported for tomato/P. ramosa pathotype [34, 35]. Shamsullah et al. [35], found that, compared to noninfected plants, P. ramosa decreased chlorophyll content in tomato leaves by 29.17%. Shen et al., [23] reported also similar results with Mikania micrantha/Cuscuta campestris and showed, also, that despite the CCI decrease observed on the M. micrantha leaves, there was no significant effects of C. campestris parasitism on chlorophyll a:b ratio. In our study, CCI decreases were associated with photosynthetic characteristics variation in the host plant leaves. O. foetida affected the photosynthetic system through significant decreases of the leaves CCI and Fv/Fm ratio which was increasingly pronounced over time, especially for the susceptible check Badi. For all the genotypes, O. foetida parasitism significant decreased Fv/Fm ratio after 146 DAP. compared to non-infected plants. Before Orobanche emergence, only resistant genotypes showed significant difference in Fv/Fm between infected and free Orobanche plant. Despite Orobanche parasitism effect, the two genotypes XAR-VF00.13-1-2-1-2-1 and XBJ90.04-2-3-1-1-1-2A were able to maintain a normal functioning of their PSII to the same level as the free-Orobanche plants even after Orobanche emergence. This was not the case for the susceptible check Badi. These results along with the chlorophyll fluorescence analyses indicated that Fv/Fm could be used not only for the quantification of stress caused by Orobanche parasitism and early detection of the underground infestation but also the screening and identification of high resistant genotypes. Similar results were reported by Mauromicale et al. [34] who showed that Fv/Fm, which is proportional to the PS II quantum yield and well correlated with the photosynthesis quantum yield [36], was significantly decreased by P. ramosa attack on tomato plants. In the same study, the authors demonstrated that the Fv/Fm reduction is mainly induced by an effect on the variable fluorescence (Fv) resulting in PS II electron transport damage. Similarly, Rousseau et al. [18], reported that Fv/Fm in Arabidopsis thaliana leaves was impacted by P. ramosa. Also, other studies showed that C. reflexa induced a sink-dependent stimulation of net photosynthesis on Ricinus communis [37] and that such infestation by C. campestris decreases host stomatal conductance, transpiration, chlorophyll content, and soluble protein concentration on M. micrantha [23]. These results are contrasting with other studies [38, 39] who reported that broomrape affects host biomass and yield and related traits with only minor disturbance in host’s leaves tissue but no perceptible effects on photosynthetic rate. More recently, Ennami et al. [29] showed that effective quantum yield of open photosystem II, (Fm’-F)/Fm’, was significantly reduced by O. crenata attack on susceptible faba bean and lentil genotypes. The effects caused cause by the parasitic weeds on the different parameters may directly or/and indirectly affect the functioning of the photosynthetic system and rate and therefore affect the growth of the host plant.
Conclusions
O. foetida can affect faba bean host plants in/through different ways and at a big range of scales, from the root to the leaves through the whole plant. Out of the initially larger tested faba bean collection, the two genotypes XAR-VF00.13-1-2-1-2-1 and XBJ90.04-2-3-1-1-1-2A expressed the highest resistance level to O. foetida and showed a moderate and limited effects of the parasite on plant development and seed production. For both genotypes, the high resistant level was reflected by limited effects of the parasite on plant growth, biomass production, seed yield and physiological functioning of the host plants. Significant variations in CCI and Fv/Fm were observed from individual plants between the tested genotypes and between infected and noninfected plants. The significant positive correlation observed between CCI, Fv/Fm and high resistance level to Orobanche may suggest the integration of these physiological traits in plant selection and screening for resistance to broomrapes. These practical screening tools could be coupled with other new smart imaging technologies for early detection of the root parasitic weeds infestation.
Acknowledgments
The authors are thankful to all the field crop laboratory’s technical staff for their assistance, particularly Leila Dakhli, Fadhel Sellami, Hadhemi Abidli, Besma Soltani and Olfa Mlayeh.
References
- 1. Kharrat M, Abbes Z, Amri M. A new faba bean small seeded variety “Najeh” tolerant to Orobanche registered in the Tunisian catalogue. Tunisian Journal of Plant Protection. 2010; 5: 125–130.
- 2. Abbes Z, Sellami F, Amri M, Kharrat M. Variation in the resistance of some faba bean genotypes to Orobanche crenata. Pak. J. Bot. 2011; 43(4): 2017–2021.
- 3. Ennami M, Briache FZ, Gaboun F, Abdelwahd R, Ghaouti L, Belqadi L, et al. Genetic diversity of Moroccan Orobanche crenata populations revealed by sequence-related amplified polymorphism markers. The Journal of Agricultural Science. 2017; 9(4):164–175
- 4.
Kharrat M. Etude de la virulence de l’écotype de Beja d’Orobanche foetida sur différentes espèces de légumineuses. In: Proceedings of the 2nd seminar of REMAFEVE/REMALA Network, pp. 89, 2002; Hammamet, Tunisia.
- 5. Amri M, Abbes Z, Bouhadida M, Kharrat M. First Report of the Parasitic Plant Phelipanche ramosa on berseem clover (Trifolium alexandrium L.) in Tunisia. Tunisian Journal of Plant Protection. 2013; 8(2): 127–132.
- 6.
Millan T, Madrid E, Cubero JI, Amri M, Castro P, Robio J. Chickpea in: Antonio , DeRon M, (ed.) Grain Legumes, Series Handbook of Plant Breeding. Springer Science+Business Media, New York. 2015; 10: pp 499.
- 7. Nefzi F, Trabelsi I, Amri M, Triki E, Kharrat M, Abbes Z. Response of some chickpea (Cicer arietinum L.) genotypes to Orobanche foetida Poir. Parasitism. Chilean Journal of Agricultural Research. 2016; 76(2): 270–278.
- 8. Habimana SA, Nduwumuremyi JD, Chinama R. Management of Orobanche in field crops- A review. Journal of Soil Science and Plant Nutrition. 2014; 14(1): 43–62.
- 9. Abbes Z, Sellami F, Amri M, Kharrat M. Effect of sowing date on Orobanche foetida infection and seed yield of resistant and susceptible faba bean cultivars. Acta Phytopathologica et Entomologica Hungarica. 2010; 45(2): 267–275.
- 10. Amri M, Trabelsi I, Abbes Z, Kharrat M. Release of a new faba bean variety "Chourouk" resistant to the parasitic plants Orobanche foetida and O. crenata in Tunisia. Intl. J. Agric. Biol. 2019; 21(3): 499‒505
- 11. Briache FZ, Ennami M, Mbasani-Mansi J, Lozzi A, Abousalim A, El Rodeny W, et al. Effects of salicylic acid and indole acetic acid exogenous applications on induction of faba bean resistance against Orobanche crenata. The plant pathology journal. 2020; 36(5): 476–490. pmid:33082732
- 12.
Abu-Irmaileh BE, Labrada R. The problem of Orobanche spp. in Africa and Near East. FAO, 2017; http://www.fao.org/agriculture/crops/thematic-sitemap/theme/biodiversity/weeds/issues/oro/en/
- 13. Trabelsi I, Abbes Z, Amri M, Kharrat M. Performance of faba bean genotypes with Orobanche foetida and Orobanche crenata infestation in Tunisia. Chilean Journal of Agricultural Research. 2015; 75 (01): 27–34.
- 14. Trabelsi I, Yoneyama K, Abbes Z, Xie X, Amri M, Kharrat M. et al. Characterization of strigolactones produced by Orobanche foetida and Orobanche crenata resistant and -susceptible faba bean genotypes and effect of phosphorous, nitrogen, and potassium deficiencies on strigolactone production. South Africain Journal of Botany. 2017; 108: 15–22.
- 15. Perez-De-Luque A, Rubiales D, Cubero JI, Press MC, Scholes J, Yoneyama K, et al. Interaction between Orobanche crenata and its host legumes: unsuccessful haustorial penetration and necrosis of the developing parasite. Annals of Botany. 2005; 95: 935–942. pmid:15749751
- 16. Briache FZ, Ennami M, Mansi JM, Gaboun F, AbdelWahd R, Fatimi ZA, et al. Field and controlled conditions screenings of faba bean genotypes for resistance to Orobanche crenata Forsk. and investigation of resistance mechanisms. J. Plant Dis. Prot. 2019; 126(3): 211–224
- 17. Abbes Z, Kharrat M, Simier S, Chaïbi W. Characterization of resistance to crenate broomrape (Orobanche crenata) in a new small-seeded line of Tunisian faba beans. Phytoprotection. 2007; 88: 83–92.
- 18. Rousseau C, Hunault G, Gaillard S, Bourbeillon J, Montiel G, et al. Phenoplant: A web resource for the exploration of large chlorophyll fluorescence image datasets. Plant Methods, BioMed Central, 2015; 11(24): 1–12 pmid:25866549
- 19. Korres NE, Froud-Williams RJ, Moss SR. Chlorophyll fluorescence technique as a rapid diagnostic test of the effects of the photosynthetic inhibitor chlorotoluron on two winter wheat cultivars. Annals of Applied Biology. 2003; 143(1): 53–56.
- 20. Pavlovic D, Vrbnicanin S, Bozic D, Fischer AJ. Morpho-physiological traits and atrazine sensitivity in Chenopodium album L. Pest Management Science. 2008; 64(2): 101–107. pmid:18022828
- 21. Amri M, El-Ouni MH, Ben Salem M. Waterlogging affect the development, yield and components, chlorophyll content and chlorophyll fluorescence of six bread wheat genotypes (Triticum aestivum l.). Bulg. J. Agric. Sci. 2014; 20(3): 647–657.
- 22. Cameron DD, Hwangbo JK, Keitha M, Geniez JM, Kraushaardar D, Rowntree J, et al. Interactions between the hemiparasitic angiosperm Rhinanthus minor and its hosts: from the cell to the ecosystem. Folia Geobotanica. 2005; 40: 217–229.
- 23. Shen H, Hong L, Chen H, Ye WH, Cao HL, Wang ZM. The response of the invasive weed Mikania micrantha to infection density of the obligate parasite Cuscuta Campestris and its implications for biological control of M. micrantha. Botanical Studies 2011; 52: 89–97.
- 24.
Walters DR. Photosynthesis in Attacked Plants and Crops. In: Physiological Responses of Plants to Attack. Crop & Soil Systems Research Group SRUC Edinburgh, (Eds Walters D.R.), pp. 248. 2015; Wiley-Blackwell, UK
- 25. Maxwell K, Johnson GN. Chlorophyll fluorescence—A practical guide. Journal of Experimental Botany. 2000; 51(345): 659–668. pmid:10938857
- 26. Cameron DD, Geniez JW, Seel LJ, Irving IJ. Suppression of host photosynthesis by the parasitic plant Rhinanthus minor. Annals of Botany. 2008; 101: 573–578. pmid:18211886
- 27. Nadal S, Moreno JI, Cubero MT. Registration of ‘Baraca’ Faba Bean. Crop Science. 2004; 44(5).
- 28. Abbes Z, Kharrat M, Delavault P, Simier P, Chaibi W. Field evaluation of the resistance of some faba bean (Vicia faba L.) genotypes to the parasitic weed Orobanche foetida Poiret. Crop Protection. 2007; 26: 1777–1784.
- 29. Ennami M, Mansi MJ, Briache FZ, Oussible N, Gaboun F, Ghaouti L, et al. Growth-defense tradeoffs and source-sink relation explain the responses of susceptible and resistant faba bean and lentil genotypes to infection by Orobanche crenata. J. of Crop protection. 2020; 127:
- 30.
Kharrat M, Souissi T. Research on Orobanche foetida and O. crenata in Tunisia. In: Integrated management of orobanche in food legumes in the Near East and North Africa., Proceedings of the expert consultation on IPM for Orobanche in Food Legume Systems in the Near East and North Africa, (Eds Dahan R., El Mourid M.), 2004; 106–110.
- 31. Trabelsi I, Abbes Z, Amri M, Kharrat M. Study of some resistance mechanisms to Orobanche spp. infestation in faba bean (Vicia faba L.) breeding lines in Tunisia. Plant Production Science. 2016; 19(4): 562–573
- 32. Yordanov I, Velikova V, Tsonev T. Plant responses to drought, acclimation, and stress tolerance. Photosynthetica. 2000; 38: 171–186.
- 33. Valladares F, Niinemets U. Shade tolerance, a key plant feature of complex nature and consequences. Annu. Rev. Ecol. Evol. Syst. 2008; 39: 237–257.
- 34. Mauromicale G, Monaco AL, Longo AMG. Effect of Branched Broomrape (Orobanche ramosa) Infection on the Growth and Photosynthesis of Tomato. Weed Science. 2008; 56: 574–581.
- 35. Shamsullah SKL, Panezai MA, Mengal MA, Kakar SR, Saeed S, Ahmed A. Parasitic effects of broomrape (Orobanche spp.) on growth, yield and quality of tomato and its economic loss in agroecological conditions of Khanozai (Karezat Region) District Pishin, Balochistan, Pakistan. International Journal of Biosciences. 2019; 15(6): 126–136.
- 36. Butler WL, Kitajima M. Fluorescence quenching in photosystem II of chloroplasts. Biochim Biophys Acta. 1975; 376(1):116–25. pmid:1125216
- 37. Jeschke WD, Hilpert A. Sink-stimulated photosynthesis and sink dependent increase in nitrate uptake: nitrogen and carbon relations of the parasitic association Cuscuta reflexa-Ricinus communis. Plant, Cell and Environment. 1997; 20: 47–56.
- 38. Dale H, Press MC. Elevated atmospheric CO2 influences the interaction between the parasitic angiosperm Orobanche minor and its host Trifolium repens. New Phytol. 1998; 140: 65–73.
- 39. Hibberd JM, Quick WP, Press MC, Scholes JD. Can source–sink relations explain responses of tobacco to infection by the root holoparasitic angiosperm Orobanche cernua? Plant, Cell and Environment. 1998; 21: 333–340.