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Crenate broomrape (Orobanche crenata) infection in field pea cultivars
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Crop Protection 22 (2003) 865–872
Crenate broomrape (Orobanche crenata) infection in field pea cultivars D. Rubialesa,*, A. Pe! rez-de-Luqueb, J.I. Cuberob, J.C. Silleroc a
! CSIC, Instituto de Agricultura Sostenible, Apdo. 4084, E-14080 Cordoba, Spain b ! ETSIAM-UCO, Dep. Gen!etica, Apdo. 3048, E-14080 Cordoba, Spain c ! CIFA, Dep. Mejora y Agronom!ıa, Apdo. 3092, E-14080 Cordoba, Spain
Received 20 February 2003; received in revised form 21 February 2003; accepted 1 March 2003
Abstract Orobanche crenata is a major constraint for winter pea production in Mediterranean and East Asian countries. Screening for resistance performed under field conditions in 20 field pea cultivars showed that very low levels of genetic resistance were available. The resistance proved to be highly influenced by environmental conditions and needs to be supplemented with other control measures. Infection is greatly reduced in later sowing being highest in plots sown by October–December, and much reduced in plots sown by January–February. Imazethapyr applied pre- and post-emergence of the late crop sowings significantly reduced the infection and increased yield. r 2003 Elsevier Science Ltd. All rights reserved. Keywords: Broomrape; Chemical control; Genetic resistance; Orobanche crenata; Pea; Pisum sativum; prometryn; Imazethapyr
1. Introduction Orobanche infestations can be devastating to crops and remove otherwise productive land from effective use for very long periods of time. Crenate broomrape (Orobanche crenata) is well known as a major constraint for faba bean, vetches and lentil, being of importance also on other grain and forage legumes. Although pea was known to be a suitable host, there has been little concern on broomrape incidence on the pea crop. However, there are recent reports of severe damage on pea in Southern Spain (Garc!ıa-Torres et al., 1996; Rubiales et al., 1999), Morocco (Mabsoute and Saadaoui, 1996), Egypt (Korashi et al., 1996) and Israel (Bernhard et al., 1998), being at present acknowledged as the major constraint for pea cultivation in the Mediterranean area and Middle East. The problem of broomrape in this area is dramatic due to its broad distribution, the long survival of the seed-bank in the soil and the extreme susceptibility of the cultivars available to the farmer. Yield loss can be huge, as high
*Corresponding author. Tel.: +34-957499215; fax: +34-957499252. E-mail address: [email protected] (D. Rubiales).
as 80% (Korashi et al., 1996) or even 100% (Bernhard et al., 1998). There is a risk for O. crenata spread to other areas with similar weather conditions, as happened with O. cumana that quickly spread in south-eastern Europe since the first reports at the beginning of the 20th century on sunflower in Russia, and reached Spain in the late 1970s (Melero-Vara, 1999). In a similar way, recent introductions of O. ramosa in Australia (Carter et al., 1996) and Chile (D!ıaz and Norambuena, 2001) and of O. minor in USA (Osterbauer and Rehms, 2002) have been reported. The consequences of potential climate change are uncertain, but there exits a serious possibility that this could lead to more favourable conditions for O. crenata in more northern latitudes and thus pose serious threat to cool season food legume production as a whole. Some strategies of broomrape control have been developed, from cultural practices to chemical control (Parker, 1991; Rubiales et al., 2003) but all without unequivocal success, being either not feasible, uneconomic, hard to achieve or resulting in incomplete protection. Breeding for resistance is still the most economical, feasible, and environmental-friendly method of control. Useful levels of resistance have been
0261-2194/03/$ - see front matter r 2003 Elsevier Science Ltd. All rights reserved. doi:10.1016/S0261-2194(03)00070-X
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found in several hosts against parasitic plants, like in sorghum against Striga hermonthica, cowpea against S. gesnerioides, sunflower against O. cumana, and faba bean, chickpea and vetch against O. crenata, among others (Cubero, 1991; Parker, 1991; Rubiales et al., 2002) but little is known on the levels of resistance to O. crenata available in pea. The purposes of the present study are to determine the level of resistance available in pea cultivars, to determine the effects of sowing date on broomrape establishment and development, and to assess the feasibility of combining the slight levels of resistance available with chemical control and delayed sowing dates.
2. Materials and methods In a first experiment 20 top commercial cultivars of pea were screened for broomrape resistance under field conditions in two locations across Andaluc!ıa (southern Spain) (Table 1) during the field seasons 1995–1996 and 1996–1997. Screenings were performed in plots in which high and uniform broomrape infestation was known from previous year observations. Each cultivar was represented by a double row 2 m long with four replications in a completely randomised design. The number of emerged broomrape shoots per host plant was determined at crop maturity by counting the number of broomrapes and pea plants in the rows. In a separate experiment the pea cultivars Messire and Ballet were studied for broomrape resistance under field conditions at different sowing dates during the field seasons 1996–1997, 1997–1998, 1998–1999 and 1999– 2000, at CIFA Alameda del Obispo experimental farm, ! Cordoba, Spain, which has a deep loam soil (Typic Xerofluvent). As faba bean is the best-studied host of O. crenata, the susceptible faba bean cultivar Prothabon was added as a reference. Each line was represented by a single 2 m row with 0.7 m of row spacing. Twenty plants were grown per row. Five sowings were made at 4 weeks intervals from middle October to middle February, with four replications per accession per sowing date. Broomrape infection was determined at crop maturity by counting the number of emerged broomrape shoots per host plant in the row. Additionally, in the plots sown in seasons 1998–1999 and 1999–2000, observations were made also on number of underground, non-emerged attachments at 20 days intervals from middle March to middle May. Three to five plants per row were carefully dug up from the soil to count the total number of broomrape establishments, either emerged or nonemerged. The number of established tubercles and their developmental stage were recorded according to ter Borg et al. (1994), where stage 1: tubercles smaller than 2 mm; 2: tubercles greater than 2 mm, without roots development; 3: tubercles with crown roots, without
Table 1 Number of emerged O. crenata shoots per host plant on 20 pea ! cultivars under field conditions at Cordoba and Mengibar, southern Spain Pea cultivar
Crop season 1995/1996 ! Cordoba
Messire Baroness Bacar!a Radley Rustic Renata Cambar Amadeus Esla Loto Solara Azur Jami Leo Cea Orb Brent Malta Spring Ballet
a
3.6 a 3.7 a 3.7 a 3.7 a 3.7 a 3.5 ab 3.3 ab 3.2 ab 3.2 ab 3.2 ab 3.1 ab 3.1 ab 3.1 ab 3.1 ab 3.0 ab 2.8 ab 2.3 b 2.3 b —b 1.3 c
1996/1997 Meng!ıbar
! Cordoba
Meng!ıbar
5.9 4.9 5.0 4.9 4.9 5.2 5.6 5.3 5.0 5.2 5.2 4.8 5.0 5.0 5.2 4.9 5.8 5.0 5.0 4.2
3.9 2.6 1.3 2.8 2.1 0.3 1.3 1.4 2.1 2.2 0.8 0.3 0.8 1.1 0.8 0.9 1.4 1.7 0.8 0.5
0.7 0.6 0.5 0.6 0.5 0.3 0.3 0.2 0.8 0.5 0.1 0.6 0.5 0.8 0.7 0.8 0.5 0.5 0.4 0.3
a cde cd cde cde bcd ab abc cd bcd bcd de cd cd bcd cde a cd cd e
a ab ab ab ab b ab ab ab ab b b b ab b ab ab ab b b
a a a a a a a a a a a a a a a a a a a a
a Data with the same letter per column are not significantly different (Po0:05; Duncan test). b —: not determined.
shoot formation; 4: shoot formation, remaining underground; 5: shoot emergence; 6: flowering; and 7: setting of seeds. A final count of emerged O. crenata plants per host plant was recorded at the end of the crop cycle on the remaining plants. The efficacy of imazethapyr on broomrape control on the pea cvs. Ballet and Messire was tested under field conditions at different sowing dates during the field season 2001–2002, at the same experimental farm. Five sowings were made at 2 weeks intervals from early November to middle January with four replications per accession per sowing date. Each treatment was represented by a 8 m2 plot at 0.7 m of row spacing. Standard crop pre-emergence treatment for weed control with prometryn was always applied. Treatments were: (1) control, only pre-emergence prometryn for weed control; (2) prometryn+imazethapyr (adjusted at 75 g ma/ ha) at crop pre-emergence; and (3) prometryn preemergence+imazethapyr (adjusted at 150 g ma/ha) postemergence. Broomrape infection was determined at crop maturity by counting the number of emerged broomrape shoots per host plant. Then the plots were harvested and seed yield (kg/ha) determined. The scores were angular transformed and an analysis of variance was carried out using the SPSS for windows version 10.0.
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3. Results High levels of infection were obtained during the season 1995–1996 on the 20 pea cultivars (Table 1) with an average of 3.1 and 5.1 emerged broomrapes per pea ! plant at Cordoba and Mengibar, respectively. The infection was much lower during the 1996–1997 season with averages of 1.5 and 0.5 broomrapes per plant at ! Cordoba and Mengibar, respectively. All cultivars were severely infected, but there were significant genotypic effects, with cv. Ballet, significantly less infected than cv. Messire in all instances but for the season 1996–1997 at Mengibar, where the level of infection was rather low and differences among cultivars were not significant. ANOVA (arcsin transformed data) showed significant differences in broomrape emergence among cultivars (Po0:05), among locations (Po0:001) and among years (Po0:001). There was a significant year location interaction (Po0:001), but not cultivar location and cultivar year. Differences in infection among years can be ascribed to varying climatic factors that are known to influence O. crenata infection. Weather conditions were very conducive for broomrape infection during the 1996– 1997 season due to a mild temperature (11–16 C average air temperature) and high rain (600 mm) in winter (Table 2), although the spring was rather dry. The season 1997–1998 was also conducive with a mild temperature (11–15 C) and a sufficiently rainy winter (270 mm). The spring was warm (15–20 C) although rainy (170 mm). The season 1998–1999 was not very conducive with a relatively cold (8–10 C) and dry winter (180 mm) as well as a dry spring (90 mm). The season 1999–2000 was moderate, with a moderate winter (10– 15 C and 120 mm) and a rainy spring (120 mm). Pea cvs. Ballet and Messire tended to display lower numbers of emerged broomrape shoots per plant than the faba bean check cv. Prothabon (Fig. 2); however, the differences were only significant in the earlier sowing dates. Ballet tended to display lower numbers of emerged broomrape shoots per plant than Messire, but differences were not significant. Both pea cvs. as well as the faba bean check were more heavily infected in the plots sown early (October—December) (Fig. 2). By then, broomrape infection, as determined by number of emerged broomrapes per host plant, decreased with sowing date, being this decrease in emergence more marked in the less favourable 1998–1999 season in which broomrape emergence did not occur in the plots sown in February. Infection on both faba bean and pea was very high in the plots sown in January during the season 1996–1997 and low in the remaining seasons. This heavy infection can be explained by the unusual heavy rain occurred in December 1996 and January 1997 and the milder temperatures of that season. Broomrape emergence was neither reduced the season
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Table 2 Effect on broomrape emergence and yield of different foliarly applied herbicide treatment on plots of pea (cvs. Messire and Ballet) sown at ! different sowing dates at Cordoba (2001–2002) Sowing date
Herbicide treatmenta
Number of emerged broomrape shoots per host plant
November 15
1 2 3 1 2 3 1 2 3 1 2 3 1 2 3
2.1 1.2 1.1 1.8 1.3 1.1 1.6 0.7 0.8 2.6 0.5 0.5 2.0 0.3 0.6
1 2 3
2.0 a 0.8 b 0.8 b
December 5
December 20
January 5
January 18
Overall
ab b b a ab b a b b a b b a c b
Host yield (kg/ha) 0a 0a 0a 0b 150 a 293 a 0b 214 a 500 a 485 b 1385 a 1477 a 563 b 1437 a 2123 a 210 b 637 a 879 a
a
Herbicide treatment: 1: control, only Gesagard applied at crop preemergence; 2: Pursuit applied at crop pre-emergence; and 3: Gesagard applied at crop pre-emergence and Pursuit at crop post-emergence. b Letters in common per column within a sowing date indicates that different treatment did not have a significant influence on broomrape infection or yield (Duncan test, Po0:05).
2001–2002 in the later sowing dates (Table 2). This might be explained by the fact that unusual rain occurred during March and April (Fig. 1) allowing emergence of established tubercles. The high infection in the earlier sowing dates resulted in a complete loss of yield (0 kg/ha) in the two pea cultivars (Table 2). In the later sowing dates, even when broomrape emergence was similarly high, untreated plants were able to yield around 600 kg/ha. Digging up and extracting whole plants to record the number of underground, non-emerged attachments allowed the observation of further differences among accessions that were not detectable when only the number of emerged broomrapes was considered. Most of the established parasites remained underground and did not emerge (Figs. 2 and 3). Pea plots shown in October were less infected than those sown in November and December. Infection decreased in plots sown in January and February. In the season 1998–1999 plots sown in January displayed little broomrape emergence, and those sown in February did not show any emergence at all, but infection was high as shown by the high number of underground non-emerged attachments. This tendency was observed in both pea cultivars and the faba bean check. In the 1999–2000 season, broomrape emergence was similar to that in the previous
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Fig. 1. Average air temperature ( Spain.
D. Rubiales et al. / Crop Protection 22 (2003) 865–872
! ) and rainfall ( ) during the seasons 1996–1997, 1997–1998, 1998–1999, 1999–2000, and 2001–2002 at Cordoba,
season, but the most favourable weather conditions (more rain during spring) allowed a higher emergence of established broomrape tubercles, and there was some emergence even in the plots sown in February. In the Messire plots sown in October there was already a substantial number of underground attachments (stages 1–4) and a minor amount of emerged broomrapes by March (Fig. 3). Few attachments were formed on cv. Ballet, none of which emerged. Underground infection increased markedly from March to April and little from April to May in which most emergence took place. Both pea cultivars followed a similar pattern, although infection remained lower in Ballet. In the plots sown in November there was also a substantial number of underground attachments (stages 1–4) but no emergence on Messire and Ballet by the
March scoring date. In the plots sown in October, underground infection increased markedly from March to April, and little from April to May in which most emergence took place. In the plots sown in December and January there was a substantial number of underground attachments (stages 1–4) but no emergence on Messire and Ballet by the April scoring date. From April underground infection did not increase and some emergence took place. In the plots sown in February there was some underground attachments but no emergence on Messire and Ballet by the April scoring date. Underground infection increased till May, but no emergence took place. Pre- and post-crop-emergence treatments with imazethapyr provided similar levels of protection against broomrape. There was no treatment cultivar
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Fig. 2. Number of broomrape (O. crenata) emerged shoots per host plant in pea cultivars Messire ( ) and Ballet (&) and the reference faba bean cv. ! Prothabon ( ) in field experiments at Cordoba at different sowing dates (from mid October till mid March) during the field seasons 1996–1997, 1997– 1998, 1998–1999 and 1999–2000. The same letters per host plant per season indicate that differences in broomrape emerge at the varying sowing dates were not statistically significant (Duncan, Po0:05).
interaction, and thus data of the two cultivars are presented together (Table 2). Reduction of broomrape emergence by the herbicide treatment was significant across all sowing dates but more marked in later sowing dates. Both herbicide treatments were similarly effective and provided a similar increase in yield in intermediate and late sowing dates. The early establishment of broomrape in earlier sowing dates strongly affected the yield.
4. Discussion Although O. crenata is potentially the major constraint for pea cultivation in the Mediterranean area and Middle East, it has received little attention and was not even mentioned as a curiosity in recent reviews on the pea crop and its constraints (Hagedorn, 1984; Ali et al., 1994; Cousin, 1997), probably due to the fact that pea is a minor crop in the area of O. crenata distribution. But, O. crenata problem on pea is not new in the area. Moreno (1944) considered broomrape a major problem for pea cultivation, pointing that pea is more sensitive to broomrape damage than faba bean. Thus, it seems more likely that we are not facing a new problem, but just a neglected one. The broomrape problem might have relegated the culture of pea in the area, and with time, the give-up of pea cultivation in the area has neglected the broomrape problem. However, since the 1990s, there has been in the area an increasing interest in pea cultivation due to its high potential and the increasing demand of rich
protein plants for animal feed. As it could have been predicted, the broomrape problem on pea quickly reappeared with the increase in pea acreage (Rubiales et al., 1999). This was predictable as, first, O. crenata is very common in Mediterranean region, and maintained by the tradition of legume cultivation and the fact that it has a broad host range; second, all the cultivars used were susceptible as no selection for resistance had been made; third, the weather conditions are usually conducive to the disease; fourth, broomrape seeds can be dispersed short distances by wind, but also long distances mixed in pea seed lots; fifth, soil seed-bank can increase very rapidly, as a single broomrape plant can produce hundred thousands of seeds; and sixth, the seeds remain viable in the soil for many years and germinate only after stimulation by root exudates of the host. The growth and development of broomrape, like that of the host plant, is affected by the environmental conditions. High rainfall and mild soil temperature during December–February, months of crop vegetative growth, favour growth of the crop root system as well as ! the germination and attachment of broomrape (LopezGranados and Garc!ıa-Torres, 1993). This can explain the differences in incidence among years. The season 1996–1997 and 1997–1998 were rather unusual in Southern Spain, characterised by soft and rainy winter and fresh and rainy spring. Such years are known to be more conducive to the disease. Thus, the establishment of broomrape was higher. Similarly, the unusually rainy spring of season 2001–2002 allowed high broomrape
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Fig. 3. Evolution of the broomrape (O. crenata) attachments (stages of development according to ter Borg et al. (1994) where S1=tubercles smaller than 2 mm; S2=tubercles greater than 2 mm, without roots development; S3=tubercles with crown roots, without shoot formation; S4=shoot formation, remaining underground; S5=shoot emergence; S6=flowering; and S7=setting of seeds) per host plant at different dates on susceptible check pea cvs. Messire (n) and Ballet (J) and the reference faba bean cv. Prothabon (&), depending on the sowing date, during the field season 1998–1999.
incidence in later sowing dates, that would have been little affected in normal seasons. Standard field scorings are based on number of emerged broomrapes, assuming that this is a good estimation of the total level of infection (Rubiales et al., 2002). However, this study shows that only a small proportion of the established tubercles emerge. Plants might be suffering a substantial level of infection in later
sowing dates by tubercles that might not have the chance to emerge in less favourable springs. Any scoring performed in these conditions would be overestimating the level of resistance available. Only moderate-to-low levels of resistance to O. crenata were found in some cultivars. Similarly, only incomplete resistance to O. crenata has also been found in faba bean (Cubero, 1991) that has been successfully
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accumulated by breeding, allowing the release of resistant faba bean cultivars (Cubero and Moreno, 1999; Khalil and Erskine, 1999). A similar effort on pea breeding for broomrape resistance was however not made. The actual low levels of broomrape resistance would suffice to retard broomrape attachment and/or development in normal years, but would not be enough in conductive years and in heavily infested fields. Pea crop should, therefore, be protected with other control measures. Knowledge of the developmental stage of broomrape is crucial to achieve an effective control with herbicides. It has been shown that good broomrape control can be achieved in faba bean by the application of glyphosate at low rates when S3–S4 (still underground) are the predominant stages of broomrape attachments (MesaGarc!ıa and Garc!ıa-Torres, 1985). This is however not possible in pea as it is far more sensitive to the herbicide even at lower rates than recommended on faba bean (Sillero et al., 2001). Pea tolerates well pre- and postemergence treatment of other herbicides suitable for broomrape control such as imazethapyr (Garc!ıa-Torres et al., 1998; Jacobsohn et al., 1998). However, imazethapyr treatment was less effective in the earlier sowing dates. This might be explained by dissipation of the herbicide from the early sowing date till the time of broomrape seed germination and establishment. A similar effect was previously observed on faba beans ! (Garc!ıa-Torres and Lopez-Granados, 1991). In this situation a double treatment of imazethapyr might provide a good control (Garc!ıa-Torres et al., 1998; Jacobsohn et al., 1998). Even when the double treatment might be effective, farmers are reluctant to adopt the technology, as field pea in the area is a low-input crop of low yield, with little margin for treatments. It has been shown that in broomrape yield decrease is higher in early than in late sowing dates, even for a similar final number of emerged broomrapes. This might be explained by an earlier establishment and a higher number of underground non-emerged tubercles (Pe! rez-de-Luque et al., 2003). Accordingly, even the moderate protection given by imazetaphyr was not sufficient to allow a reasonable yield in the earlier sowing dates. Thus, more research is needed to adjust timing and rates of herbicide treatment and its combination with other control approaches. Particularly, there is an urgent need to increase the level of genetic resistance in the crop. In contrast to O. cumana infecting sunflower, in which up to seven races have been described (Melero-Vara, 1999), there is no evidence for the existence of races of O. crenata neither for host-specialisation in O. crenata populations collected on different hosts (Roma! n et al. 2001). This is supported by the lack of cultivar location interaction found in this study. However, we cannot exclude the possibility of selection of more aggressive O. crenata populations. In addition
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to new races of O. crenata, attention should also be paid to other broomrape species such as O. foetida that has recently been reported on faba bean and chickpea in Tunisia (Kharrat et al., 1992). The same applies for O. aegyptiaca that is widespread in east side of Mediterranean area and might seriously affect pea plants.
Acknowledgements The authors are greatly indebted to Projects 1FD970393 and AGL2002-03248 for financial support and to Ana Moral and Roc!ıo Cantarero for technical assistance.
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Plant Health Progress, Online, DOI 10.1094/PHP-2002-1111-01RS. Parker, C., 1991. Protection of crops against parasitic weeds. Crop Prot. 10, 6–22. P!erez-de-Luque, A., Sillero, J.C., Moral, A., Cubero, J.I., Rubiales, D., 2003. Effect of sowing date and host resistance on the establishment and development of Orobanche crenata in faba bean and common vetch. Weed Res., in press. Rom!an, M.B., Rubiales, D., Cubero, J.I., Torres, A.M., Satovic, Z., 2001. Genetic diversity in Orobanche crenata populations from southern Spain. Theor. Appl. Genet. 103, 1108–1114. Rubiales, D., Sillero, J.C., Cubero, J.I., 1999. Broomrape (Orobanche crenata) as a major constraint for pea cultivation in southern Spain. In: Cubero, J.I., Moreno, M.T., Rubiales, D., Sillero, J.C. (Eds.), Resistance to Orobanche: The State of the Art. Junta de Andaluc!ıa, Sevilla, pp. 83–89. Rubiales, D., P!erez-de-Luque, A., Sillero, J.C., Cubero, J.I., 2002. Screening for resistance to broomrape (Orobanche crenata) in grain legumes. In: Ramos, A., Laguna, R. (Eds.), Standardisation Diseases Resistance Screenings in Grain Legumes Germplasm ! Spain, pp. 79–90. Banks. Junta de Castilla-Leon, Rubiales, D., Moreno, M.T., Kharrat, M., Zermane, N., Khalil, S., 2003. Broomrape (Orobanche crenata) control in sustainable agriculture. In: AEP (Ed.), LEGUMED Symposium on Grain Legumes in the Mediterranean Agriculture. AEP, Rabat, 25–27 October 2001, pp. 27–36. ! Sillero, J.C., del Moral, J., Cubero, J.I., Rubiales, D., 2001. Busqueda de tolerancia al glifosato en guisante como estrategia de control del jopo (Orbanche crenata). In: De Prado, R., Jorr!ın, J.V. (Eds.), II Simposium Int. Uso de herbicidas en la agricultura del siglo XXI. ! Servicio Publicaciones Universidad de Cordoba, pp. 677–684.
Crop Protection 22 (2003) 865–872
Crenate broomrape (Orobanche crenata) infection in field pea cultivars D. Rubialesa,*, A. Pe! rez-de-Luqueb, J.I. Cuberob, J.C. Silleroc a
! CSIC, Instituto de Agricultura Sostenible, Apdo. 4084, E-14080 Cordoba, Spain b ! ETSIAM-UCO, Dep. Gen!etica, Apdo. 3048, E-14080 Cordoba, Spain c ! CIFA, Dep. Mejora y Agronom!ıa, Apdo. 3092, E-14080 Cordoba, Spain
Received 20 February 2003; received in revised form 21 February 2003; accepted 1 March 2003
Abstract Orobanche crenata is a major constraint for winter pea production in Mediterranean and East Asian countries. Screening for resistance performed under field conditions in 20 field pea cultivars showed that very low levels of genetic resistance were available. The resistance proved to be highly influenced by environmental conditions and needs to be supplemented with other control measures. Infection is greatly reduced in later sowing being highest in plots sown by October–December, and much reduced in plots sown by January–February. Imazethapyr applied pre- and post-emergence of the late crop sowings significantly reduced the infection and increased yield. r 2003 Elsevier Science Ltd. All rights reserved. Keywords: Broomrape; Chemical control; Genetic resistance; Orobanche crenata; Pea; Pisum sativum; prometryn; Imazethapyr
1. Introduction Orobanche infestations can be devastating to crops and remove otherwise productive land from effective use for very long periods of time. Crenate broomrape (Orobanche crenata) is well known as a major constraint for faba bean, vetches and lentil, being of importance also on other grain and forage legumes. Although pea was known to be a suitable host, there has been little concern on broomrape incidence on the pea crop. However, there are recent reports of severe damage on pea in Southern Spain (Garc!ıa-Torres et al., 1996; Rubiales et al., 1999), Morocco (Mabsoute and Saadaoui, 1996), Egypt (Korashi et al., 1996) and Israel (Bernhard et al., 1998), being at present acknowledged as the major constraint for pea cultivation in the Mediterranean area and Middle East. The problem of broomrape in this area is dramatic due to its broad distribution, the long survival of the seed-bank in the soil and the extreme susceptibility of the cultivars available to the farmer. Yield loss can be huge, as high
*Corresponding author. Tel.: +34-957499215; fax: +34-957499252. E-mail address: [email protected] (D. Rubiales).
as 80% (Korashi et al., 1996) or even 100% (Bernhard et al., 1998). There is a risk for O. crenata spread to other areas with similar weather conditions, as happened with O. cumana that quickly spread in south-eastern Europe since the first reports at the beginning of the 20th century on sunflower in Russia, and reached Spain in the late 1970s (Melero-Vara, 1999). In a similar way, recent introductions of O. ramosa in Australia (Carter et al., 1996) and Chile (D!ıaz and Norambuena, 2001) and of O. minor in USA (Osterbauer and Rehms, 2002) have been reported. The consequences of potential climate change are uncertain, but there exits a serious possibility that this could lead to more favourable conditions for O. crenata in more northern latitudes and thus pose serious threat to cool season food legume production as a whole. Some strategies of broomrape control have been developed, from cultural practices to chemical control (Parker, 1991; Rubiales et al., 2003) but all without unequivocal success, being either not feasible, uneconomic, hard to achieve or resulting in incomplete protection. Breeding for resistance is still the most economical, feasible, and environmental-friendly method of control. Useful levels of resistance have been
0261-2194/03/$ - see front matter r 2003 Elsevier Science Ltd. All rights reserved. doi:10.1016/S0261-2194(03)00070-X
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found in several hosts against parasitic plants, like in sorghum against Striga hermonthica, cowpea against S. gesnerioides, sunflower against O. cumana, and faba bean, chickpea and vetch against O. crenata, among others (Cubero, 1991; Parker, 1991; Rubiales et al., 2002) but little is known on the levels of resistance to O. crenata available in pea. The purposes of the present study are to determine the level of resistance available in pea cultivars, to determine the effects of sowing date on broomrape establishment and development, and to assess the feasibility of combining the slight levels of resistance available with chemical control and delayed sowing dates.
2. Materials and methods In a first experiment 20 top commercial cultivars of pea were screened for broomrape resistance under field conditions in two locations across Andaluc!ıa (southern Spain) (Table 1) during the field seasons 1995–1996 and 1996–1997. Screenings were performed in plots in which high and uniform broomrape infestation was known from previous year observations. Each cultivar was represented by a double row 2 m long with four replications in a completely randomised design. The number of emerged broomrape shoots per host plant was determined at crop maturity by counting the number of broomrapes and pea plants in the rows. In a separate experiment the pea cultivars Messire and Ballet were studied for broomrape resistance under field conditions at different sowing dates during the field seasons 1996–1997, 1997–1998, 1998–1999 and 1999– 2000, at CIFA Alameda del Obispo experimental farm, ! Cordoba, Spain, which has a deep loam soil (Typic Xerofluvent). As faba bean is the best-studied host of O. crenata, the susceptible faba bean cultivar Prothabon was added as a reference. Each line was represented by a single 2 m row with 0.7 m of row spacing. Twenty plants were grown per row. Five sowings were made at 4 weeks intervals from middle October to middle February, with four replications per accession per sowing date. Broomrape infection was determined at crop maturity by counting the number of emerged broomrape shoots per host plant in the row. Additionally, in the plots sown in seasons 1998–1999 and 1999–2000, observations were made also on number of underground, non-emerged attachments at 20 days intervals from middle March to middle May. Three to five plants per row were carefully dug up from the soil to count the total number of broomrape establishments, either emerged or nonemerged. The number of established tubercles and their developmental stage were recorded according to ter Borg et al. (1994), where stage 1: tubercles smaller than 2 mm; 2: tubercles greater than 2 mm, without roots development; 3: tubercles with crown roots, without
Table 1 Number of emerged O. crenata shoots per host plant on 20 pea ! cultivars under field conditions at Cordoba and Mengibar, southern Spain Pea cultivar
Crop season 1995/1996 ! Cordoba
Messire Baroness Bacar!a Radley Rustic Renata Cambar Amadeus Esla Loto Solara Azur Jami Leo Cea Orb Brent Malta Spring Ballet
a
3.6 a 3.7 a 3.7 a 3.7 a 3.7 a 3.5 ab 3.3 ab 3.2 ab 3.2 ab 3.2 ab 3.1 ab 3.1 ab 3.1 ab 3.1 ab 3.0 ab 2.8 ab 2.3 b 2.3 b —b 1.3 c
1996/1997 Meng!ıbar
! Cordoba
Meng!ıbar
5.9 4.9 5.0 4.9 4.9 5.2 5.6 5.3 5.0 5.2 5.2 4.8 5.0 5.0 5.2 4.9 5.8 5.0 5.0 4.2
3.9 2.6 1.3 2.8 2.1 0.3 1.3 1.4 2.1 2.2 0.8 0.3 0.8 1.1 0.8 0.9 1.4 1.7 0.8 0.5
0.7 0.6 0.5 0.6 0.5 0.3 0.3 0.2 0.8 0.5 0.1 0.6 0.5 0.8 0.7 0.8 0.5 0.5 0.4 0.3
a cde cd cde cde bcd ab abc cd bcd bcd de cd cd bcd cde a cd cd e
a ab ab ab ab b ab ab ab ab b b b ab b ab ab ab b b
a a a a a a a a a a a a a a a a a a a a
a Data with the same letter per column are not significantly different (Po0:05; Duncan test). b —: not determined.
shoot formation; 4: shoot formation, remaining underground; 5: shoot emergence; 6: flowering; and 7: setting of seeds. A final count of emerged O. crenata plants per host plant was recorded at the end of the crop cycle on the remaining plants. The efficacy of imazethapyr on broomrape control on the pea cvs. Ballet and Messire was tested under field conditions at different sowing dates during the field season 2001–2002, at the same experimental farm. Five sowings were made at 2 weeks intervals from early November to middle January with four replications per accession per sowing date. Each treatment was represented by a 8 m2 plot at 0.7 m of row spacing. Standard crop pre-emergence treatment for weed control with prometryn was always applied. Treatments were: (1) control, only pre-emergence prometryn for weed control; (2) prometryn+imazethapyr (adjusted at 75 g ma/ ha) at crop pre-emergence; and (3) prometryn preemergence+imazethapyr (adjusted at 150 g ma/ha) postemergence. Broomrape infection was determined at crop maturity by counting the number of emerged broomrape shoots per host plant. Then the plots were harvested and seed yield (kg/ha) determined. The scores were angular transformed and an analysis of variance was carried out using the SPSS for windows version 10.0.
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3. Results High levels of infection were obtained during the season 1995–1996 on the 20 pea cultivars (Table 1) with an average of 3.1 and 5.1 emerged broomrapes per pea ! plant at Cordoba and Mengibar, respectively. The infection was much lower during the 1996–1997 season with averages of 1.5 and 0.5 broomrapes per plant at ! Cordoba and Mengibar, respectively. All cultivars were severely infected, but there were significant genotypic effects, with cv. Ballet, significantly less infected than cv. Messire in all instances but for the season 1996–1997 at Mengibar, where the level of infection was rather low and differences among cultivars were not significant. ANOVA (arcsin transformed data) showed significant differences in broomrape emergence among cultivars (Po0:05), among locations (Po0:001) and among years (Po0:001). There was a significant year location interaction (Po0:001), but not cultivar location and cultivar year. Differences in infection among years can be ascribed to varying climatic factors that are known to influence O. crenata infection. Weather conditions were very conducive for broomrape infection during the 1996– 1997 season due to a mild temperature (11–16 C average air temperature) and high rain (600 mm) in winter (Table 2), although the spring was rather dry. The season 1997–1998 was also conducive with a mild temperature (11–15 C) and a sufficiently rainy winter (270 mm). The spring was warm (15–20 C) although rainy (170 mm). The season 1998–1999 was not very conducive with a relatively cold (8–10 C) and dry winter (180 mm) as well as a dry spring (90 mm). The season 1999–2000 was moderate, with a moderate winter (10– 15 C and 120 mm) and a rainy spring (120 mm). Pea cvs. Ballet and Messire tended to display lower numbers of emerged broomrape shoots per plant than the faba bean check cv. Prothabon (Fig. 2); however, the differences were only significant in the earlier sowing dates. Ballet tended to display lower numbers of emerged broomrape shoots per plant than Messire, but differences were not significant. Both pea cvs. as well as the faba bean check were more heavily infected in the plots sown early (October—December) (Fig. 2). By then, broomrape infection, as determined by number of emerged broomrapes per host plant, decreased with sowing date, being this decrease in emergence more marked in the less favourable 1998–1999 season in which broomrape emergence did not occur in the plots sown in February. Infection on both faba bean and pea was very high in the plots sown in January during the season 1996–1997 and low in the remaining seasons. This heavy infection can be explained by the unusual heavy rain occurred in December 1996 and January 1997 and the milder temperatures of that season. Broomrape emergence was neither reduced the season
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Table 2 Effect on broomrape emergence and yield of different foliarly applied herbicide treatment on plots of pea (cvs. Messire and Ballet) sown at ! different sowing dates at Cordoba (2001–2002) Sowing date
Herbicide treatmenta
Number of emerged broomrape shoots per host plant
November 15
1 2 3 1 2 3 1 2 3 1 2 3 1 2 3
2.1 1.2 1.1 1.8 1.3 1.1 1.6 0.7 0.8 2.6 0.5 0.5 2.0 0.3 0.6
1 2 3
2.0 a 0.8 b 0.8 b
December 5
December 20
January 5
January 18
Overall
ab b b a ab b a b b a b b a c b
Host yield (kg/ha) 0a 0a 0a 0b 150 a 293 a 0b 214 a 500 a 485 b 1385 a 1477 a 563 b 1437 a 2123 a 210 b 637 a 879 a
a
Herbicide treatment: 1: control, only Gesagard applied at crop preemergence; 2: Pursuit applied at crop pre-emergence; and 3: Gesagard applied at crop pre-emergence and Pursuit at crop post-emergence. b Letters in common per column within a sowing date indicates that different treatment did not have a significant influence on broomrape infection or yield (Duncan test, Po0:05).
2001–2002 in the later sowing dates (Table 2). This might be explained by the fact that unusual rain occurred during March and April (Fig. 1) allowing emergence of established tubercles. The high infection in the earlier sowing dates resulted in a complete loss of yield (0 kg/ha) in the two pea cultivars (Table 2). In the later sowing dates, even when broomrape emergence was similarly high, untreated plants were able to yield around 600 kg/ha. Digging up and extracting whole plants to record the number of underground, non-emerged attachments allowed the observation of further differences among accessions that were not detectable when only the number of emerged broomrapes was considered. Most of the established parasites remained underground and did not emerge (Figs. 2 and 3). Pea plots shown in October were less infected than those sown in November and December. Infection decreased in plots sown in January and February. In the season 1998–1999 plots sown in January displayed little broomrape emergence, and those sown in February did not show any emergence at all, but infection was high as shown by the high number of underground non-emerged attachments. This tendency was observed in both pea cultivars and the faba bean check. In the 1999–2000 season, broomrape emergence was similar to that in the previous
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Fig. 1. Average air temperature ( Spain.
D. Rubiales et al. / Crop Protection 22 (2003) 865–872
! ) and rainfall ( ) during the seasons 1996–1997, 1997–1998, 1998–1999, 1999–2000, and 2001–2002 at Cordoba,
season, but the most favourable weather conditions (more rain during spring) allowed a higher emergence of established broomrape tubercles, and there was some emergence even in the plots sown in February. In the Messire plots sown in October there was already a substantial number of underground attachments (stages 1–4) and a minor amount of emerged broomrapes by March (Fig. 3). Few attachments were formed on cv. Ballet, none of which emerged. Underground infection increased markedly from March to April and little from April to May in which most emergence took place. Both pea cultivars followed a similar pattern, although infection remained lower in Ballet. In the plots sown in November there was also a substantial number of underground attachments (stages 1–4) but no emergence on Messire and Ballet by the
March scoring date. In the plots sown in October, underground infection increased markedly from March to April, and little from April to May in which most emergence took place. In the plots sown in December and January there was a substantial number of underground attachments (stages 1–4) but no emergence on Messire and Ballet by the April scoring date. From April underground infection did not increase and some emergence took place. In the plots sown in February there was some underground attachments but no emergence on Messire and Ballet by the April scoring date. Underground infection increased till May, but no emergence took place. Pre- and post-crop-emergence treatments with imazethapyr provided similar levels of protection against broomrape. There was no treatment cultivar
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Fig. 2. Number of broomrape (O. crenata) emerged shoots per host plant in pea cultivars Messire ( ) and Ballet (&) and the reference faba bean cv. ! Prothabon ( ) in field experiments at Cordoba at different sowing dates (from mid October till mid March) during the field seasons 1996–1997, 1997– 1998, 1998–1999 and 1999–2000. The same letters per host plant per season indicate that differences in broomrape emerge at the varying sowing dates were not statistically significant (Duncan, Po0:05).
interaction, and thus data of the two cultivars are presented together (Table 2). Reduction of broomrape emergence by the herbicide treatment was significant across all sowing dates but more marked in later sowing dates. Both herbicide treatments were similarly effective and provided a similar increase in yield in intermediate and late sowing dates. The early establishment of broomrape in earlier sowing dates strongly affected the yield.
4. Discussion Although O. crenata is potentially the major constraint for pea cultivation in the Mediterranean area and Middle East, it has received little attention and was not even mentioned as a curiosity in recent reviews on the pea crop and its constraints (Hagedorn, 1984; Ali et al., 1994; Cousin, 1997), probably due to the fact that pea is a minor crop in the area of O. crenata distribution. But, O. crenata problem on pea is not new in the area. Moreno (1944) considered broomrape a major problem for pea cultivation, pointing that pea is more sensitive to broomrape damage than faba bean. Thus, it seems more likely that we are not facing a new problem, but just a neglected one. The broomrape problem might have relegated the culture of pea in the area, and with time, the give-up of pea cultivation in the area has neglected the broomrape problem. However, since the 1990s, there has been in the area an increasing interest in pea cultivation due to its high potential and the increasing demand of rich
protein plants for animal feed. As it could have been predicted, the broomrape problem on pea quickly reappeared with the increase in pea acreage (Rubiales et al., 1999). This was predictable as, first, O. crenata is very common in Mediterranean region, and maintained by the tradition of legume cultivation and the fact that it has a broad host range; second, all the cultivars used were susceptible as no selection for resistance had been made; third, the weather conditions are usually conducive to the disease; fourth, broomrape seeds can be dispersed short distances by wind, but also long distances mixed in pea seed lots; fifth, soil seed-bank can increase very rapidly, as a single broomrape plant can produce hundred thousands of seeds; and sixth, the seeds remain viable in the soil for many years and germinate only after stimulation by root exudates of the host. The growth and development of broomrape, like that of the host plant, is affected by the environmental conditions. High rainfall and mild soil temperature during December–February, months of crop vegetative growth, favour growth of the crop root system as well as ! the germination and attachment of broomrape (LopezGranados and Garc!ıa-Torres, 1993). This can explain the differences in incidence among years. The season 1996–1997 and 1997–1998 were rather unusual in Southern Spain, characterised by soft and rainy winter and fresh and rainy spring. Such years are known to be more conducive to the disease. Thus, the establishment of broomrape was higher. Similarly, the unusually rainy spring of season 2001–2002 allowed high broomrape
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Fig. 3. Evolution of the broomrape (O. crenata) attachments (stages of development according to ter Borg et al. (1994) where S1=tubercles smaller than 2 mm; S2=tubercles greater than 2 mm, without roots development; S3=tubercles with crown roots, without shoot formation; S4=shoot formation, remaining underground; S5=shoot emergence; S6=flowering; and S7=setting of seeds) per host plant at different dates on susceptible check pea cvs. Messire (n) and Ballet (J) and the reference faba bean cv. Prothabon (&), depending on the sowing date, during the field season 1998–1999.
incidence in later sowing dates, that would have been little affected in normal seasons. Standard field scorings are based on number of emerged broomrapes, assuming that this is a good estimation of the total level of infection (Rubiales et al., 2002). However, this study shows that only a small proportion of the established tubercles emerge. Plants might be suffering a substantial level of infection in later
sowing dates by tubercles that might not have the chance to emerge in less favourable springs. Any scoring performed in these conditions would be overestimating the level of resistance available. Only moderate-to-low levels of resistance to O. crenata were found in some cultivars. Similarly, only incomplete resistance to O. crenata has also been found in faba bean (Cubero, 1991) that has been successfully
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accumulated by breeding, allowing the release of resistant faba bean cultivars (Cubero and Moreno, 1999; Khalil and Erskine, 1999). A similar effort on pea breeding for broomrape resistance was however not made. The actual low levels of broomrape resistance would suffice to retard broomrape attachment and/or development in normal years, but would not be enough in conductive years and in heavily infested fields. Pea crop should, therefore, be protected with other control measures. Knowledge of the developmental stage of broomrape is crucial to achieve an effective control with herbicides. It has been shown that good broomrape control can be achieved in faba bean by the application of glyphosate at low rates when S3–S4 (still underground) are the predominant stages of broomrape attachments (MesaGarc!ıa and Garc!ıa-Torres, 1985). This is however not possible in pea as it is far more sensitive to the herbicide even at lower rates than recommended on faba bean (Sillero et al., 2001). Pea tolerates well pre- and postemergence treatment of other herbicides suitable for broomrape control such as imazethapyr (Garc!ıa-Torres et al., 1998; Jacobsohn et al., 1998). However, imazethapyr treatment was less effective in the earlier sowing dates. This might be explained by dissipation of the herbicide from the early sowing date till the time of broomrape seed germination and establishment. A similar effect was previously observed on faba beans ! (Garc!ıa-Torres and Lopez-Granados, 1991). In this situation a double treatment of imazethapyr might provide a good control (Garc!ıa-Torres et al., 1998; Jacobsohn et al., 1998). Even when the double treatment might be effective, farmers are reluctant to adopt the technology, as field pea in the area is a low-input crop of low yield, with little margin for treatments. It has been shown that in broomrape yield decrease is higher in early than in late sowing dates, even for a similar final number of emerged broomrapes. This might be explained by an earlier establishment and a higher number of underground non-emerged tubercles (Pe! rez-de-Luque et al., 2003). Accordingly, even the moderate protection given by imazetaphyr was not sufficient to allow a reasonable yield in the earlier sowing dates. Thus, more research is needed to adjust timing and rates of herbicide treatment and its combination with other control approaches. Particularly, there is an urgent need to increase the level of genetic resistance in the crop. In contrast to O. cumana infecting sunflower, in which up to seven races have been described (Melero-Vara, 1999), there is no evidence for the existence of races of O. crenata neither for host-specialisation in O. crenata populations collected on different hosts (Roma! n et al. 2001). This is supported by the lack of cultivar location interaction found in this study. However, we cannot exclude the possibility of selection of more aggressive O. crenata populations. In addition
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to new races of O. crenata, attention should also be paid to other broomrape species such as O. foetida that has recently been reported on faba bean and chickpea in Tunisia (Kharrat et al., 1992). The same applies for O. aegyptiaca that is widespread in east side of Mediterranean area and might seriously affect pea plants.
Acknowledgements The authors are greatly indebted to Projects 1FD970393 and AGL2002-03248 for financial support and to Ana Moral and Roc!ıo Cantarero for technical assistance.
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