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Australasian Plant Pathology, 2009, 38, 228–234

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Population genetics in weedy species of Orobanche Z. Satovic A,F, D. M. Joel B, D. Rubiales C, J. I. Cubero D and B. Román E A

Department of Seed Science and Technology, Faculty of Agriculture, University of Zagreb, Svetosimunska 25, 10000 Zagreb, Croatia. B Newe-Ya’ar Research Center, ARO, PO Box 1021, 30095 Ramat-Yishay, Israel. C Insituto de Agricultura Sostenible, CSIC, Apdo. 4084, 14080 Córdoba, Spain. D Departamento de Genética, ETSIAM, Universidad de Córdoba, Apdo. 3048, 14080 Córdoba, Spain. E IFAPA-CICE, Centro Alameda del Obispo, Área de Mejora y Biotecnologıa, Apdo. 3092, 14080 Córdoba, Spain. F Corresponding author. Email: [email protected]

Abstract. Broomrapes (Orobanche spp.) are holoparasitic plants without chlorophyll, parasitising roots of a wide range of hosts. Some species are noxious weeds having a devastating effect on many important crops. Knowledge of the variability in the population genetics of weedy broomrapes is important in any attempt to develop resistance-breeding strategies for the relevant host crops against these parasites. The distribution of genetic variation in O. aegyptiaca, O. cumana, O. crenata, O. foetida, O. gracilis, O. hederae, O. minor and O. ramosa populations has been reviewed in relation to (1) the amount and structure of population genetic diversity as a consequence of the mating system, (2) the geographic differentiation as shaped by migration, (3) the spread of infestations into new areas followed by genetic drift, and (4) the host-differentiation owing to the host-induced selection. It has been shown that dominant markers such as RAPDs and AFLPs can be used efficiently in the analysis of predominant mating system and in the analysis of host-differentiation. As crop-seed exchange and transport play an important role in migration of seeds of Orobanche, geographical differentiation is difficult to discern from molecular data. Finally, in analysing genetic drift, co-dominant markers such as microsatellites are clearly needed.

Introduction The genus Orobanche (broomrape) comprises ~170 holoparasitic species (Uhlich et al. 1995), including several serious agricultural pests that cause major crop losses throughout the world (Parker and Riches 1993; Wegmann 1998; Joel et al. 2007). Parasitism has allowed simplification in shoot morphology of the holoparasites, including a reduction in features that are commonly used in plant taxonomy (Musselman 1994), and therefore the features used to distinguish species of Orobanche are poorly defined (Musselman 1986). Similarly, practical diagnosis of the species that are serious weeds in agricultural fields has been problematic, particularly the analyses of soil seed banks, notonlybecause theseed-coattexture of some species does not show a sufficient number of differential features (Joel 1987), but also because the seeds tend to lose diagnostic surface features when buried in soil for a long period of time, resulting from biotic activities (Joel et al. 1998a). Molecular analysis has allowed for the study of genetic relationships among species of Orobanche, first by using RAPD markers (Román et al. 2003) and later also by sequencing the internal transcribed spacer (ITS) region of the nuclear rDNA (Schneeweiss et al. 2004; Wolfe et al. 2005) and specific genes of the plastid genome (Manen et al. 2004). As a result, the use of DNA-fingerprinting for species discrimination, including the accurate identification of soil-borne seeds, has also been made possible (Joel et al. 1998a), although the wide applicability of diagnostic markers is still limited because of intraspecific species variability. Ó Australasian Plant Pathology Society 2009

The understanding of the variability within and among pathogenic populations is particularly important if selection programs and breeding strategies of host crops need to target specific parasite races at various geographical areas. Information on population genetics in broomrape species is limited, especially with regard to molecular analysis, mainly because of the lack of suitable co-dominant markers such as single sequence repeats (SSRs; i.e. microsatellites), limited geographical scope of sampling and rather low sample sizes of the analysed populations. Variability within and among populations of some species of Orobanche has been observed on the morphological level (Musselman and Parker 1982; Musselman 1994), and also on the host-range and host-preference levels. In O. cumana, a specific parasite of sunflower, Vrânceanu et al. (1986) described five races in Romania (A–E) by using a set of sunflower differentials. Variations in aggressiveness among O. crenata populations attacking faba bean have also been reported (Cubero and Moreno 1979; Radwan et al. 1988). Nevertheless, the question has been raised whether observed variation in aggressiveness of this species was genetically determined or induced by environmental conditions (Zeid et al. 1997). In recent decades, several molecular techniques were developed to complement traditional methods for population genetic analysis. While a wide range of markers is available, only few techniques have so far been applied to study broomrape populations, including isozymes, RAPDs and ISSRs. Moreover, the population genetic studies of Orobanche have been limited 10.1071/AP08100

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mainly to the weedy species, i.e. O. aegyptiaca (Paran et al. 1997; Joel et al. 1998b), O. crenata (Verkleij et al. 1991a, 1991b; Paran et al. 1997; Zeid et al. 1997; Román et al. 2001, 2002), O. cumana (Castejón-Muñoz et al. 1991; Gagne et al. 1998), O. foetida (Román et al. 2007b; Vaz Patto et al. 2008), O. minor (Westwood and Fagg 2004) and O. ramosa (Benharrat et al. 2005; Buschmann et al. 2005; Brault et al. 2007). Analyses of natural populations of non-weedy species were conducted on O. hederae (Benharrat et al. 2002) and O. gracilis (Román et al. 2007a). The purpose of the present paper is to review the literature on the population genetics of Orobanche and to formulate testable hypotheses to explain the observed phenomena concerning (1) the amount and structure of population genetic diversity as a consequence of the mating system, (2) the geographic differentiation as shaped by migration, (3) the spread of infestations into new areas followed by genetic drift and (4) the host-differentiation resulting from host-induced selection. Life-history traits The gene-pool dynamics of a species is closely associated with several life-history traits. Some of them are universal for all species of Orobanche, such as sexual propagation, extremely high fecundity (a single plant of O. crenata can produce more than 105 seeds; Pieterse 1979) and production of long-lived dormant seeds that are chemically triggered to germinate by stimuli from host plants (Joel et al. 1994, 2007). Nevertheless, some very important life history traits differ among species of Orobanche, namely life cycle (annual v. perennial), geographical range (narrow v. widespread), breeding system (self-pollinators cf. cross-pollinators), host range (generalists v. specialists) and host status (wild cf. cultivated) (Parker and Riches 1993; Verkleij and Pieterse 1994). It is conceivable that weedy populations parasitising crop species would have distinct gene-pool dynamics in comparison to those found in natural habitats. Primarily, owing to the global crop-seed exchange and transport, the patterns of genetic distribution of the parasites would depend more on the history of trade routes rather than predominantly on natural seeddispersion systems per se (Gagne et al. 1998). This is particularly feasible because seeds of Orobanche are tiny (0.2–0.4 mm) and can easily contaminate crop-seed stocks. Additionally, parasite populations in agricultural fields may, on the one hand, rapidly expand because of the availability of host plants and lack of competition and predation, whereas on the other hand, they may suffer from reductions in population size as the result of crop rotation, the introduction of tolerant/resistant crop cultivars and the application of various control measures. Thus, the bottleneck effect (Dlugosch and Parker 2008) could be more pronounced in cultivated fields than in undisturbed environments. Population genetic studies tend to focus on the amount and distribution of genetic diversity within and among populations, as shaped by the interplay of the following five evolutionary forces: mutation, recombination, migration, genetic drift and selection. The relative roles of these forces may differ markedly between different broomrape species and populations. The interaction of evolutionary forces may result in striking differences in the gene and genotypic diversity of species as well as in the distribution of

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genotypic diversity within and among populations. Thus, the comparison and interpretation of the results obtained by different studies has to be carried out with caution. Moreover, the application of different sampling strategies, molecular-marker systems (dominant cf. co-dominant) and statistical approaches make this comparison even more difficult. The amount and structure of population genetic diversity as a consequence of the mating system As with most plant species, recombination in Orobanche occurs through sexual reproduction but its outcome heavily depends on the mating system involved. Mating systems, varying from strict inbreeding to obligate outcrossing, greatly affect the amount and partitioning of genetic diversity within and among populations of broomrape species. Their mating systems are commonly correlated with flower morphology. Whereas some selfpollinating species (e.g. O. cumana) develop bent tubular corollas with small lower lips that do not provide a landing platform for pollinators, other species (e.g. O. crenata) have large lower lips that serve as landing platforms for pollinating insects. As self-pollinating species have much less gene flow among populations via pollen than do mixed-mating or outcrossing species, they are expected to promote differentiation among populations, whereas in mixed-mating and out-crossing species, the among-population differences are less marked (Hamrick and Godt 1989; Sweigart and Willis 2003). Consequently, out-crossing species should have higher proportions of polymorphic loci, more alleles per polymorphic locus and more genetic diversity (Hamrick and Nason 1996; Dubois et al. 2003; Nybom 2004). It is likely that the overall genetic diversity in self-pollinating species would be limited compared with that in out-crossing species, because a novel mutation arising in a population of a self-pollinating species has a lower probability of spreading to other populations than that of an out-crossing species, even if the allele reaches a high frequency within the population of origin (Slatkin 1980). Moreover, in self-pollinating species slightly deleterious mutations are more likely to be found in homozygous states, and, thus, are more likely to be eliminated by selection (Hamrick and Godt 1997). Population genetics studies in broomrape species have clearly shown the differences in population genetic structure between a self-pollinating species O. cumana (Castejón-Muñoz et al. 1991; Gagne et al. 1998), and a predominantly out-crossing species O. crenata (Verkleij et al. 1991a, 1991b; Zeid et al. 1997; Román et al. 2001, 2002). Gagne et al. (1998) reported the results of a study carried out on eight O. cumana populations (three from Bulgaria, one from Romania and Turkey, and three from Spain), analysed with the use of RAPD markers. By using the analysis of molecular variance (AMOVA; Excoffier et al. 1992) approach, 15% of the total genetic (or actually RAPD phenotypic) diversity was attributable to divergence between regions (Spain cf. Eastern countries), 47% to among-population differentiation (within regions) and 38% to within-population diversity. Whereas Román et al. (2002), in their analysis of six O. crenata populations (three from Spain and three from Israel) by using ISSR markers and the same statistical method, obtained the following results: 24% of the total diversity was attributable to

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divergence between regions (Israel cf. Spain), 5% to amongpopulation diversity and as high as 71% to within-population diversity. The direct comparison of the results of these studies is tentative because the populations were sampled from different geographical regions. Nevertheless, the general difference in intra-population variation levels between self-pollinating (38% in O. cumana) and out-crossing (71% in O. crenata) species is readily seen. In the case of O. crenata, its out-crossing behaviour was confirmed by analyses carried out by Verkleij et al. (1991a, 1991b), using isozymes. In the case of two Syrian populations of O. crenata analysed by using five isozyme systems (revealing five loci), genotypic frequencies at most loci did not deviate significantly form Hardy–Weinberg equilibrium (HWE), whereas the average inbreeding coefficient FIS (i.e. Wright’s fixation index) was close to zero (0.074) (Verkleij et al. 1991a). By analysing three Spanish populations of O. crenata, Verkleij et al. (1991b) found out that for most of the isozyme loci the populations were in HWE. The average FIS had a somewhat higher value (0.159); however, the observed heterozygote deficiency could be caused by Wahlund effect (see below). As population genetic theory predicts that self-pollinating species should harbour relatively low levels of genetic variation within populations and substantial divergence among populations, it is possible to infer the mating system even from dominant marker data by calculating the individual pairwisedistance matrix and subjecting it to the AMOVA (Excoffier et al. 1992). Thus, O. cumana and O. ramosa (Benharrat et al. 2005; Buschmann et al. 2005) are predominantly self-pollinating species, whereas O. crenata and O. foetida are out-crossers (Román et al. 2007b). Geographic differentiation as shaped by migration Apart from the mating system, the vastly different ecological constraints and changing opportunities imposed by agricultural plant communities, as opposed to natural habitats, have substantial effects on the basic principles of population dynamics. Joel et al. (1998b) showed an increase in genetic distance between Orobanche populations that correlates with geographical distance, even within small agricultural regions. As well as persistent seed banks, a consequence of long-lived dormant seeds typical for this genus, the current genetic structure of an agricultural Orobanche population also reflects a long history of human migrations and crop-seed trade. Spatial genetics analysis is traditionally aimed at identifying natural barriers of pollen and seed dispersal, followed by isolation-bydistance. The emergence of the field of landscape genetics (Manel et al. 2003), which is an amalgamation of molecular population genetics and landscape ecology (Turner et al. 2001), would greatly improve our knowledge of the interaction between landscape features and micro-evolutionary processes and their effect on population substructuring in Orobanche. In the study reported by Gagne et al. (1998) concerning O. cumana, very little gene exchange appeared to occur between different populations, corroborating the self-pollinating nature of the species. The highest values of genetic differentiation (Nei’s Gst, assuming that all individuals were homozygous) were determined between Spanish and Bulgarian populations

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whereas the lowest Gst values were between Bulgarian populations and a Turkish one. The minimum spanning tree calculated from the Gst matrix indicated that the population from Romania could be seen as a link between Spanish populations on one side and Turkish and Bulgarian ones on the other, suggesting that one particular Spanish population, which was found to be most closely related to the Romanian one, could actually come from Romania, apparently imported with sunflower seeds. This simple and plausible explanation raises an important question in Orobanche population-genetics studies concerning agricultural ecosystems and it is especially accentuated in the case of selfpollinators as mentioned. Depending on the origin of the crop seeds, not only could the Orobanche populations found in the same geographical region be very distinct but also the plants sampled in the same field could exhibit genetic variation even in selfpollinating species. The latter case would be a consequence of the use of sunflower seeds from different origins contaminated with seeds of different broomrape populations, the sharing of contaminated machinery between farmers and the fact that seeds of some broomrape species may remain viable in soil for decades (Joel et al. 2007). Molecular marker analyses carried out among O. crenata populations from Egypt (Zeid et al. 1997), Israel (Paran et al. 1997; Román et al. 2002), Syria (Verkleij et al. 1991a) and Spain (Verkleij et al. 1991b; Román et al. 2001, 2002) have generally revealed low inter-population differentiation within countries. Considering two Syrian populations proved to be genetically very similar although sampled from two localities 100 km apart and interrupted by mountains, Verkleij et al. (1991a, 1991b) offered the following two possible explanations on the basis of isozyme analysis: (a) gene exchange took place as a result of seed transport by animal and man, or (b) Orobanche plants (from which the tissue was used for the analysis) were raised from collected seeds and cultivated on faba beans under greenhouse conditions and, thus, a selection owing to uniform microclimatic conditions occurred, levelling out possible genetic differences between the two populations. Although the former explanation seems utterly plausible, the latter one is of more importance for future studies in order to avoid false conclusions; i.e. plant material should be collected in situ. Nevertheless, Román et al. (2001), in their analysis of individual O. crenata plants collected in situ from six faba-bean fields in the south of Spain (the province of Andalusia), detected that as high as 95% of the variability was attributable to differences among individuals within a population. The obvious conclusion was that in spite of geographical distances between populations, the genemigration forces were continuous and strongly favoured by an efficient dispersal of the parasite seeds by humans, machinery, animals or wind, as well as on host seeds. However, the genetic differentiation between distant countries has been shown in the case of Spain and Syria (Verkleij et al. 1991b) by using isozyme analysis, as well as between Spain and Israel (Román et al. 2002) by using ISSR analysis, indicating that geographic distance basically provides a substantial barrier to gene flow as long as there is no commercial exchange of host seeds between the regions. As increasing global crop-seed exchange and transport play an important role in migration of Orobanche seeds, geographical differentiation would be difficult to discern because the population substructure may not depend

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on spatial distances or barriers of gene flow, such as mountains and rivers that are common in natural ecosystems. Spread of infestations into new areas followed by genetic drift Two main causes of genetic drift in Orobanche populations can be hypothesised as follows: (a) seasonal reductions in population size resulting from unfavourable environmental conditions and (b) founder effects. It is likely that particularly in agricultural ecosystems, the Orobanche populations undergo regular, severe changes in allele frequencies because of the application of weedcontrol measures and the avoidance of growing crops that are already known as susceptible hosts for the parasite. For this reason, it would be interesting to monitor the changes in genetic diversity of Orobanche populations sampled in the same field for several consecutive years, taking into account diverse crops grown in the field and the control methods such as hand-weeding and chemical or biological control, which are applied there. Founder events are to be expected following the spread of infestations into new, previously unoccupied areas. Founder populations typically contain only a small fraction of the genetic variation found in the original source populations. Geographic ranges of most of the species of Orobanche, and in particular those attacking crops, have almost certainly expanded dramatically in historical times, and even more so currently with globalisation. Thus, all populations outside of the centre of origin of a species would most likely be severely reduced in genetic variability compared with those found in the centre of origin. Castejón-Muñoz et al. (1991), after analysing five Spanish populations of O. cumana attacking confectionery and oil sunflower by using isozymes, were the first to suggest the founder effect as a possible explanation for the differences in within-population variability. They argued that the higher diversity of the parasite population from confectionery sunflower of El Coronil (Spain) than that of the other four populations could be attributed to the higher number of years that the susceptible sunflower crop had been grown in that area, and consequently to the very high infection severity. The lesser variability, which was mainly manifested by the loss and fixation of some alleles in the other four populations, was due to a more recent origin of the populations from a few individuals by seed dispersal on the sunflower achenes (Castejón-Muñoz 1989). ISSR analysis of five O. minor populations in the USA was reported by Westwood and Fagg (2004). O. minor is native to Europe, and has been spread around the world (James 1976; Parker and Riches 1993; Musselman 1994; Hassan 1998), with a long history of introduction into the USA (Frost and Musselman 1980), possibly in fodder or bedding for livestock or in contaminated crop seed. The striking outcome of the analysis was the very low level of polymorphisms in the USA, with individuals within populations having nearly all ISSR fragments in common. Westwood and Fagg (2004) argued that the reason for such a low diversity was that the populations originated from just a few founder plants. Two clearly different groups of populations were detected suggesting that the populations may have developed from two separate

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introduction events. However, such outstanding results may also be due to apomixis, i.e. the plant’s ability to form seeds without fertilisation, a common feature in the Orobanchaceae (Teryokhin 1997; Pazy 1998; Plitmann 2002). This phenomenon may be more common in some populations than in others. By analysing the genetic structures and testing for evidence of recent bottleneck events of broomrape populations in different geographical regions, some valuable insights could be obtained concerning the native range of a species and its introductions, adaptations and proliferations in the new environments. Indeed, several statistical methods for identifying populations that have recently experienced a severe reduction in effective population size, by detecting significant deviations from population mutation-drift equilibrium, have been described (Cornuet and Luikart 1996). However, all available methods were exclusively developed for co-dominant markers (e.g. microsatellites) which are currently not available for any of the broomrape species. Host-differentiation owing to the host-induced selection The reproductive success among different phenotypes as measured by fitness is ultimately determined by selection, causing changes in the genetic structure of a population and increasing the adaptation of an organism to its environment. Perhaps the most important aspect concerning selection forces in Orobanche is the host-induced selection. On the species level, one can find large differences in both host preferences and host ranges. Most of the weedy broomrape species are generalists, having a broad to extremely broad host range (Verkleij and Pieterse 1994). However, some hosts allow better development of the parasite and, thus, production of more seeds than do other hosts. Thus, the important issue concerning within-species diversity would be the existence of host-differentiation owing to the host-induced selection and the possibilities of adaptation of a species of Orobanche to a new, possibly cultivated host. When analysing populations of O. aegyptiaca attacking five different crops (eggplant, vetch, tomato, chickpea and faba bean) by using RAPD markers, Paran et al. (1997) found no evidence for host differentiation, as shown by almost no difference between the mean Jaccard’s distance between plants collected from the same host and with that from different hosts. The same was true for populations of O. crenata collected from faba bean, vetch and carrot fields. Hence, as both species are out-crossers, most of the variations were detected among individuals within populations. Nevertheless, host-induced selection could play an important role in population dynamics of these species without even being noticed by overall genome scans. Theoretically, the selection could act upon just a single gene or very small portions of the genome while the rest of the genome is predominantly shaped by other evolutionary forces, namely recombinations (by pollen flow) and migrations (by seed dispersal). The first clear case of host-differentiation was described for O. cumana, which is exceptional in having only a limited host range, with host preference almost exclusively on sunflower. For this species, new races have frequently been selected in the field following the introduction of sunflower cultivars with various Orobanche resistance (R) genes (Sackston 1992; Ruso et al. 1996; Sukno et al. 1999; Fernández-Martınez et al. 2000; Lu et al. 2000;

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Rubiales 2003; Tang et al. 2003; Eizenberg et al. 2004; PérezVich et al. 2004). Another clear case of host-differentiation was reported for O. foetida by Román et al. (2007b). Although O. foetida is widely distributed in the western Mediterranean, it is known to occur on wild legumes and only recently attacks on cultivated legumes have been reported in north–central Tunisia (Kharrat et al. 1992) and Morocco (Rubiales et al. 2005). Román et al. (2007b) detected, at a molecular level, a significant divergence between O. foetida populations infesting chickpea and those infecting faba bean in Tunisia. As the parasite has been described in cropping lands only recently, the specialisation process seems to be the consequence of a recent adaptation forced by a strong selection pressure. In a recent study concerning genetic diversity of Moroccan populations of O. foetida (Vaz Patto et al. 2008), with four populations infecting wild plants (Scorpiurus muricatius and Ornithopus sativus) and one infecting cultivated vetch (Vicia sativa), a certain level of host-differentiation was also detected. However, the vetch-infecting population was closer to the three populations infecting S. muricatus, whereas the population collected on O. sativus was the most divergent one. The results seem to suggest that the population of O. foetida infecting S. muricatus gave rise to a new population able to infect a cultivated species and that the vetch-infecting population is not a new introduction. Host-induced selection is thus one of the most important issues for further studies concerning population genetics of broomrape species. Consequently, there is need for large resistance-breeding efforts to cope with the problems caused by the parasite in agriculture. Some immediate questions concerning this issue would include the following: (a) what is the genetic background of different races/biotypes described for O. cumana, and the genetic background of variations in aggressiveness among populations of O. crenata populations; (b) is there a genetic difference between plants of O. crenata growing on highly susceptible and on tolerant legume plants; and (c) what is the genetic background of broomrape populations attacking a variety of host species. Similar to the analysis of predominant mating systems in broomrapes, host-differentiation would possibly be inferred from dominant marker data using AMOVA combined with the Bayesian model-based clustering method (Pritchard et al. 2000) as applied by Vaz Patto et al. (2008) in analyzing Moroccan populations of O. foetida. References Benharrat H, Veronesi C, Theodet C, Thalouarn P (2002) Orobanche species and population discrimination using intersimple sequence repeat (ISSR). Weed Research 42, 470–475. doi: 10.1046/j.1365-3180.2002.00305.x Benharrat H, Boulet C, Theodet C, Thalouarn P (2005) Virulence diversity among branched broomrape (O. ramosa L.) populations in France. Agronomy for Sustainable Development 25, 123–128. doi: 10.1051/ agro:2004059 Brault M, Betsou F, Jeune B, Tuquet C, Sallé G (2007) Variability of Orobanche ramosa populations in France as revealed by cross infestations and molecular markers. Environmental and Experimental Botany 61, 272–280. doi: 10.1016/j.envexpbot.2007.06.009 Buschmann H, Gonsior G, Sauerborn J (2005) Pathogenicity of branched broomrape (Orobanche ramosa) populations on tobacco cultivars. Plant Pathology 54, 650–656. doi: 10.1111/j.1365-3059.2005.01211.x

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Manuscript received 21 November 2007, accepted 27 November 2008

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