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Bulletin UASVM Agriculture 69(2)/2012 Print ISSN 1843-5246; Electronic ISSN 1843-5386

The Diversity of the Genus Diplotaxis and the Spreading of the Species Worldwide and in Romania

Simona Laura LAZAR, Doru PAMFIL, Marin ARDELEAN, Mirela Irina CORDEA

Faculty of Horticulture, University of Agricultural Sciences and Veterinary Medicine Cluj- Napoca, 3-5 Manastur Street, 400372, Cluj, Romania, [email protected]

Abstract. The neglected and underutilized crops are more and more advertised due to the recognition of their nutritional value. Some of these species are used as crop wild relatives in breeding, for the infusion of useful characters in the commercial varieties and others are used as fourth generation vegetables. Different scientific reports on their chemical composition and the benefic effect on the human health to the conclusion that the wild rocket is a desirable vegetable. This is the case of the genus Diplotaxis, with its 31 species showing a wide degree of heterogeneity in the morphology, chromosome number and geographical distribution of these species. The accessions within the genus Diplotaxis are investigated worldwide especially D. tenuifolia and D. muralis, because there is an increasing interest in them due to the fact that they are picked or cultivated for human consumption. The origin of the genus Diplotaxis is considered the and the Middle East but its area of spreading is very wide. It was observed that the only areas that have not entered this very adaptable species are arctic and subarctic areas and East Asia. Although the species are so cosmopolitan, it is important to keep their diversity especially in the original places such as Romania for D. tenuifolia and D. muralis.

Keywords: Diplotaxis, wild rocket, biodiversity, crop wild relatives

INTRODUCTION

Horticulture is one of the main preoccupations of mankind, a theory endorsed by George (2004), who states that the horticultural species emerged by selection from their wild forms. However, some of the vegetables, especially the ones used at the regional level, remained the same to this day, with a minimal human intervention. Such are harvested straight from the spontaneous flora, sometimes endangering their very existence. Promoting better use of plant genetic resources is one of great activities in FAO and EU policy. As proof of the above mentioned one can remember IPGRI initiative to create UMS program in 1994 and other initiatives for the neglected species, insufficiently used in spite of their value as food. The ultimate goal of all these efforts is the creation of a sustainable agriculture through conservation of these species, by promoting their use and a variety of healthy food for the population (www.bioversityinternational.org). Wild arugula and other minor species which IPGRI are taking in account, is a key crop, selected to increase awareness of the high potential of the agro biodiversity of the world, and to show on how little of this wealth is, in fact, based our farming systems. It is estimated that out of 7000 edible species worldwide, only a small fraction, about 150, are in fact grown and marketed. Greater attention accorded to these neglected species, Cinderellas of agriculture, is an important step both for farming and agriculture to diversify the diet, which ultimately contributes to improving the quality of life (Padulosi, 1997).

64 UTILIZATION

The wild rocket, used widely in Europe and in many other parts of the world, is considered a specialty food or delicacy. Although the Romans and medieval physicians stated only observations on their health beneficial effects on humans, in the modern days well- documented studies complement, deepen and recommend for consumption the species of the genus Diplotaxis. The genus Diplotaxis is an important and well known member of the family, which is widespread in the world; this genus is comparising 32 species (Warwick and Hall., 2009), some of which are considered weeds while others are important as food, herbal medicines, animal feed and a source of cytoplasm male sterility genes in Brassicaceae crops. In figure 1, the use of Diplotaxis sp. is indicated. In Europe is used mainly as condiment and food (Facciola, 1990, Bianco 1995, Silva Dias (1997), Baldrati, 1950 cited by Bianco et al. (1997), Bianco et Boari, 1997). In Africa species of the genus Diplotaxis are used as medicine and food (Mohamedien (1995) cited by Padulosi (1997), Yaniv, 1997), but also as fodder for the cattle (Hedge Et Al., 1980 Negre, (1961); Baulas, (1977), Martinez-Laborde, (1987) cited by Martinez-Laborde (1997). Wild rocket reached the two Americas with the european immigrants (Pignone, 1997). In India and Pakistan, the seeds of rocket (cultivated-Eruca sativa and wild-Diplotaxis sp.) are used to obtain a jamba oil with multiple utilization (Bandhari and Chandell, 1997). In Australia, Parsons et al. (2004) mention and D. muralis as invader weeds.

Fig.1 Utilization of the species belonging to Diplotaxis genus

A number of authors cited by Traka et al. (2009), suggest a negative correlation between the consumption of vegetables belonging to Brassicaceae family and the risk of developing lung cancer (London et al., 2000, Spitz et al., 2000), stomach cancer (Keck and Finley., 2004), colon cancer (Seow et al., 2002), breast cancer (Fowke et al. 2003), urinary bladder cancer (Zhao et al. 2007) and prostate cancer (Kristal and Lampe 2002), or myocardial infarction(Cornelis et al. 2007). The amount of the glcosinolates and isotiocianates was quantified by Fahey et al., (2001) in different plant species and then state that the rocket contains 4-metiltiobutil glucosinolate with health benefits. Saphiro et al., 1998 emphasize the importance of

65 isotiocianates additional contribution for consumption of antibiotics, which destroy the intestinal flora and make impossible the conversion of the glucosinolates in isotiocianates Tram Lam Kim et al., (2010) present a study conducted on cancer due to smoking, on smokers and those who quit smoking. In that study he emphasizes that in all three categories studied, the consumption of glucosinolates improved health, even on the final stage of cancer. Traka et al., (2009), highlight the extraordinary power of isotiocianats to block the carcinogenesis even in angiogenesis and metastasis phases. In recent years arises increasing emphasis on sustainable agriculture and attempting to use least possible pesticides in controling pests and diseases, both in the field and food warehouses. Thus Shayaa et al. (2009) mention the use with positive results of Diplotaxis tenuifolia essential oil as biofumigant in food warehouses. It has been used because of high concentration of isotiocianats from plant leaves which are not toxic to humans. Klein et al., (2009) point the use of the same species as green manure in tomato and snapdragon crops to reduce infestation with Meloidogyne javanica in greenhouses. About the effects of the chemical elements from wild rocket leaves on the soil and soil organisms, more research is done, all with positive results (Yulianti et al., 2007, Lu et al., 2010).

TAXONOMY AND DISTRIBUTION

Tab. 1 List of genera and species from the tribe Brassiceae covered by the two lines Brassica (Rapa) and Sinapis (Nigra) reported by various authors processed LAKSHMIKUMARAN (GOMEZ-CAMPO et al., 1999)

SONG et al. WARWICK et al. PRADHAN et al. 1990 1991 și 1992 1992 Line Line Line Line Line Line BRASSICA SINAPIS BRASSICA SINAPIS BRASSICA SINAPIS B.rapa B.fruticosa B.rapa B.nigra B.rapa B.nigra B.oleracea B.nigra B.oleracea S.arvensis B.juncea B.carinata D.erucoides S.arvensis D.erucoides S.alba B.oleracea S.arvensis B.tournefortii S.alba B.deflexa S.flexuosa B.napus S.flexuosa E.sativa S.aucheri D.siettiana D.erucoides S.alba H.incana R.sativus B.fruticosa R.sativus D.siettiana B.oxyrrhina S.pubescens S.aucheri D.siifolia B.barrelieri B.tournefortii B.gravinae S.pubescens D.harra H.incana D.muralis H.incana E.sativa D.siifolia B.oxyrrhina B.maurorum B.gravinae E.sativa B.spinescens D.muralis D.harra B.fruticosa Er.abyssinicum B.tournefortii M.arvensis Er.varium B.souliei B. = Brassica, D. = Diplotaxis, E. = Eruca, Er. = Erucastrum, H. = Hirschfeldia, M. = Moricardia, R. = Raphanus, S. = Sinapis According to some authors (Takahata and Hinata, 1986, Song et al., 1990, Warwick and Black in 1991, 1993, 1994, 1997, Warwick et al., 1992 and Pradham et.al. 1992 cited by Gomez-Campo et al., 1999) this tribe, at least phylogenetically speaking, is divided into two lines/clans: the line "rapa/oleracea" and the line "nigra", shown in table 2. Members of numerous genra including Diplotaxis, are represented in both lines. This may explain the possibility of crossing between different species of this tribe. More than this, some authors

66 consider D. erucoides as the ancestor of B. oleracea and B. rapa species (Song et al., 1990, Warwick and Black 1991, Pradhan et al., 1992 cited by Purty et al., 2008). Genus Diplotaxis contains 31 species, divided into three subgenres. The subgenus Diplotaxis contains two major horticultural species: D. muralis and D. tenuifolia. A classification of these species (Tab.3) is made by Gomez Campo (1999) based on research done by the team of researchers from the Gene Bank in Madrid. (Gomez-Campo and Martinez-Laborde, 1998; Martinez-Laborde, 1991, 1997; Sanchez-Yelamo, 1994, 2009).

Tab. 2 Genus Diplotaxis

II. Subgen. Hesperidium (DC.) III. Subgen. Rhynchocarpum I. Subgen. Diplotaxis Mart.-Lab. (Prantl) Mart.-Lab. 1. D. tenuifolia (L.)DC. ssp, tenuifolia 5. D. harra (Forsk.) Boiss. A. Sect. Rhynchocarpum Prantl - ssp, cretacica (Kotov)Sobrino- -ssp, harra 19. D. assurgens (Del.) Gren. Vesperinas -ssp, confusa Mart.-Lab. 2. D. muralis (L.) DC. ssp, muralis -ssp, crassifolia (Rafin) Maire 20. D. tenuisiliqua Del. ssp, -ssp. ceratophylla (Batt.) Mart.-Lab -ssp, lagascana (DC.) O.Bolos tenuisiliqua and J.Vigo - ssp, rupestris (J. Ball.) Mart.-Lab. 3. D. viminea (L.) DC. 6. D. antoniensis Rustan 21. D. brachycarpa Godr. 4. D. simplex (Viv.) Spr. 7. D. glauca (Schmidt) 22. D. virgata (Cav.) DC. ssp, O.E.Schulz virgata 8. D. gorgadensis Rustan ssp, - ssp, australis Mart.-Lab. gorgadensis - ssp, rivulorum (Br.-B1. and Maire) - ssp, brochmanii Rustan Mart.-Lab. 9. D. gracilis (Webb) O.E.Schulz -ssp, sahariensis (Coss.) Mart.-Lab. 10. D. hirta (Chev.) Rustan and 23. D. berthautii Br.-B1. and Maire Borgen 11. D. sundingii Rustan 24. D. catholica (L.) DC. 12. D. varia Rustan 25. D. ollivieri Maire 13. D. vogelii (Webb) Cout. 26. D. siifolia G. Kunze. ssp, siifolia 14. D. pitardiana Maire -ssp, bipinnatifida (Coss.) Mart.-Lab. 15. D. acris (Forsk.) Boiss. -ssp, vicentina (P.Cout.) Mart.-Lab. 16. D. villosa Boul. and Jail. B. Sect. Heterocarpum Mart.-Lab. 17. D. griffithii (Hook.f. and 27. D. ibicensis (Pau) Gomez-Campo Thorns.) Boiss. 18. D. nepalensis Hara 28. D. siettiana Maire 29. D. brevisiliqua (Coss.) Mart.- Lab. 30. D. ilorcitana (Sennen) Aedo and Mart.-Lab. C. Sect. Erucoides Mart.-Lab. 31. D. erucoides (L.) DC. ssp, erucoides - ssp, longisiliqua (Coss.)Gomez- Campo

Results of research on taxonomic classification, which coincide with the one of the authors mentioned above, have been made by Martin et al., (2000) using ISSR markers and by Warwick et al., (2009b). The number of chromosomes of the species from this genus was studied by different authors (Harberd and McArthur 1980, Harberd, 1976, Harberd and McArthur 1980, Takahata and Hinata, 1983, Eschmann-Groupe et al., 2004, Sanchez-Yelamo, 2009). The smallest gametic chromosome number (n) is observed in D. erucoides (n=7), than n=8 to D. brevisiliqua, D. siettiana, D. ibicensis, D. ilorcitana. The biggest gametic chromosome number (n=21) is observed at D. muralis with the note that D.

67 muralis is considered amfidiploid dervived from D. tenuifolia (n=11) and D. viminea (n=10). Tab. 3 Areas of distribution of Diplotaxis species in the world

No Area Specie 1. Egypt, Near East and Iraq D. acris (Forsk.) Boiss. var. acris 2. S Algeria, S Tunisia, S Libya, N Chad var. duveyrieriana (Coss.) Coss. 3. Centre and N Morocco D. assurgens (Del.) Thell. 4. Central Morocco D. berthautii Br.-Bl. and Maire 5. N Algeria D. brachycarpa Godr. 6. NE Morocco, NV Algeria D. brevisiliqua (Coss.) Mart.-Laborde 7. Spain, Portugal, N Morocco D. catholica (L.) DC. var. catholica 8. Central Morocco var. rivulorum (Br.-Bl. and Maire) Maire 9. Europe, Africa de Nord, Near East to Iraq D. erucoides (L.) DC. ssp. erucoides 10. N Algeria ssp. longisiliqua (Coss.) Gómez-Campo 11. Cape Verde D. glauca (J. A. Schmidt) O.E. Schulz 12. Cape Verde D. gracilis (Webb) O.E. Schulz 13. Afghanistan, Pakistan D. griffitthii (Hook.f. and Thomps.) Boiss. 14. North Africa, V Asia, Iran D. harra (Forsk.) Boiss. ssp. harra 15. Sicilia ssp. crassifolia (Rafin.) Maire 16. SE Spain ssp. lagascana (DC.) O. Bolòs and Vigo 17. Cape Verde D. hirta (Chev.) Rustan and Borgen 18. Formentera, Cabrera, E Spain D. ibicensis (Pau) Gómez-Campo Ibiza, 19. E Spain D. ilorcitana (Sennen) Aedo et al. 20. Yemen D. kohlaanensis A. Miller and J. Nyberg N 21. Europe, N Algeria, Near East, America, etc. D. muralis (L.) DC. ssp. muralis 22. NE Algeria, N Tunisia ssp. ceratophylla (Batt.) Mart.-Laborde 23. W Nepal D. nepalensis Hara 24. S Morocco D. ollivierii Maire 25. S Morocco, S Algeria, Mauritania D. pitardiana Maire 26. Lampedusa D. scaposa DC. 27. Alboran D. siettiana Maire 28. SV Spain, N Morocco, NW Algeria D. siifolia Kunze ssp. siifolia 29. S Morocco ssp. bipinnatifida (Coss.) Mart.-Laborde 30. SV Portugal ssp. vicentina (Samp.) Mart.-Laborde 31. S Morocco to Egypt D. simplex (Viv.) Sprengel 32. Europe, Africa de N, Near East, America D. tenuifolia (L.) DC. ssp. tenuifolia 33. NE Ukraine, S Russia ssp. cretacea (Kotov) Sobr. Vesp. 34. Centre and N Morocco D. tenuisiliqua Del. ssp. tenuisiliqua 35. NW Algeria Centre Morocco ssp. rupestris (J. Ball) Mart.-Laborde 36. Jordan D. villosa Boulos and Jallad 37. Europe, Africa de Nord, Near East D. viminea (L.) DC. var. viminea 38. Europe, Africa de Nord, Near East var. integrifolia Guss. 39. Spain and Portugal, Morocco D. virgata (Cav.) DC. 40. SE Morocco, SV Algeria f. sahariensis Coss. 41. Cape Verde D. vogelii (Webb) O.E. Schulz (Martinez-Laborde, 1997) Its common name, in Romanian, is “puturoasă”, “cerenţel”, “ridichioară” (Pârvu, 2005). Worldwide the plant is known by different names: lincoln weed, mustard sand, sand large rocket, slimleaf rocket in Australia, sand rocket, wall rocket in the United States, perennial wall rocket, wild rocket in UK and rucola silvatica in Italy. The plant's scientific name combines the Greek word diploos that means double and taxis which means line and it refer to the two rows of seeds that develop in the siliqua. Although the origin of the species belonging to the genus Diplotaxis is considered the Mediterranean Basin and the Middle East, their area of distribution is very large as can be seen in Tab. 3. Koch and Kieffer (2006) observed that the only areas that have not entered this

68 very adaptable species are arctic and subarctic areas and East Asia. Hurka et al. (2003) consider that two species (D. muralis and D. tenuifolia) have the behavior of invaders. D. muralis is autogamous and polyploid, conditions necessary to acquire the status of invasive plant. Arianoutsou et al. (2010) draw attention on D.erucoides whom the authors confer the same status as the other two species mentioned above. Another factor is global warming that allows invasion of warmth loving these species even in Scandinavia or colder regions from China (Weber et al., 2008). As an assessment of the species found in the Mediteranean Basin, Martinez-Laborde (1997) stipulates that the country with the most species is Morocco with 18 representatives of this genus, followed by Algeria with 15 and Spain with 12. In Tunisia one can found seven species, in Portugal seven, in France, Greece, Syria, Lebanon and Egypt there are four representatives. In the Balcans and SE Europe three species are present: D. tenuifolia, D. muralis and D. erucoides. In Romania, wild rocket culture is virtually unknown; there are no reports or articles on these species as cultivated plants. On the other hand, some Romanian authors have found representatives of this genus in wild flora. D. muralis is found by Arsene et al. in 2006 in Banat, in Timis and Caras-Severin countys and by Făgărăs et al. (2006) at the border of the Black Sea, in Constanta county. Also Făgăras and Jianu (2007) found these species at the border of the Black Sea on Cape Midia- Corbu seashore. Mardari (2008 and 2009) claims the existance of D. muralis in the Eastern Carpathians. Also Zamfirescu (2006) founds D. muralis in the Eastern Carpathians at Izvoarele Bicazului and in Iași county at Valea lui David, Zamfirescu (2010). Arsene et al., in 2006, points out the existence of D. tenuifolia in Timis and Caras- Severin countys next to D. muralis. There are other authors that found D. tenuifolia in Romania (Făgăras et al., 2006, Pârvu, 2005). In Transylvania, Săvulescu (1952) confirms the existence of D. tenuifolia and D. muralis in the county of Cluj, in the Aries Valley and also at Cojocna and Mociu. D. erucoides is present only in Dobrogea according to Anastasiu et al., (2006).

CONCLUSION

Conservation of these species in the Romanian area is required because their great diversity. This plant can be considered important in terms of biodiversity primarily due to the need of storing a large number of ecotypes from agrobotanic species. Germplasm collection and preservation of these plants should be done also due to their character of neglected and underutilized plants.

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