Ass. Univ. Bull. Environ. Res. Vol. 22 No. 1 March 2019

AUCES

REVIEW ARTICLE: AN OVERVIEW ON BIOLOGY AND

ECOLOGY OF ALBUS L. Omnia M Arief a,* Mahmoud El- Shafiea, Dina Barakaa and Kamal H. Shaltout b aBotany and Microbiology Department, Faculty of Science, Benha University, b Botany Department, Faculty of Science, Tanta University, Egypt * Corresponding author. Email: [email protected] REVIEW ARTICLE ABSTRACT: Lupinus albus L. is usually cultivated for its edible seeds. In Egypt it is frequent an escape from cultivation in Nile Delta and Oases of the Libyan Desert. Lupin has a tap root system, the main root reaches depth of 1-2 m which bears nodules formed by Bradyrhizobium for nitrogen fixation. Lupinus albus adapts to phosphorus (P) deficiency with a highly coordinated modification of root development and biochemistry resulting in short, densely clustered secondary roots called proteoid or cluster that release vast amounts of phosphate- mobilizing carboxylates capable of making poorly available nutrients more available.. It has the ability of accessing sparingly available P, as well as being able to symbiotically fixation of N2, thus it would provide Lupinus species possess ideal combination of traits to act as ecosystem engineers. This was important to many Mediterranean civilizations and was domesticated in the old world and new world. It is known to have been cultivated since ancient times in , Italy, Egypt and Cyprus. It has unique traits of protein, low starch, and contains alkaloids that provide the plant a chemical defense against herbivores. It adapts best in well-drained, mildly acid or neutral soils of light to medium texture. INTRODUCTION: Lupinus albus L., commonly known Shaltout et al. (2010) recorded it in the as the white lupin or field lupine, is a abandoned fields as well as in the fields of member of the Lupinus (family winter crops, and evaluated as a very ). Lupinus albus L. did not record common in Nile Region and Oases of the in the Egyptian flora since Täckholm (1956) Western Desert. In the Egyptian flora while Täckholm (1974) recorded it as a (Boulos199: Lupinus digitatus Forssk. is cultivated plant for its edible seeds and endemic to Egypt and L. angustifolius L. frequent as an escape from cultivation in which inhabit the edges of fields , Lupinus Nile Delta and Oases of the Libyan Desert. palaestinus Boiss. Is near-endimic to Sanai Also, it was recorded in Boulos (1995),El– and Palestine, L. albus L. is cultivated and Hadidi and Fayed (1995) and Boulos (2009). also occurs as a causal or escape from

33

Ass. Univ. Bull. Environ. Res. Vol. 22 No. 1 March 2019

cultivation (Shaltout 2014). Its vernacular Gaertn. and Lupinus termis Forssk name is termis, of which two cultivars: Giza Common names are bitter white lupin, 1 cultivated in north Egypt and Giza 2 broad-leaved lupin, broadleaf lupin, cultivated in south Egypt. Egyptian lupin, European white lupin, The review reports on the current Mediterranean white lupin, white lupin and knowledge about biology and ecology of white lupine (Lim 2012). There are many Lupinus albus L. vernacular names in many languages (Table : 1). Lupinus albus L. (Fabaceae), have the following synonyms: Lupinus sativus Table (1) Vernacular names of Lupinus albus L. (Lim 2012).

Country Common name Arabic world Bâqilâ Shâmî and Turmus China Bai Hua Yu Shan Dou and Bai Yu Shan Dou Denmark Lupina Bílá and Vlčí Bob Bílý Czech Holland hvid bitterlupin and hvid lupin; bittere lupine, lupine, lupine sort and witte lupine Estonia valge lupiin Ethiopia gibto and finnish Valkolupiini France lupin blanc, lupin llanc amer, lupin d’egypte Germany ägyptische lupin, weisse lupine, weiße lupine, weiße bitterlupine and wolfsbohne; turmus lavan Italy lupino bianco, lupino bianco amaro and lupino egiziano Japan shiro bana ruupin Korea paek saek ru p’in Norway hvit lupin polish and lubin biały; tremoceiro branco and tremoço branco amargo Romania lupin alb, Russia ljupin belyj altramuz, alttrramuz blanco, altramuz blanco amargo and tramuso Sweden vitlupin; Turkey aci bakla, ak aci bakla, misir baklasi and yahudi bakla

PLANT MORPHOLOGY: racemes with leaves digitate with many leaflets, seeds of L. albus larger than in Lupinus albus L. is an annual, others and about 12-4 mm across. erect, branched, bushy, short-hairy herb (Täckholm 1974). with a strong taproot. Leaves are alternate and compound with 5-9 leaflets, nearly SEED CHARACTERISTICS: smooth above and hairy beneath. Individual Flowering time extends from produce several orders of February to April. Seed shape is slightly inflorescences and branches, resulting in flattened, oval in shape, while seed color is clusters of long, oblong pods, each cluster light yellow, the hilum shape is groove, having 3-7 pods, and each pod containing 3- hilum elevation is sunken, and hilum 7 seeds (Jansen 2006; Lim 2012). Annual position is basal. Seed texture is smooth, herb with white flowers in long terminal while seed outline is curved (Fig. 1).

34

Ass. Univ. Bull. Environ. Res. Vol. 22 No. 1 March 2019

Fig. (1). Fig. 1 Line drawing of Lupinus albus entire with pod, after Philibert (2019). The quantitative characters of Lupinus albus seeds shows that the mean of the seed

length and width almost the same in 0.4 to 1.1 cm seed-1 (Table 2), Also the seed the two varieties (Giza1 and Giza 2), while weight varied from 33.7 to 34.2 mg seed -1 the mean of its seed weight varies from 36.7 in both varieties. to 37.6 mg seed -1, thickness ranged from Table (2) seed characteristics of Lupinus albus varieties (Giza 1 and Giza 2); recent data estimated by the first author. Character Giza1 Giza2 Max. Min. M. SD Max. Min. M. SD Length (cm seed-1) 1.3 0.7 0.98 0.092 1.5 0.5 0.98 0.15 Width (cm seed-1) 1.2 0.6 0.98 0.11 1.9 0.1 0.98 0.19 Thickness (cm seed-1) 1.1 0.1 0.26 0.103 0.4 0.1 0.25 0.064 Weight (mg seed-1) 36.69 30.96 33.65 1.62 37.55 30.54 34.22 2.10

PROTEOID ROOTS: Lupin species with a tap root increased nutrient uptake. Proteoid roots system, the main root reaches the depth of that also known as cluster roots, can form in 1-2 metres. Lupin roots, especially the main response to phosphorus or iron deficiency axis, bear nodules formed by (Gardner et al. 1982; White & Robson 1989; Bradyrhizobium for nitrogen fixation. Gilbert et al. 2000; Lambers et al. 2006b). In addition, morphological Lupinus albus L. adapts to phosphorus (P) adaptations occur in many plants for deficiency with a highly coordinated 35

Ass. Univ. Bull. Environ. Res. Vol. 22 No. 1 March 2019

modification of root development and deficit conditions; cluster roots releases biochemistry resulting in short, densely citrate and some malate. clustered secondary roots called proteoid or Nitrogen nutrition deficiency can cluster roots (Uhde-Stone et al. 2005). influence cluster root formation in many Cluster roots can be induced by phosphorus wild species, but the effect of N form on (P) or iron (Fe) deficiency (Zhibin et al. cluster root formation and root exudation 2012). by white lupin is not known. Sas et al. Lupin has the most characterized (2002) found that NH4-N nutrition response to P shortage by plant roots with stimulated cluster root formation and H+ its shape and structured development, extrusion by roots of P-deficient lupin Li et which can be considered as an evolutionary al. (2008) investigated the critical level of response (Niu et al. 2013). Vigorous cluster shoot phosphorus concentration for cluster- root growth under low P availability in the root formation in Lupinus albus and found soil of lupin have the ability of secreting that the localized phosphorus (P) supply phosphotase-sAPase, under conditions of affects cluster-root formation and citrate low phosphorus which hydrolyze organic exudation; The formation of cluster roots is phosphate in the rhizosphere and providing regulated by shoot P concentration with a inorganic phosphate to the plant (Wasaki et critical level of 2-3 mg g-1 , citrate al. 2003). Formation of cluster roots is one exudation is predominantly governed by of the most specific root adaptations to shoot P status, whereas proton release nutrient deficiency, controlled by both shoot strongly responds to local P supply. Lin and root P concentrations. Cluster root Shen et al. (2005) found a similar results release mainly citrate, but also some malate; when studying white lupin plants grown in while the major organic acid released by nutrient solution, using a split-root system root tips of both non-proteoid and proteoid with two compartments to examine the roots was malate. (Chunjian & Ruixia effect of localized P supply on nutrient 2005). The role of proteoid roots formation uptake, cluster root formation and root under P, Fe or K deficiencies were studied exudation that cluster root formation and by Ruixia and Chunjian (2003) and found citrate exudation are regulated by the shoot that root clusters formed when plants were P and affected by localized supply of grown under P and Fe, but not under K external P..

36

Ass. Univ. Bull. Environ. Res. Vol. 22 No. 1 March 2019

- Fig. (2): Lupinus albus entire root with proteoid roots; photos taken by the first author.

Lupin produce cluster roots, which low-P environment. Schulze et al. (2006) release vast amounts of phosphate- found that enhanced nodulation in cluster mobilizing carboxylates (inorganic anions) root zones and increased potential for mainly citrate and protons that capable of organic acid production in root nodules making poorly available nutrients, in appear to contribute to lupin's elasticity to particular P, more available (Lambers et al. P-deficiency. 2013). ORGIN AND GEOGRAPHICAL NITROGEN FIXATION: DISTRIBUTION: lupin are modulated lupin crops were important to capable of nitrogen fixation by nitrogen many Mediterranean civilizations and was fixing Bradyrhizobium bacteria in its root domesticated in the Old and New World nodules and increases the nitrogen level of (Putnam 1993). It originates from south- the soil (Lim 2012).Therefore, they are eastern Europe and western Asia where tolerant to infertile soils and have long been wild types still occur (Lim 2012). It is known incorporated in agricultural practice as to have been cultivated since ancient times green manure, and in rotation with other in Greece, Italy, Egypt and Cyprus crops. In Australia, a modern farming (Nigussie 2012). It is mainly distributed system based on wheat:lupin rotation has around the Mediterranean (Gladstones, been in place for over 40 years (DAFWA 1974 as quoted by Huyghe (1997) and along 2010). David et al. (2014) found that white Nile Valley. In these areas, it has been lupine (Lupinus albus L.) fit to improve acid traditionally cultivated for several thousand soils in south-western Romania and years. These cultivated populations cultivation of wheat after white lupin constitute the genetic resources of the increased of the yield with 26%. This means species and are all bitter materials with an that white lupin ensures the most indeterminate growth habit (Huyghe 1997). economically advantageous increase in yield. It is highly adapted to growth in a 37

Ass. Univ. Bull. Environ. Res. Vol. 22 No. 1 March 2019

Lupinus cultivated types are during the history of its cultivation; at distinguished as subsp. albus (synonym: present it has almost disappeared in central Lupinus termis Forssk.). The distribution Europe, while it is becoming more widely area of lupin is in South Africa and grown in the Americas. (Fig. 3) Today it is a Americas where mostly sweet low-alkaloid traditional minor pulse crop, grown around modern cultivars are grown, whereas in the the Mediterranean and the Black Sea, and Mediterranean region and eastern Africa in the Nile valley, extending to Sudan and bitter landraces prevail (Jansen 2006). The Ethiopia (Nigussie 2012). importance of lupin has fluctuated often

Fig. (3). Global distribution of Lupinus albus L. (grey color) in the World (prepared by the first author)

In Egypt, Lupinus albus is Suef , Ismailia, Minea, Assiut , Suhag Qena cultivated in nearly all the country (Fig. 4): and Aswan (Statistical information Minstry Sharkia, Ismaillia , Menoufia, Giza , Beni of cultivation in Egypt 2001-2014).

Fig. (4). Map showing Lupinus Cultivation In Egypt. Ismailia, Giza, Beni Suef, Minea, Assuit, Qena, Aswan.

38

Ass. Univ. Bull. Environ. Res. Vol. 22 No. 1 March 2019

PHYTOCHEMISTRY: make lupin an excellent component in many healthy diets (Prusinski 2017). Methanolic seed extract of Lupinus albus contains , reducing sugars, glycosides, HABITAT: , while no carboxylic acid, lipids of fatty Lupin adapts best in well-drained, acids present (Abdallah et al. 2017). Lupin mildly acid or neutral soils of light to seed storage protein is made up of 85% medium texture, with pH 4.5–7.5. Growth is globulins and 15% albumins (Petterson hindered on heavy clays and waterlogged 1998). Compared to other grain soils. Calcareous or alkaline soils cause such as peas, and string , chlorosis and reduce growth although some lupins appear to contain the least amount of cultivars are more tolerant to soil salinity proteins having anti-nutritious properties: and heavy soils.(Lim 2012); In Egypt it is inhibitors of proteinase and hemagglutinins reported that Lupinus albus could tolerate (Kurlovich et al. 2002). Lupins are typically pH 7.5- 9.4 (Christiansen et al. 1999; Kerley low in starch and most species contain less et al. 2002). High-yielding, high-pH-tolerant, than 1.5% in the seeds. Therefore, the non- frost-tolerant dwarf cultivars, well adapted starch polysaccharides (NSP) constitute the to local ecological conditions. It appears that major portion of the carbohydrate fraction bitter cultivars tolerate cold and disease of all lupin species, typically being about stress better than sweet ones (Jansen 2006). 40% (Glencross 2001). Lupinus contains In Egypt, The greatest area alkaloids that it’s main role is to provide the cultivated with lupin (7253 fed) was plant a chemical defense against herbivores achieved in 2011 with a yield of 3.967 ton (Wink 1992). Also, lupin has a unique traits fed-1 and a total production of 6300 ton of protein, fatty acids with a desirable ratio (Table 3). The minimum area cultivated of omega-6 to omega-3 acids, and fibre as with lupin (2390 fed) was obtained in 2013 well as other specific components, the with a yield of 3.549 ton fed-1 and a total presence of oligosaccharides and production of 1760 ton (CLWR 2014). antioxidants or non-starch carbohydrates, Table (3) Area (fed), yield (ton fed-1) and production (ton) of lupin crop during 2000 to 2014. Total New Land Old Land year Area Yield Prod. Area Yield Prod. Area Yield Prod. (fed) (ton fed-1) (ton) (fed) (ton fed-1) (ton) (fed) (ton fed-1) (ton) 2000 6354 0.671 4264 1960 0.397 778 4394 0.793 3486 2006 3417 0.815 2784 823 0.617 508 2594 0.877 2276 2007 3745 0.770 2885 1695 0.625 1060 2050 0.890 1825 2008 3098 0.770 2384 1524 0.730 1113 1574 0.807 1271 2009 7025 3.95 5735 4065 2.041 2738 2960 4.202 3024 2010 7126 3.923 6128 3429 2.21 2577 3697 4.163 3551 2011 7253 3.967 6300 4102 2216 3246 3151 4.198 3054 2012 2603 3.78 3068 1379 3.133 1064 2224 4.241 2004 2013 2390 3.549 1760 1363 2.246 999 1054 3.499 761 2014 2570 3.468 1839 1796 1.416 1271 774 0.734 568

39

Ass. Univ. Bull. Environ. Res. Vol. 22 No. 1 March 2019

USES: seeds for human and animal consumption, as well as for cosmetics 1. In Italy, Greece, Spain, Portugal and and medicine and during 1000-800 BC. some regions in , white lupin seeds It was also, used as green manure in are consumed as a popular snack (Lim ancient Rome and, in other 2012). lupin is considered to be a rich Mediterranean countries (Kurlovich source of protein with a notable content 2002; Clements et al. 2005). Nowadays, of lysine and is being increasingly used in lupin used as a fodder and food crop, bakery, confectionery, snacks and pastry as well as an ornamental plant, and products due to its multifunctional used as traditional food in the properties (Guillamón et al. 2010). Mediterranean region and the Andean 2. In Ethiopia, lupin seeds are used as highland in South America (DAFWA roasted bean (called kolo) and to 2010). prepare a local alcoholic drink called 6. Seeds are used among others for the katikala and other food products production of gluten-free flour, especially in the north-western part of bacterial and fungal fermented the country (Tizazu & Emire 2010; products, noodle and pasta products, Zelalem & Chandravanshi 2014). Also as substitutes of meat, egg protein and it cultivated in Ethiopia and used as sausages. Also it is cooked, roasted and 'Shiro' flour for the people living in the ground and mixed with cereal flour in north western part of Ethiopia. It is the production of bread, crisps, pasta, also used for maintaining soil fertility crisps and dietary dishes (Prusinski and as a food (Zelalem & 2017). Chandravanshi 2014). 7. In traditional medicine, lupin is used 3. The composition of the seed and for various disorders, for example its especially the high protein content meal added with honey or vinegar is makes lupin highly suitable for used as a treatment for worms, while livestock diets as a protein-rich infusions or poultices are applied for product in intensive farming systems. boils and skin complaints (Lim 2012). The low level of antinutritional factors Lupin is also used as green manure facilitates a direct on-farm use of white crop, as forage and as livestock feed. lupin in self-sustained systems. 8. In southern Europe it is still a 4. Since it often can grow on land traditional green manure crop in unsuitable for other crops (too saline, vineyards and olive plantations. Lupin heavy, acid or poor), the development is a good honey plant and an attractive of cultivars adapted to tropical African annual ornamental; its inflorescences conditions is highly recommended. are used in floral arrangements. (Jansen 2006). Burning seeds are used as an insect 5. Before 2000 BC., L. albus in ancient repellent. (Lim 2012). Greece and Egypt was used to produce

40

Ass. Univ. Bull. Environ. Res. Vol. 22 No. 1 March 2019

GENETIC RESOURCES AND ASSOCIATED WEEDS: BREEDING: Unfortunately, there areno recent studies about the associated weeds with Major germplasm collections of lupin cultivation. In Egypt, In general, the lupin are available in France (INRA, Station weeds of winter crops, particularly the sand d’Amélioration des Plantes Fourragères, soils dominate the lupin cultivation (Morsi Lusignan, 1400 accessions), United & Abd-Elgwad 1965). Among the weeds Kingdom (University of Reading, Reading, that expected to invade the lupin cultivation 1100 accessions), Australia (Western are: Vicia sativa L., Sonchus oleraceus L., Australian Department of Agriculture, Rumex dentatus L., Urtica urens L., South Perth, 890 accessions) and Spain Melilotus indica (L.) All., Malva parviflora (Servicio de Investigación y Desarrollo L., Lathyrus hirsutus L., Ammi majus L., Tecnológico, Guadajira, 690 accessions). In Cichorium endivia L., Anagallis arvensis L., tropical Africa, small collections are held in Beta vulgaris L. and Emex spinosus (L.) Ethiopia (International Livestock Research Campd. (CLWR 2014) . Institute, Addis Ababa, Ethiopia, 25 accessions) and Kenya (National Genebank DISEASES: of Kenya, Crop Plant Genetic Resources Lupins are susceptible to a wide Centre, KARI, Kikuyu, 20 accessions) range of diseases. Although lupin diseases (Jansen 2006). Major objectives in breeding caused by bacterial pathogens (Lu & Gross of white lupin are to produce rapid- 2010). The major diseases of lupin are root growing, alkaloid-free, disease-resistant rot and brown leaf spot caused by cultivars (particularly against anthracnose). Pleiochaeta setosa, anthracnose The level of cross-pollination may limit the (Colletotrichum acutatum), resulting in relevance of sweet white lupin cultivars in early plant death through stem breakage, regions where also bitter weedy or and rust (Uromyces lupinicolus). Sources of cultivated types are present, because pollen resistance to anthracnose have been found of the latter would reintroduce the bitter in Ethiopian landraces, but resistant character in farm-saved sowing seed. Sweet cultivars are not yet available. Bean Yellow cultivars, however, are a prerequisite for Mosaic Virus (BYMV) is the major virus any further breeding advancement. disease; it is transmitted by seed. No Commercial cultivars are pure lines bred sources of resistance have yet been through pedigree selection. Some well- identified. Lupin is immune to Cucumber known cultivars of white lupin are: Eldo, Mosaic Virus (CMV), a major disease of Kiev, Multolupa and Ultra. From Ethiopia other Lupinus spp. Pathogens that might Bahar Dar is known. (Jansen 2006; Wolko affect Lupin are shown in Table (4). et al. 2011).

41

Ass. Univ. Bull. Environ. Res. Vol. 22 No. 1 March 2019

In Ethiopia harvesting is in al. 2007). The fungal pathogen P. setosa is December. Seed yields are 500–4000 kg/ha responsible for both brown leaf spot and (Jansen 2006). Anthracnose has been found Pleiochaeta root rot diseases of lupins. It has in most lupin producing areas of Western affected lupin production in all continents Australia and South Australia, but it is where lupins are cultivated and is the most most serious in the high rainfall zone of the widespread and damaging pathogen of northern agricultural region in Western lupins in Australia, particularly in Western Australia (Thomas 2003). The disease is not Australia (Sweetingham 1997; Sweetingham known to occur in lupin crops in New South et al. 1998). Wales, Victoria or Tasmania (Davidson et Table (4) Pest and pathogen cause that might affect Lupinus albus L. Pest Pathogen Cause Bean seedling maggot (Delia platura seedlings to wilt and die and moth larvae (Agriotes and Agrotis spp. killing seedlings Slugs attacking leaves (Frankliniella spp. attacking flower buds and leaves Mirid bugs attacking young pods Budworms Helicoverpa armigera feeding on pod and seed

ECOLOGICAL SIGNIFICANCE: REFERENCES: Regular use of P fertilizers in Abdallah E M, Qureshi K A and agricultural system has raised the soil P Musa K H (2017). Antimicrobial, status. This P is not readily available for antioxidant and phytochemical screening of plant growth, except for species like Lupin seeds (Lupinus termis Forrsk.) from Lupinus which has a phosphorus– Sudan. CIBTech Journal of Microbiology 6, acquisition strategy (Lambers et al. 2013). 1-8. Accessing sparingly available P, as well as Boulos L (1995). Flora of Egypt: being able to symbiotically fix N2 would checklist. . Al – Hadara Publishing, Cairo. . provide Lupinus species with an ideal Boulos L (2009). Flora of Egypt: combination of traits to act as ecosystem checklist. Cairo: Al–Hadara Publishing. engineers (Lambers et al. 2013). The Christiansen J L, Raza S and Ortiz efficiency of acquisition of immobile R (1999). White lupin (Lupinus albus L.) nutrients such as P depends on root germplasm collection and preliminary in architecture, function (including root hairs situ diversity assessment in Egypt. Genetic and cluster roots), rhizosphere modification Resources and Crop Evolution 46 (2), 169- (carboxylate and proton exudation), 174. rhizosphere organisms, symbiotic Chunjian L and Ruixia L (2005). associations (mycorrhizal and rhizobial) Root cluster formation and citrate (Lambers et al. 2006a).

42

Ass. Univ. Bull. Environ. Res. Vol. 22 No. 1 March 2019

exudation of white lupin (Lupinus albus L.) Glencross B D (2001). Feeding as related to phosphorus availability. lupins to fish : A review of the nutritional Journal of Integrative Plant Biology 47 (2), and biological value of lupins in aquaculture 172-177. feeds. . The Department of Fisheries, Clements J C, Buirchell B J, Yang Government of Western Australia (DFWA). H, Smith P M C, Sweetingham M W and Guillamón E, Rodríguez J, Smith C G (2005). Lupin Chapter 9 In R Burbano C, Muzquiz M, Pedrosa M M, Singh, P Jauhar, eds. Genetic Resources, Cabanillas B, Crespo J F, Sancho A I, Mills Chromosome Engineering, and Crop E N C and Cuadrado C (2010). Improvement: Volume 1. Grain Legumes.: Characterization of lupin major allergens ( CRC Press. Lupinus albus L.) Molecular Nutrition & CLWR (2014). Central lab of weed Food Research 54 (11 ), 1668–1676. research (CLWR): Winter weeds Huyghe C (1997). White lupin DAFWA (2010). Lupin in Western (Lupinus albus L.). Field Crops Research 53 Australian farming. . (Ed G. o. W. A. (1), 147-160. Department of Agriculture and Food). Jansen P C M (2006). Lupinus David G, Borcean A, Imbrea F and albus L. Wageningen, Netherlands.: Botos L (2014). White lupin (Lupinus albus PROTA (Plant Resources of Tropical Africa L.): a plant fit to improve acid soils in south- / Ressources végétales de l’Afrique western Romania and an important source tropicale). of protein. Research Journal of Agricultural Kerley S J, Norgaard C, Leach J E, Science 46 (1), 198-202. Christiansen J L, Huyghe C and Römer P Davidson J, Egan J, Hannay J and (2002). The development of potential screens Hawthorne W (2007). Lupin anthracnose based on shoot calcium and iron disease. Fact Sheet No. 52/00 (Ed D. o. P. I. concentrations for the evaluation of a. R. S. Australia). tolerance in Egyptian genotypes of white El–Hadidi M N and Fayed A lupin ( Lupinus albus L.) to limed soils. (1995). Material for excursion flora of Egypt Annals of Botany 89 (3), 341-349. (EFE). Taeckholmia 15, 1 - 233. Kurlovich B S (2002). The history Gardner W K, Parbery D G and of lupin domestication. Chapter 5. In BS Barber D A (1982). The acquisition of Kurlovich, ed. Lupins (Geography, phosphorus by Lupinus albus L. I. Some classification, genetic resources and characteristics of the soil/root interface. breeding) pp. 147-164. OY International Plant and Soil 68 (1), 19-32. North Express. St. Petersburg, Russia - Gilbert G A, Knight J D, Vance C P Pellosniemi, Finland. and Allan D L (2000). Proteoid Root Kurlovich B S, Kartuzova L T, Development of Phosphorus Deficient Lupin Heinanen J, Benken I I, Chmeleva Z V and is Mimicked by Auxin and Phosphonate. Bernatskaya M L (2002). Biochemical Annals of Botany 85 (921-928). composition. Chapter 9. In Lupins

43

Ass. Univ. Bull. Environ. Res. Vol. 22 No. 1 March 2019

(Geography, classification, genetic resources localized supply of phosphorus in a split- and breeding) (Ed e. BS Kurlovich), pp. root system. Plant Science 168 (3), 837-845. 241-268. OY International North Express. Lu S E and Gross D C (2010). St. Petersburg, Russia - Pellosniemi, Drippy pod of white lupine: A new bacterial Finland. disease caused by a pathovar of Brenneria Lambers H, Shane M W, Cramer quercina. Plant Disease 94, 1431-1440. M D, Pearse S J and Veneklaas E J (2006a). Morsi M A and Abd-Elgwad A-E Root Structure and Functioning for (1965). Field crops, part 1: The basics of Efficient Acquisition of Phosphorus: crop production. Matching Morphological and Physiological Nigussie Z (2012). contribution of Traits. pp. 693-713. Oxford University white lupin (Lupinus albus L.) for food Press. security in north- western Ethiopia: A Lambers H, Shane M W, Cramer review. Asian Journal of Plant Sciences 11 M D, Pearse S J and Veneklaas E J (2006b). (5), 200-205. Root structure and functioning for efficient Niu Y F, Chai R S, Jin G L, Wang acquisition of phosphorus: Matching H, Tang C X and Zhang Y S (2013). morphological and physiological traits. Ann Responses of root architecture development Bot 98 (4), 693-713. to low phosphorus availability: a review. Lambers H, Clements J C and Ann Bot 112 (2), 391-408. Nelson M N (2013). How a phosphorus‐ Petterson D S (1998). Composition acquisition strategy based on carboxylate and food uses of lupins. Chapter 12. In exudation powers the success and Lupins as crop plants: biology, production agronomic potential of lupines (Lupinus, and utilization (Ed C. A. JS Gladstones, J Fabaceae). American Journal of Botany 100 Hamblin, eds. ), pp. 353-384. UK: CAB (2), 263-288. International Wallingford. Li H G, Shen J B, Zhang F S, Tang Philibert N (2019). White lupin C X and Lambers H (2008). Is there a (Lupinus albus) entire flowering plant with critical level of shoot phosphorus pod. Coloured etching by C. Pierre, c. 1865, concentration for cluster-root formation in after P. Naudin. Lupinus albus? Functional Plant Biology 35 Prusinski J (2017). White Lupin (4), 328-336. (Lupinus albus L.) - Nutritional and Health Lim T K (2012). Lupinus albus. In Values in Human Nutrition - a Review. Edible medicinal and non-medicinal plants Czech Journal of Food Sciences 35 (2), 95- pp. 763-769. Netherlands: Dordrecht: 105. Springer Putnam D H (1993). An Lin Shen J, Li H, G. N and Zhang F interdisciplinary approach to the (2005). Nutrient uptake, cluster root development of lupin as an alternative crop. formation and exudation of protons and . In New crops pp. 266-277. John Wiley and citrate in Lupinus albus as affected by Sons, Inc.

44

Ass. Univ. Bull. Environ. Res. Vol. 22 No. 1 March 2019

Ruixia L and Chunjian L (2003). management. Farmnote No. 15/2003 (Ed W. Differences in cluster-root formation and A. Department of Agriculture and Food). carboxylate exudation in Lupinus albus L. Tizazu H and Emire S A (2010). under different nutrient deficiencies. Plant Chemical composition, physicochemical and and Soil 248 (1-2), 221-227. functional properties of lupin seeds grown Sas L, Rengel Z and Tang C (2002). in Ethiopia. Afr J Food Agric Nutr Dev 10 The effect of nitrogen nutrition on cluster (8). root formation and proton extrusion by Uhde-Stone C, Liu J, Zinn K E, Lupinus albus. Annals of Botany 89 (4), 435- Allan D and Vance C P (2005). Transgenic 442. proteoid roots of white lupin: a vehicle for Schulze J, Temple G, Temple S J, characterizing and silencing root genes Beschow H and Vance C P (2006). Nitrogen involved in adaptation to P stress. Plant fixation by white lupin under phosphorus Journal. 44 (5), 840-853. deficiency. Annals of Botany 98 (4), 731-740. Wasaki J, Yamamura T, Shinano T Shaltout K, Sharaf El-Din A and and Osaki M (2003). Secreted acid Ahmed D (2010). Plant Life in the Nile phosphatase is expressed in cluster roots of Delta. lupin in response to phosphorus deficiency. Shaltout S K (2014). Ecological Plant & Soil. 248 (1-2), 129-136. study on the alien species in the Egyptian White P and Robson A (1989). flora. . Faculty of Science, Tanta University, Rhizosphere acidification and Fe3+ Tanta. reduction in lupins and peas: Iron Sweetingham M (1997). Brown spot deficiency in lupins is not due to a poor and Pleiochaeta root rot of lupins. Farmnote ability to reduce Fe3+. Plant and Soil 119, No. 5/96 Department of Agriculture and 163-175. Food, Western Australia. Wink M (1992). The role of Sweetingham M W, Jones R A C quinolizidine alkaloids in plant insect and Brown A G P (1998). Diseases and interactions. In EA Bernays, ed. Insect-plant pests. Chapter 9. In JS Gladstones, CA interactions pp. 133-169. CRC-Press Boca Atkins, J Hamblin, eds. Lupins as crop Raton. plants: biology, production and utilization Wolko B, Clements J, Naganowska pp. 263-289. CAB International B, Nelson M and Yang H (2011). Lupinus. Wallingford, UK. In Wild Crop Relatives : Genomic and Täckholm V (1956). Students’ Flora Breeding Resources : Legume Crops and of Egypt.: Anglo-Egyptian Bookshop, Cairo. Forages pp. 153-206. Springer Heidelberg. Täckholm V (1974). Students’ Flora Zelalem K A and Chandravanshi B of Egypt: 2nd edition. Cairo: Cairo S (2014). Levels of essential and non- University Press. essential elements in raw and processed Thomas G (2003). Lupin Lupinus albus L. (white lupin, Gibto) anthracnose - identification and cultivated in Ethiopia. African Journal of

45

Ass. Univ. Bull. Environ. Res. Vol. 22 No. 1 March 2019

Food, Agriculture, Nutrition and molecule in phosphorus- and iron- Development 14 (5), 2015-2035. deficiency-induced formation of cluster Zhibin M, Liqian C, Dong S, roots in white lupin (Lupinus albus). Annals Guixin L, Caixian T and Shaojian Z (2012). of Botany 109 (6), 1055-1064. Nitric oxide is the shared signalling

بيولوجية وبيئة نبات الرتمس .Lupinus albus L: رؤية مرجعية.

امللخص العربي :

46