REVIEW ARTICLE: AN OVERVIEW ON BIOLOGY AND ECOLOGY OF LUPINUS ALBUS L. بيولوجية وبيئة نبات الترمس:Lupinus albus L. رؤية مرجعية.

Review article: an overview on biology and ecology of  Lupinus albus L.

Omnia M Arief ^a,*   Mahmoud El- Shafie^a, Dina Baraka^a and Kamal H. Shaltout ^b

^aBotany and Microbiology Department, Faculty of Science, Benha University, Egypt

^b Botany Department, Faculty of Science, Tanta University, Egypt

^* Corresponding author. Email:  omnia.arief@fsc.bu.edu.eg

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 plant 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 Greece, 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 as the white lupin or field lupine, is a member of the genus Lupinus (family Fabaceae). Lupinus albus L. did not record in the Egyptian flora since Täckholm (1956) while Täckholm (1974) recorded it as a cultivated plant for its edible seeds and frequent as an escape from cultivation in Nile Delta and  Oases of the Libyan Desert. Also, it was recorded in Boulos (1995),El–Hadidi and Fayed (1995) and  Boulos (2009).

Shaltout et al. (2010) recorded it in the abandoned fields as well as in the fields of winter crops, and evaluated as a very common in Nile Region and Oases of the Western Desert. In the Egyptian flora (Boulos199: Lupinus digitatus Forssk. is endemic to Egypt and L. angustifolius L. which inhabit the edges of fields , Lupinus palaestinus Boiss. Is near-endimic to Sanai and Palestine, L. albus L. is cultivated and also occurs as a causal or escape from

cultivation (Shaltout 2014). Its vernacular name is termis, of which two cultivars: Giza 1 cultivated in north Egypt and Giza 2 cultivated in south Egypt.

The review reports on the current knowledge about biology and ecology of Lupinus albus L.

TAXONOMY :

 Lupinus albus L. (Fabaceae), have the following synonyms: Lupinus sativus Gaertn. and Lupinus termis Forssk Common names are bitter white lupin, broad-leaved lupin, broadleaf lupin, Egyptian lupin, European white lupin,  Mediterranean white lupin, white lupin and white lupine (Lim 2012). There are many vernacular names in many languages (Table 1).

Table (1) Vernacular names of Lupinus albus L. (Lim 2012).

PLANT MORPHOLOGY:

Lupinus albus L. is an annual, erect, branched, bushy, short-hairy herb with a strong taproot. Leaves are alternate and compound with 5-9 leaflets, nearly smooth above and hairy beneath. Individual plants produce several orders of inflorescences and branches, resulting in clusters of long, oblong pods, each cluster having 3-7 pods, and each pod containing 3-7 seeds (Jansen 2006; Lim 2012). Annual herb with white flowers in long terminal

racemes with leaves digitate with many leaflets,  seeds of L. albus larger than in others and about 12-4 mm across. (Täckholm 1974).

SEED CHARACTERISTICS:

Flowering time extends from February to April. Seed shape is slightly flattened, oval in shape, while seed color is light yellow, the hilum shape is groove, hilum elevation is sunken, and hilum position is basal. Seed texture is smooth, while seed outline is curved (Fig. 1).

Fig. (1). Fig. 1 Line drawing of Lupinus albus entire flowering plant 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 the two varieties (Giza1 and Giza 2), while the mean of its seed weight varies from 36.7 to 37.6 mg seed -1, thickness ranged from 0.4 to 1.1 cm seed-1 (Table 2), Also the seed weight varied from 33.7 to 34.2 mg seed -1 in both varieties.  

Table (2) seed characteristics of Lupinus albus varieties (Giza 1 and Giza 2); recent data estimated by the first author.

PROTEOID ROOTS:

Lupin species with a tap root system, the main root reaches the depth of 1-2 metres. Lupin roots, especially the main axis, bear nodules formed by Bradyrhizobium for nitrogen fixation.

In addition, morphological adaptations occur in many plants for

increased nutrient uptake. Proteoid roots that also known as cluster roots, can form in response to phosphorus or iron deficiency (Gardner et al. 1982; White & Robson 1989; Gilbert et al. 2000; Lambers et al. 2006b).  Lupinus albus L. 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 roots (Uhde-Stone et al. 2005).  Cluster roots can be induced by phosphorus (P) or iron (Fe) deficiency (Zhibin et al. 2012).

Lupin has the most characterized response to P shortage by plant roots with its shape and structured development, which can be considered as an evolutionary response (Niu et al. 2013). Vigorous cluster root growth under low P availability in the soil of lupin have the ability of secreting phosphotase-sAPase, under conditions of low phosphorus which hydrolyze organic phosphate in the rhizosphere and providing inorganic phosphate to the plant (Wasaki et al. 2003). Formation of cluster roots is one of the most specific root adaptations to nutrient deficiency, controlled by both shoot and root P concentrations. Cluster root release mainly citrate, but also some malate; while the major organic acid released by root tips of both non-proteoid and proteoid roots was malate. (Chunjian & Ruixia 2005).   The role of proteoid roots formation under P, Fe or K deficiencies were studied by Ruixia and Chunjian (2003) and found that root clusters formed when plants were grown under P and Fe, but not under K deficit conditions; cluster roots releases citrate and some malate.

 Nitrogen nutrition deficiency can influence cluster root formation in many wild species, but the effect of N form on cluster root formation and root exudation by white lupin is not known.  Sas et al. (2002) found that NH4-N nutrition stimulated cluster root formation and H+ extrusion by roots of P-deficient lupin Li et al. (2008) investigated the critical level of shoot phosphorus concentration for cluster-root formation in Lupinus albus and found that the localized phosphorus (P) supply affects cluster-root formation and citrate exudation; The formation of cluster roots is regulated by shoot P concentration with a critical level of 2-3 mg g-1 , citrate exudation is predominantly governed by shoot P status, whereas proton release strongly responds to local P supply.  Lin Shen et al. (2005) found a similar results when studying white lupin plants grown in nutrient solution, using a split-root system with two compartments to examine the effect of localized P supply on nutrient uptake, cluster root formation and root exudation that cluster root formation and citrate exudation are regulated by the shoot P and affected by localized supply of external P.. 

Lupin produce cluster roots, which release vast amounts of phosphate-mobilizing carboxylates (inorganic anions) mainly citrate and protons  that capable of making poorly available nutrients, in particular P, more available (Lambers et al. 2013). 

NITROGEN FIXATION:

 lupin are modulated legume capable of nitrogen fixation by nitrogen fixing Bradyrhizobium bacteria in its root nodules and increases the nitrogen level of the soil (Lim 2012).Therefore, they are tolerant to infertile soils and have long been incorporated in agricultural practice as green manure, and in rotation with other crops. In Australia, a modern farming system based on wheat:lupin rotation has been in place for over 40 years (DAFWA 2010). David et al. (2014) found that white lupine (Lupinus albus L.) fit to improve acid soils in south-western Romania  and  cultivation of  wheat  after white lupin  increased of the yield with 26%. This means that white lupin ensures the most economically advantageous increase in yield.  It is highly adapted to growth in a low-P environment. Schulze et al. (2006) found that enhanced nodulation in cluster root zones and increased potential for organic acid production in root nodules appear to contribute to lupin's elasticity to P-deficiency.

ORGIN AND GEOGRAPHICAL DISTRIBUTION:

 lupin crops were important to many Mediterranean civilizations and was domesticated in the Old and New World (Putnam 1993).  It originates from south-eastern Europe and western Asia where wild types still occur (Lim 2012). It is known to have been cultivated since ancient times in Greece, Italy, Egypt and Cyprus (Nigussie 2012). It is mainly distributed around the Mediterranean (Gladstones, 1974 as quoted by Huyghe (1997) and along  Nile Valley. In these areas, it has been traditionally cultivated for several thousand years. These cultivated populations constitute the genetic resources of the species and are all bitter materials with an indeterminate growth habit (Huyghe 1997).

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

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

PHYTOCHEMISTRY:

Methanolic seed extract of  Lupinus albus contains , reducing sugars, glycosides, , while no carboxylic acid, lipids of fatty acids present (Abdallah et al. 2017). Lupin seed storage protein is made up of 85% globulins and 15%  albumins (Petterson 1998). Compared to other grain legumes such as peas, soybean and string bean, lupins appear to contain the least amount of proteins having anti-nutritious properties: inhibitors of proteinase and hemagglutinins (Kurlovich et al. 2002). Lupins are typically low in starch and most species contain less than 1.5% in the seeds. Therefore, the non-starch polysaccharides (NSP) constitute the major portion of the carbohydrate fraction of all lupin species, typically being about 40%  (Glencross 2001). Lupinus contains alkaloids that it’s main role is to provide the plant a chemical defense against herbivores (Wink 1992).  Also, lupin has a unique traits of protein, fatty acids with a desirable ratio of omega-6 to omega-3 acids, and fibre as well as other specific components, the presence of oligosaccharides and antioxidants or non-starch carbohydrates, make lupin an excellent component in many healthy diets (Prusinski 2017).

HABITAT:

Lupin adapts best in well-drained, mildly acid or neutral soils of light to medium texture, with pH 4.5–7.5. Growth is hindered on heavy clays and waterlogged soils. Calcareous or alkaline soils cause chlorosis and reduce growth although some cultivars are more tolerant to soil salinity and heavy soils.(Lim 2012);  In Egypt it is reported that Lupinus albus could tolerate pH 7.5- 9.4 (Christiansen et al. 1999; Kerley et al. 2002). High-yielding, high-pH-tolerant, frost-tolerant dwarf cultivars, well adapted to local ecological conditions. It appears that bitter cultivars tolerate cold and disease stress better than sweet ones (Jansen 2006).

 In Egypt, The greatest area cultivated with lupin (7253 fed) was achieved in 2011 with a yield of 3.967 ton fed-1 and a total production of 6300 ton (Table 3). The minimum area cultivated with lupin (2390 fed) was obtained in 2013 with a yield of 3.549 ton fed-1 and a total production of 1760 ton (CLWR 2014).

Table (3) Area (fed), yield (ton fed-1) and production (ton) of lupin crop during 2000 to 2014.

USES:

1. In Italy, Greece, Spain, Portugal and some regions in Brazil, white lupin seeds are consumed as a popular snack (Lim 2012).  lupin is considered to be a rich source of protein with a notable content of lysine and is being increasingly used in bakery, confectionery, snacks and pastry products due to its multifunctional properties (Guillamón et al. 2010).
   1. In Ethiopia, lupin seeds are used as roasted bean (called  kolo) and to prepare a local alcoholic drink called katikala and other food products especially in the north-western part of the country (Tizazu & Emire 2010; Zelalem & Chandravanshi 2014). Also it cultivated in Ethiopia and used as 'Shiro' flour for the people living in the north western part of Ethiopia. It is also used for maintaining soil fertility and as a food (Zelalem & Chandravanshi 2014).  
   2. The composition of the seed and especially the high protein content makes lupin highly suitable for livestock diets as a protein-rich product in intensive farming systems. The low level of antinutritional factors facilitates a direct on-farm use of white lupin in self-sustained systems.
   3. Since it often can grow on land unsuitable for other crops (too saline, heavy, acid or poor), the development of cultivars adapted to tropical African conditions is highly recommended. (Jansen 2006).
   4. Before 2000 BC., L. albus in ancient Greece and Egypt was used to produce

seeds for human and animal consumption, as well as for cosmetics and medicine and during 1000-800 BC. It was also,usedas green manure in ancient Rome and, in other Mediterranean countries (Kurlovich 2002; Clements et al. 2005).  Nowadays, lupin used as a fodder and food crop, as well as an ornamental plant, and used as traditional food in the Mediterranean region and the Andean highland in South America (DAFWA 2010).

1. Seeds are used among others for the production of gluten-free flour, bacterial and fungal fermented products, noodle and pasta products, as substitutes of meat, egg protein and sausages. Also it is cooked, roasted and ground and mixed with cereal flour in the production of bread, crisps, pasta, crisps and dietary dishes (Prusinski 2017).
2. In traditional medicine, lupin is used for various disorders, for example its meal added with honey or vinegar is used as a treatment for worms, while infusions or poultices are applied for boils and skin complaints (Lim 2012). Lupin is also used as green manure crop, as forage and as livestock feed.
3. In southern Europe it is still a traditional green manure crop in vineyards and olive plantations. Lupin is a good honey plant and an attractive annual ornamental; its inflorescences are used in floral arrangements. Burning seeds are used as an insect repellent. (Lim 2012).

GENETIC RESOURCES AND BREEDING:

            Major germplasm collections of lupin are available in France (INRA, Station d’Amélioration des Plantes Fourragères, Lusignan, 1400 accessions), United Kingdom (University of Reading, Reading, 1100 accessions), Australia (Western Australian Department of Agriculture, South Perth, 890 accessions) and Spain (Servicio de Investigación y Desarrollo Tecnológico, Guadajira, 690 accessions). In tropical Africa, small collections are held in Ethiopia (International Livestock Research Institute, Addis Ababa, Ethiopia, 25 accessions) and Kenya (National Genebank of Kenya, Crop Plant Genetic Resources Centre, KARI, Kikuyu, 20 accessions) (Jansen 2006). Major objectives in breeding of white lupin are to produce rapid-growing, alkaloid-free, disease-resistant cultivars (particularly against anthracnose). The level of cross-pollination may limit the relevance of sweet white lupin cultivars in regions where also bitter weedy or cultivated types are present, because pollen of the latter would reintroduce the bitter character in farm-saved sowing seed. Sweet cultivars, however, are a prerequisite for any further breeding advancement. Commercial cultivars are pure lines bred through pedigree selection. Some well-known cultivars of white lupin are:  Eldo, Kiev, Multolupa and Ultra. From Ethiopia Bahar Dar is known. (Jansen 2006; Wolko et al. 2011).

ASSOCIATED WEEDS:

            Unfortunately, there areno recent studies about the associated weeds with lupin cultivation. In Egypt, In general, the weeds of winter crops, particularly the sand soils dominate the lupin cultivation (Morsi & Abd-Elgwad 1965). Among the weeds that expected to invade the lupin cultivation are: Vicia sativa L., Sonchus oleraceus L., Rumex dentatus L., Urtica urens L., Melilotus indica (L.) All., Malva parviflora L., Lathyrus hirsutus L., Ammi majus L., Cichorium endivia L., Anagallis arvensis L., Beta vulgaris L. and Emex spinosus (L.) Campd. (CLWR 2014) .

DISEASES:

            Lupins are susceptible to a wide range of diseases. Although lupin diseases caused by bacterial pathogens (Lu & Gross 2010). The major diseases of lupin are root rot and brown leaf spot caused by Pleiochaeta setosa, anthracnose (Colletotrichum acutatum), resulting in early plant death through stem breakage, and rust (Uromyces lupinicolus). Sources of resistance to anthracnose have been found in Ethiopian landraces, but resistant cultivars are not yet available. Bean Yellow Mosaic Virus (BYMV) is the major virus disease; it is transmitted by  seed. No sources of resistance have yet been identified.  Lupin is immune to Cucumber Mosaic Virus (CMV), a major disease of other Lupinus spp.  Pathogens that might affect Lupin are shown in Table (4).

In Ethiopia harvesting is in December. Seed yields are 500–4000 kg/ha (Jansen 2006). Anthracnose has been found in most lupin producing areas of Western Australia  and South Australia, but it is most serious in the high rainfall zone of the northern agricultural region in Western Australia  (Thomas 2003). The disease is not known to occur in lupin crops in New South Wales, Victoria or Tasmania (Davidson et al. 2007). The fungal pathogen P. setosa is responsible for both brown leaf spot and Pleiochaeta root rot diseases of lupins. It has affected lupin production in all continents where lupins are cultivated and is the most widespread and damaging pathogen of lupins in Australia, particularly in Western Australia (Sweetingham 1997; Sweetingham et al. 1998).

Table (4) Pest and pathogen cause that might affect Lupinus albus L.

ECOLOGICAL SIGNIFICANCE:

 Regular use of P fertilizers in agricultural system has raised the soil P status. This P is not readily available for plant growth, except for species like Lupinus which has a phosphorus–acquisition strategy (Lambers et al. 2013). Accessing sparingly available P, as well as being able to symbiotically fix N2 would provide Lupinus species with an ideal combination of traits to act as ecosystem engineers (Lambers et al. 2013). The efficiency of acquisition of immobile nutrients such as P depends on root architecture, function (including root hairs and cluster roots), rhizosphere modification (carboxylate and proton exudation), rhizosphere organisms, symbiotic associations (mycorrhizal and rhizobial) (Lambers et al. 2006a).

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