Lupins are known for their ability to thrive on soils of low fertility. However, there is distinct variation among lupin species in responses to various abiotic stresses, given the range of environments in which lupins are distributed. Lupins characteristically grow on well-drained acidic to neutral soils and are generally intolerant to extremely alkaline or saline soils and waterlogging (Dracup et al. 1998b).
6.1 Abiotic stresses
6.1.1 Nutrient stress
Due to their capability to fix atmospheric nitrogen through nodulation of nitrogen fixation bacteria, most lupin crops are used as a source of nitrogen in farming systems and nitrogen deficiency is generally not a concern. However, deficiency of other minerals such as phosphorus, cobalt, copper and iron can all affect nodulation and nitrogen fixation and therefore lead to nitrogen deficiency (Longnecker et al. 1998). For some nutrients, such as phosphorus, manganese and boron, stress comes from either deficiency of the element, which leads to reduced growth or other abnormal symptoms, or toxic effects when the concentration of the element exceeds certain levels in the plant (Brennan et al. 2008).
Without water limitation, inadequate phosphorus is frequently the limiting factor for lupin growth. Seed phosphorus concentration has been shown to have an effect on early vigour and even final grain yield (Bolland et al. 1990). Seedlings of L. angustifolius grown from seed with low phosphorus concentration (less than 0.021 %) had decreased early growth even if adequate phosphorus was supplied (Thomson et al. 1992). Phosphorus deficiency in soil also limits vegetative growth and nodulation, and leads to decreased harvest index for L. angustifolius (Jarvis & Bolland 1991).
Iron deficiency is one cause of the poor growth of lupin on fine-textured alkaline soils (White & Robson 1989b). The primary symptom of iron deficiency is interveinal chlorosis, the development of a yellow leaf with a network of dark green veins. When grown on the same alkaline soil deficient in iron, L. angustifolius, L. luteus and L. albus showed more severe chlorosis than L. atlanticus, L. pilosus and L. cosentinii (Tang et al. 1995).
In general, lupin crops are less susceptible to zinc deficiency than cereal crops such as corn, wheat and oats. Sensitivity to zinc-deficient soil also varies among species. L. albus is more sensitive than L. angustifolius and sensitivity to zinc deficiency has not been observed in rough-seeded L. atlanticus and L. pilosus (Longnecker et al. 1998). On the other hand, excessive zinc can cause phytotoxicity. Pastor et al. (2003) showed that L. albus growth was severely affected when zinc concentration in soil exceeded 300 ppm.
Cobalt is not required by lupins but it is required by the Bradyrhizobia (nitrogen fixing bacteria) in root nodules (Brennan et al. 2008). Cobalt deficiency is likely to limit nitrogen fixation by effects on both multiplication of bradyrhizobial and nodule function. L. angustifolius is particularly sensitive to cobalt deficiency. Seeds with low cobalt concentrations sown into soils deficient in cobalt will produce poorly-nodulated roots with ineffective nodules (Brennan et al. 2008).
Grain yields of lupin can be substantially reduced by manganese deficiency, but shoot yields are generally not affected (Brennan 1999). L. angustifolius has a poor ability to accumulate manganese in its grain and low availability is a common problem in soils used for production of L. angustifolius in WA (Longnecker et al. 1998). Manganese deficiency leads to split seed disorder (also called split seed syndrome) and sometimes to discolouration around the margins of the split seed (Brennan et al. 2008; Perry & Gartrell 1976; Walton 1978). The seed may also be small, shrivelled and poorly developed. Plants suffering from this deficiency show delayed maturity and produce lower yields (Brennan et al. 2008). The viability of seeds with manganese content less than 13 mg/kg, is greatly reduced compared with concentrations higher than 13 mg/kg (Brennan & Longnecker 2001).
There is a narrow range of boron levels in soil between deficiency and toxicity for most crop species (Brennan et al. 2008). Lupin plants grown in soils deficient in boron may have reduced pod set (Wong 2003).
6.1.2 Temperature stress
As mentioned in Section 4.4, the optimum temperature for lupin germination and growth is around 20°C.
Lupins are generally cold tolerant. For a majority of lupin species, minimum temperature for seed germination is low at about 2 to 3°C (Kurlovich & Heinanen 2002). According to Barbacki (1960), annual lupin species are capable of enduring severe frost. For instance, L. albus, L. luteus and L. angustifolius can tolerate temperatures as low as -6, -8 and -9°C, respectively. However, tolerance to low temperatures also depends on the interaction of a genotype with ecological and geographical features and the phase of plant development.
Germination and emergence of L. angustifolius are reduced when soil temperature is higher than 20°C, with almost no germination and emergence at 30°C (Dracup et al. 1993).
Reproductive tissues are particularly sensitive to high temperature. Likely consequences of high temperatures (above 30°C) around flowering include male sterility, reduced pollen tube elongation, and lowered pod and seed set (Dracup et al. 1998b).
6.1.3 Water stress
In the Mediterranean environment of WA, lupin yields have been variable, largely attributed to the amount and distribution of rainfall, and the water-holding capacity of the soil. For example, drought terminates the growing season of L. angustifolius, and the timing and intensity of this terminal drought are among the main causes of the variability of yield and harvest index (Dracup et al. 1998a). Water deficit during seed filling can hasten seed development and cause pod and seed abortion, therefore the effect of terminal stress is greater on the later formed pods (Dracup & Kirby 1996b).
Under water-stress conditions, lupin switches quickly from vegetative to reproductive mode, shortening the post-flowering phases, and the duration of pod and seed-filling (Dracup & Kirby 1996b; French & Turner 1991). However, lupins are also able to avoid reproductive failure caused by water deficit through accumulating reserves (eg sugars) in certain organs (Pinheiro et al. 2001; Rodrigues et al. 1995). Rodrigues et al. (1995) showed that L. albus responded to water deficit during flowering by losing 50% of the total leaf canopy and increasing stem dry weight by 55%, whilst maintaining total seed production.
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Lupins are considered relatively intolerant to waterlogging, although tolerance within the genus varies. The adaptation of some cultivated lupin species to waterlogging is shown in Table 2 in Section 2.3.2. Symptoms of waterlogging include wilting, chlorosis and pigmentation of the oldest leaves and cotyledons, but which of these responses occur first depends on the species and conditions (Davies et al. 2000; Dracup et al. 1998b).
Seeds, seedlings and mature plants respond to waterlogging differently. The growth stage at which waterlogging occurs and its duration are important in determining the overall damages. Lupin seeds are sensitive to waterlogging. For example, in waterlogged soil L. angustifolius seeds did not germinate and died within four days (Sarlistyaningsih et al. 1995). Generally, waterlogging decreases growth of roots and root extension is particularly sensitive (Jackson & Drew 1984). Secondary to those on roots are the effects of waterlogging on shoots and stem elongation, leaf expansion and dry matter accumulation. During waterlogging, yellowing of the cotyledons and chlorosis of the older leaves occur, and the rate of growing leaf expansion reduces (Davies et al. 2000).
Waterlogging also limits symbiotic nitrogen fixation by bradyrhizobia (Dracup et al. 1998b). When the external oxygen concentration declines (as a result of waterlogging for example), acetylene reduction by lupin nodules also declines (Trinick et al. 1976). Waterlogging may lead to the breakdown of the nodules, but once it is relieved, the plant is able to form new nodules to fix nitrogen (Farrington et al. 1977).
6.1.4 Other stresses
Lupins do not tolerate high levels of salinity (Dracup et al. 1998b). Lupin species vary in their tolerance but generally are moderately sensitive to salinity. Symptoms of salt toxicity in lupin include a gray blotching of leaflets first, then developing marginal to complete leaf necrosis followed by wilting and abscission of leaflets (Munns et al. 1988; Treeby & van Steveninck 1988).
6.2 Abiotic tolerances
Lupins are tolerant to a range of heavy metals. Those tested include: aluminium (Penaloza et al. 2000), arsenic (Vazquez et al. 2006), cadmium (Carpena et al. 2003; Page et al. 2006; Vazquez & Carpena-Ruiz 2005; Ximénez-Embùn et al. 2001; Zornoza et al. 2002), chromium and lead (Gwozdz et al. 1997; Page et al. 2006; Ximénez-Embùn et al. 2001), nickel (Page et al. 2006) and mercury (Page et al. 2006; Zornoza et al. 2010). In Europe, lupin plants have been tested and shown potential to be used for bioremediation based on their ability to solubilize and absorb elements through extensive cluster roots, with the help of nodulation with Bradyrhizobium (Fernandez-Pascual et al. 2007).
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