Exploring the Potential of Quinoa Accessions for Salt Tolerance in Soilless Culture.
Pakistan has more than 6 million hectares of salt affected land and quinoa is tested as a facultative halophyte having super food characteristics. A hydroponic study was conducted to explore salt tolerance of two quinoa accessions, Ames-13737 (Q7) and PI-634919 (Q9) under a range of NaCl levels (0, 100, 200 and 300 mM) in wirehouse during 2016. Plant nursery was raised, and at four leaf stage, the seedlings were transferred to plastic tubs containing 20 L half strength Hoagland's solution as nutrient source. Salinity was developed incrementally to avoid osmotic shock after two days of transplanting. Results showed that growth (shoot length, root length and dry weight/plant) reduced drastically in Q9 by increasing the salinity level as compared to Q7. However, a comparable growth was observed in Q-7 at 0 and 100 mM i.e. the dry weight at 0 and 100 mM salinity were 0.8643 g and 0.8125 g, respectively.
Furthermore, genotype Q7 was found better than Q9 by producing 10% more dry weight (0.2790 g) at the highest salinity level which was linked to 57% more leaf K+ accumulation (28.64 mg K+ g-1 dry weight) as compared to Q9 (12.54 mg K+ g-1 dry weight). It is concluded that tolerance of Q7 to salt stress might be due to more absorption of K+ by the roots at increased Na+ level.
Keywords: Hydroponics; Quinoa; Salt stress; Potassium; Growth
Increasing salinity has become a global threat to agriculture, particularly in arid and semi-arid regions including Pakistan (Panta et al., 2014). According to FAO and ITPS report (2015), more than 100 countries have salt affected soils and their global extent is evaluated at about 1 billion hectares. Martinez-Beltran and Manzur (2005) reported that irrigated area of 0.25-0.5 million hectares becomes unproductive globally due to salinity buildup every year. These soils considerably decrease the growth and development of plants and thus are considered problematic soils. In Pakistan, salinity buildup usually occurs by the application of saline water. On an average, 26% of irrigated area in Pakistan is salt affected (Shahid et al., 2013). Irrigated area of estimated 6 million hectares is affected by soil salinity resulting in a loss of 62% in agricultural returns in Pakistan (Kazmi et al., 2012).
As most of the crop plants are salt sensitive non-halophytes (Greenway and Munns, 1980; Koyro and Huchzermeyer, 1999), the losses are incalculable. Primary salinity is caused due to the disintegration of primary minerals from the surface rocks (weathering). Munns and Tester (2008) reported another cause of primary salinity which is the deposition of salts carried in water and wind near coastal areas. Secondary salinity, which is caused by anthropogenic activities is especially important in Pakistan, where saline underground water used for irrigation causes the buildup of salts. According to a report , about 23% of irrigated lands in Pakistan are being deteriorated due to saline intrusion from un-irrigated lands (FAO and ITPS, 2015).
Harmful effects of salinity include decreased water availability due to increased osmotic stress usually triggered by high amounts of dissolved salts in the soil, toxicity of ions due to increased concentrations of sodium, magnesium and chloride ions, production of reactive oxygen species (ROS) and mineral imbalances especially potassium deficiency (Munns and Tester, 2008; Shabala and Cuin, 2008). Thus, major physiological phenomena like photosynthesis, lipid metabolism and protein synthesis are hampered (Heuer, 2005), which have severe effect on growth and performance of plants. Elevated Na+ concentrations in cytosol triggers cell death due to membrane disintegration (Shabala, 2009). Thus, it is need of the day to counter and alleviate the harmful effects of salinity on arable crop production. It is necessary to introduce new approaches to tackle these issues.
Different solutions to increasing salinity have been introduced i.e. reclamation of salt affected areas, breeding, use of salt tolerant germplasm etc. (Yilmaz et al., 2004). One potential and climate resilient strategy is the introduction of those new crops, which can tolerate high levels of salinity in soil and may allow irrigation with saline water i.e., the use of halophytic crop plants (Koyro et al., 2008).
Family Amaranthaceae is famous for having potential halophytes. Quinoa (Chenopodium quinoa Willd.) is one of the most potential members of this family. It is a facultative halophyte with its germplasm being able to handle salinity even at the levels that exist in sea water of 400 mM NaCl (Jacobsen et al., 2001, 2003; Hariadi et al., 2011). Pearsall (1992) reported quinoa cultivation in the Andes region for over 7000 years, which is known for its poor soil conditions and harsh climate. Thus, quinoa can acclimatize accordingly to tolerate frequent drought, frost and other harsh conditions (Jacobsen et al., 2009). Quinoa not only has outstanding ability to tolerate stress environments but it is also considered a super-food for its nutrition.
Quinoa grain has exceptional composition of vital amino acids, is abundant in vitamins (A, B2 and E) and contains many minerals like copper, magnesium, iron, calcium, lithium and zinc, and it also proves to be an excellent source of carbohydrates and fatty acids crucial for human nourishment (Repo-Carrasco et al., 2003). Due to low input requirement but high nutrition, the crop has also been nominated by FAO to guarantee food security in the 21st century (FAO, 1998). Despite the potential of quinoa as a high nutrition, low input and climate resilient crop and the work of many scientists, there are still some efforts to be put in the adaptation and screening of salt tolerant germplasm in Pakistan.
Large amount of energy is required for the biosynthesis of organic solutes causing yield losses (Shabala and Shabala, 2011). Thus, facultative halophytes like quinoa may balance their turgor by compartmentalizing Na+ and Cl- in cell vacuoles of shoot and produce compatible solutes just for cytosolic osmotic adjustment (Flowers and Colmer, 2008; Shabala and Mackay, 2011). It is believed that this sequestration of sodium ions is attained by tonoplast Na+/H+ antiporters (Flowers and Colmer, 2008) and pyrophosphatase (Guo et al., 2006; Krebs et al., 2010). Furthermore, Na+ and Cl ions stored in cell vacuoles serves as cheap osmolyte to maintain cell turgor by replacing potassium in halophytes (Flowers et al., 1977; Glenn et al., 1999).
Mannitol, proline and myo-inositol are the compatible solutes present in quinoa (Rufno et al., 2010) with the ability to scavenge ROS (Szabados and Savoure, 2010). Tolerance of quinoa to salinity may be credited to its efficient retention of K+ (Ruffino et al., 2010). Salinity caused a decrease in transpiration and thus gas exchange in quinoa (Sanchez et al., 2003). It has been reported that quinoa reduces stomatal density and cuticular pores under salinity (Razzaghi et al., 2011), which may adjust water use efficiency in these conditions (Orsini et al., 2011; Shabala et al., 2012).
Although, quinoa is a facultative halophyte but still huge diversity exists in its germplasm for salinity tolerance under different salinity and climatic conditions. Hence, the proposed study was conducted with objective to identify salt tolerant quinoa genotype on the basis of morphological, physiological, biochemical responses at different salinity levels in local climatic conditions.
Materials and Methods
Plant Material and Growth Conditions
The plant material used for the experiment consisted of two quinoa genotypes Q7 and Q9 originated from New Mexico (USA) and Chile respectively. These genotypes were screened and multiplied by Alternate Crops Lab, Department of Agronomy, University of Agriculture, Faisalabad, Pakistan.
Nursery of both genotypes was grown in a wire house at the experimental station of University of Agriculture, Faisalabad, Pakistan (31.4180o N, 73.0790o E) with average temperature of 12.35oC and relative humidity ranging from 46% to 85%. Nursery was grown in plastic bags containing about 1.5 kg of an equal mixture of sand, soil (loam) and leaf compost. 15 to 20 seeds were sown per bag and plants were watered every second day. Transplanting was done to hydroponic culture after 22 days at two to four-leaf stage.
Seedlings were transplanted into plastic tubs containing growth medium of half strength Hoagland's solution. Seedlings were grown under normal hydroponic conditions to minimize transplantation shock for two days. Seedlings were raised using float hydroponic technique in which porous thermopore sheets were used to support plants and strips of thin (1.3 cm wide) foam were used to fix seedlings in the pores. Four tubs for each variety were used. Air pumps were used to aerate the roots of the plants and growth medium and salts were changed fortnightly. Temperature recorded during the period was 19+-2oC and relative humidity was ranging from 35% to 79%.
Salt treatment was given two days after transplanting seedlings. To avoid osmotic shock, salt (NaCl) was applied in nutrient medium incrementally in phases of 100 mM NaCl per day. In all, there were four treatments with 3 replicates each: Control (0), 100, 200 and 300 mM NaCl which was equal to 0, 20, 40 and 60% seawater salinity (Eisa et al., 2012).
Four weeks after transplanting, five plants were chosen randomly for shoot length, root length, total fresh weight and total dry weight. Leaf and root samples for ionic analysis were also taken and reserved after drying.
Leaf samples of plants were harvested and immediately stored at -40oC for the quantitative biochemical analysis.
Chlorophyll Content Index (CCI) and Gaseous Exchange Parameters
CCI of the young fully expanded leaves was measured with chlorophyll index meter. Two weeks after imposition of salinity, three plants from each replication were chosen randomly to measure gaseous exchange parameters (net photosynthesis rate, stomatal conductance and transpiration rate) of fourth uppermost young fully expanded leaves. These parameters were recorded using an infrared gas analyzer LCA-4 (ADC, England) under different salinity levels at saturating radiation of 580 umol photon m-2 s-1.
Free proline content of young fully expanded leaves was spectrophotometrically (UV 4000, O.R.I., Germany) determined at 520 nm by the using the method described by Bates et al. (1973). Quantitative estimation of leaf ascorbic acid was done by using the method described by Kampfenkel et al. (1995). Carotenoids were calculated by the method and equation described by Arnon (1949).
Membrane Thermostability Index
Four uppermost fully expanded leaves of both genotypes were cut from each replication. Leaves were divided into two parts from each treatment to be used as control and heat treated. The leaves were placed in two test tubes with 10 mL deionized water and 15 mL water was added again. One test tube was placed at 45oC for 1 h in water bath while the other was kept at room temperature. Then conductivity readings were taken as the test tubes cooled down to room temperature using an EC meter for control and heat treated samples. Leaf membrane thermostability was estimated by using equations by Blum and Ebercon (1981).
Third leaf and portion of primary roots were taken to analyze ionic contents in leaves and roots and flame photometry (Sherwood Model 360, Flame Photometer) was used to determine concentrations of Na+ and K+ (Yuri et al., 2009). Selective absorption of K+ vs Na+ from the medium by roots (SA) and the selective transport of K+ vs Na+ from root to shoot (ST) was calculated by using the following equations (Debez et al., 2010):
The experiment was conducted in Completely Randomized Design with factorial arrangement. Data collected on all parameters were analyzed statistically to compare means (Steel et al., 1997) using the computer statistical program "Statistix 8.1", while Tukey's HSD (Honest Significant Difference) test at 5% level of probability was applied to distinguish significant treatments.
Data presented in Table 1 depict that interactive effect of salinity levels and genotypes was highly significant (p0.001). Q9 plants exhibited maximum shoot length under nonsaline conditions but as the salinity level increased, shoot length in Q9 decreased and least shoot length was observed at 60% sea water salinity in genotype Q9. While in Q7 plants, there was no significant (p >0.05) reduction in shoot length by the addition of NaCl up to 100 mM, however, as the salinity level increased over 100 mM, the shoot length decreased significantly (p <0.001). It was observed that decrease in shoot length in Q7 was not as intense as in the plants of Q9.
Control plants produced maximum root length, however, significantly (p <0.001) shorter roots were noted with increasing salt regimes in both genotypes, however, genotype Q9 produced more root length at control while genotype Q7 increased more root length than Q9 at 100 and 200 mM NaCl concentration.
Although Q9 plants gained more fresh weight at control, but a highly significant (p <0.001) decline in total fresh weight was recorded in Q9 at increasing salinity level as compared to Q7, which also decreased with increased salinity level. Maximum dry weight was recorded from Q9 plants at control and then it decreased significantly (p <0.001) at each salinity level while different trend was observed in Q7. Dry weights of Q7 plants were almost equal at control and 100 mM salinity level which then decreased significantly (p<0.05) as the salinity level was increased to 200 and 300 mM.
Different trends of leaf chlorophyll content index were observed at different salinity levels in both the genotypes (shown in Table 2 and Fig. 1). Chlorophyll index in leaves was found to be increased significantly (p 0.05) in leaf ascorbic acid was found among the genotypes under increased salinity levels. Same trend was observed in the concentrations of free proline which was also found non-significant (p >0.05). Concentration of carotenoids was also non-significant (p >0.05) among the treatments and genotypes (Table 2).
Maximum leaf membrane thermostability was observed in control of Q7 plants (Fig. 2). Membrane thermal stability index slightly increased at 100 mM in leaves of Q7 plants, then it started decreasing significantly (p <0.001) as the salinity level increased. While in Q9 plants, the membrane thermostability index significantly decreased (p <0.05) at 100 mM NaCl and remained almost same till salinity at 200 mM and then it declined at 300 mM concentration. Overall membrane stability in Q7 leaves was significantly (p Q9 up to 100 mM then it decreased consistently in both the genotypes.
Table 1: Influence of salt stress on the growth characteristics of quinoa genotypes
Parameters###Shoot Length (cm)###Root Length (cm)###Fresh weight (g)###Dry weight (g)
Table 2: Comparison of biochemical parameters from leaves of the quinoa genotypes under nonsaline and saline conditions. (fwt. indicates Fresh Weight)
Parameters###Chlorophyll Index###Free proline (umol g-1 fwt.)###Ascorbic acid (ug g-1 f.wt.)###Carotenoids (ug mL-1 f.wt.)
Gaseous Exchange Parameters
Highly significant (p <0.001) decrease in photosynthetic rates was recorded for every increase in salinity level in both genotypes. Same trend was observed in stomatal conductance which was also found to be significantly (p <0.001) decreased in both genotypes at increasing NaCl concentrations (Fig. 3a).
Another parameter was transpiration rate of plants, in which maximum transpiration rate was observed in non-saline conditions in genotype Q9 and then it decreased significantly (p <0.05) at each level. At 100 mM, transpiration rate in Q9 was recorded to be significantly (p<0.05) higher than Q7 which then decreased at higher salinity levels (Fig. 3b). As for the genotype Q7, the transpiration rate increased non-significantly at salinity levels up till 200 mM and then, it decreased significantly at 300 mM.
K+ over Na+ absorption ratio (SA) of roots significantly (p<0.001) increased from the medium in both genotypes as the salinity level increased (Fig. 4). However, Q7 plants showed higher absorption of K+ as compared to Q9 and maximum absorption of Q7 plants was recorded at 60% sea water salinity. Similar linear increase in SA was also recorded in Q9 plants as well.
Different trends among genotypes were observed for selective transport ratio (ST) of K+ vs Na+ from root to leaves. In genotype Q7, as the salinity level increased, the selective transport of K+ decreased significantly (p <0.001) from root to leaves while in genotype Q9, the ratio increased at increasing salinity levels and maximum transport of K+ was observed at 200 mM concentration in Q9 (Fig. 4).
In leaves of Q7 K+ decreased significantly (p <0.001) at all salinity levels as compared to control. The decrease was linear until 200 mM and then at 300 mM, the K+ concentration in Q7 plants increased and was significantly (p <0.001) more than the concentration at 200 mM (Fig. 5). As for genotype Q9, the potassium concentration in leaves increased with increasing salinity up to 200 mM which decreased significantly (p 0.05) to control (Fig. 5).
Na+ concentrations in leaves increased significantly (p<0.001) in Q7 plants with increasing salinity levels and the concentration of Na+ in Q7 plants was significantly (p0.05) change among genotypes and the concentration increased significantly (p <0.001) with increasing salinity and maximum sodium concentration in roots was found at 300 mM in both genotypes (Interactions of Na+ concentrations in leaves and roots can be observed in Fig 6).
Growth of quinoa genotype Q7 was unaffected by the NaCl up to the 100 mM except for root length which declined at increasing NaCl concentrations. Soil salinity may induce drought stress due to an increase in extracellular solute concentration which may cause a decline in water potential resulting in loss of cellular turgor (Taiz et al., 2015). So, the decline in growth parameters especially fresh and dry weights of the plants under increasing salinity levels is linked to a rise in osmotic potential in water stressed plants (Turner, 1981) which may be due to high extra cellular solute concentration or decreased volumes of cell under drought. Jacobsen et al. (2009) reported that minute thick walled cells of quinoa plants acclimated to water losses under drought do not lose turgor even under severe water limitations. Plant height in quinoa is one of the most sensitive characteristics under salinity (Jacobsen et al., 2001).
In our study, the variation in height of both genotypes in response to salinity was distinct. Q7 plants maintained height upto 100 mM NaCl level then onwards, there was a continuous reduction in shoot length, while in Q9, the plant height declined at all saline treatments.
Genotype Q7 maintained plant growth up to 100 mM NaCl concentration and then salinity affected its growth at further levels, which may be due to capability of quinoa plants to maintain water status even under saline environment while Q9 plants showed sensitivity even at 100 mM salinity. This decrease in growth may be linked with photosynthesis rate and stomatal conductance, which have been found to reduce under high salinity stress (Razzaghi et al., 2011). Similar situation was noted in our study except for transpiration rate in Q7 plants in which it increased at 200 mM salinity then it declined at further salinity level. A severe decline in photosynthesis activity was correlated with a significant reduction in stomatal conductance and high levels of Na+ accumulation in leaf tissues, which also strongly decrease photosynthetic capacity of plants.
Decrease in photosynthetic capacity might be due to the decreased activity of photosynthetically active enzymes like RubisCO, which decreases under salinity (Rivelli et al., 2002). As salinity is the main reason for drop in gas exchange, it is also responsible for the decline in transpiration of quinoa plants (Sanchez et al., 2003). Although, transpiration rates were found to be decreased in Q9 plants with increasing salinity, similar rates were observed in Q7 plants up to 200 mM salinity level. This behavior shows the tolerance of quinoa to highly saline environments by acquiring salt ions and regulating leaf osmotic potential, thus sustaining turgor and transpiration (Jacobsen et al., 2003).
Antioxidants i.e., free proline, ascorbic acid and carotenoids were observed in leaves at all concentrations of NaCl. There was no significant difference from control in the concentrations of ascorbic acid and carotenoids under salinity. Although, free proline concentration increased at 100 mM, it was found to be decreasing with increased salinity. Chen et al. (2007) reported K+ to be the main contributor in cytoplasmic osmolality in salt tolerant barley while free proline and glycinebetaine compensated for reduced cytosolic K+ levels. These organic osmolytes may be involved indirectly in osmotic adjustment by modifying K+ movement across membranes thus limiting sodium induced efflux of this inorganic osmolyte (Cuin and Shabala, 2007). Current and previous observations of high K+ levels in quinoa under stress together with inadequate free proline, ascorbic acid and carotenoids buildup corroborate with the concept.
Thus, it can be said that inorganic ions like sodium and potassium are mainly responsible for the osmotic adjustment in quinoa.
Salinity induced reduction in chlorophyll content has been observed in NaCl susceptible plants (Jamil et al., 2007). However, in salinity tolerant plants, the chlorophyll contents have been found to increase under salt stress (Khan et al., 2009). Hence, improved chlorophyll contents in both genotypes showed the ability of quinoa to thrive under severe salt stress.
Plant growth and CO2 exchange rate may be reduced by several factors but salinity induced ion exchange is debatably most important among these factors (Adolf et al., 2012). Competition is found between K+ and Na+ due to similarities in their physiochemical properties and sodium is known to compete with potassium for most of the binding sites (Kronzucker, 2013). Hence, a sharply reduced leaf K+: Na+ ratio by an accumulation of high levels of Na+ was observed in both genotypes. Loss of K+ from leaves under salinity may cause programmed cell death by activating enzymes like proteases (Shabala, 2009) thus increasing drop of older leaves (data not given).
Na+ increased significantly with increasing salinity in the leaves of Q7 plants, while the abrupt rise of Na+ concentration was found only in 300 mM concentration. Same trend was observed in genotype Q9 as well. As for the K+ content in leaves, it decreased with increasing salinity levels and at 300 mM, there was a significant improvement in its contents in genotype Q7. Orsini et al. (2011) reported that K+ concentrations declined at levels starting from 150 mM and increased at higher salinity levels. In the genotype Q9, K concentration increased up till 200 mM and then decreased at 300 mM. The increase in Na+ concentration may be due to fact that quinoa plants accumulate Na+ which is readily available for cytosolic osmotic adjustment and sustaining turgor pressure, so to manage a suitable K+: Na+ concentration in leaves, the increased Na+ uptake should be followed by enhanced K+ transport from root to shoot (Cuin et al., 2009).
Potassium is believed to activate more than 50 enzymes including RUBISCO and those involved with chlorophyll biosynthesis (Shabala, 2003). Therefore, the specific roles of K+ cannot be replaced by Na+. It was found from our study that the selective absorption of K+ over Na+ from medium was enhanced in both genotypes as NaCl level increased while its transport to leaves by roots decreased considerably in Q7 and slightly increased in Q9 reaching maximum at 200 mM. The decrease in transport in Q7 may be due to Na+ acting as an osmolyte.
Taking all the parameters into consideration, 100 mM salinity level may be regarded as an optimum level of salinity as the plants in both genotypes were least affected at this level. Furthermore, Q7 is more salt tolerant than Q9 as most of the parameters (especially growth) were scarcely or not affected with the application of 100 mM NaCl, thus generally confirming the halophytic behavior of quinoa. Genotype Q9 produced best results under nonsaline conditions so it can be used for arable crop production However, since Q7 was least affected by moderate salt stress, it can be regarded better genotype in moderately saline soils.
Adolf, V.I., S. Shabala, M.N. Andersen, F. Razzaghi and S.E Jacobsen, 2012. Varietal differences of quinoa's tolerance to saline conditions. Plant Soil, 357: 117-129
Arnon, D.T., 1949. Copper enzyme in isolated chloroplasts polyphenols oxidase in Beta vulgaris. Plant Physiol., 24: 1-15
Bates, L.S., R.P. Waldren and I.D. Teare, 1973. Rapid determination of free proline for water stress studies. Plant Soil, 39: 205-207
Blum, A. and A. Ebercon, 1981. Cell membrane stability as a measure of drought and heat tolerance in wheat. Crop Sci., 21: 43-47
Chen, Z., T.A. Cuin, M. Zhou, A. Twomey, B.P. Naidu and S. Shabala, 2007. Compatible solute accumulation and stress-mitigating effects in barley genotypes contrasting in their salt tolerance. J. Exp. Bot., 58: 4245-4255
Cuin, T.A. and S. Shabala, 2007. Potassium efux channels mediate Arabidopsis root responses to reactive oxygen species and the mitigating effect of compatible solutes. Plant Cell Environ., 30: 875-885
Cuin, T.A., Y. Tian, S.A. Betts, R. Chalmandrier and S. Shabala, 2009. Ionic relations and osmotic adjustment in durum and bread wheat under saline conditions. Funct. Plant Biol., 36: 1110-1119
Debez, A., D. Saadaoul, I. Slama, B. Huchzermeyer and C. Abdelly, 2010. Responses of Batis Maritima plants challenged with upto two-fold seawater NaCl salinity. J. Plant Nutr. Soil Sci., 173: 291-299
Eisa, S., S. Hussin, N. Geissler and H.W. Koyro, 2012. Effect of NaCl salinity on water relations, photosynthesis and chemical composition of quinoa (Chenopodium quinoa Willd.) as a potential cash crop halophyte. Aust. J. Crop Sci., 6: 357-368
FAO and ITPS, 2015. Status of the World's Soil Resources (SWSR) - Main Report. Food and Agriculture Organization of the United Nations and Intergovernmental Technical Panel on Soils, Rome, Italy
FAO, 1998. Under-utilized Andean Food Crops. FAO, Rome, Italy
Flowers, T.J. and T.D. Colmer, 2008. Salinity tolerance in halophytes. New Phytol., 179: 945-963
Flowers, T.T., R.F. Troke and A.R. Yeo, 1977. The mechanism of salt tolerance in halophytes. Annu. Rev. Plant Physiol., 28: 89-91
Glenn, E.P., J.J. Brown and E. Blumwald, 1999. Salt tolerance and crop potential of halophytes. Crit. Rev. Plant Sci., 18: 227-255
Greenway, H. and R. Munns, 1980. Mechanisms of salt tolerance in non-halophytes. Annu. Rev. Plant Physiol., 31: 149-190
Guo, S.L., H.B. Yin, X. Zhang, F.Y. Zhao, P.H. Li, S.H. Chen, Y.X. Zhao and H. Zhang, 2006. Molecular cloning and characterization of a vacuolar H+ pyrophosphatase gene, SSVP, from the halophyte Suaeda salsa and its overexpression increases salt and drought tolerance of arabidopsis. Plant Mol. Biol., 60: 41-50
Hariadi, Y., K. Marandon, Y. Tian, S.E. Jacobsen and S. Shabala, 2011. Ionic and osmotic relations in quinoa (Chenopodium quinoa Willd.) plant grown at various salinity levels. J. Exp. Bot., 62: 185-193
Heuer, B., 2005. Photosynthetic carbon metabolism of crops under salt stress. In: Handbook of Photosynthesis, pp: 779-792. M. Pessarakli (ed.). Taylor and Francis Group, Boca Raton, Florida, USA
Jacobsen, S.E., A. Mujica and C. Jensen, 2003. The resistance of quinoa (Chenopodium quinoa Willd.) to adverse abiotic factors. Food Rev. Int., 19: 99-109
Jacobsen, S.E., F. Liu and C.R. Jensen, 2009. Does root-sourced ABA play a role for regulation of stomata under drought in quinoa (Chenopodium quinoa Willd.). Sci. Hort., 122: 281-287
Jacobsen, S.E., H. Quispe and A. Mujica, 2001. Quinoa: An Alternative Crop for Saline Soils in the Andes, Scientists and Farmer-partners in Research for the 21st Century, pp: 403-408. CIP Program Report 1999-2000
Jamil, M., S.U. Rehman, K.J. Lee, J.M. Kim, H.S. Kim and E.S. Rha, 2007. Salinity reduced growth PS2 photochemistry and chlorophyll content in radish. Sci. Agric., 64: 111-118
Kazmi, S.I., M.W. Ertsen and M.R. Asi, 2012. The impact of conjunctive use of canal and tube well water in Lagar irrigated area, Pakistan. Phys. Chem. Earth., 47: 86-98
Kampfenkel, K., M.V. Montagu and D. Inze, 1995. Extraction and determination of ascorbate and dehydroascorbate from plant tissues. Anal. Boichem., 225: 165-167
Khan, M.A., M.U. Shirazi, M.A. Khan, S.M. Mujtaba, E. Islam, S. Mumtaz, A. Shereen, R.U. Ansari and M.Y. Ashraf, 2009. Role of proline, K/Na ratio and chlorophyll content in salt tolerance of wheat (Triticum aestivum L.). Pak. J. Bot., 41: 633-638
Koyro, H.W. and B. Huchzermeyer, 1999. Salt and drought stress effects on metabolic regulation in maize. In: Handbook of Plant and Crop Stress, 2nd edition, pp: 843-878. Pessaraki, M. (ed.). Marcel Dekker, New York, USA
Koyro, H.W., N. Geissler, S. Hussin and B. Huchzermeyer, 2008. Survival at extreme locations: life strategies of halophytes - the long way from system ecology, whole plant physiology, cell biochemistry and molecular aspects back to sustainable utilization at field sites. In: Biosaline Agriculture and High Salinity Tolerance, pp: 1-20.
Abdelly, C., M. Otzturck, M. Ashraf and C. Grignon (eds.). Birkhauser Verlag, Switzerland
Krebs, M., D. Beyhl, E. Gorlich, K.A. Al-Raschied, Y.D. Stierhof, R. Hedrich and K. Schumacher, 2010. Arabidopsis V-ATPase activity at the tonoplast is required for efcient nutrient storage but not for sodium accumulation. Proc. Natl. Acad. Sci., 102: 3251-3256
Kronzucker, H.J., D. Coskun, L.M. Schulze, J.R. Wong and D.T. Britto, 2013. Sodium as nutrient and toxicant. Plant Soil, 369: 1-23
Martinez-Beltran, J. and C.L. Manzur, 2005. Overview of Salinity Problems in the World and FAO Strategies to Address the Problem, pp: 311-313. Proceedings of the international salinity forum, Riverside, California, USA
Munns, R. and M. Tester, 2008. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol., 59: 651-681
Orsini, F., M. Accorsi, G. Gianquinto, G. Dinelli, F. Antognoni, K.B.R. Carrasco, E.A. Martinez, M. Alnayef, I. Marotti, S. Bosi and S. Biondi, 2011. Beyond the ionic and osmotic response to salinity in Chenopodium Quinoa: functional elements of successful halophytism. Funct. Plant Biol., 38: 818-831
Panta, S., T. Flowers, P. Lane, R. Doyle, G. Haros and S. Shabala, 2014. Halophyte agriculture: success stories. Env. Exp. Bot., 107: 71-83
Pearsall, D., 1992. The origins of plant cultivation in South America. In: The Origins of Agriculture. An International Perspective, pp: 173-205.
Cowan, C.W. and P.J. Watson (eds.). Smithsonian Institution Press, Washington, London, UK
Razzaghi, F., S.H. Ahmadi, V.I. Adolf, C.R. Jensen, S.E. Jacobsen and M.N. Andersen, 2011. Water relations and transpiration of quinoa (Chenopodium quinoa Willd.) under salinity and soil drying. J. Agron. Crop Sci., 197: 348-360
Rivelli, A.R., S. Lovelli and M. Perniola, 2002. effect of salinity on gas exchange, water relations and growth of sunflower (Helianthus annuus). Funct. Plant Biol., 29: 1405-1415
Repo-Carrasco, R., C. Espinoza and S.E. Jacobsen, 2003. Nutritional value and use of the andean crops quinoa (Chenopodium Quinoa) and ka~niwa (Chenopodium Pallidicaule). Food Rev. Int., 19: 179-189
Rufno, A.M.C., M. Rosa, M. Hilal, J.A. Gonzalez and F.E. Prado, 2010. The role of cotyledon metabolism in the establishment of quinoa (Chenopodium quinoa) seedlings growing under salinity. Plant Soil, 326: 213-224
Sanchez, H.B., R. Lemeur, P.V. Damme and S.E. Jacobsen, 2003. Ecophysiological analysis of drought and salinity stress in quinoa (Chenopodium quinoa Willd.). Food Rev. Int., 19: 111-119
Shabala, S., 2003. Regulation of potassium transport in leaves: from molecular to tissue level. Ann. Bot., 92: 627-634
Shabala, S., 2009. Salinity and programmed cell death: unravelling mechanisms for ion specific signalling. J. Exp. Bot., 60: 709-711
Shabala, S. and A. Mackay, 2011. Ion transport in halophytes. Adv. Bot. Res., 57: 151-199
Shabala, S. and L. Shabala, 2011. Ion transport and osmotic adjustment in plants and bacteria. Biomol. Concepts, 2: 407-419
Shabala, S. and T.A. Cuin, 2008. potassium transport and plant salt tolerance. Physiol. Plant., 133: 651-669
Shahid, S.A., 2013. Developments in Soil Salinity Assessment, Modeling, Mapping and Monitoring from Regional to Submicroscopic Scales. In: Developments in Soil Salinity Assessment and Reclamation, pp: 3-43. Springer, New York, USA
Steel, R.C.D., J.H. Torrie and D.A. Deeky, 1996. Principles and Procedures of Statistics a Biometric Approach, 3rd edition, pp: 400-428. McGraw Hill Book Co. New York, USA
Szabados, L. and A. Savoure, 2010: Proline: a multifunctional amino acid. Trends Plant. Sci., 15: 89-97
Taiz, L., E. Zeiger, I.M. Moller and A. Murphy, 2015. Plant Physiology and Development, 6th edition. Sinauer Associates Publishers, Sunderland, Massachusetts, USA
Turner, N.C., 1981. Techniques and experimental approaches for the measurement of plant water status. Plant Soil, 58: 339-366
Yilmaz, K., I.E. Akinci and S. Akincim, 2004. Effect of salt stress on growth and Na, K contents of pepper (Capsicum annuum L.) in germination and seedling stages. Pak. J. Biol. Sci., 7: 606-610
Yuri, S., P. Langridge and M. Tester, 2009. Salinity tolerance and sodium exclusion in genus Triticum. Breed. Sci., 59: 671-678
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|Author:||Saleem, Muhammad Aamir; Basra, Shahzad Maqsood Ahmed; Afzal, Irfan; Rehman, Hafeez-ur; Iqbal, Shahid|
|Publication:||International Journal of Agriculture and Biology|
|Date:||Apr 30, 2017|
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