Tolerance Indices of Some Quinoa (Chenopodium Quinoa Wild) Genotypes under Different Salinity Levels

 

Amal Ahmed Mohammed Al-Ghamdi1*, Manal El-Zohri1,2

1Department of Biological Sciences, Faculty of Science, King Abdulaziz University, Jeddah 21488, Saudi Arabia.

2Department of Botany and Microbiology, Faculty of Science, Assiut University, Assiut 71516, Egypt.

 

*Email: [email protected]


ABSTRACT

The experiment was conducted to determine differential responses of four quinoa genotypes irrigated with water at different salinity levels (800, 4000, and 8000 ppm) during the growing season (2019). The effect of the three salinity levels on quinoa growth was investigated depend on some characters including plant height, chlorophyll content, days of flowering, the weight of grains/plant, and the weight of 1000 seeds of four tested genotypes (Chenopodium quinoa Willd). According to salinity resistance indices, the Chipaya variety was the most tolerant to salinity stress while the Ollague variety was the most sensitive. The results stated that all characters were affected, especially under high salinity level conditions. In general, the most of tested traits displayed recorded obvious variations between the four genotypes and salinity levels on quinoa plants. The correlation and tolerance indices analysis of data has been calculated based on yield grain and its components. The results confirm that the tested varieties can be divided into three groups according to their performance under environmental stress compared to normal conditions.

Key words:Quinoa, Salt stress, Genotypes, Tolerance, Yield, Correlation


INTRODUCTION

Plant production and soil salinity are inextricably linked where salinity has always been an important factor for limiting crop production in much of the world [1, 2]. With increasing competition for finite food resources worldwide, the invitation appeared to evaluate and improve cultivated varieties depending on genetic drift and selection in different environmental conditions to ensure future food security [3, 4].

Quinoa (Chenopodium quinoa Willd), a food plant belonging to the family Chenopodiaceae [5], has edible parts that include leaves and grains, with the latter reported as the most economically and scientifically investigated [6-8]. It is native to the Andean regions of Chile, Peru, Ecuador, and Bolivia and has been used as a source providing useful food to low-income farmers in these regions thousands of years ago [9]. During the last decades, scientists have become increasingly interested in studying quinoa due to the high nutrition content of its seeds [10, 11], including its high concentration in protein. Additionally, quinoa seeds are rich in unsaturated fatty acids, minerals, and antioxidants [12] and have been reported to be beneficial to patients with celiac disease to their poor gluten content [13]. Quinoa seeds are regarded as good functional food ingredients due to their capacity to decrease the risk of various diseases; thus, the demand for quinoa products increased, leading to an increase in the prices of these products during the last decade [14]. The food and agriculture organization (FAO) has been chosen as one of the plants prepared to provide food safety [15]. Recently, Cao et al. (2020) reported that dietary supplementation with quinoa polysaccharide was associated with an improvement in hyperlipidemia caused by the consumption of a high-fat diet [16]. Furthermore, Pereira et al. (2020) demonstrated that quinoa varieties represent a good source of bioactive compounds with antibacterial and antifungal activities [17].

The adaption of certain quinoa varieties is possible even under marginal environments where it is notified to be tolerant to many environmental stress conditions including salinity [15, 18-20].

Quinoa belongs to a halophyte with over 3000 accessions presenting a large scale of the diversity of salinity tolerance and other traits. It has been shown that varieties from the Bolivian Altiplano are more tolerant to salinity than varieties from the other areas [21]. However, the determination of parameters that plant breeders might carry out in the field to get better quinoa varieties, for their tolerance to salinity stress, is yet an issue of search [22, 23].

There is a shortage of references related to quinoa growth under salinity stress in our Arab countries. Therefore, we aim to extend a review of crop performances and adaptability based on the studying of genetic variation of four quinoa genotypes through different salinity levels.

MATERIALS AND METHODS

Experiment conditions and experimental design

This study was held using four economical quinoa varieties (Ollague, CO 407, Chipaya, and CICA-17) which have been tested under three salinity irrigation levels (800, 4000, and 8000 ppm) were applied after 20 days from cultivation during season 2019. The experiment was designed in a split-plot design where the salinity levels were placed in the main plot while the tested varieties were placed in a sub plot in three replicates. The sample of soil in the pots was sandy loam with pH 7.8 where the pot height is 60 cm and its diagonal 40 cm.

Plant measurements

Characteristics of quinoa plants were evaluated as follow:

  1. Height of plants (cm) at harvest.
  2. Leaf area was measured using leaf area device (cm2) as the mean of three leaves (Leaf number 4, 5, and 6 from top of the plant).
  3.  Chlorophyll content (SPAD units) was determined using chlorophyll Meter SPAD-502.
  4. The number of days of 50 % flowering in plants.
  5. Weight of grains/plant (g) using a sensitive digital balance at harvesting.
  6. Weight of 1000 seeds (g) using a sensitive digital balance after harvesting.

Tolerance parameter of tested genotypes

Different tolerance parameters to salinity were determined for grain yield/plant of tested genotypes under normal (Yn) and salinity stress conditions (Ys) as indicated in Table 1.

Table 1. Salinity stress tolerance indices, equation, and reference

No.

parameter

Equation

Reference

1

Stress susceptibility index (SSI)

SSI = 1 – (Ys ÷ Yn) ÷ SI, where SI = 1 – (Ŷs ÷ Ŷn) where Ŷs and Ŷn represent the average of all tested genotypes under high salinity and normal conditions, respectively.

[24]

2

Tolerance index (TOL)

TOL = Yn – Ys

[25]

3

Mean productivity (MP)

MP = (Yn +Ys) ÷ 2

[25]

4

Harmonic mean (HM)

HM = 2(Yn × Ys) ÷ (Yn + Ys)

[26]

5

Geometric mean productivity (GMP)

GMP = (Yn × Ys)½

[27, 28]

6

Stress tolerance index (STI)

STI = (Yn × Ys) ÷ (Ŷ n)2

[27, 26]

7

Superiority measure (SM)

SM = Ys ÷ Yn

[28]

8

Relative performance (RP)

RP = (Ys ÷ Yn) ÷ R where R = (Ýs ÷ Ýn).

[29]

9

Yield injury (YI)

YI = (Yn-Ys) ÷ Yn * 100

[30]

 

RESULTS AND DISCUSSION

Analysis of variance

The results in Table 2 indicate that there are significant differences between the studied characteristics in general. The data also indicates the presence of clear differences between salinity levels, especially the high level and both other levels (Figure 1a). Also, the results also show that all studied traits decrease their values by increasing the level of salinity except for the characteristic of the number of days required for flowering that go in the opposite direction as they decrease by increasing the influence of the salinity level (Table 2).

On the other hand, Figure 1b shows the differences between the tested genotypes through grain yields/plant a cross salinity levels but the figure shows that there is no significant difference between varieties 4 and 3, but they outperform the cultivar 1.

 

The correlation coefficient among tested characters

The results in Table 3 indicate that the correlation coefficients between the characteristics studied across the trial conditions were strong and positive and ranged from 0. 727 to 0.964 where the lowest value ​​was recorded between leaf area and Chlorophyll content while the highest value was recorded between days of flowering and weight of grains/plant.

 

Table 2. Mean performance of tested genotypes for tested traits under three salinity levels.

Salinity

level

Genotype

Plant height (cm)

Leaf area (cm2)

Chlorophyll content (SPAD)

Days

of 50% flowering

Weight of grains /plant (g)

Weight of 1000 seeds (g)

Low

Ollague

107.67

18.00

53.33

81.67

48.33

3.167

CO 407

96.00

18.60

50.33

78.33

47.00

3.367

Chipaya

103.00

19.33

51.00

80.67

49.00

3.200

CICA-17

109.67

21.53

48.33

82.67

51.33

3.400

Middle

Ollague

82.33

15.50

45.57

77.00

40.67

2.933

CO 407

81.33

16.87

44.67

77.00

42.67

3.000

Chipaya

95.00

18.23

46.87

75.00

42.33

3.133

CICA-17

95.00

17.50

42.00

76.33

43.33

3.000

High

Ollague

57.33

10.83

34.67

66.67

28.00

2.533

CO 407

61.67

15.00

36.33

71.67

34.33

2.933

Chipaya

81.67

16.00

37.50

70.67

37.00

3.033

CICA-17

73.33

16.67

35.67

67.67

34.33

2.617

LSD(0.05)

1.145

0.14

1.56

0.82

2.16

0.02

 

a)

b)

Figure 1. a) Comparison between varieties across salinity levels. Salinity level 1, 2, and 3 are 800, 4000, and 8000 respectively. b) Comparison between salinity levels of all tested varieties. Varieties 1, 2, 3, and 4 are Ollague, CO 407, Chipaya, and CICA-17 respectively.

 

Table 3. Correlation between tested characters and grain yield.

Correlation coefficient

Plant height

Leaf area

Chlorophyll content

Days of flowering

Weight of 1000 seeds

Leaf area

0.888

 

 

 

 

Chlorophyll content

0.879

0.727

 

 

 

Days of flowering

0.885

0.796

0.927

 

 

Weight of 1000 grains

0.839

0.846

0.812

0.861

 

Weight of grains/plant

0.955

0.908

0.918

0.964

0.901

Tolerance parameters

The results presented in Table 4 showing a clear difference between the results of the grain yield/plant under the high salinity level (Ys) compared to normal conditions (Yn) through the tolerance indices of the tested cultivars.

Through the stress susceptibility index (SSI) parameter, one or two tolerant cultivars to salinity can be determined. When the value of SSI is less, this meant that the tolerance of cultivar to salinity stress will be higher. Table 3 shows the SSI values for grain yield which was in the range from 0.773 in Chipaya cultivar as a tolerant to 1.327 in Ollague as a sensitive cultivar. While CICA-17 cultivar can be considered as moderate salinity tolerance (1.045).

Estimation of tolerance indices stated that the highest stress tolerance (TOL) value as stress susceptibility index (SSI) value was related to Ollague cultivar indicating this cultivar had higher grain yield reduction under high salinity level compared with normal conditions and the highest salinity sensitivity (Table 3).

Chipaya and CICA-17 were the tolerant cultivars according to mean productivity (MP), harmonic mean (HM), geometric mean productivity (GMP), and stress tolerance index (STI) were recorded the highest values which greater than the general mean of all cultivars (41.17, 39.61, 40.38 and 0.684 respectively).

Based on the superiority measure (SM) and relative performance (RP), the cultivars Chipaya and CO 407 had the highest values which exceeded the mean of all tested cultivars while the Ollague cultivar recorded the lowest value. According to the yield injury (YI) parameter, the Ollague cultivar is ranked the first in the damage and consequently, the crop is decreased by exposure to high salinity while the least affected (least harmful) cultivar was the Chipaya variety (Table 4).

 

Table 4. Tolerance parameters of quinoa cultivars under high salinity level (Ys) and normal (Y n) conditions based on grain yield/plant.

Cultivar

Y(n)

Y(s)

SSI

TOL

MP

HM

GMP

STI

SM

RP

YI

Ollague

48.33

28.00

1.327

20.33

38.17

35.46

36.79

0.566

0.579

0.848

42.06

CO 407

47.00

34.33

0.851

12.67

40.67

39.68

40.17

0.674

0.730

1.069

26.96

Chipaya

49.00

37.00

0.773

12.00

43.00

42.16

42.58

0.758

0.755

1.105

24.49

CICA-17

51.33

34.33

1.045

17.00

42.83

41.14

41.98

0.736

0.669

0.979

33.12

Mean

48.92

33.42

0.999

15.50

41.17

39.61

40.38

0.684

0.683

1.000

31.66

Yn = mean grain yield/plant of studied cultivar under non-stress condition, Ys = mean grain yield/plant tested variety under high salinity stress, SSI = stress susceptibility index, TOL = tolerance index, MP = mean productivity, HM = Harmonic mean, GMP = geometric mean productivity, STI = stress tolerance index, SM= Superiority measure, RP= Relative performance and Yi= Yield injury

The presence of significant differences between studied characteristics under various environmental conditions, as well as between a group of genotypes indicates the importance of distributing these genotypes according to their compatibility with these different conditions.

The Correlation between two characters can be affected by inheritance, environmental condition, or the interaction between them. The characteristics selected for the study were considered as they all recorded a high correlation with the yield of grains (Table 4), especially the number of days until flowering, which confirms that it is strongly related to the grain yield, which they nominate as an important quality of selection for them under salinity conditions. In the same manner, Cruz et al. (2019) and Carvalho et al. (2018) stated that the simple correlation between two characters is usually determined using the Pearson's linear correlation coefficient, which depends on the ratio of the two-variable joint difference known as covariance and the output of their respective standard deviations [31, 32].

Therefore, attention to focus on the parameters of stress tolerance is a requirement to determine the possibility of sharing each genotype in an environment. Salinity tolerant variety can satisfy is determined as genotype which achieves considerably greater productivity than average under salinity stress. The data in Table 3 can distribute the studied quinoa cultivars based on grain yield under both non-stress and salinity stress and these results are harmonic with Majidi et al. (2011), and Badran and Moustafa (2014) and Badran (2015) who stated that STI, HM (harmonic mean) and MP (geometric mean productivity) can be effective indices for pick out high productivity varieties under both non-stress and salinity stress [3, 33, 34]. According to the results in Table 4 can be useful to divide the tested cultivars into three groups based on their grain yield as follow: the first group, good express cultivar behavior in both normal and salinity stress (i.e. Chipaya cultivar), the second group: cultivars with good behavior under non-stress only (i.e. Ollague cultivar), the third group: genotype medium in performance in both normal conditions and salinity stress (i.e. CO 407 and CICA-17 cultivars). These results are similar to Fernández (1992) who reported that the cultivars were classified into four groups according to their behavior under normal conditions and stress conditions [27].

CONCLUSION

The study focused on evaluating a group of genotypes of quinoa under different levels of salinity. The study was based on the calculation of a set of tolerance parameters for saline stress, and accordingly, the four genotypes tested were classified into three groups. The Chipaya variety expresses itself well under salinity stress and normal conditions. Ollague variety expresses itself well under normal conditions only (non-stress). The third group includes CICA-17 and CO 407 and they occupy a middle case under the conditions of the experiment.

ACKNOWLEDGMENTS : This work was sponsored by the Deanship of Scientific Research (DSR) at King Abdulaziz University, Jeddah [grant numbers G-233-247-1440]. Therefore, the authors wish to thank DSR for providing technical and financial support.

CONFLICT OF INTEREST : None

FINANCIAL SUPPORT : This study received grant from funding the Deanship of Scientific Research (DSR) at King Abdulaziz University.

ETHICS STATEMENT : None

References

1.       Shokat S, Großkinsky DK. Tackling salinity in sustainable agriculture—What developing countries may learn from approaches of the developed world. Sustainability. 2019;11(17):4558.

2.       Minhas PS, Ramos TB, Ben-Gal A, Pereira LS. Coping with salinity in irrigated agriculture: Crop evapotranspiration and water management issues. Agric Water Manag. 2020;227:105832.

3.       Badran AE, Moustafa ES. Drought resistance indices and path analysis in some wheat genotypes. World Appl Sci J. 2014;30(12):1870-6.

4.       Cheeseman J. Food security in the face of salinity, drought, climate change, and population growth. InHalophytes for food security in dry lands. Acad Press. 2016:111-23.

5.       Fuentes FF, Bazile D, Bhargava A, Martinez EA. Implications of farmers’ seed exchanges for on-farm conservation of quinoa, as revealed by its genetic diversity in Chile. J Agric Sci-Lond. 2012;150(6):702-16.

6.       Spehar CR. Adaptação da quinoa (Chenopodium quinoa Willd.) para incrementar a diversidade agrícola e alimentar no Brasil. Cad Ciênc Tecnol. 2006;23(1):41-62.

7.       Kanjikar AP. On Anti-Diabetic Potential of Phyto-nanoparticles Comparison with Hormonal Therapy and Medicinal Plants. Int J Pharm Phytopharmacol Res. 2019;9(1):103-11.

8.       Morilla LJ, Demayo CG. Medicinal plants used by traditional practitioners in two selected villages of Ramon Magsaysay, Zamboanga del Sur. Pharmacophore. 2019;10(1):84-92.

9.       Basantes-Morales ER, Alconada MM, Pantoja JL. Quinoa (Chenopodium quinoa Willd) Production in the Andean Region: Challenges and Potentials. J Exp Agric Int. 2019:1-18.

10.    Jacobsen SE. The worldwide potential for quinoa (Chenopodium quinoa Willd.). Food Rev Int. 2003;19(1-2):167-77.

11.    Maradini-Filho AM. Quinoa: nutritional aspects. J Nutraceuticals Food Sci. 2017;2(1):1-5.

12.    Paśko P, Bartoń H, Zagrodzki P, Gorinstein S, Fołta M, Zachwieja Z. Anthocyanins, total polyphenols and antioxidant activity in amaranth and quinoa seeds and sprouts during their growth. Food Chem. 2009;115(3):994-8.

13.    Peñas E, Uberti F, di Lorenzo C, Ballabio C, Brandolini A, Restani P. Biochemical and immunochemical evidences supporting the inclusion of quinoa (Chenopodium quinoa Willd.) as a gluten-free ingredient. Plant Foods Hum Nutr. 2014;69(4):297-303.

14.    Bazile D, Jacobsen SE, Verniau A. The global expansion of quinoa: trends and limits. Front Plant Sci. 2016;7:622.

15.    Jacobsen SE, Mujica A, Jensen CR. The resistance of quinoa (Chenopodium quinoa Willd.) to adverse abiotic factors. Food Rev Int. 2003;19(1-2):99-109.

16.    Cao Y, Zou L, Li W, Song Y, Zhao G, Hu Y. Dietary quinoa (Chenopodium quinoa Willd.) polysaccharides ameliorate high-fat diet-induced hyperlipidemia and modulate gut microbiota. Int J Biol Macromol. 2020;163:55-65.

17.    Pereira E, Cadavez V, Barros L, Encina-Zelada C, Stojković D, Sokovic M, et al. Chenopodium quinoa Willd.(quinoa) grains: A good source of phenolic compounds. Food Res Int. 2020;137:7-20.

18.    Yazar A, Incekaya Ç, Sezen SM, Jacobsen SE. Saline water irrigation of quinoa (Chenopodium quinoa) under Mediterranean conditions. Crop Pasture Sci. 2015;66(10):993-1002.

19.    Algosaibi AM, El-Garawany MM, Badran AE, Almadini AM. Effect of irrigation water salinity on the growth of Quinoa plant seedlings. J Agric Sci. 2015;7(8):205-14.

20.    Choukr-Allah R, Rao NK, Hirich A, Shahid M, Alshankiti A, Toderich K, et al. Quinoa for marginal environments: toward future food and nutritional security in MENA and Central Asia regions. Front Plant Sci. 2016;7:346.

21.    Adolf VI, Jacobsen SE, Shabala S. Salt tolerance mechanisms in quinoa (Chenopodium quinoa Willd.). Environ Exp Bot. 2013;92:43-54.

22.    Razzaghi F, Ahmadi SH, Jacobsen SE, Jensen CR, Andersen MN. Effects of salinity and soil–drying on radiation use efficiency, water productivity and yield of quinoa (Chenopodium quinoa Willd.). J Agron Crop Sci. 2012;198(3):173-84.

23.    Bhargava A, Ohri D. Origin of genetic variability and improvement of quinoa (Chenopodium quinoa Willd.) In: Rajpal V., Rao S., Raina S., editors. Gene Pool Diversity and Crop Improvement. Springer; Cham, Switzerland. 2016:241-70.

24.    Fischer RA, Maurer R. Drought resistance in spring wheat cultivars. I. Grain yield responses. Aust J Agric Res. 1978;29(5):897-912.

25.    Rosielle AA, Hamblin J. Theoretical aspects of selection for yield in stress and non‐stress environment 1. Crop Sci. 1981;21(6):943-6.

26.    Schneider KA, Rosales‐Serna R, Ibarra‐Perez F, Cazares‐Enriquez B, Acosta‐Gallegos JA, Ramirez‐Vallejo P, et al. Improving common bean performance under drought stress. Crop Sci. 1997;37(1):43-50.

27.    Fernández GCJ. Effective selection criteria for assessing plant stress tolerance. Proceedings of the International Symposium on “Adaptation of Vegetables and Other Food Crops in Temperature and Water Stress”, Taiwan. 1992:257-70.

28.    Lin CS, Binns MR. A superiority measure of cultivar performance for cultivar× location data. Can J Plant Sci. 1988;68(1):193-8.

29.    Abo-Elwafa A, Bakheit BR. Performance, correlation and path coefficient analysis in faba bean. Assiut J Agric Sci. 1999;30:77-91.

30.    Blum A, Mayer J, Gozlan G. Associations between plant production and some physiological components of drought resistance in wheat. Plant Cell Environ. 1983;6(3):219-25.

31.    Cruz CD, Regazzi AJ, Carneiro PCS. Modelos Biométricos Aplicados ao Melhoramento Genético. Viçosa: Editora UFV. 2019;1:514.

32.    Carvalho IR, Szareski VJ, Mambrin RB, Ferrari M, Pelegrin AJ, da Rosa TC, et al. Biometric models and maize genetic breeding: A review. Aust J Crop Sci. 2018;12(11):1796-805.

33.    Majidi MM, Tavakoli V, Mirlohi A, Sabzalian MR. Wild safflower species ('Carthamus oxyacanthus' Bieb.): A possible source of drought tolerance for arid environments. Aust J Crop Sci. 2011;5(8):1055-63.

34.    Badran AE. Comparative analysis of some garlic varieties under drought stress conditions. J Agric Sci. 2015;7(10):271.