Crops ›› 2023, Vol. 39 ›› Issue (3): 221-229.doi: 10.16035/j.issn.1001-7283.2023.03.031

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Response of Quinoa to Low Nitrogen Stress

Guo Hongxia1(), Wang Chuangyun2(), Deng Yan2, Zhao Li2, Zhang Liguang2, Guo Hongxia2, Qin Lixia2, Gao Fei2, Xi Ruizhen2   

  1. 1School of Life Sciences, Shanxi University, Taiyuan 030006, Shanxi, China
    2College of Agriculture, Shanxi Agricultural University, Taiyuan 030031, Shanxi, China
  • Received:2021-12-05 Revised:2022-05-12 Online:2023-06-15 Published:2023-06-16

Abstract:

In order to explore the response mechanism of quinoa to low nitrogen environment and select quinoa varieties with low nitrogen tolerance. The agronomic traits, some physiological characteristics and nitrogen utilization indexes of nine different genotypes of quinoa under different nitrogen levels treatments (normal N supply and low N stress) were determined by pot cultivation, and the comprehensive low nitrogen tolerance capacities of the lines were evaluated by principal component analysis and cluster analysis. The results showed that under low nitrogen stress, the shoot growth of the quinoa was inhibited, plant height, thick stem, and shoot dry weight showed a downward trend. The primary root length and root-shoot ratio rose increased obviously, while root volume, root surface area and average root diameter decreased. Chlorophyll content, maximum fluorescence parameter (Fm) and maximum photochemical efficiency (Fv/Fm) were reduced, while the initial fluorescence parameter Fo was increased. Root activity, nitrate reductase activity, glutamine synthase activity, glutamate synthase activity, and soluble protein content decreased, while the activities of superoxide dismutase and peroxidase, the contents of malondialdehyde, soluble sugar and free proline were increased. The total nitrogen content and nitrogen accumulation were reduced, while the nitrogen utilization efficiency was increased. The 26 individual indicators were transformed into four independent comprehensive indicators (cumulative contribute rate was 83.959%) by principal component analysis, and nine quinoa lines were classified into low-nitrogen tolerance, intermediate and low nitrogen sensitive types by cluster analysis, and one low-nitrogen- resistant line BL22 was selected.

Key words: Quinoa, Low nitrogen stress, Comprehensive evaluation, Variety screening

Table 1

Information of tested nine quinoa materials"

材料
Material
相关信息
Relevant information
HL58 红藜,千粒重3.27g,生育期约120d
G68 白藜,千粒重3.19g,生育期约120d,高秆
A29 白藜,千粒重3.34g,生育期约120d,矮秆
G36 白藜,千粒重3.26g,生育期约120d,高秆
BL23 白藜,千粒重3.07g,生育期约120d
A86 白藜,千粒重3.15g,生育期约120d,矮秆
HL93 红藜,千粒重3.21g,生育期约120d
BL77 白藜,千粒重3.16g,生育期约120d
BL22 白藜,千粒重3.46g,生育期约120d

Fig.1

Effects of low nitrogen stress on aboveground partial growth of different quinoa lines The different lowercase letters indicate significant difference at P < 0.05 level, the same below"

Table 2

Effects of low nitrogen stress on the root growth of quinoa"

处理
Treatment
藜麦品系
Quinoa
line
最大根长
Maximum root
length (cm)
根系平均直径
Root average
diameter (mm)
根系表面积
Root surface
area (cm2)
根系体积
Root volume
(cm3)
根系干重
Root dry
weight (g)
根冠比
Root-shoot
ratio
CK HL58 12.43±0.16abA 0.32±0.01aAB 48.58±2.39aA 0.65±0.02aAB 0.21±0.01aAB 0.14±0.00bB
G68 10.98±0.31cdBCD 0.22±0.01dDE 45.48±0.08abAB 0.58±0.01bBC 0.16±0.01deDE 0.11±0.01dC
A29 10.43±0.25deCDE 0.26±0.02cCD 45.32±0.70abAB 0.55±0.02bcCD 0.18±0.01bcBCD 0.14±0.01bB
G36 12.87±0.35aA 0.34±0.01aA 36.69±2.10cC 0.44±0.03eE 0.15±0.01eE 0.12±0.01cdBC
BL23 9.99±0.48eDE 0.21±0.01dE 45.28±1.22abAB 0.54±0.02bcCD 0.18±0.01cdCD 0.14±0.00bB
A86 11.99±0.17bAB 0.29±0.01bBC 45.85±1.88abAB 0.70±0.01aA 0.22±0.01aA 0.14±0.00bcB
HL93 11.25±0.28cBC 0.27±0.02bcC 48.04±0.75aA 0.58±0.02bBCD 0.20±0.01abABC 0.17±0.01aA
BL77 9.86±0.34eE 0.28±0.01bcBC 36.51±1.51cC 0.46±0.04deE 0.16±0.01eDE 0.11±0.00dC
BL22 10.48±0.39deCDE 0.25±0.02cCD 42.81±0.86bB 0.50±0.02cdDE 0.20±0.01aAB 0.14±0.01bB
LN HL58 12.77±0.28abAB 0.29±0.02aA 46.67±1.30aA 0.62±0.02aA 0.22±0.01abAB 0.15±0.01bcdBC
G68 11.93±0.34bcBC 0.26±0.02abAB 40.35±0.78cB 0.51±0.01bcBC 0.17±0.01defEF 0.13±0.00fgD
A29 11.10±0.42cdCD 0.23±0.02bcdABC 41.65±1.47bcAB 0.51±0.02bcBC 0.19±0.01cdCDE 0.16±0.00bAB
G36 13.35±0.58aA 0.27±0.03abA 34.03±3.48dC 0.36±0.02fE 0.16±0.00fF 0.14±0.00efCD
BL23 10.59±0.14dD 0.20±0.01dC 42.20±0.47bcAB 0.43±0.03eD 0.18±0.00deDEF 0.15±0.00cdeBC
A86 13.15±0.56aAB 0.25±0.01abABC 41.65±0.92bcAB 0.53±0.03bBC 0.24±0.01aA 0.16±0.01bcB
HL93 11.32±0.20cdCD 0.26±0.01abAB 43.92±1.00abAB 0.56±0.02bAB 0.21±0.00bcBC 0.18±0.00aA
BL77 10.55±0.44dD 0.21±0.01cdBC 39.47±0.80cB 0.44±0.02deD 0.17±0.01efEF 0.12±0.00gD
BL22 10.56±0.08dD 0.24±0.01bcABC 41.40±1.58bcB 0.48±0.02cdCD 0.21±0.01cBCD 0.14±0.01deBC

Fig.2

Effects of low nitrogen stress on the chlorophyll content of different quinoa lines"

Fig.3

Effects of low nitrogen stress on the chlorophyll fluorescence parameters of different quinoa lines"

Table 3

Effects of low nitrogen stress on enzyme activities and MDA content in quinoa"

处理
Treatment
藜麦品系
Quinoa line
NR活性
NR activity (U/g)
POD活性
POD activity (U/g)
SOD活性
SOD activity (U/g)
MDA含量
MDA content (nmol/g)
CK HL58 0.54±0.02aA 722.93±29.78bB 145.56±6.00abA 25.61±1.06aA
G68 0.42±0.02cC 836.99±34.48aA 118.50±4.88cC 21.28±0.87cBC
A29 0.16±0.01eE 661.04±27.23cdBC 139.07±5.73bAB 18.65±0.77dDE
G36 0.48±0.02bB 619.38±25.51dC 113.99±3.16cCD 16.59±0.68eE
BL23 0.18±0.01eE 716.67±19.87bcB 145.92±6.01abA 19.28±0.79dCD
A86 0.24±0.01dD 881.64±36.32aA 97.70±1.37dD 10.01±0.41gG
HL93 0.40±0.02cC 617.29±25.43dC 123.48±7.44cBC 19.09±0.66dCDE
BL77 0.17±0.01eE 616.73±12.89dC 117.52±4.84cC 23.38±0.96bAB
BL22 0.40±0.02cC 608.14±20.98dC 153.10±6.31aA 13.49±0.56fF
LN HL58 0.47±0.01aA 748.98±18.16bcABC 153.39±3.72abA 31.89±0.77bB
G68 0.19±0.01cC 782.80±18.98abAB 106.41±2.58eDE 36.04±0.87aA
A29 0.11±0.00eD 678.92±16.46cdBCD 148.93±1.56abA 28.24±0.31cBC
G36 0.40±0.01bB 641.99±15.56dCD 122.05±2.96dCD 25.45±0.62dCD
BL23 0.14±0.00dD 730.46±12.84bcBCD 142.33±3.45bcAB 19.84±0.28eEF
A86 0.06±0.00fE 853.51±23.49aA 100.16±2.43eE 23.78±0.58dDE
HL93 0.39±0.01bB 629.56±15.26dD 125.67±3.05dBC 17.98±0.44eF
BL77 0.12±0.00deD 637.34±9.05dD 130.04±3.15cdBC 38.13±0.92aA
BL22 0.39±0.01bB 625.04±15.15dD 158.97±0.84aA 13.70±0.33fG

Table 4

Effects of low nitrogen stress on quinoa root activity and enzyme activities related to nitrogen metabolism"

处理
Treatment
藜麦品系
Quinoa line
根系活力
Root activity [μg(h·g)]
GS活性
GS activity (U/g)
GOGTA活性
GOGTA activity (U/g)
CK HL58 76.03±3.13aA 65.61±2.70cdBC 26.47±1.59bBC
G68 63.04±1.75bB 69.67±0.98bcABC 29.80±1.23aAB
A29 47.52±1.96cC 63.22±3.81dC 23.18±0.95cCD
G36 40.22±0.56efDE 61.56±2.54dC 29.85±1.23aAB
BL23 43.68±2.63cdeCDE 66.88±2.75bcdBC 20.23±0.83dD
A86 42.62±1.76deCDE 75.98±3.13aA 30.76±1.27aA
HL93 46.16±1.90cdCD 72.12±2.97abAB 28.65±0.79abAB
BL77 36.94±1.52fE 70.06±2.89abcABC 23.02±0.95cCD
BL22 61.99±2.55bB 64.71±1.79cdBC 23.35±0.33cCD
LN HL58 80.52±0.84aA 59.18±1.43cdB 21.82±0.53cdCD
G68 44.73±1.08cC 60.74±1.47cdB 33.29±0.81aA
A29 41.08±0.91cC 58.96±1.43dB 20.34±0.11eDE
G36 31.29±0.76dD 65.49±1.59bcB 24.56±0.60cBC
BL23 41.23±1.00cC 61.30±0.32bcdB 18.47±0.45eE
A86 29.88±0.72dD 66.92±1.18bAB 24.09±0.25cC
HL93 42.60±0.22cC 74.70±1.81aA 27.83±0.67bB
BL77 31.57±0.77dD 64.49±0.67bcdB 20.46±0.50deDE
BL22 59.63±1.45bB 63.24±1.53bcdB 23.43±0.57cCD

Table 5

Effects of low nitrogen stress on quinoa osmotic mediation substances"

处理
Treatment
藜麦品系
Quinoa line
可溶性蛋白
Soluble protein (mg/g)
可溶性糖
Soluble sugar (mg/g)
Pro
(μg/g)
CK HL58 6.31±0.26cdCD 1.84±0.07eDE 92.78±3.82cdCDE
G68 6.83±0.28cBC 1.62±0.06fE 90.97±3.14dDE
A29 4.70±0.19eE 2.48±0.10abAB 105.41±4.34bBC
G36 4.17±0.17eE 2.60±0.10aA 110.00±4.53bAB
BL23 3.11±0.13fF 2.21±0.09cdBC 84.78±2.35deE
A86 8.62±0.36aA 2.07±0.08dCD 101.51±5.52bcBCD
HL93 7.60±0.31bB 2.43±0.09abAB 120.04±4.94aA
BL77 5.92±0.24dD 2.35±0.09bcAB 106.37±4.38bB
BL22 5.81±0.20dD 1.60±0.06fE 79.56±3.28eE
LN HL58 5.41±0.13cB 2.41±0.04eE 100.98±2.45cBC
G68 5.21±0.13cdBC 2.58±0.05dCD 70.21±1.70eE
A29 3.85±0.09eD 3.21±0.05abA 114.66±2.78bAB
G36 3.36±0.08efD 3.08±0.04bAB 127.03±3.08aA
BL23 3.18±0.08fD 2.55±0.04dD 94.16±2.28cCD
A86 7.11±0.18bA 2.84±0.04cBC 82.09±1.99dDE
HL93 7.89±0.19aA 2.64±0.05dCD 117.09±3.22abAB
BL77 4.72±0.10dC 3.35±0.06aA 115.02±2.79bAB
BL22 5.74±0.14cB 1.65±0.03fF 82.61±2.00dDE

Table 6

Effects of low nitrogen stress on quinoa nitrogen content and nitrogen utilization efficiency"

处理
Treatment
藜麦品系
Quinoa line
全氮含量
N content (mg/g)
氮积累量(mg/株)
N accumulation (mg/plant)
氮利用效率
N utilization efficiency (g/g)
CK HL58 1.84±0.08bBC 3.17±0.05bB 542.85±22.36efDE
G68 1.68±0.07cCD 2.66±0.13cdC 596.13±24.56deCD
A29 1.22±0.05efF 1.79±0.05eD 823.47±33.92aAB
G36 1.32±0.05eEF 1.74±0.05eD 759.14±31.27bB
BL23 1.16±0.05fF 1.68±0.03eD 859.91±35.42aA
A86 2.07±0.09aA 3.68±0.04aA 483.43±19.91fE
HL93 1.99±0.08abAB 2.81±0.09cC 503.47±20.74fE
BL77 1.63±0.07cdCD 2.51±0.19dC 615.00±25.33cdCD
BL22 1.50±0.06dDE 2.50±0.13dC 665.55±27.41cC
LN HL58 1.60±0.06bB 2.77±0.07aA 624.32±23.63dCD
G68 1.30±0.05dC 2.02±0.03dD 772.96±29.26bB
A29 1.12±0.04eD 1.56±0.03eE 893.52±33.82aA
G36 1.05±0.04eD 1.37±0.07fE 954.84±36.14aA
BL23 1.08±0.04eD 1.55±0.02eE 927.56±35.11aA
A86 1.39±0.05cdC 2.43±0.09bcB 721.43±27.31bcB
HL93 1.80±0.07aA 2.54±0.08bB 556.53±21.06eD
BL77 1.39±0.06cdC 2.13±0.13dCD 718.14±31.97bcBC
BL22 1.44±0.05cBC 2.35±0.07cBC 693.95±21.60cBC

Table 7

Load coefficient and cumulative contribution rate of each comprehensive index"

指标
Index
因子1
Factor 1
因子2
Factor 2
因子3
Factor 3
因子4
Factor 4
可溶性蛋白含量
Soluble protein content
0.711 -0.288 0.243 -0.382
可溶性糖含量
Soluble sugar content
-0.837 -0.133 -0.296 0.393
MDA含量MDA content -0.869 0.419 0.114 0.160
NR活性NR activity 0.930 -0.095 -0.157 -0.176
Pro含量Pro content 0.717 0.412 -0.347 0.010
POD活性POD activity 0.803 0.476 -0.325 -0.030
SOD活性SOD activity 0.403 0.826 -0.260 0.190
根系活力Root activity 0.757 -0.167 -0.548 -0.207
GS活性GS activity 0.618 0.326 0.395 -0.285
GOGTA活性GOGTA activity 0.085 -0.853 0.296 0.315
株高Plant height 0.507 -0.126 0.598 0.531
茎粗Stem diameter 0.494 0.468 0.579 0.239
SPAD 0.523 -0.076 0.748 0.188
Fo -0.839 -0.185 -0.151 -0.425
Fm 0.304 0.343 0.489 -0.698
Fv/Fm 0.815 0.406 0.362 0.029
最大根长
Maximum root length
-0.850 0.079 0.021 0.359
根系平均直径
Root average diameter
-0.274 -0.927 0.169 -0.073
根系表面积Root surface area 0.366 0.370 -0.425 0.567
根系体积Root volume 0.578 -0.388 -0.277 0.145
根系干重Root dry weight -0.903 0.219 -0.078 -0.253
茎叶干重Shoot dry weight 0.244 -0.196 -0.300 -0.415
根冠比Root-shoot ratio -0.856 0.289 0.111 0.042
全氮含量N content 0.886 -0.285 -0.149 0.176
氮积累量N accumulation 0.910 -0.312 -0.204 0.085
氮利用效率
N utilization efficiency
-0.878 0.291 0.196 -0.188
累计贡献率
Cumulative contribute rate (%)
47.463 65.910 75.976 83.959

Table 8

Comprehensive index values, weights, D values and ranking of different quinoa lines"

藜麦品系
Quinoa line
因子1
Factor 1
因子2
Factor 2
因子3
Factor 3
因子4
Factor 4
D 排序
Ranking
HL58 0.043 -0.166 -2.285 -1.087 0.413 7
G68 -1.492 -1.838 0.258 0.564 0.204 9
A29 0.027 0.316 -0.039 0.944 0.615 5
G36 0.092 1.361 0.548 -0.717 0.655 4
BL23 0.500 -0.638 -0.065 -0.434 0.592 6
A86 -1.655 0.995 0.747 -0.638 0.324 8
HL93 0.914 -0.446 0.751 -0.914 0.699 2
BL77 0.191 0.901 -0.757 1.869 0.682 3
BL22 1.380 -0.483 0.842 0.413 0.835 1
权重Weight 0.558 0.194 0.140 0.108

Fig.4

Cluster diagram of low nitrogen tolerance of nine quinoa strains"

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