Scientia Agricultura Sinica ›› 2022, Vol. 55 ›› Issue (13): 2509-2525.doi: 10.3864/j.issn.0578-1752.2022.13.003


Effects of NaCl Stress on the Chlorophyll Fluorescence Characteristics of Seedlings of Japonica Rice Germplasm with Different Salt Tolerances

ZHU ChunYan1(),SONG JiaWei1,BAI TianLiang1,WANG Na1,2,MA ShuaiGuo1,3,PU ZhengFei1,DONG Yan1,LÜ JianDong1,LI Jie1,TIAN RongRong1,LUO ChengKe1,ZHANG YinXia1,MA TianLi1,LI PeiFu1,TIAN Lei1()   

  1. 1College of Agriculture, Ningxia University/Key Laboratory of Modern Molecular Breeding for Dominant and Characteristic Crops in Ningxia, Yinchuan 750021
    2AVIC (Ning Xia) Biology Co., Ltd., Yinchuan 750002
    3College of Agriculture, Tarim University, Alar 843300, Xinjiang
  • Received:2021-10-14 Accepted:2021-12-14 Online:2022-07-01 Published:2022-07-08
  • Contact: Lei TIAN;


【Objective】Chlorophyll fluorescence parameters can reflect the damage degrees and stress resistance of the plant photosynthetic machinery under salt stress. In this study, the analysis of effects of salt stress on chlorophyll fluorescence characteristics of japonica rice with different salt tolerances was performed to reveal its induced kinetic characteristics and preliminarily elucidate the mechanism of OsHCF222 and OsABCI7 regulating salt tolerance of japonica rice at seedling stage, so as to provide a theoretical foundation for screening and breeding salt-tolerant rice varieties.【Method】Eight salt-tolerant and eight salt-sensitive japonica rice germplasm accessions were used as experimental materials in this study. Leaf chlorophyll fluorescence parameters were measured for these materials after treatment using 0 mmol·L-1 or 125 mmol·L-1 NaCl for 3 or 6 days. Principal component analysis (PCA) was used to screen the key indexes for salt tolerance, and a comprehensive evaluation of japonica rice germplasm was carried out with membership functions and weighted standard deviation coefficient method. The resulting salt-tolerant and salt-sensitive germplasm were used to analyze the relative expressions of OsHCF222 and OsABCI7, two chlorophyll fluorescence related genes. 【Result】Compared with the control (CK, 0 mmol·L-1 NaCl for 3 days or 6 days), the salt stress treatment (125 mmol·L-1 NaCl 3 days or 6 days) significantly reduced the maximal fluorescence (Fm) and maximum quantum efficiency of PSII (Fv/Fm) of japonica rice germplasm. For salt tolerant germplasm accessions, the non-photochemical quenching coefficient (NPQ) and coefficient of non-photochemical quenching of variable fluorescence (qN) decreased significantly at 3 days after salt stress, while the initial fluorescence yield (Fo) increased significantly at 6 days after salt stress. The photochemical quenching coefficient (qP) and qN of the salt-sensitive germplasm accessions decreased significantly on the 3rd day after salt stress treatment, while the indexes including yield (Y), NPQ and photosynthetic electron transfer rate (ETR) decreased significantly on the 3rd and 6th day after salt stress treatment. Under salt stress, Fm, Fv/Fm, Y, NPQ and ETR were positively correlated with salt tolerance score (STS), and there were significant differences between salt-tolerant and salt-sensitive japonica rice germplasm accessions. PCA with eight chlorophyll fluorescence parameters revealed two major components, with a cumulative contribution rate of 88.018%. Five key indexes, including Fm, Fv/Fm, Y, NPQ and ETR, were selected based on the loading of each component. The 16 accessions were subsequently assigned to salt tolerant and salt sensitive groups by cluster analysis. A comprehensive evaluation value D (DCF) of chlorophyll fluorescence characteristics under salt stress was obtained by using membership function combined with the index weight method, and then the ranking of the 16 accessions was obtained. Chlorophyll fluorescence induction curves of salt-tolerant Cigalon and Bertone, salt-sensitive Xinzhu8 and Sachiminori under salt stress and CK were created using the Kinetic model. Under CK condition, the four japonica rice germplasm accessions showed similar curve shapes with a large slope and the occurrence time of P peak was basically the same. Under the salt stress treatment, peak P, peak M and the curve slope of salt-sensitive accessions decreased rapidly, while the salt-tolerant accessions still maintained high P peak and curve slope. Through quantitative real-time PCR analysis of OsHCF222 and OsABCI7 in Cigalon and Sachiminori at different times under NaCl stress, the dynamic changes and correlation between leaf chlorophyll content and five key chlorophyll fluorescence parameters, the potential role of the two genes in salt tolerance of japonica rice were preliminarily clarified. 【Conclusion】Chlorophyll fluorescence parameters of japonica rice germplasm with different salt tolerances responded differently to salt stress. Fm, Fv/Fm, Y, NPQ and ETR were closely related to salt tolerance in rice. The expression levels of OsHCF222 and OsABCI7 directly affected the salt tolerance of japonica rice germplasm at seedling stage. In salt-tolerant japonica rice, NPQ and Fv/Fm played as key indexes, while Fm might play an important role in salt-sensitive japonica rice.

Key words: Oryza sativa japonica, salt stress, chlorophyll fluorescence parameters, chlorophyll fluorescence induction curves, quantitative real-time PCR

Table 1

Origins and names of 16 japonica rice germplasm with different salt tolerance, their salt tolerance type, DST value and salt tolerance score (STS)"

Name of germplasm
Salt tolerance
DST value
1 Bertone 葡萄牙 Portugal 耐盐 ST 0.810 7.5
2 Agostono 意大利 Italy 耐盐 ST 0.716 7.2
3 法国稻 Faguodao 法国 France 耐盐 ST 0.708 6.5
4 湟罗 Huangluo 俄罗斯 Russia 耐盐 ST 0.681 6.6
5 漾濞光壳陆稻Yangbiguangkeludao 中国云南 Yunnan, China 耐盐 ST 0.627 6.3
6 Gostima 阿尔巴尼亚 Aerbaerya 耐盐 ST 0.623 5.8
7 Cigalon 法国 France 耐盐 ST 0.621 6.5
8 Banat2951 澳大利亚 Australia 耐盐 ST 0.612 6.5
9 幸实 Sachiminori 日本 Japan 盐敏感 SS 0.426 2.0
10 加合1号 Jiahe 1 中国浙江 Zhejiang, China 盐敏感 SS 0.389 2.4
11 京香2号 Jingxiang 2 中国北京 Beijing, China 盐敏感 SS 0.361 2.3
12 辽丰8号 Liaofeng 8 中国辽宁 Liaoning, China 盐敏感 SS 0.347 3.1
13 越光 Koshihikari 日本 Japan 盐敏感 SS 0.312 1.8
14 嘉南8号 Jianan 8 中国台湾 Taiwan, China 盐敏感 SS 0.261 2.2
15 Banat 725 澳大利亚 Australia 盐敏感 SS 0.252 2.6
16 新竹8号 Xinzhu 8 中国台湾 Taiwan, China 盐敏感 SS 0.243 2.1

Table 2

Gene names and primer sequences for quantitative real-time PCR"

基因 Gene 正向引物 Forward primer 反向引物 Reverse primer

Table 3

Distribution range, coefficient of variation, F value and t value of chlorophyll fluorescence parameters under control and salt stress of japonica rice germplasm resources"

Chlorophyll fluorescence parameters
Salt treatment time
耐盐种质Salt tolerant germplasm 盐敏感种质Salt sensitive germplasm
CV (%)
CV (%)
Fo 0 mmol·L-1 3d 610.00-704.00 6.12 2.93 1.53 544.00-848.00 15.62 1.38 0.67
125 mmol·L-1 3d 586.00-675.67 4.36 524.00-711.50 9.82
0 mmol·L-1 6d 560.00-716.00 9.02 0.15 -2.20* 614.00-845.00 14.69 2.68 1.43
125 mmol·L-1 6d 629.33-798.50 7.99 331.00-882.00 28.44
Fm 0 mmol·L-1 3d 3006.00-3801.00 6.75 3.07 4.35** 2631.00-3833.00 12.79 1.41 4.86**
125 mmol·L-1 3d 3008.33-3177.00 2.04 1058.00-3016.00 31.01
0 mmol·L-1 6d 3344.00-3831.00 5.88 0.12 2.36* 3350.00-3836.00 9.56 6.96 15.07**
125 mmol·L-1 6d 2949.00-3675.00 7.59 584.00-1684.00 46.93
Fv/Fm 0 mmol·L-1 3d 0.79-0.82 1.23 0.90 3.63** 0.76-0.83 2.50 9.20 3.14**
125 mmol·L-1 3d 0.77-0.80 1.27 0.37-0.79 21.88
0 mmol·L-1 6d 0.80-0.83 1.22 7.98 2.58* 0.78-0.83 2.47 7.28 9.18**
125 mmol·L-1 6d 0.74-0.81 3.80 0.43-0.80 21.43
Y 0 mmol·L-1 3d 0.03-0.08 33.33 0.13 0.52 0.02-0.08 40.00 0.35 3.38**
125 mmol·L-1 3d 0.04-0.07 20.00 0.00-0.04 50.00
0 mmol·L-1 6d 0.03-0.08 40.00 0.28 -0.27 0.03-0.08 40.00 0.30 4.24**
125 mmol·L-1 6d 0.03-0.07 40.00 0.00-0.04 50.00
qP 0 mmol·L-1 3d 0.06-0.92 76.19 12.07 1.86 0.06-0.45 65.00 3.17 2.31*
125 mmol·L-1 3d 0.12-0.31 40.00 0.03-0.17 66.67
0 mmol·L-1 6d 0.09-0.90 108.00 0.40 -0.18 0.07-0.21 33.33 14.57 -1.20
125 mmol·L-1 6d 0.11-0.59 59.26 0.01-0.51 95.00
qN 0 mmol·L-1 3d 0.81-0.99 6.45 1.02 2.87* 0.82-0.96 5.62 0.81 2.57*
125 mmol·L-1 3d 0.79-0.90 4.65 0.72-0.89 7.41
0 mmol·L-1 6d 0.84-0.95 4.40 0.02 0.38 0.81-0.95 32.14 3.97 1.31
125 mmol·L-1 6d 0.81-0.96 5.56 0.24-0.94 29.33
NPQ 0 mmol·L-1 3d 1.83-3.98 23.08 3.44 3.63** 1.68-3.55 29.46 1.50 4.05**
125 mmol·L-1 3d 1.59-2.60 18.98 0.47-2.14 42.40
0 mmol·L-1 6d 2.25-3.48 15.65 0.48 1.33 1.76-3.02 20.00 0.18 6.25**
125 mmol·L-1 6d 1.53-3.49 23.55 0.11-0.52 47.13
ETR 0 mmol·L-13d 1.48-4.22 28.42 0.16 0.39 1.08-3.86 35.29 0.43 3.95**
125 mmol·L-13d 1.78-3.66 23.25 0.10-1.90 67.39
0 mmol·L-1 6d 1.58-3.94 35.47 0.25 -0.37 1.52-4.13 36.36 4.44 5.86**
125 mmol·L-1 6d 1.20-3.66 36.55 0.16-2.00 80.82

Table 4

Significance analysis of chlorophyll fluorescence parameters of japonica rice germplasm with different salt tolerance under NaCl stress"

Salt treatment
可变荧光的非光化学猝灭系数qN 非光化学荧光淬灭系数NPQ 表观光合电子传递速率ETR
0 mmol·L-1 3d 耐盐 ST 655.13±40.09a 3428.75±231.36a 0.81±0.01a 0.06±0.02a 0.42±0.32a 0.93±0.06a 3.25±0.75a 2.85±0.81a
盐敏感 SS 650.38±101.61a 3410.75±436.31a 0.80±0.02a 0.05±0.02a 0.20±0.13a 0.89±0.05a 2.58±0.76a 2.38±0.84a
0 mmol·L-1 6d 耐盐 ST 641.81±57.89a 3644.44±214.33a 0.82±0.01a 0.05±0.02a 0.25±0.07a 0.91±0.04a 2.94±0.04a 2.34±0.83a
盐敏感 SS 695.00±88.29a 3683.00±172.73a 0.81±0.02a 0.05±0.02a 0.12±0.02a 0.86±0.27a 2.20±0.05b 2.31±0.84a
125 mmol·L-1 3d 耐盐 ST 628.93±27.41a 3060.08±62.55a 0.79±0.01a 0.05±0.01a 0.20±0.08a 0.86±0.04a 2.16±0.41a 2.71±0.63a
盐敏感 SS 622.25±61.12a 2075.87±63.76b 0.64±0.14b 0.02±0.01b 0.09±0.06b 0.81±0.06a 1.25±0.53b 0.92±0.62b
125 mmol·L-1 6d 耐盐 ST 704.61±56.31a 3366.42±255.35a 0.79±0.03a 0.05±0.02a 0.27±0.16a 0.90±0.04a 2.59±0.61a 2.49±0.91a
盐敏感 SS 598.06±170.10a 1319.86±404.97b 0.52±0.08b 0.02±0.01b 0.20±0.19a 0.75±0.22a 0.87±0.41b 0.47±0.25b

Table 5

Correlation coefficient matrix between chlorophyll fluorescence parameters, relative SPAD and salt tolerance score at seedling stage of japonica rice germplasm resources under salt stress"

参数Parameter Fo Fm Fv/Fm Y qP qN NPQ ETR STS RSPAD
Fo 1.000
Fm 0.524* 1.000
Fv/Fm 0.253 0.928** 1.000
Y 0.329 0.894** 0.835** 1.000
qP 0.391 0.224 0.033 0.402 1.000
qN 0.703** 0.558* 0.452 0.462 0.632** 1.000
NPQ 0.369 0.915** 0.872** 0.906** 0.427 0.611* 1.000
ETR 0.329 0.893** 0.834** 1.000** 0.406 0.465 0.905** 1.000
STS 0.409 0.918** 0.840** 0.856** 0.304 0.485 0.933** 0.853** 1.000
RSPAD 0.525* 0.896** 0.824** 0.814** 0.272 0.603* 0.921** 0.810** 0.909** 1.000

Table 6

Eigenvector of principal component, load matrix, eigenvalue and contribution rate of each comprehensive parameter"

主成分1 CI1 主成分2 CI2
特征向量 Feature vector 载荷 Load 特征向量Feature vector 载荷Load
F0 0.201 0.484 0.636 0.717
Fm 0.391 0.940 -0.215 -0.243
Fv/Fm 0.365 0.876 -0.333 -0.376
Y 0.396 0.951 -0.162 -0.183
qP 0.276 0.664 0.483 0.545
qN 0.346 0.831 0.367 0.414
NPQ 0.404 0.971 -0.152 -0.171
ETR 0.396 0.951 -0.144 -0.162
初始特征值 Eigen value 5.769 1.273
贡献率 Contribution (%) 72.108 15.910
累积贡献率 Cumulative contribution (%) 72.108 88.018

Fig. 1

Cluster analysis of 16 japonica rice germplasm resources based on 5 chlorophyll fluorescence parameters under salt stress"

Table 7

Chlorophyll fluorescence comprehensive index, weight, membership function value, DCF value and ranking of 16 japonica rice germplasm resources"

Name of germplasm
u( X1 )
u( X2 )
DCF value
1 Bertone 2.857 1.170 0.661 0.992 0.721 2
2 Agostono 2.785 0.162 0.638 0.000 0.523 4
3 法国稻 Faguodao 2.929 0.676 0.684 0.506 0.652 3
4 湟罗 Huangluo 2.532 0.272 0.557 0.108 0.476 5
5 漾濞光壳陆稻
2.059 0.632 0.407 0.462 0.417 7
6 Gostima 2.203 0.344 0.453 0.179 0.403 8
7 Cigalon 3.393 0.602 0.831 0.433 0.759 1
8 Banat2951 2.272 0.518 0.475 0.350 0.452 6
9 幸实 Sachiminori 0.781 0.505 0.000 0.338 0.061 16
10 加合 1 号 Jiahe 1 1.567 1.002 0.250 0.826 0.355 11
11 京香 2 号 Jingxiang 2 1.430 0.842 0.207 0.669 0.290 13
12 辽丰 8 号 Liaofeng 8 1.610 0.355 0.264 0.190 0.251 15
13 越光 Koshihikari 1.820 0.605 0.331 0.436 0.350 12
14 嘉南 8 号 Jianan 8 1.840 0.838 0.337 0.665 0.396 9
15 Banat 725 1.756 0.789 0.310 0.617 0.366 10
16 新竹8 号 Xinzhu 8 1.508 0.419 0.231 0.253 0.235 14
权重Index weight 0.819 0.181

Fig. 2

Chlorophyll fluorescence kinetics curves of japonica rice germplasm with different salt tolerance under CK and salt stress a, b, c and d represent chlorophyll fluorescence kinetic curves of 0 mmo·L-1 3d, 125 mmol·L-1 3d, 0 mmol·L-1 6d, and 125 mmol·L-1 6 d, respectively"

Fig. 3

Relative gene expression, chlorophyll content and chlorophyll fluorescence parameters of japonica rice germplasm resources with different salt tolerance under salt stress at different times A, B, C, D, E, F, G and H represent the relative expression of OsHCF222 and OsABCI7, the total chlorophyll content (mg·g-1), the actual photochemical quantum yield (Y), the maximum fluorescence value (Fm), maximum quantum efficiency of PSII (Fv/Fm), photosynthetic electron transfer rate (ETR) and non photochemical quenching coefficient (NPQ) in Cigalon and Sachiminori, respectively. * indicates significant differences among different japonica rice germplasm types at the same treatment (P<0.05), * * indicates significant differences among different japonica rice germplasm types at the same treatment (P<0.01). Different lowercase letters in the same germplasm indicate significant differences among the same japonica rice germplasm types in different treatments (P<0.05)"

Fig. 4

Hypothetical model of the role of OsABCI7 and OsHCF222 on chlorophyll fluorescence parameters and salt resistance under salinity stress in rice The size of the protein circle represents the amount of protein formed. The larger the circle, the more protein formed. The value in the figure is the correlation coefficient (R2), ** indicates significant correlation at 0.01 level;* indicates significant correlation at 0.05 level"

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