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Relationship of Photosynthetic Carbon Assimilation Related Traits of Flag Leaves with Yield Heterosis in a Wheat Diallel Cross
ACTA AGRONOMICA SINICA Volume 36, Issue 6, June 2010 Online English edition of the Chinese language journal Cite this article as: Acta Agron Sin, 2010, 36(6): 1003–1010.
RESEARCH PAPER
Relationship of Photosynthetic Carbon Assimilation Related Traits of Flag Leaves with Yield Heterosis in a Wheat Diallel Cross WANG Xiu-Li1,2, HU Zhao-Rong1,2, PENG Hui-Ru1,2, DU Jin-Kun1,2, SUN Qi-Xin1,2, WANG Min1,2, and NI Zhong-Fu1,2,* 1
Key Laboratory of Crop Heterosis and Utilization, Ministry of Education/ State Key Laboratory for Agrobiotechnology/ Key Laboratory of Crop Genomics and Genetic Improvement, Ministry of Agriculture/ Beijing Key Laboratory of Crop Genetic Improvement, China Agricultural University, Beijing 100193, China
2
National Plant Gene Research Centre (Beijing), Beijing 100193, China
Abstract: In spite of commercial use of heterosis in agriculture, the physiological basis of heterosis is poorly understood. Photosynthetic carbon assimilation related traits of flag leaves, including photosynthetic capacity, stomatal conductance, intercellular CO2 concentration, transpiration rate, water use efficiency, and efficiency of primary conversion of light energy, were measured at early, middle, and post grain-filling stages in a wheat (Triticum aestivum L.) diallel cross containing 20 hybrids and 9 parents. The purpose of this study was to determine the relationship between yield heterosis and these traits. The magnitude of heterosis varied subject to cross combination, trait, and developmental stage. Further analysis indicated that heterosis of photosynthetic carbon assimilation related traits was not correlated with that of spike length and spike number per plant, but significantly correlated with that of other yield components. At middle grain-filling stage, the heterosis of photosynthetic rate, intercellular CO2 concentration, water use efficiency, and efficiency of primary conversion of light energy were significantly and positively correlated with those of fertile spikelets per plant, thousand-grain weight, yield per plant, and yield of main stem. These results suggested that higher photosynthetic capacity and water use efficiency could be one of the important physiological bases of wheat hybrid vigor. Keywords: wheat; photosynthetic carbon assimilation; yield; heterosis
Heterosis or hybrid vigor is defined as the advantage of hybrid performance over its parents in terms of viability, growth, and productivity, and has been widely used in agriculture. However, up to date, the mechanism of heterosis is still an area to be elucidated. Although all the genes in hybrid are inherited from its 2 parental inbreds, hybrid performance or phenotype can be quite different from its parents [1]. Recently, genome-wide studies described differences in gene expression of hybrids and their parental inbred lines, and both additive and nonadditive expression patterns were observed [2–15]. These differentially expressed genes, though functionally not known yet, play an important role for hybrids to demonstrate heterosis. At the level of physiology and
biochemistry, it has proven that hybrids are quite different from their parental lines in enzyme composition, photosynthetic rate, respiratory intensity, and assimilation transportation [16–21]. Photosynthetic carbon assimilation is an important basis for crop yield, but also closely related with heterosis. For example, Wang et al. [22] reported that better photosynthetic functions, higher water use efficiency, and strong resistance to photo-inhibition might be the physiological basis for the super high-yield of super hybrid rice. In a study of inter-subspecific hybrid between Brassica campestris subsp. chinensis ‘Aijiaohuang’ and B. campestris subsp. rapifera ‘Baimanjing’, higher photosynthetic capacity, and stomatal conductance were detected in hybrid than that in their parents, but no
Received: 4 January 2010; Accepted: 15 March 2010. * Corresponding author. E-mail: [email protected] Copyright © 2010, Crop Science Society of China and Institute of Crop Sciences, Chinese Academy of Agricultural Sciences. Published by Elsevier BV. All rights reserved. Chinese edition available online at http://www.chinacrops.org/zwxb/ DOI: 10.1016/S1875-2780(09)60057-2
WANG Xiu-LI et al. / Acta Agronomica Sinica, 2010, 36(6): 1003–1010
difference for intercellular CO2 concentration [23]. In maize (Zea mays L.) hybrids, higher photosynthetic capacity was also observed during the period of grain filling, as compared to their inbred lines [24]. More recently, many genes involved in photosynthetic carbon assimilation were up-regulated in hybrids of rice (Oryza sativa L.) and Arabidopsis [25, 26]. Remarkably, it is found that Arabidopsis hybrids may gain advantages from the control of circadian-mediated physiological and metabolic pathways, leading to growth vigor and increased biomass [26]. Hybrid wheat (Triticum aestivum L.) exhibits heterosis for photosynthetic carbon assimilation related traits [27], among which maternal effect may play a vital role [28]. However, the number of hybrid combinations used in previous studies was limited, and their relationships with yield-related traits remain to be unveiled. In the present study, the relationship of yield heterosis with photosynthetic carbon assimilation related traits of flag leaves were investigated, and significantly correlation was detected. Most importantly, at middle grain-filling stage, the heterosis of photosynthetic rate, intercellular CO2 concentration, water use efficiency, and efficiency of primary conversion of light energy were significantly and positively correlated with those of fertile spikes per plant, thousandgrain weight, yield per plant, and yield of main stem. This result suggested that higher photosynthetic capacity and water use efficiency could be one of the important physiological bases of wheat hybrid vigor, which may provide valuable information for further investigation on the mechanism of wheat yield heterosis.
1
Materials and methods
1.1
Plant materials and field experiment
Four wheat female lines (3338, 3235, 227, and 101) and 5 male lines (F390, Jindong 6, Jing 411, 3214, and Yuandong 8790) were intercrossed according to the NCII design to form a diallel set of 20 hybrids. The parental lines 3338, 227, 101, and 3214 were bred by China Agricultural University, Beijing, China. The other parental lines 3535, F390, Jindong 6, Jing 411, and Yuandong 8790 (designated as 8790) derived from Hebei University of Agriculture (Baoding, China), Beijing Agricultural College (Beijing, China), Beijing Academy of Agricultural and Forestry Sciences (Beijing, China), Beijing Seed Company (Beijing, China), and Chinese Academy of Agricultural Sciences (Beijing, China), respectively. In autumn of 2004, each cross was planted in a 5-row plot in the Science Park of China Agricultural University, Beijing, China with 30 seedlings per row. Each cross had 3 replicates. 1.2 Measurement of photosynthetic carbon assimilation related traits LI-6400 portable photosynthesis system (LI-COR, USA)
was used to measure photosynthesis rate (Pn), stomatal conductance (Gs), intercellular CO2 concentration (Ci), and transpiration rate (Tr). Water use efficiency (WUE) was calculated using the equation of WUE = Pn/Tr. Parameter values for leaf temperature, light intensity, and CO2 concentration were 25°C, 1500 µmol m2 s1, and 360 μmol mol1, respectively. Portable FIM-1500 (Analytical Development Company Limited, UK) was used to measure chlorophyll fluorometer parameters and efficiency of primary conversion of light energy (Fv/Fm) was calculated, which reflects the maximum photochemical efficiency. The above traits were recorded at 4, 15, and 40 d after flowering (DAF) as described by Tang et al. [29] and Zhang et al. [30], which corresponding to early, middle, and post grain-filling stages, respectively. For each replicate, flag leaves of 10 plants with same phenotypes were selected for analysis. To avoid the influence of circadian clock and light intensity, the time for measurement was between 11:00 and 13:00 on sunny day. 1.3
Estimation of yield and its components
Spike length, spike number per plant, fertile spikelets per plant, grain number per spike, thousand-grain weight, yield of main stem, and yield per plant from the hybrids and their parents were recorded from 10 plants for each replicate. 1.4
Data analysis
Mid-parent heterosis (MPH) was calculated as (F1 MP)/ MP) ×100%, where F1 is the mean of hybrid, and MP is the average of the 2 parents. Paired t-test was used to determine the significance of differences between hybrids and their corresponding parents. DPS 3.01 software was used for simple, canonical, and partial correlation analysis.
2 2.1
Results Heterosis in yield and its components
Greater variations were detected for heterosis of spike length, spike number per plant, fertile spikelets per plant, grain number per spike, thousand-grain weight, yield of main stem, and yield per plant, with the ranges of −5.10% to +31.37%, −11.68% to +43.39%, −3.88% to +10.94%, −21.15% to +19.38, −12.86% to +25.98%, −15.95% to +34.18%, and −11.01% to +123.08%, respectively (Table 1). For each cross combination, the magnitude of heterosis was also variable for different traits. For example, MPH of thousand-grain weight in hybrid 101/3214 (20.28%) was significantly higher than that of grain number per spike (−21.25%). Moreover, the numbers of correlation coefficient that were significant (P < 0.05) for heterosis of spike length, spike number per plant, fertile spikelets per plant, grain number per spike, thousand-grain weight, yield of main stem,
WANG Xiu-LI et al. / Acta Agronomica Sinica, 2010, 36(6): 1003–1010
Table 1 Mid-parent heterosis in yield and its components in 20 hybrids of wheat (%) Cross
Spike length
Spike number
Fertile spikelets
Grain number
Thousand-grain
Yield of main
per plant
per plant
per spike
weight
stem
Yield per plant
3338/F390
1.05
5.38*
2.83
8.08**
5.80*
13.05**
20.71*
3338/Jingdong 6
3.01
12.68**
5.48*
3.40
10.40**
15.35**
22.86*
11.68**
6.09**
4.18*
17.04*
20.75**
6.89*
12.86**
15.95**
11.01**
3338/Jing 411
11.94**
3338/3214
2.70
2.44
3.88*
3.47
3338/8790
0.99
35.50*
4.21*
7.90**
3235/F390
0.12
4.55*
5.36*
6.63*
3235/Jingdong 6
3.87
7.48**
3235/Jing 411
7.76*
43.39**
3235/3214
3.12
3235/8790
5.10**
227/F390
3.75
14.12**
8.94*
17.65**
70.40**
25.98**
34.18**
31.98*
16.73*
4.00
20.20**
30.32**
7.81*
5.42*
16.44**
30.56**
6.13**
5.58*
2.53
12.12**
35.43**
2.62
2.30
16.35*
13.34**
80.89**
1.45
1.50
2.99
12.84**
16.78**
26.15**
31.23*
227/Jingdong 6
0.58
2.81
3.41*
1.78
7.80*
5.03
1.34
227/Jing 411
31.37**
12.14*
3.61*
0.98
20.08**
18.09**
29.55*
19.79**
7.32**
12.01**
11.70*
17.47**
55.39* 20.93*
227/3214 227/8790 101/F390 101/Jingdong 6 101/Jing 411 101/3214 101/8790
2.40 4.01* 3.91 5.55*
13.93**
9.71**
41.92**
1.96
23.93**
28.32**
2.38
1.80
3.82
15.42**
10.27*
7.50
12.33*
1.27
3.66
12.51**
5.08*
38.21*
12.31*
23.48**
3.48
7.07*
19.38**
8.75**
17.71**
10.94**
21.15**
20.28**
24.06**
2.80
18.23**
19.17*
0.15
123.08*
23.98**
45.19**
10.50*
7.09
6.48*
19.17*
*P < 0.05; ** P < 0.01.
and yield per plant in all 20 cross combinations were 8, 15, 13, 12, 19, 18, and 17, respectively. This indicates that the crosses can be used as ideal materials for studying wheat hetesosis (Table 1). 2.2 Heterosis in photosynthetic carbon assimilation related traits For the same trait, the magnitude of heterosis varied among cross combinations and developmental stages. For example, Gs heterotic values at 4, 15, and 40 DAF in hybrid 3235/3214 were 27.27%, −11.85%, and 73.14%, respectively, which was different from those in hybrid 227/8790 (−38.02%, 12.25%, and −64.64%). For the same cross combination, the heterotic values of different traits were also different. For example, Pn and Tr heterotic values at 15 DAF in hybrid 3235/Jingdong 6 were 14.35% and 13.77%, respectively, but Ci heteosis was as low as 0.13% (Table 2). The results of t-test indicated that heterosis of most photosynthetic carbon assimilation related traits in the 20 cross combinations was significant (P < 0.05), especially the Pn heterosis, with the number of 17 (85%) at 4 DAF, 17 (85%) at 15 DAF, and 18 (90%) at 40 DAF. Although heterotic values of some traits were relatively high, there were no significant differences between hybrids and their corresponding parents. This may be caused by different physiological status of sampling plants in each replicate and/or experimental error. At the 3 developmental stages tested, Pn heterosis was significantly and positively correlated with Gs and Tr heterosis.
In addition, Gs heterosis was significantly and positively correlated with Tr heterosis, but WUE was significantly and negatively correlated with Ci heterosis (Table 3). 2.3 Correlation analysis of heterosis between yield and photosynthetic carbon assimilation Firstly, canonical correlation was used to determine the relationship of photosynthetic carbon assimilation related traits with yield heterosis in the wheat diallel cross. The results exhibited that the values of correlation coefficients λ1 to λ4 were significant (P < 0.01), indicating that there was true correlation between the 2 variables (Data not shown). Secondly, the partial correlation coefficients between heterosis in yield and photosynthetic carbon assimilation were estimated to remove the effects of other variables (Table 4). The heterosis of photosynthetic carbon assimilation was not correlated with the heterosis of spike length and spike number per plant. However, it was significantly correlated with other yield-related traits at certain stages. For example, the numbers of significant partial correlation coefficient were 7 for heterosis of fertile spikelets per plant, 8 for thousand-grain weight, 13 for grain number per spike, 15 for yield per plant, and 17 for yield of main stem (Table 4). Further analysis revealed that there was good correlation between the heterosis of photosynthetic carbon assimilation and yield-related traits. Firstly, at the 3 grain-filling stages tested, with an exception at 40 DAF (r = −0.96), the other 11 partial correlation coefficients between heterosis of Pn and 4
WANG Xiu-LI et al. / Acta Agronomica Sinica, 2010, 36(6): 1003–1010
Table 2 Mid-parent heterosis of photosynthetic carbon assimilation traits in 20 hybrids (%) Cross
Pn
Gs
DAF4
DAF15
DAF40
DAF15
DAF40
3338/F390
23.85*
3.87*
4.63
33.36**
4.16
4.37
14.40**
8.04**
3338/Jingdong 6
39.36**
4.55*
50.42**
48.02**
11.81**
41.07**
0.62
7.90*
3338/Jing 411
20.43**
1.42
28.23**
18.03**
21.84
33.90**
16.36*
3338/3214
31.24**
4.84*
55.45**
25.61**
2.57
65.25**
23.81**
5.33*
3338/8790
1.64**
5.19
24.52*
18.30*
9.32
41.40**
18.01**
5.04**
12.37*
1.52
15.09**
3235/F390 3235/Jingdong 6
4.97
16.22*
DAF4
Ci
8.96**
14.35**
1.32
5.18
DAF4
DAF15
5.14
DAF40 0.72 4.34 2.60** 8.34** 3.49
65.78**
0.61
2.68**
9.70**
8.68*
84.92**
3.91
0.13
12.58** 2.80**
13.37**
1.09**
76.38**
15.85**
9.21*
62.74**
7.75
0.02
3235/3214
17.51*
0.70**
24.00**
27.27*
11.85**
73.14**
0.78
5.64*
5.66**
3235/8790
12.20**
0.67**
43.33**
23.22**
12.19**
22.37**
23.50**
7.65*
16.37**
0.68
54.32**
9.54*
5.43**
3235/Jing 411
227/F390
11.48*
4.19
42.41**
5.58
227/Jingdong 6
16.92**
8.95**
45.91**
14.02
5.93
14.06**
7.66**
11.49*
2.72
20.17**
227/3214
21.50**
4.52**
32.36*
16.69*
6.88*
7.12*
227/8790
24.39**
9.66**
16.40**
38.02**
12.25**
64.64**
101/F390
12.88**
11.54**
5.74**
18.76**
9.38**
60.72*
7.20*
8.67**
14.15**
0.36
4.01
2.34**
44.34**
16.89**
101/3214
11.95**
5.27**
53.05**
101/8790
2.19**
3.37**
29.35**
227/Jing 411
101/Jingdong 6 101/Jing 411
Cross
DAF4
DAF15
23.90**
9.54
3338/Jingdong 6
34.38**
3338/Jing 411
11.35**
3338/3214
18.31**
3338/8790
22.45**
3235/F390
0.89
3235/Jingdong 6
2.27**
16.01** 10.18 7.38** 19.82* 16.72 13.77*
17.92**
7.75**
1.71
1.81 19.18** 0.71
0.00
0.69
1.80
4.04
0.15
2.00**
27.19**
0.12*
2.17
8.34**
5.80
19.13**
7.13*
2.64
30.39**
10.10
43.18**
13.12**
3.22
1.28
24.73**
12.32*
48.06**
5.96
4.94
7.20**
WUE DAF40
1.71
5.09
3.15*
10.15*
2.19
2.74**
Tr
3338/F390
6.40** 4.51*
DAF4 0.08**
Fv/Fm
DAF15
DAF40
12.22**
12.16**
3.12*
DAF40
1.63*
22.25**
0.78
1.61
7.70* 10.38**
9.74
49.86**
19.31**
12.19**
31.09**
16.06**
11.38**
10.90**
57.56**
4.10
0.59
45.19**
4.97
0.71*
4.98
0.51
31.31**
3.08**
0.20**
14.96**
38.80** 9.59**
1.28
DAF15
23.87**
6.54**
23.24**
DAF4
34.98**
48.46**
17.71*
7.10**
4.58** 0.49 1.83**
2.07* 0.80 1.17*
3.71 42.00* 3.07
15.84**
1.19
34.68**
2.93
0.10
63.84**
1.08**
1.92*
22.73**
3235/3214
12.28**
5.10
70.02**
42.66*
11.83
27.81**
1.06
0.94**
13.51*
3235/8790
21.82**
10.01
19.60**
4.66**
6.11*
26.99**
2.01
0.09
227/F390
3.08
3.36
19.25**
14.11**
0.79**
19.04**
0.44*
1.74*
227/Jingdong 6
9.69*
5.93
3.69**
8.03**
2.85
43.21**
3.35*
3.18*
227/Jing 411
12.68**
8.13
18.43**
5.98**
5.47
11.23
3.93
1.99
26.49**
9.42*
5.01*
3235/Jing 411
1.34 1.90* 8.81**
14.42**
1.31*
9.02**
0.34
38.30*
1.82
2.89
227/8790
30.73**
10.03**
39.85*
11.07**
11.56
31.22**
3.05
0.05
9.07
101/F390
12.98**
1.39*
3.36**
0.53*
0.89
227/3214
101/Jingdong 6 101/Jing 411
47.56**
0.08
9.88**
29.30**
4.41*
0.05
8.78**
2.68
8.51**
21.16**
1.31
1.77
13.13*
15.03*
6.38
2.96**
12.95
9.31*
44.78**
0.96
0.30
32.31**
31.19**
16.17
101/3214
18.16**
101/8790
22.22**
0.81** 0.06
36.68**
5.27*
3.39
11.43**
4.40*
31.73**
3.47**
3.57
0.03
1.59**
0.42 33.37**
Pn: Photosynthesis rate; Gs: Stomatal conductance; Ci: Intercellular CO2 concentration; Tr: Transpiration rate; WUE: Water use efficiency; Fv/Fm: Efficiency of primary conversion of light energy. DAF4, DAF15, and DAF40 denote 4, 15, and 40 d after flowering. *P < 0.05; **P < 0.01.
yield-related traits (grain number per spike, thousand-grain weight, yield per plant, and yield of main stem) were positive, among which 8 were significant (P < 0.05). On the contrary, all the 12 correlation coefficients between the heterosis of Gs
and the above 4 yield-related traits were negative, among which 10 were significant (P < 0.05). Secondly, the heterosis of Gi at 4 and 15 DAF was positively correlated with grain number per spike, thousand-grain weight, yield per plant, and
WANG Xiu-LI et al. / Acta Agronomica Sinica, 2010, 36(6): 1003–1010
Table 3 Correlation coefficient between heterosis in photosynthetic carbon assimilation related traits Pn
Gs
Ci
Tr
WUE
Gs DAF4
0.81**
DAF15
0.52*
DAF40
0.66*
Ci DAF4
0.22
0.20
DAF15
0.08
0.70**
DAF40
0.29
0.30
Tr DAF4
0.73**
0.98**
0.28
DAF15
0.48*
0.82**
0.74**
DAF40
0.62**
0.96**
0.26
WUE DAF4
0.41
0.10
0.48*
0.04
DAF15
0.40
0.34
0.81**
0.51
DAF40
0.44*
0.24
0.49*
0.30
Fv/Fm DAF4
0.22
0.04
0.39
0.03
DAF15
0.19
0.12
0.31
0.16
0.30 0.20
DAF40
0.29
0.38
0.13
0.37
0.04
Pn: Photosynthesis rate; Gs: Stomatal conductance; Ci: Intercellular CO2 concentration; Tr: Transpiration rate; WUE: Water use efficiency; Fv/Fm: Efficiency of primary conversion of light energy. DAF4, DAF15, and DAF40 denote 4, 15, and 40 d after flowering. *P < 0.05; **P < 0.01.
Table 4 Yield-related trait
Partial correlation coefficients between heterosis in yield and photosynthetic carbon assimilation Pn
Gs
Ci
DAF4
DAF15
DAF40
DAF4
DAF15
DAF40
DAF4
DAF15
DAF40
Spike length
0.57
0.52
0.09
0.72
0.53
0.84
0.73
—
0.56
Spike number per plant
0.64
0.84
0.73
0.69
0.88
0.86
0.27
0.85
0.12
Fertile spikelets per plant
0.28
0.54
—
0.40
0.80
0.97**
—
0.21
0.93*
Grain number per spike
0.86
0.99*
Thousand-grain weight
0.98*
0.90
0.99* 0.96
1.00**
0.99*
1.00**
0.99*
0.99*
0.19
0.99*
0.17
0.97
0.95
0.58
1.00**
Yield of main stem
1.00**
1.00**
0.98*
1.00**
0.99*
1.00**
1.00**
1.00**
1.00**
Yield per plant
0.98*
0.99*
0.93
0.99*
0.99*
0.99*
0.99*
0.99*
0.97
Yield-related trait
Tr
WUE
Fv/Fm
DAF4
DAF15
DAF40
DAF4
DAF15
DAF40
DAF4
DAF15
DAF40
Spike length
0.38
0.56
0.85
0.70
0.79
0.59
0.75
0.83
0.77
Spike number per plant
0.76
0.69
0.72
0.89
0.37
0.62
0.86
0.15
0.63
0.76
0.97**
0.88*
0.96**
0.83
0.91*
0.97**
Fertile spikelets per plant
0.91 0.41
Grain number per spike
0.99*
0.99*
1.00**
1.00**
0.88
0.95
1.00**
0.99*
0.96
Thousand-grain weight
0.89
0.82
0.98*
0.93
0.98*
0.99*
0.98*
0.99*
0.95
Yield of main stem
1.00**
1.00**
1.00**
1.00**
0.99*
1.00**
1.00**
1.00**
0.93
Yield per plant
0.99*
0.99*
0.99*
1.00**
0.78
0.99*
1.00**
0.98*
0.98*
Pn: Photosynthesis rate; Gs: Stomatal conductance; Ci: Intercellular CO2 concentration; Tr: Transpiration rate; WUE: Water use efficiency; Fv/Fm: Efficiency of primary conversion of light energy. DAF4, DAF15, and DAF40 denote 4, 15, and 40 d after flowering. *P < 0.05; **P < 0.01.
yield of main stem, among which 6 were significant (P < 0.05), but the opposite trend was observed at 40 DAF. In addition, heterosis of Tr at 4 and 40 DAF were also positively
correlated with the above 4 yield-related traits, among which 7 were significant (P < 0.05), but the opposite trend was observed at 15 DAF. Finally, a total of 8 partial correlation
WANG Xiu-LI et al. / Acta Agronomica Sinica, 2010, 36(6): 1003–1010
coefficients at 4 DAF between the heterosis of WUE and Fv/Fm and 5 yield-related traits (fertile spikelets per plant, grain number per spike, thousand-grain weight, yield per plant, and yield of main stem) were negative, among which 7 were significant (P < 0.05), but the opposite trend was observed at 15 and 40 DAF.
3
Discussion
As a key metabolic process for matter production in plants, photosynthesis is the physiological basis of crop biomass yield. Plant hybrids exhibited higher rates of photosynthesis compared to their parental inbred lines [24–27]. In this study, the magnitudes of heterosis of Pn at the 3 grain-filling stages tested were variable in different cross combinations, but 11 out of 12 partial correlation coefficients between heterosis of Pn and 4 yield-related traits (grain number per spike, thousand-grain weight, yield per plant, and yield of main stem) were positive, among which 8 were significant. Therefore, it can be concluded that this advantage of photosynthesis rate in wheat hybrid may contribute to the observed yield heterosis. Among all the yield components tested, spike length and spike number per plant were developed before flowering, whereas photosynthetic carbon assimilation related traits were recorded at the stages of grain filling. Theoretically, there was no relationship of photosynthetic carbon assimilation related traits with the heterosis of spike length and spike number per plant, which is consistent with the results of our partial correlation analysis. Importantly, the heterosis of most partial correlation Pn, Ci, WUE, and Fv/Fm were positively correlated with the heterosis of grain number per spike, thousand-grain weight, yield per plant, and yield of main stem, and most of which were significant. In rice, Wang et al. [22] reported that super hybrid exhibited better photosynthetic functions, higher WUE and stronger photochemical efficiency of photosystem II than their parents. Taken together, we propose that both Pn and WUE may be the physiological basis for the super high-yield of crop hybrids. Up to date, there are many reports about the relationship of yield heterosis with photosynthetic carbon assimilation related traits in wheat, but the results are still controversial. Lupton [31] reported that hybrid wheat exhibited the heterosis of Pn before flowering, whereas Borghiet et al. [32] found that this advantage was mainly in the reproductive stage. Xiao et al. [27] proposed that the Pn heterosis was obvious during the process of flag leaf senescence, but Zhang et al. [28] reported that it depended on maternal effect. Taken our present results together, we speculate that this may be related to complexity of heterosis of yield and photosynthetic carbon assimilation related traits. Firstly, the magnitude of heterosis of yield and its components varied among cross combinations. For instance, higher heterosis of spike number per plant were detected in hybrids
3235/Jing 411 and 3338/8790 (23.93% and 25.98%) and higher heterosis of thousand-grain weight were observed in hybrids 227/8790 and 3235/F390 (43.39% and 35.50%) compared to other yield components. The development of spike number per plant has been completed before ear emergence. Although no significant heterosis was detected for photosynthesis rate, yield heterosis was still relative high in hybrids 3235/Jing 411 and 3338/8790 (123.08% and 70.40%, respectively). Secondly, variations in the magnitudes of heterosis of photosynthetic carbon assimilation related traits were observed among cross combinations and developmental stages. For instance, high heterosis of Pn was observed in hybrid 101/F390 at 4, 15, and 40 DAF (12.88%, 11.54%, and 5.74%), followed by hybrid 227/Jing 411 at 4 and 15 DAF (5.93% and 14.06%) and hybrid 3235/8790 at 4 DAF (12.20%). It must be noted, however, that the data presented here is mainly derived from statistical analysis, and further experiment in molecular biology should be undertaken to investigate the relationship between gibberellins and heterosis in wheat plant height. In order to further elucidate the relationship of yield heterosis with photosynthetic carbon assimilation related traits, the priorities are to select the cross combination and trait for investigation and to determine its key developmental stage.
4
Conclusions
There was true correlation between heterosis of yield and photosynthetic carbon assimilation related traits, and high photosynthetic capacity and water use efficiency could be one of the important physiological bases of wheat hybrid vigor. Moreover, mid-grain-filling stage may be the key developmental stage for wheat yield heterosis.
Acknowledgments This study was funded by the National Basic Research Program of China (2007CB109000), the National Foundation for Outstanding Young Scientists of China (30925023), and the National Natural Science Foundation of China (30671297 and 30771342).
References [1] [2]
[3]
Hochholdinger F, Hoeckera N. Towards the molecular basis of heterosis. Trend Plant Sci, 2007, 12: 427–432 Ni Z F, Sun Q X Wu L M. Differential gene expression between wheat hybrids and their parental inbreds in seedling leaves of early and vigorous tillering stages. J China Agric Univ, 2000, 5: 1–8 (in Chinese with English abstract) Bao J, Lee S, Chen C, Zhang X, Zhang Y, Liu S, Clark T, Wang J, Cao M, Yang H, Wang S, Yu J. Serial analysis of gene expression study of a hybrid rice strain (LYP9) and its parental cultivars. Plant Physiol, 2005, 138: 1216–1231
WANG Xiu-LI et al. / Acta Agronomica Sinica, 2010, 36(6): 1003–1010
[4]
[5]
[6]
[7]
[8]
[9]
[10]
[11]
[12]
[13]
[14]
[15]
[16]
[17]
Hoecker N, Keller B, Muthreich N, Chollet D, Descombes P, Piepho H P, Hochholdinger F. Comparison of maize (Zea mays L.) F1-hybrid and parental inbred line primary root transcriptomes suggests organ-specific patterns of nonadditive gene expression and conserved expression trends. Genetics, 2008, 179: 1275–1283 Ge X, Chen W, Song S, Wang W, Hu S, Yu J. Transcriptomic profiling of mature embryo from an elite super-hybrid rice LYP9 and its parental lines. BMC Plant Biol, 2008, 8: 114 Ni Z, Sun Q, Wu L, Xie C. Differential gene expression between wheat hybrids and their parental inbreds in primary roots. Acta Bot Sin, 2002, 44: 457–462 Song S, Qu H, Chen C, Hu S, Yu J. Differential gene expression in an elite hybrid rice cultivar (Oryza sativa L.) and its parental lines based on SAGE data. BMC Plant Biol, 2007, 7: 49 Huang Y, Zhang L D, Zhang J W, Yuan D, Xu C, Li X, Zhou D, Wang S, Zhang Q. Heterosis and polymorphisms of gene expression in an elite rice hybrid as revealed by a microarray analysis of 9198 unique ESTs. Plant Mol Biol, 2006, 62: 579–591 Wu H L, Ni Z F, Yao Y Y, Guo G G, Sun Q X. Cloning and expression profiles of 15 genes encoding WRKY transcription factor in wheat (Triticum aestivum L.). Prog Nat Sci, 2008, 18: 697–706 Zhang Y H, Ni Z F, Yao Y Y, Zhao J, Sun Q X. Analysis of genome-wide gene expression in root of wheat hybrid and its parents using Barley1 GeneChip. Prog Nat Sci, 2006, 16: 712–720 Romagnoli S, Maddaloni M, Livini C, Motto M. Relationship between gene expression and hybrid vigor in primary root tips of young maize (Zea mays L.) plantlets. Theor Appl Genet, 1990, 80: 769–775 Hoecker N, Lamkemeyer T, Sarholz B, Paschold A, Fladerer C, Madlung J, Wurster K, Stahl M, Piepho H P, Nordheim A, Hochholdinger F. Analysis of nonadditive protein accumulation in young primary roots of a maize (Zea mays L.) F1-hybrid compared to its parental inbred lines. Proteomics, 2008, 8: 3882–3894 Wang W, Meng B, Ge X, Song S, Yang Y, Wang L, Hu S, Liu S, Yu J. Proteomic profiling of rice embryos from a hybrid rice cultivar and its parental lines. Proteomics, 2008, 8: 4808–4821 Song X, Ni Z F, Yao Y Y, Xie C J, Li Z X, Wu H Y, Zhang Y H, Sun Q X. Wheat (Triticum aestivum L.) root proteome and differentially expressed root proteins between hybrid and parents. Proteomics, 2007, 7: 3538–3557 Song X, Ni Z F,Yao Y Y, Zhang Y H, Sun Q X. Identification of differentially expressed proteins between hybrid and parents in wheat (Triticum aestivum L.) seedling leaves. Theor Appl Genet, 2009, 118: 213–225 Yang T X, Zeng M Q, Li J G. Corn heterosis and isozyme studies: IV. Analysis of the hybrid enzyme on the peroxidase isoenzyme. Hereditas (Beijing), 1981, 3(6): 31–33 (in Chinese with English abstract) Dai J R, Luo M Z, Han Y S. Relationship of maize peroxidase, esterase isozyme and hybrid production. Acta Agron Sin, 1989, 15: 193–201 (in Chinese with English abstract)
[18] Li Z Q, Wang Z R. Relationship between heterosis and endogenous plant hormones in liriodendron. Acta Bot Sin, 2002, 44: 698–701 [19] Zhao Q Z, Lü D B, Cheng X Y, Chen J Y, Liang J J. The heterosis of canopy photosynthetic rate and bleeding intensity of hybrid wheat. Sci Agric Sin, 2002, 35: 925–928 (in Chinese with English abstract) [20] Mohammad A, Sarker Z, Murayama S, Ishimine Y, Tsuzuki E. Physio-Morphological characters of F1 hybrid of rice (Oryza sativa L.) in japanica-india crosses. Plant Proc Sci, 2001, 4: 196–201 [21] You M A, Gai J Y, Ma Y H. Relationship of leaf photosynthetic rate with stomatal and mesophyll conductance in soybeans. Acta Agron Sin, 1995, 21: 145–149 (in Chinese with English abstract) [22] Wang Q, Zhang Q D, Jiang G M, Lu C M, Kuang T Y, Wu S, Li C Q, Jiao D M. Photosynthetic characteristics of two super high-yield hybrid rice. Acta Bot Sin, 2000, 42: 1285–1288 (in Chinese with English abstract) [23] Dong D K, Shi K, Cao J S. The photosynthetic heterosis and its mechanisms of an inter-subspecific hybrid between Brassica campestris ssp. chinensis and B. campestris ssp. rapifera. Sci Agric Sin, 2007, 40: 2804–2810 (in Chinese with English abstract) [24] Tollenaar M, Ahmadzadeh A, Lee E A. Physiological basis of heterosis for grain yield in maize. Crop Sci, 2004, 44: 2086–2094 [25] Wei G, Tao Y, Liu G Liu G, Chen C, Luo R, Xia H, Gan Q, Zeng H, Lu Z, Han Y, Li X, Song G, Zhai H, Peng Y, Li D, Xu H, Wei X, Cao M, Deng H, Xin Y, Fu X, Yuan L, Yu J, Zhu Z, Zhu L. A transcriptomic analysis of super hybrid rice LYP9 and its parents. Proc Natl Acad Sci USA, 2009, 106: 7695–7701 [26] Ni Z, Kim E, Ha M, Lackey E, Liu J, Zhang Y, Sun Q, Chen Z. Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids. Nature, 2009, 457: 327–331 [27] Xiao K, Gu J T, Zou D H, Zhang R X. Studies on CO2 conductance during flag leaf aging of hybrid wheats and their parents. Acta Agron Sin, 1998, 24: 503–508 (in Chinese with English abstract) [28] Zhang Q D, Zhu X G, Wang Q, Lu C M, Kuang T Y, Zhang W X, Zhang J H. Photosynthetic characters of F1 hybrids in winter wheat and their parents. Acta Agron Sin, 2001, 27: 653–657 (in Chinese with English abstract) [29] Tang W, Li W J, Zhang D M, Dong H Z. Drought effects on POD, MDA and photosynthetic rate in seedling leaves of transgenic cotton. China Cotton, 2002, 29(2): 23–24 (in Chinese) [30] Zhang Y P, Wang Z M, Wang P, Zhao M. Canopy photosynthetic characteristics of population of winter wheat in water-saving and high-yielding cultivation. Sci Agric Sin, 2003, 36: 1143–1149 (in Chinese with English abstract) [31] Lupton F G H. Physiological bases of heterosis in wheat. In: Janossy A, Lupton F G H, eds. Heterosis in Plant Breeding. New York: Academic Press, 1974. pp 71–80 [32] Borghi B M, Perenzin, Nash R J. Agronomic and qualitative characteristics of ten bread wheat hybrids produced using a chemical hybridizing agent. Euphytica, 1988, 39: 185–194
RESEARCH PAPER
Relationship of Photosynthetic Carbon Assimilation Related Traits of Flag Leaves with Yield Heterosis in a Wheat Diallel Cross WANG Xiu-Li1,2, HU Zhao-Rong1,2, PENG Hui-Ru1,2, DU Jin-Kun1,2, SUN Qi-Xin1,2, WANG Min1,2, and NI Zhong-Fu1,2,* 1
Key Laboratory of Crop Heterosis and Utilization, Ministry of Education/ State Key Laboratory for Agrobiotechnology/ Key Laboratory of Crop Genomics and Genetic Improvement, Ministry of Agriculture/ Beijing Key Laboratory of Crop Genetic Improvement, China Agricultural University, Beijing 100193, China
2
National Plant Gene Research Centre (Beijing), Beijing 100193, China
Abstract: In spite of commercial use of heterosis in agriculture, the physiological basis of heterosis is poorly understood. Photosynthetic carbon assimilation related traits of flag leaves, including photosynthetic capacity, stomatal conductance, intercellular CO2 concentration, transpiration rate, water use efficiency, and efficiency of primary conversion of light energy, were measured at early, middle, and post grain-filling stages in a wheat (Triticum aestivum L.) diallel cross containing 20 hybrids and 9 parents. The purpose of this study was to determine the relationship between yield heterosis and these traits. The magnitude of heterosis varied subject to cross combination, trait, and developmental stage. Further analysis indicated that heterosis of photosynthetic carbon assimilation related traits was not correlated with that of spike length and spike number per plant, but significantly correlated with that of other yield components. At middle grain-filling stage, the heterosis of photosynthetic rate, intercellular CO2 concentration, water use efficiency, and efficiency of primary conversion of light energy were significantly and positively correlated with those of fertile spikelets per plant, thousand-grain weight, yield per plant, and yield of main stem. These results suggested that higher photosynthetic capacity and water use efficiency could be one of the important physiological bases of wheat hybrid vigor. Keywords: wheat; photosynthetic carbon assimilation; yield; heterosis
Heterosis or hybrid vigor is defined as the advantage of hybrid performance over its parents in terms of viability, growth, and productivity, and has been widely used in agriculture. However, up to date, the mechanism of heterosis is still an area to be elucidated. Although all the genes in hybrid are inherited from its 2 parental inbreds, hybrid performance or phenotype can be quite different from its parents [1]. Recently, genome-wide studies described differences in gene expression of hybrids and their parental inbred lines, and both additive and nonadditive expression patterns were observed [2–15]. These differentially expressed genes, though functionally not known yet, play an important role for hybrids to demonstrate heterosis. At the level of physiology and
biochemistry, it has proven that hybrids are quite different from their parental lines in enzyme composition, photosynthetic rate, respiratory intensity, and assimilation transportation [16–21]. Photosynthetic carbon assimilation is an important basis for crop yield, but also closely related with heterosis. For example, Wang et al. [22] reported that better photosynthetic functions, higher water use efficiency, and strong resistance to photo-inhibition might be the physiological basis for the super high-yield of super hybrid rice. In a study of inter-subspecific hybrid between Brassica campestris subsp. chinensis ‘Aijiaohuang’ and B. campestris subsp. rapifera ‘Baimanjing’, higher photosynthetic capacity, and stomatal conductance were detected in hybrid than that in their parents, but no
Received: 4 January 2010; Accepted: 15 March 2010. * Corresponding author. E-mail: [email protected] Copyright © 2010, Crop Science Society of China and Institute of Crop Sciences, Chinese Academy of Agricultural Sciences. Published by Elsevier BV. All rights reserved. Chinese edition available online at http://www.chinacrops.org/zwxb/ DOI: 10.1016/S1875-2780(09)60057-2
WANG Xiu-LI et al. / Acta Agronomica Sinica, 2010, 36(6): 1003–1010
difference for intercellular CO2 concentration [23]. In maize (Zea mays L.) hybrids, higher photosynthetic capacity was also observed during the period of grain filling, as compared to their inbred lines [24]. More recently, many genes involved in photosynthetic carbon assimilation were up-regulated in hybrids of rice (Oryza sativa L.) and Arabidopsis [25, 26]. Remarkably, it is found that Arabidopsis hybrids may gain advantages from the control of circadian-mediated physiological and metabolic pathways, leading to growth vigor and increased biomass [26]. Hybrid wheat (Triticum aestivum L.) exhibits heterosis for photosynthetic carbon assimilation related traits [27], among which maternal effect may play a vital role [28]. However, the number of hybrid combinations used in previous studies was limited, and their relationships with yield-related traits remain to be unveiled. In the present study, the relationship of yield heterosis with photosynthetic carbon assimilation related traits of flag leaves were investigated, and significantly correlation was detected. Most importantly, at middle grain-filling stage, the heterosis of photosynthetic rate, intercellular CO2 concentration, water use efficiency, and efficiency of primary conversion of light energy were significantly and positively correlated with those of fertile spikes per plant, thousandgrain weight, yield per plant, and yield of main stem. This result suggested that higher photosynthetic capacity and water use efficiency could be one of the important physiological bases of wheat hybrid vigor, which may provide valuable information for further investigation on the mechanism of wheat yield heterosis.
1
Materials and methods
1.1
Plant materials and field experiment
Four wheat female lines (3338, 3235, 227, and 101) and 5 male lines (F390, Jindong 6, Jing 411, 3214, and Yuandong 8790) were intercrossed according to the NCII design to form a diallel set of 20 hybrids. The parental lines 3338, 227, 101, and 3214 were bred by China Agricultural University, Beijing, China. The other parental lines 3535, F390, Jindong 6, Jing 411, and Yuandong 8790 (designated as 8790) derived from Hebei University of Agriculture (Baoding, China), Beijing Agricultural College (Beijing, China), Beijing Academy of Agricultural and Forestry Sciences (Beijing, China), Beijing Seed Company (Beijing, China), and Chinese Academy of Agricultural Sciences (Beijing, China), respectively. In autumn of 2004, each cross was planted in a 5-row plot in the Science Park of China Agricultural University, Beijing, China with 30 seedlings per row. Each cross had 3 replicates. 1.2 Measurement of photosynthetic carbon assimilation related traits LI-6400 portable photosynthesis system (LI-COR, USA)
was used to measure photosynthesis rate (Pn), stomatal conductance (Gs), intercellular CO2 concentration (Ci), and transpiration rate (Tr). Water use efficiency (WUE) was calculated using the equation of WUE = Pn/Tr. Parameter values for leaf temperature, light intensity, and CO2 concentration were 25°C, 1500 µmol m2 s1, and 360 μmol mol1, respectively. Portable FIM-1500 (Analytical Development Company Limited, UK) was used to measure chlorophyll fluorometer parameters and efficiency of primary conversion of light energy (Fv/Fm) was calculated, which reflects the maximum photochemical efficiency. The above traits were recorded at 4, 15, and 40 d after flowering (DAF) as described by Tang et al. [29] and Zhang et al. [30], which corresponding to early, middle, and post grain-filling stages, respectively. For each replicate, flag leaves of 10 plants with same phenotypes were selected for analysis. To avoid the influence of circadian clock and light intensity, the time for measurement was between 11:00 and 13:00 on sunny day. 1.3
Estimation of yield and its components
Spike length, spike number per plant, fertile spikelets per plant, grain number per spike, thousand-grain weight, yield of main stem, and yield per plant from the hybrids and their parents were recorded from 10 plants for each replicate. 1.4
Data analysis
Mid-parent heterosis (MPH) was calculated as (F1 MP)/ MP) ×100%, where F1 is the mean of hybrid, and MP is the average of the 2 parents. Paired t-test was used to determine the significance of differences between hybrids and their corresponding parents. DPS 3.01 software was used for simple, canonical, and partial correlation analysis.
2 2.1
Results Heterosis in yield and its components
Greater variations were detected for heterosis of spike length, spike number per plant, fertile spikelets per plant, grain number per spike, thousand-grain weight, yield of main stem, and yield per plant, with the ranges of −5.10% to +31.37%, −11.68% to +43.39%, −3.88% to +10.94%, −21.15% to +19.38, −12.86% to +25.98%, −15.95% to +34.18%, and −11.01% to +123.08%, respectively (Table 1). For each cross combination, the magnitude of heterosis was also variable for different traits. For example, MPH of thousand-grain weight in hybrid 101/3214 (20.28%) was significantly higher than that of grain number per spike (−21.25%). Moreover, the numbers of correlation coefficient that were significant (P < 0.05) for heterosis of spike length, spike number per plant, fertile spikelets per plant, grain number per spike, thousand-grain weight, yield of main stem,
WANG Xiu-LI et al. / Acta Agronomica Sinica, 2010, 36(6): 1003–1010
Table 1 Mid-parent heterosis in yield and its components in 20 hybrids of wheat (%) Cross
Spike length
Spike number
Fertile spikelets
Grain number
Thousand-grain
Yield of main
per plant
per plant
per spike
weight
stem
Yield per plant
3338/F390
1.05
5.38*
2.83
8.08**
5.80*
13.05**
20.71*
3338/Jingdong 6
3.01
12.68**
5.48*
3.40
10.40**
15.35**
22.86*
11.68**
6.09**
4.18*
17.04*
20.75**
6.89*
12.86**
15.95**
11.01**
3338/Jing 411
11.94**
3338/3214
2.70
2.44
3.88*
3.47
3338/8790
0.99
35.50*
4.21*
7.90**
3235/F390
0.12
4.55*
5.36*
6.63*
3235/Jingdong 6
3.87
7.48**
3235/Jing 411
7.76*
43.39**
3235/3214
3.12
3235/8790
5.10**
227/F390
3.75
14.12**
8.94*
17.65**
70.40**
25.98**
34.18**
31.98*
16.73*
4.00
20.20**
30.32**
7.81*
5.42*
16.44**
30.56**
6.13**
5.58*
2.53
12.12**
35.43**
2.62
2.30
16.35*
13.34**
80.89**
1.45
1.50
2.99
12.84**
16.78**
26.15**
31.23*
227/Jingdong 6
0.58
2.81
3.41*
1.78
7.80*
5.03
1.34
227/Jing 411
31.37**
12.14*
3.61*
0.98
20.08**
18.09**
29.55*
19.79**
7.32**
12.01**
11.70*
17.47**
55.39* 20.93*
227/3214 227/8790 101/F390 101/Jingdong 6 101/Jing 411 101/3214 101/8790
2.40 4.01* 3.91 5.55*
13.93**
9.71**
41.92**
1.96
23.93**
28.32**
2.38
1.80
3.82
15.42**
10.27*
7.50
12.33*
1.27
3.66
12.51**
5.08*
38.21*
12.31*
23.48**
3.48
7.07*
19.38**
8.75**
17.71**
10.94**
21.15**
20.28**
24.06**
2.80
18.23**
19.17*
0.15
123.08*
23.98**
45.19**
10.50*
7.09
6.48*
19.17*
*P < 0.05; ** P < 0.01.
and yield per plant in all 20 cross combinations were 8, 15, 13, 12, 19, 18, and 17, respectively. This indicates that the crosses can be used as ideal materials for studying wheat hetesosis (Table 1). 2.2 Heterosis in photosynthetic carbon assimilation related traits For the same trait, the magnitude of heterosis varied among cross combinations and developmental stages. For example, Gs heterotic values at 4, 15, and 40 DAF in hybrid 3235/3214 were 27.27%, −11.85%, and 73.14%, respectively, which was different from those in hybrid 227/8790 (−38.02%, 12.25%, and −64.64%). For the same cross combination, the heterotic values of different traits were also different. For example, Pn and Tr heterotic values at 15 DAF in hybrid 3235/Jingdong 6 were 14.35% and 13.77%, respectively, but Ci heteosis was as low as 0.13% (Table 2). The results of t-test indicated that heterosis of most photosynthetic carbon assimilation related traits in the 20 cross combinations was significant (P < 0.05), especially the Pn heterosis, with the number of 17 (85%) at 4 DAF, 17 (85%) at 15 DAF, and 18 (90%) at 40 DAF. Although heterotic values of some traits were relatively high, there were no significant differences between hybrids and their corresponding parents. This may be caused by different physiological status of sampling plants in each replicate and/or experimental error. At the 3 developmental stages tested, Pn heterosis was significantly and positively correlated with Gs and Tr heterosis.
In addition, Gs heterosis was significantly and positively correlated with Tr heterosis, but WUE was significantly and negatively correlated with Ci heterosis (Table 3). 2.3 Correlation analysis of heterosis between yield and photosynthetic carbon assimilation Firstly, canonical correlation was used to determine the relationship of photosynthetic carbon assimilation related traits with yield heterosis in the wheat diallel cross. The results exhibited that the values of correlation coefficients λ1 to λ4 were significant (P < 0.01), indicating that there was true correlation between the 2 variables (Data not shown). Secondly, the partial correlation coefficients between heterosis in yield and photosynthetic carbon assimilation were estimated to remove the effects of other variables (Table 4). The heterosis of photosynthetic carbon assimilation was not correlated with the heterosis of spike length and spike number per plant. However, it was significantly correlated with other yield-related traits at certain stages. For example, the numbers of significant partial correlation coefficient were 7 for heterosis of fertile spikelets per plant, 8 for thousand-grain weight, 13 for grain number per spike, 15 for yield per plant, and 17 for yield of main stem (Table 4). Further analysis revealed that there was good correlation between the heterosis of photosynthetic carbon assimilation and yield-related traits. Firstly, at the 3 grain-filling stages tested, with an exception at 40 DAF (r = −0.96), the other 11 partial correlation coefficients between heterosis of Pn and 4
WANG Xiu-LI et al. / Acta Agronomica Sinica, 2010, 36(6): 1003–1010
Table 2 Mid-parent heterosis of photosynthetic carbon assimilation traits in 20 hybrids (%) Cross
Pn
Gs
DAF4
DAF15
DAF40
DAF15
DAF40
3338/F390
23.85*
3.87*
4.63
33.36**
4.16
4.37
14.40**
8.04**
3338/Jingdong 6
39.36**
4.55*
50.42**
48.02**
11.81**
41.07**
0.62
7.90*
3338/Jing 411
20.43**
1.42
28.23**
18.03**
21.84
33.90**
16.36*
3338/3214
31.24**
4.84*
55.45**
25.61**
2.57
65.25**
23.81**
5.33*
3338/8790
1.64**
5.19
24.52*
18.30*
9.32
41.40**
18.01**
5.04**
12.37*
1.52
15.09**
3235/F390 3235/Jingdong 6
4.97
16.22*
DAF4
Ci
8.96**
14.35**
1.32
5.18
DAF4
DAF15
5.14
DAF40 0.72 4.34 2.60** 8.34** 3.49
65.78**
0.61
2.68**
9.70**
8.68*
84.92**
3.91
0.13
12.58** 2.80**
13.37**
1.09**
76.38**
15.85**
9.21*
62.74**
7.75
0.02
3235/3214
17.51*
0.70**
24.00**
27.27*
11.85**
73.14**
0.78
5.64*
5.66**
3235/8790
12.20**
0.67**
43.33**
23.22**
12.19**
22.37**
23.50**
7.65*
16.37**
0.68
54.32**
9.54*
5.43**
3235/Jing 411
227/F390
11.48*
4.19
42.41**
5.58
227/Jingdong 6
16.92**
8.95**
45.91**
14.02
5.93
14.06**
7.66**
11.49*
2.72
20.17**
227/3214
21.50**
4.52**
32.36*
16.69*
6.88*
7.12*
227/8790
24.39**
9.66**
16.40**
38.02**
12.25**
64.64**
101/F390
12.88**
11.54**
5.74**
18.76**
9.38**
60.72*
7.20*
8.67**
14.15**
0.36
4.01
2.34**
44.34**
16.89**
101/3214
11.95**
5.27**
53.05**
101/8790
2.19**
3.37**
29.35**
227/Jing 411
101/Jingdong 6 101/Jing 411
Cross
DAF4
DAF15
23.90**
9.54
3338/Jingdong 6
34.38**
3338/Jing 411
11.35**
3338/3214
18.31**
3338/8790
22.45**
3235/F390
0.89
3235/Jingdong 6
2.27**
16.01** 10.18 7.38** 19.82* 16.72 13.77*
17.92**
7.75**
1.71
1.81 19.18** 0.71
0.00
0.69
1.80
4.04
0.15
2.00**
27.19**
0.12*
2.17
8.34**
5.80
19.13**
7.13*
2.64
30.39**
10.10
43.18**
13.12**
3.22
1.28
24.73**
12.32*
48.06**
5.96
4.94
7.20**
WUE DAF40
1.71
5.09
3.15*
10.15*
2.19
2.74**
Tr
3338/F390
6.40** 4.51*
DAF4 0.08**
Fv/Fm
DAF15
DAF40
12.22**
12.16**
3.12*
DAF40
1.63*
22.25**
0.78
1.61
7.70* 10.38**
9.74
49.86**
19.31**
12.19**
31.09**
16.06**
11.38**
10.90**
57.56**
4.10
0.59
45.19**
4.97
0.71*
4.98
0.51
31.31**
3.08**
0.20**
14.96**
38.80** 9.59**
1.28
DAF15
23.87**
6.54**
23.24**
DAF4
34.98**
48.46**
17.71*
7.10**
4.58** 0.49 1.83**
2.07* 0.80 1.17*
3.71 42.00* 3.07
15.84**
1.19
34.68**
2.93
0.10
63.84**
1.08**
1.92*
22.73**
3235/3214
12.28**
5.10
70.02**
42.66*
11.83
27.81**
1.06
0.94**
13.51*
3235/8790
21.82**
10.01
19.60**
4.66**
6.11*
26.99**
2.01
0.09
227/F390
3.08
3.36
19.25**
14.11**
0.79**
19.04**
0.44*
1.74*
227/Jingdong 6
9.69*
5.93
3.69**
8.03**
2.85
43.21**
3.35*
3.18*
227/Jing 411
12.68**
8.13
18.43**
5.98**
5.47
11.23
3.93
1.99
26.49**
9.42*
5.01*
3235/Jing 411
1.34 1.90* 8.81**
14.42**
1.31*
9.02**
0.34
38.30*
1.82
2.89
227/8790
30.73**
10.03**
39.85*
11.07**
11.56
31.22**
3.05
0.05
9.07
101/F390
12.98**
1.39*
3.36**
0.53*
0.89
227/3214
101/Jingdong 6 101/Jing 411
47.56**
0.08
9.88**
29.30**
4.41*
0.05
8.78**
2.68
8.51**
21.16**
1.31
1.77
13.13*
15.03*
6.38
2.96**
12.95
9.31*
44.78**
0.96
0.30
32.31**
31.19**
16.17
101/3214
18.16**
101/8790
22.22**
0.81** 0.06
36.68**
5.27*
3.39
11.43**
4.40*
31.73**
3.47**
3.57
0.03
1.59**
0.42 33.37**
Pn: Photosynthesis rate; Gs: Stomatal conductance; Ci: Intercellular CO2 concentration; Tr: Transpiration rate; WUE: Water use efficiency; Fv/Fm: Efficiency of primary conversion of light energy. DAF4, DAF15, and DAF40 denote 4, 15, and 40 d after flowering. *P < 0.05; **P < 0.01.
yield-related traits (grain number per spike, thousand-grain weight, yield per plant, and yield of main stem) were positive, among which 8 were significant (P < 0.05). On the contrary, all the 12 correlation coefficients between the heterosis of Gs
and the above 4 yield-related traits were negative, among which 10 were significant (P < 0.05). Secondly, the heterosis of Gi at 4 and 15 DAF was positively correlated with grain number per spike, thousand-grain weight, yield per plant, and
WANG Xiu-LI et al. / Acta Agronomica Sinica, 2010, 36(6): 1003–1010
Table 3 Correlation coefficient between heterosis in photosynthetic carbon assimilation related traits Pn
Gs
Ci
Tr
WUE
Gs DAF4
0.81**
DAF15
0.52*
DAF40
0.66*
Ci DAF4
0.22
0.20
DAF15
0.08
0.70**
DAF40
0.29
0.30
Tr DAF4
0.73**
0.98**
0.28
DAF15
0.48*
0.82**
0.74**
DAF40
0.62**
0.96**
0.26
WUE DAF4
0.41
0.10
0.48*
0.04
DAF15
0.40
0.34
0.81**
0.51
DAF40
0.44*
0.24
0.49*
0.30
Fv/Fm DAF4
0.22
0.04
0.39
0.03
DAF15
0.19
0.12
0.31
0.16
0.30 0.20
DAF40
0.29
0.38
0.13
0.37
0.04
Pn: Photosynthesis rate; Gs: Stomatal conductance; Ci: Intercellular CO2 concentration; Tr: Transpiration rate; WUE: Water use efficiency; Fv/Fm: Efficiency of primary conversion of light energy. DAF4, DAF15, and DAF40 denote 4, 15, and 40 d after flowering. *P < 0.05; **P < 0.01.
Table 4 Yield-related trait
Partial correlation coefficients between heterosis in yield and photosynthetic carbon assimilation Pn
Gs
Ci
DAF4
DAF15
DAF40
DAF4
DAF15
DAF40
DAF4
DAF15
DAF40
Spike length
0.57
0.52
0.09
0.72
0.53
0.84
0.73
—
0.56
Spike number per plant
0.64
0.84
0.73
0.69
0.88
0.86
0.27
0.85
0.12
Fertile spikelets per plant
0.28
0.54
—
0.40
0.80
0.97**
—
0.21
0.93*
Grain number per spike
0.86
0.99*
Thousand-grain weight
0.98*
0.90
0.99* 0.96
1.00**
0.99*
1.00**
0.99*
0.99*
0.19
0.99*
0.17
0.97
0.95
0.58
1.00**
Yield of main stem
1.00**
1.00**
0.98*
1.00**
0.99*
1.00**
1.00**
1.00**
1.00**
Yield per plant
0.98*
0.99*
0.93
0.99*
0.99*
0.99*
0.99*
0.99*
0.97
Yield-related trait
Tr
WUE
Fv/Fm
DAF4
DAF15
DAF40
DAF4
DAF15
DAF40
DAF4
DAF15
DAF40
Spike length
0.38
0.56
0.85
0.70
0.79
0.59
0.75
0.83
0.77
Spike number per plant
0.76
0.69
0.72
0.89
0.37
0.62
0.86
0.15
0.63
0.76
0.97**
0.88*
0.96**
0.83
0.91*
0.97**
Fertile spikelets per plant
0.91 0.41
Grain number per spike
0.99*
0.99*
1.00**
1.00**
0.88
0.95
1.00**
0.99*
0.96
Thousand-grain weight
0.89
0.82
0.98*
0.93
0.98*
0.99*
0.98*
0.99*
0.95
Yield of main stem
1.00**
1.00**
1.00**
1.00**
0.99*
1.00**
1.00**
1.00**
0.93
Yield per plant
0.99*
0.99*
0.99*
1.00**
0.78
0.99*
1.00**
0.98*
0.98*
Pn: Photosynthesis rate; Gs: Stomatal conductance; Ci: Intercellular CO2 concentration; Tr: Transpiration rate; WUE: Water use efficiency; Fv/Fm: Efficiency of primary conversion of light energy. DAF4, DAF15, and DAF40 denote 4, 15, and 40 d after flowering. *P < 0.05; **P < 0.01.
yield of main stem, among which 6 were significant (P < 0.05), but the opposite trend was observed at 40 DAF. In addition, heterosis of Tr at 4 and 40 DAF were also positively
correlated with the above 4 yield-related traits, among which 7 were significant (P < 0.05), but the opposite trend was observed at 15 DAF. Finally, a total of 8 partial correlation
WANG Xiu-LI et al. / Acta Agronomica Sinica, 2010, 36(6): 1003–1010
coefficients at 4 DAF between the heterosis of WUE and Fv/Fm and 5 yield-related traits (fertile spikelets per plant, grain number per spike, thousand-grain weight, yield per plant, and yield of main stem) were negative, among which 7 were significant (P < 0.05), but the opposite trend was observed at 15 and 40 DAF.
3
Discussion
As a key metabolic process for matter production in plants, photosynthesis is the physiological basis of crop biomass yield. Plant hybrids exhibited higher rates of photosynthesis compared to their parental inbred lines [24–27]. In this study, the magnitudes of heterosis of Pn at the 3 grain-filling stages tested were variable in different cross combinations, but 11 out of 12 partial correlation coefficients between heterosis of Pn and 4 yield-related traits (grain number per spike, thousand-grain weight, yield per plant, and yield of main stem) were positive, among which 8 were significant. Therefore, it can be concluded that this advantage of photosynthesis rate in wheat hybrid may contribute to the observed yield heterosis. Among all the yield components tested, spike length and spike number per plant were developed before flowering, whereas photosynthetic carbon assimilation related traits were recorded at the stages of grain filling. Theoretically, there was no relationship of photosynthetic carbon assimilation related traits with the heterosis of spike length and spike number per plant, which is consistent with the results of our partial correlation analysis. Importantly, the heterosis of most partial correlation Pn, Ci, WUE, and Fv/Fm were positively correlated with the heterosis of grain number per spike, thousand-grain weight, yield per plant, and yield of main stem, and most of which were significant. In rice, Wang et al. [22] reported that super hybrid exhibited better photosynthetic functions, higher WUE and stronger photochemical efficiency of photosystem II than their parents. Taken together, we propose that both Pn and WUE may be the physiological basis for the super high-yield of crop hybrids. Up to date, there are many reports about the relationship of yield heterosis with photosynthetic carbon assimilation related traits in wheat, but the results are still controversial. Lupton [31] reported that hybrid wheat exhibited the heterosis of Pn before flowering, whereas Borghiet et al. [32] found that this advantage was mainly in the reproductive stage. Xiao et al. [27] proposed that the Pn heterosis was obvious during the process of flag leaf senescence, but Zhang et al. [28] reported that it depended on maternal effect. Taken our present results together, we speculate that this may be related to complexity of heterosis of yield and photosynthetic carbon assimilation related traits. Firstly, the magnitude of heterosis of yield and its components varied among cross combinations. For instance, higher heterosis of spike number per plant were detected in hybrids
3235/Jing 411 and 3338/8790 (23.93% and 25.98%) and higher heterosis of thousand-grain weight were observed in hybrids 227/8790 and 3235/F390 (43.39% and 35.50%) compared to other yield components. The development of spike number per plant has been completed before ear emergence. Although no significant heterosis was detected for photosynthesis rate, yield heterosis was still relative high in hybrids 3235/Jing 411 and 3338/8790 (123.08% and 70.40%, respectively). Secondly, variations in the magnitudes of heterosis of photosynthetic carbon assimilation related traits were observed among cross combinations and developmental stages. For instance, high heterosis of Pn was observed in hybrid 101/F390 at 4, 15, and 40 DAF (12.88%, 11.54%, and 5.74%), followed by hybrid 227/Jing 411 at 4 and 15 DAF (5.93% and 14.06%) and hybrid 3235/8790 at 4 DAF (12.20%). It must be noted, however, that the data presented here is mainly derived from statistical analysis, and further experiment in molecular biology should be undertaken to investigate the relationship between gibberellins and heterosis in wheat plant height. In order to further elucidate the relationship of yield heterosis with photosynthetic carbon assimilation related traits, the priorities are to select the cross combination and trait for investigation and to determine its key developmental stage.
4
Conclusions
There was true correlation between heterosis of yield and photosynthetic carbon assimilation related traits, and high photosynthetic capacity and water use efficiency could be one of the important physiological bases of wheat hybrid vigor. Moreover, mid-grain-filling stage may be the key developmental stage for wheat yield heterosis.
Acknowledgments This study was funded by the National Basic Research Program of China (2007CB109000), the National Foundation for Outstanding Young Scientists of China (30925023), and the National Natural Science Foundation of China (30671297 and 30771342).
References [1] [2]
[3]
Hochholdinger F, Hoeckera N. Towards the molecular basis of heterosis. Trend Plant Sci, 2007, 12: 427–432 Ni Z F, Sun Q X Wu L M. Differential gene expression between wheat hybrids and their parental inbreds in seedling leaves of early and vigorous tillering stages. J China Agric Univ, 2000, 5: 1–8 (in Chinese with English abstract) Bao J, Lee S, Chen C, Zhang X, Zhang Y, Liu S, Clark T, Wang J, Cao M, Yang H, Wang S, Yu J. Serial analysis of gene expression study of a hybrid rice strain (LYP9) and its parental cultivars. Plant Physiol, 2005, 138: 1216–1231
WANG Xiu-LI et al. / Acta Agronomica Sinica, 2010, 36(6): 1003–1010
[4]
[5]
[6]
[7]
[8]
[9]
[10]
[11]
[12]
[13]
[14]
[15]
[16]
[17]
Hoecker N, Keller B, Muthreich N, Chollet D, Descombes P, Piepho H P, Hochholdinger F. Comparison of maize (Zea mays L.) F1-hybrid and parental inbred line primary root transcriptomes suggests organ-specific patterns of nonadditive gene expression and conserved expression trends. Genetics, 2008, 179: 1275–1283 Ge X, Chen W, Song S, Wang W, Hu S, Yu J. Transcriptomic profiling of mature embryo from an elite super-hybrid rice LYP9 and its parental lines. BMC Plant Biol, 2008, 8: 114 Ni Z, Sun Q, Wu L, Xie C. Differential gene expression between wheat hybrids and their parental inbreds in primary roots. Acta Bot Sin, 2002, 44: 457–462 Song S, Qu H, Chen C, Hu S, Yu J. Differential gene expression in an elite hybrid rice cultivar (Oryza sativa L.) and its parental lines based on SAGE data. BMC Plant Biol, 2007, 7: 49 Huang Y, Zhang L D, Zhang J W, Yuan D, Xu C, Li X, Zhou D, Wang S, Zhang Q. Heterosis and polymorphisms of gene expression in an elite rice hybrid as revealed by a microarray analysis of 9198 unique ESTs. Plant Mol Biol, 2006, 62: 579–591 Wu H L, Ni Z F, Yao Y Y, Guo G G, Sun Q X. Cloning and expression profiles of 15 genes encoding WRKY transcription factor in wheat (Triticum aestivum L.). Prog Nat Sci, 2008, 18: 697–706 Zhang Y H, Ni Z F, Yao Y Y, Zhao J, Sun Q X. Analysis of genome-wide gene expression in root of wheat hybrid and its parents using Barley1 GeneChip. Prog Nat Sci, 2006, 16: 712–720 Romagnoli S, Maddaloni M, Livini C, Motto M. Relationship between gene expression and hybrid vigor in primary root tips of young maize (Zea mays L.) plantlets. Theor Appl Genet, 1990, 80: 769–775 Hoecker N, Lamkemeyer T, Sarholz B, Paschold A, Fladerer C, Madlung J, Wurster K, Stahl M, Piepho H P, Nordheim A, Hochholdinger F. Analysis of nonadditive protein accumulation in young primary roots of a maize (Zea mays L.) F1-hybrid compared to its parental inbred lines. Proteomics, 2008, 8: 3882–3894 Wang W, Meng B, Ge X, Song S, Yang Y, Wang L, Hu S, Liu S, Yu J. Proteomic profiling of rice embryos from a hybrid rice cultivar and its parental lines. Proteomics, 2008, 8: 4808–4821 Song X, Ni Z F, Yao Y Y, Xie C J, Li Z X, Wu H Y, Zhang Y H, Sun Q X. Wheat (Triticum aestivum L.) root proteome and differentially expressed root proteins between hybrid and parents. Proteomics, 2007, 7: 3538–3557 Song X, Ni Z F,Yao Y Y, Zhang Y H, Sun Q X. Identification of differentially expressed proteins between hybrid and parents in wheat (Triticum aestivum L.) seedling leaves. Theor Appl Genet, 2009, 118: 213–225 Yang T X, Zeng M Q, Li J G. Corn heterosis and isozyme studies: IV. Analysis of the hybrid enzyme on the peroxidase isoenzyme. Hereditas (Beijing), 1981, 3(6): 31–33 (in Chinese with English abstract) Dai J R, Luo M Z, Han Y S. Relationship of maize peroxidase, esterase isozyme and hybrid production. Acta Agron Sin, 1989, 15: 193–201 (in Chinese with English abstract)
[18] Li Z Q, Wang Z R. Relationship between heterosis and endogenous plant hormones in liriodendron. Acta Bot Sin, 2002, 44: 698–701 [19] Zhao Q Z, Lü D B, Cheng X Y, Chen J Y, Liang J J. The heterosis of canopy photosynthetic rate and bleeding intensity of hybrid wheat. Sci Agric Sin, 2002, 35: 925–928 (in Chinese with English abstract) [20] Mohammad A, Sarker Z, Murayama S, Ishimine Y, Tsuzuki E. Physio-Morphological characters of F1 hybrid of rice (Oryza sativa L.) in japanica-india crosses. Plant Proc Sci, 2001, 4: 196–201 [21] You M A, Gai J Y, Ma Y H. Relationship of leaf photosynthetic rate with stomatal and mesophyll conductance in soybeans. Acta Agron Sin, 1995, 21: 145–149 (in Chinese with English abstract) [22] Wang Q, Zhang Q D, Jiang G M, Lu C M, Kuang T Y, Wu S, Li C Q, Jiao D M. Photosynthetic characteristics of two super high-yield hybrid rice. Acta Bot Sin, 2000, 42: 1285–1288 (in Chinese with English abstract) [23] Dong D K, Shi K, Cao J S. The photosynthetic heterosis and its mechanisms of an inter-subspecific hybrid between Brassica campestris ssp. chinensis and B. campestris ssp. rapifera. Sci Agric Sin, 2007, 40: 2804–2810 (in Chinese with English abstract) [24] Tollenaar M, Ahmadzadeh A, Lee E A. Physiological basis of heterosis for grain yield in maize. Crop Sci, 2004, 44: 2086–2094 [25] Wei G, Tao Y, Liu G Liu G, Chen C, Luo R, Xia H, Gan Q, Zeng H, Lu Z, Han Y, Li X, Song G, Zhai H, Peng Y, Li D, Xu H, Wei X, Cao M, Deng H, Xin Y, Fu X, Yuan L, Yu J, Zhu Z, Zhu L. A transcriptomic analysis of super hybrid rice LYP9 and its parents. Proc Natl Acad Sci USA, 2009, 106: 7695–7701 [26] Ni Z, Kim E, Ha M, Lackey E, Liu J, Zhang Y, Sun Q, Chen Z. Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids. Nature, 2009, 457: 327–331 [27] Xiao K, Gu J T, Zou D H, Zhang R X. Studies on CO2 conductance during flag leaf aging of hybrid wheats and their parents. Acta Agron Sin, 1998, 24: 503–508 (in Chinese with English abstract) [28] Zhang Q D, Zhu X G, Wang Q, Lu C M, Kuang T Y, Zhang W X, Zhang J H. Photosynthetic characters of F1 hybrids in winter wheat and their parents. Acta Agron Sin, 2001, 27: 653–657 (in Chinese with English abstract) [29] Tang W, Li W J, Zhang D M, Dong H Z. Drought effects on POD, MDA and photosynthetic rate in seedling leaves of transgenic cotton. China Cotton, 2002, 29(2): 23–24 (in Chinese) [30] Zhang Y P, Wang Z M, Wang P, Zhao M. Canopy photosynthetic characteristics of population of winter wheat in water-saving and high-yielding cultivation. Sci Agric Sin, 2003, 36: 1143–1149 (in Chinese with English abstract) [31] Lupton F G H. Physiological bases of heterosis in wheat. In: Janossy A, Lupton F G H, eds. Heterosis in Plant Breeding. New York: Academic Press, 1974. pp 71–80 [32] Borghi B M, Perenzin, Nash R J. Agronomic and qualitative characteristics of ten bread wheat hybrids produced using a chemical hybridizing agent. Euphytica, 1988, 39: 185–194