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Mapping of QTLs for Leaf Malondialdehyde Content Associated with Stress Tolerance in Rice
Rice Science, 2009, 16(1): 72–74 Copyright © 2009, China National Rice Research Institute. Published by Elsevier BV. All rights reserved DOI: 10.1016/S1672-6308(08)60059-1
Mapping of QTLs for Leaf Malondialdehyde Content Associated with Stress Tolerance in Rice JIANG Jing1, ZHUANG Jie-yun2, FAN Ye-yang2, SHEN Bo1 (1College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou 310012, China; 2Chinese National Center for Rice Improvement/State Key Laboratory of Rice Biology, China National Rice Research Institute, Hangzhou 310006, China)
Abstract: Malondialdehyde (MDA) is the final product of lipid peroxidation, and MDA content can reflect the stress tolerance of plants. To map QTLs conditioning the MDA content in rice leaves, a recombinant inbred line (RIL) population with 247 lines derived from an indica-indica cross Zhenshan 97BuMilyang 46, and a linkage map consisting of 207 DNA markers were used. The RIL population showed a transgressive segregation in the MDA content of rice leaves. Two QTLs for the MDA content in rice leaves were detected in the intervals RG532–RG811 and RG381–RG236 on chromosome 1, with the additive effects from maternal and paternal parents, accounting for 4.33% and 4.62% of phenotype variations, respectively. Key words: rice; malondialdehyde content; quantitative trait locus; leaf; stress tolerance
Free radical reaction and subsequent lipid peroxidation in plants have important influences on normal metabolic processes [1]. To minimize oxidative damage, plants have evolved multiple detoxification mechanisms, including the synthesis of antioxidants (e.g. ascorbic acid) and various enzymes (e.g. superoxide dismutase). Thus, the production and destruction of free radicals are well in balance under normal conditions, and plants show tolerance to oxidative stress [2]. When rice plants are subjected to environmental stresses or during leaf senescence, the activities of intracellular enzymes against oxidative damage are declined, and subsequent accumulation of free radicals and buildup of lipid peroxides, such as malondialdehyde (MDA), are performed [3-6]. MDA is a naturally occurring product of lipid peroxidation, which reacts with lipid, nucleic acid, glucose and protein. As a result, there are downstream decreases in the content of unsaturated fatty acid and the membrane resistance and fluidity, along with an increase in the quantity of electrolyte leakage. Therefore, the function and structure of cytoplasmic membrane are damaged and a series of physiological metabolisms are changed [7-8]. With the advances in molecular marker technique in recent decade, the genetic analyses of complex quantitative traits have been available [9]. DNA markers and genetic linkage maps become an effective way to detect QTLs. Nowadays, many studies have been undertaken to decipher the genetic basis of physiological traits in different crops by QTL mapping [10]. However, QTL analyses combining with biochemical traits are seldom reported in rice [11]. In this study, we analyzed QTLs Received: 4 September 2008; Accepted: 1 December 2008 Corresponding author: SHEN Bo ([email protected]) This is an English version of the paper published in Chinese in Chinese Journal of Rice Science, Vol. 21, No. 4, 2007, Pages 436–438.
conditioning the MDA content in rice leaves using a recombinant inbred line (RIL) population derived from an indica-indica rice cross of Zhenshan 97BuMilyang 46.
MATERIALS AND METHODS Rice materials The RIL population derived from Zhenshan 97BuMilyang 46 consisted of 247 lines. In the spring of 2004, 247 lines along with the parents were transplanted in paddy fields at the China National Rice Research Institute, Hangzhou, China, in randomized complete block design with two replications. Twelve plants per replication were planted with a spacing of 17 cm u 20 cm. Field management essentially followed the normal agronomic procedures. At the 6-leaf stage, rice leaves were sampled and kept frozen before measurement. Measurement of malondialdehyde content MDA content was measured according to Li et al [12]. One gram of frozen leaf for each sample was ground in 8 mL ice-cold phosphate buffer (0.05 mol/L, pH 7.8). The homogenate was centrifuged at 15 000 r/min for 30 min at 4°C. Then, the filtrate was diluted 5 times for the measurement of MDA content. The 1.5 mL dilution was added into 2.5 mL 0.5% thiobarbituric acid solution (dissolved in 20% trichloroacetic acid) and then boiled for 15 min. After quick cooling and filtration, MDA content (mmol/g) of filtrate was monitored with a spectrophotometer at 532 and 600 nm, respectively, and calculated by the extinction coefficient of 155 mmol-1cm-1. QTL analysis A linkage map consisting of 207 DNA markers had been
JIANG Jing, et al. Mapping of QTLs for Leaf Malondialdehyde Content Associated with Stress Tolerance in Rice
73
Table 1. Main effect QTLs conditioning the MDA content in the RIL population.
a
Aa
QTL
Chromosome
Interval
LOD value
qMDA-1a
1
RG532–RG811
7.14
-0.0061
4.33
qMDA-1b
1
RG381–RG236
5.42
0.0063
4.62
Variance explained (%)
Additive effect, the genetic effect when a maternal allele is replaced by a paternal one.
constructed in the RIL population of Zhenshan 97BuMilyang 46 [13]. QTL Mapper 1.60 of mixed linear model [14] was used to determine the main effect QTLs conditioning MDA content. The thresholds of LOD!3.0 and P<0.005 were chosen for claiming a putative QTL, and calculating the contribution and additive effect. Nomenclature for QTL followed the description of McCouch et al [15].
RESULTS Trait performance The distribution of the MDA contents in rice leaves in the RIL population of Zhenshan 97BuMilyang 46 is shown in Fig. 1. A significantly transgressive segregation for the traits was found in the population and the frequency was approximately normally distributed, indicating that the trait of the MDA content was quantitatively inherited and suitable for QTL analysis. Detection of main effect QTLs
DISCUSSION MDA is formed as an end product of lipid peroxidation, and MDA content is often adopted as a suitable physiological index to reflect the degree of lipid peroxidation and stress tolerance in plants [16-17]. At present, most domestic studies of MDA focus on physiological and biochemical aspects. Hua et al [18] reported that a marked increase of MDA content was observed during leaf senescence in hybrid rice. Under salt stress, MDA content would be elevated with the increase of salinity concentration [19]. Liang et al [20] found that the change of antioxidant enzyme activity and MDA level in growing seasons was in line with both soil and leaf moisture status, suggesting that the antioxidative defense and lipid peroxidation could be used to reflect water deficit status in both soil and rice. Jiao et al [21] investigated a transgenic rice line over-expressing maize phosphoenolpyruvate carboxylase gene (PEPC) and found that the photosynthetic capacity was improved greatly and C4 cycle was promoted under photoinhibition, resulting in a
Two putative QTLs conditioning the MDA content in rice leaves (Table 1 and Fig. 2), designated as qMDA-1a and qMDA-1b, were detected in the intervals RG532–RG811 and RG381–RG236 on chromosome 1, with 4.33% and 4.62% of phenotypic variations explained by a single QTL, respectively. The total phenotypic variations reached 8.95%. The two QTLs, qMDA-1a and qMDA-1b, had the respective additive effects of -0.0061 and 0.0063, indicating that the alleles responsible for increasing the MDA content were from maternal parent Zhenshan 97B and paternal parent Milyang 46, respectively.
Fig. 1. MDA contents in rice leaves in the RIL population of Zhenshan 97BuMilyang 46.
Fig. 2. Mapping of QTLs conditioning the MDA content.
74
Rice Science, Vol. 16, No. 1, 2009
decrease for the content of MDA that generated by lipid peroxidation. In addition, lower MDA content under photoinhibition could improve protection from photo-oxidation. In the present study, two QTLs for the MDA content in rice leaves, qMDA-1a and qMDA-1b, were respectively detected in the intervals RG532–RG811 and RG381–RG236 on chromosome 1 with the employment of the RIL population derived from the cross Zhenshan 97BuMilyang 46. qMDA-1a and qMDA-1b had similar additive effect and the alleles responsible for increasing the MDA content were from maternal and paternal parents, respectively, indicating that the two parents had genes controlling lipid peroxidation. However, the total phenotypic contribution was only 8.95%, suggesting that the MDA content in rice leaves were controlled by minor QTLs. These results, combined with QTL mapping of antioxidant enzymatic system, would be helpful for further understanding the genetic mechanisms of antioxidant stress. With the development of QTL mapping in recent years, various traits including agronomic, morphological and physiological traits, are studied using molecular and quantitative-genetic methods. Presently, if QTL analysis of biochemical phenotype were combined with related morphology, yield, physiological traits and gene expression, we could obtain insight into the genetic mechanisms of rice metabolic pathways, which could be thereby applied in marker-assisted selection.
indica-japonica hybrid rice during grain filling. Acta Agric Shanghai, 2003, 19(4): 21–24. (in Chinese with English abstract) 7
Plant Physiol, 1993, 101: 7–12. 8
in winter wheat. Acta Agron Sin, 1997, 23(3): 370–375. (in Chinese with English abstract) 9
Xu Y B. Global view of QTL: Rice as a model. In: Kang M S. Quantitative Genetics, Genomics and Plant Breeding. Oxford Shire: CAB International, 2002: 109–134.
10
Yano M, Sasaki T. Genetic and molecular dissection of quantitative traits in rice. Plant Mol Biol, 1997, 35: 145–153.
11
Obara M, Kajiura M, Fukuta Y, Yano M, Hayashi M, Yamaya T, Sato T. Mapping of QTLs associated with cytosolic
glutamine
synthetase
and
NADH-glutamate
synthase in rice. J Exp Bot, 2001, 52(359): 1209–1217. 12
Li B L, Mei H S. Relationship between oat leaf senescence and activated oxygen metabolism. Acta Phytophysiol Sin, 1989, 15(1): 6–12. (in Chinese with English abstract)
13
Shen B, Zhuang J Y, Zhang K Q, Dai W M, Lu Y, Fu L Q, Ding J M, Zheng K L. Analysis of interaction between QTL and environment on chlorophyll contents in rice. Sci Agric Sin, 2005, 38(10): 1937–1943. (in Chinese with English abstract) Wang D L, Zhu J, Li Z K, Paterson A H. QTL Mapper Version 1.6. Hangzhou: Zhejiang University, Texas A&M
ACKNOWLEDGEMENTS
REFERENCES
Xu Z Z, Yu Z W, Dong Q Y, Qi X H, Yu S L. Effects of water on cell membrane and the ultrastructure of flag leaf cell
14
This work was supported by the Super Rice Program of Ministry of Agriculture of China (Grant No. 200606), the Key Program of Zhejiang Province, China (Grant No. 2003G10028) and the China Postdoctoral Science Foundation (Grant No. 2003034232).
Scandalios J G. Oxygen stress and superoxide dismutase.
University, 2003 15
McCouch S R, Cho Y G, Yano M, Paul E, Blinstrub M. Report on QTL nomenclature. Rice Genet Newsl, 1997, 14: 11–13.
16
Shi Y L, Luo Q X, Liu P Y. Effects of CaCl2 on contents of CAM and MDA and permeability of plasma membrane of cucumber seedling under NaCl stress. Plant Physiol Comm, 1995, 31(5): 347–349. (in Chinese)
17
Cheng F Y, Shi H Y, Kao C H. Nitric oxide counteracts the senescence of detached rice leaves induced by dehydration
1
Shen C G. Plant Senescence Physiology and Molecular
and polyethylene glycol but not by sorbitol. Plant Growth
Biology. Beijing: China Agricultural Press, 2001: 30–41. (in Chinese) 2 3
Reg, 2002, 38: 265–272. 18
Cadenas E. Biochemistry of oxygen toxicity. Annu Rev
MDA content during senescence of hybrid rice and three lines
Biochem, 1989, 58: 79–110.
leaves. Acta Bot Bor-Occident Sin, 2003, 23(3): 406–409. (in
Lin Z F, Li S S, Lin G Z, Sun G S, Guo J Y. The relation among leaf senescence, activity of superoxide dismutase and
Chinese with English abstract) 19
Wang H C. Plant hardiness physiology. Plant Physiol Comm,
20
Liang Y C, Hu F, Yang M C, Yu J H. Antioxidative defenses
lipid peroxidation. Acta Bot Sin, 1984, 26(6): 605–615. (in Chinese with English abstract) 4 5
1981, 6: 72–81. (in Chinese )
Bowler C, van Camp W, van Montagu M, Inzé D. Superoxide
and water deficit-induced oxidative damage in rice (Oryza
dismutase in plants. Crit Rev Plant Sci, 1994, 13: 199–218.
sativa L.) growing on non-flooded paddy soils with ground
Duan J, Liang C Y, Huang Y W. Studies of leaf senescence of hybrid rice at flowering and grain formation stages. Acta
6
Hua C, Wang R L. Changes of SOD and CAT activities and
mulching. Plant & Soil, 2003, 257: 407–416. 21
Jiao D M, Li X, Ji B H. Photoprotective effects of high level
Phytophysiol Sin, 1997, 23(2): 139–144. (in Chinese with
expression of C4 phosphoenolpyruvate carboxylase in transgenic
English abstract)
rice during photoinhibition. Photosythetica, 2005, 43(4): 501–
Shen B. Studies on physiology of leaf senescence of
508.
Mapping of QTLs for Leaf Malondialdehyde Content Associated with Stress Tolerance in Rice JIANG Jing1, ZHUANG Jie-yun2, FAN Ye-yang2, SHEN Bo1 (1College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou 310012, China; 2Chinese National Center for Rice Improvement/State Key Laboratory of Rice Biology, China National Rice Research Institute, Hangzhou 310006, China)
Abstract: Malondialdehyde (MDA) is the final product of lipid peroxidation, and MDA content can reflect the stress tolerance of plants. To map QTLs conditioning the MDA content in rice leaves, a recombinant inbred line (RIL) population with 247 lines derived from an indica-indica cross Zhenshan 97BuMilyang 46, and a linkage map consisting of 207 DNA markers were used. The RIL population showed a transgressive segregation in the MDA content of rice leaves. Two QTLs for the MDA content in rice leaves were detected in the intervals RG532–RG811 and RG381–RG236 on chromosome 1, with the additive effects from maternal and paternal parents, accounting for 4.33% and 4.62% of phenotype variations, respectively. Key words: rice; malondialdehyde content; quantitative trait locus; leaf; stress tolerance
Free radical reaction and subsequent lipid peroxidation in plants have important influences on normal metabolic processes [1]. To minimize oxidative damage, plants have evolved multiple detoxification mechanisms, including the synthesis of antioxidants (e.g. ascorbic acid) and various enzymes (e.g. superoxide dismutase). Thus, the production and destruction of free radicals are well in balance under normal conditions, and plants show tolerance to oxidative stress [2]. When rice plants are subjected to environmental stresses or during leaf senescence, the activities of intracellular enzymes against oxidative damage are declined, and subsequent accumulation of free radicals and buildup of lipid peroxides, such as malondialdehyde (MDA), are performed [3-6]. MDA is a naturally occurring product of lipid peroxidation, which reacts with lipid, nucleic acid, glucose and protein. As a result, there are downstream decreases in the content of unsaturated fatty acid and the membrane resistance and fluidity, along with an increase in the quantity of electrolyte leakage. Therefore, the function and structure of cytoplasmic membrane are damaged and a series of physiological metabolisms are changed [7-8]. With the advances in molecular marker technique in recent decade, the genetic analyses of complex quantitative traits have been available [9]. DNA markers and genetic linkage maps become an effective way to detect QTLs. Nowadays, many studies have been undertaken to decipher the genetic basis of physiological traits in different crops by QTL mapping [10]. However, QTL analyses combining with biochemical traits are seldom reported in rice [11]. In this study, we analyzed QTLs Received: 4 September 2008; Accepted: 1 December 2008 Corresponding author: SHEN Bo ([email protected]) This is an English version of the paper published in Chinese in Chinese Journal of Rice Science, Vol. 21, No. 4, 2007, Pages 436–438.
conditioning the MDA content in rice leaves using a recombinant inbred line (RIL) population derived from an indica-indica rice cross of Zhenshan 97BuMilyang 46.
MATERIALS AND METHODS Rice materials The RIL population derived from Zhenshan 97BuMilyang 46 consisted of 247 lines. In the spring of 2004, 247 lines along with the parents were transplanted in paddy fields at the China National Rice Research Institute, Hangzhou, China, in randomized complete block design with two replications. Twelve plants per replication were planted with a spacing of 17 cm u 20 cm. Field management essentially followed the normal agronomic procedures. At the 6-leaf stage, rice leaves were sampled and kept frozen before measurement. Measurement of malondialdehyde content MDA content was measured according to Li et al [12]. One gram of frozen leaf for each sample was ground in 8 mL ice-cold phosphate buffer (0.05 mol/L, pH 7.8). The homogenate was centrifuged at 15 000 r/min for 30 min at 4°C. Then, the filtrate was diluted 5 times for the measurement of MDA content. The 1.5 mL dilution was added into 2.5 mL 0.5% thiobarbituric acid solution (dissolved in 20% trichloroacetic acid) and then boiled for 15 min. After quick cooling and filtration, MDA content (mmol/g) of filtrate was monitored with a spectrophotometer at 532 and 600 nm, respectively, and calculated by the extinction coefficient of 155 mmol-1cm-1. QTL analysis A linkage map consisting of 207 DNA markers had been
JIANG Jing, et al. Mapping of QTLs for Leaf Malondialdehyde Content Associated with Stress Tolerance in Rice
73
Table 1. Main effect QTLs conditioning the MDA content in the RIL population.
a
Aa
QTL
Chromosome
Interval
LOD value
qMDA-1a
1
RG532–RG811
7.14
-0.0061
4.33
qMDA-1b
1
RG381–RG236
5.42
0.0063
4.62
Variance explained (%)
Additive effect, the genetic effect when a maternal allele is replaced by a paternal one.
constructed in the RIL population of Zhenshan 97BuMilyang 46 [13]. QTL Mapper 1.60 of mixed linear model [14] was used to determine the main effect QTLs conditioning MDA content. The thresholds of LOD!3.0 and P<0.005 were chosen for claiming a putative QTL, and calculating the contribution and additive effect. Nomenclature for QTL followed the description of McCouch et al [15].
RESULTS Trait performance The distribution of the MDA contents in rice leaves in the RIL population of Zhenshan 97BuMilyang 46 is shown in Fig. 1. A significantly transgressive segregation for the traits was found in the population and the frequency was approximately normally distributed, indicating that the trait of the MDA content was quantitatively inherited and suitable for QTL analysis. Detection of main effect QTLs
DISCUSSION MDA is formed as an end product of lipid peroxidation, and MDA content is often adopted as a suitable physiological index to reflect the degree of lipid peroxidation and stress tolerance in plants [16-17]. At present, most domestic studies of MDA focus on physiological and biochemical aspects. Hua et al [18] reported that a marked increase of MDA content was observed during leaf senescence in hybrid rice. Under salt stress, MDA content would be elevated with the increase of salinity concentration [19]. Liang et al [20] found that the change of antioxidant enzyme activity and MDA level in growing seasons was in line with both soil and leaf moisture status, suggesting that the antioxidative defense and lipid peroxidation could be used to reflect water deficit status in both soil and rice. Jiao et al [21] investigated a transgenic rice line over-expressing maize phosphoenolpyruvate carboxylase gene (PEPC) and found that the photosynthetic capacity was improved greatly and C4 cycle was promoted under photoinhibition, resulting in a
Two putative QTLs conditioning the MDA content in rice leaves (Table 1 and Fig. 2), designated as qMDA-1a and qMDA-1b, were detected in the intervals RG532–RG811 and RG381–RG236 on chromosome 1, with 4.33% and 4.62% of phenotypic variations explained by a single QTL, respectively. The total phenotypic variations reached 8.95%. The two QTLs, qMDA-1a and qMDA-1b, had the respective additive effects of -0.0061 and 0.0063, indicating that the alleles responsible for increasing the MDA content were from maternal parent Zhenshan 97B and paternal parent Milyang 46, respectively.
Fig. 1. MDA contents in rice leaves in the RIL population of Zhenshan 97BuMilyang 46.
Fig. 2. Mapping of QTLs conditioning the MDA content.
74
Rice Science, Vol. 16, No. 1, 2009
decrease for the content of MDA that generated by lipid peroxidation. In addition, lower MDA content under photoinhibition could improve protection from photo-oxidation. In the present study, two QTLs for the MDA content in rice leaves, qMDA-1a and qMDA-1b, were respectively detected in the intervals RG532–RG811 and RG381–RG236 on chromosome 1 with the employment of the RIL population derived from the cross Zhenshan 97BuMilyang 46. qMDA-1a and qMDA-1b had similar additive effect and the alleles responsible for increasing the MDA content were from maternal and paternal parents, respectively, indicating that the two parents had genes controlling lipid peroxidation. However, the total phenotypic contribution was only 8.95%, suggesting that the MDA content in rice leaves were controlled by minor QTLs. These results, combined with QTL mapping of antioxidant enzymatic system, would be helpful for further understanding the genetic mechanisms of antioxidant stress. With the development of QTL mapping in recent years, various traits including agronomic, morphological and physiological traits, are studied using molecular and quantitative-genetic methods. Presently, if QTL analysis of biochemical phenotype were combined with related morphology, yield, physiological traits and gene expression, we could obtain insight into the genetic mechanisms of rice metabolic pathways, which could be thereby applied in marker-assisted selection.
indica-japonica hybrid rice during grain filling. Acta Agric Shanghai, 2003, 19(4): 21–24. (in Chinese with English abstract) 7
Plant Physiol, 1993, 101: 7–12. 8
in winter wheat. Acta Agron Sin, 1997, 23(3): 370–375. (in Chinese with English abstract) 9
Xu Y B. Global view of QTL: Rice as a model. In: Kang M S. Quantitative Genetics, Genomics and Plant Breeding. Oxford Shire: CAB International, 2002: 109–134.
10
Yano M, Sasaki T. Genetic and molecular dissection of quantitative traits in rice. Plant Mol Biol, 1997, 35: 145–153.
11
Obara M, Kajiura M, Fukuta Y, Yano M, Hayashi M, Yamaya T, Sato T. Mapping of QTLs associated with cytosolic
glutamine
synthetase
and
NADH-glutamate
synthase in rice. J Exp Bot, 2001, 52(359): 1209–1217. 12
Li B L, Mei H S. Relationship between oat leaf senescence and activated oxygen metabolism. Acta Phytophysiol Sin, 1989, 15(1): 6–12. (in Chinese with English abstract)
13
Shen B, Zhuang J Y, Zhang K Q, Dai W M, Lu Y, Fu L Q, Ding J M, Zheng K L. Analysis of interaction between QTL and environment on chlorophyll contents in rice. Sci Agric Sin, 2005, 38(10): 1937–1943. (in Chinese with English abstract) Wang D L, Zhu J, Li Z K, Paterson A H. QTL Mapper Version 1.6. Hangzhou: Zhejiang University, Texas A&M
ACKNOWLEDGEMENTS
REFERENCES
Xu Z Z, Yu Z W, Dong Q Y, Qi X H, Yu S L. Effects of water on cell membrane and the ultrastructure of flag leaf cell
14
This work was supported by the Super Rice Program of Ministry of Agriculture of China (Grant No. 200606), the Key Program of Zhejiang Province, China (Grant No. 2003G10028) and the China Postdoctoral Science Foundation (Grant No. 2003034232).
Scandalios J G. Oxygen stress and superoxide dismutase.
University, 2003 15
McCouch S R, Cho Y G, Yano M, Paul E, Blinstrub M. Report on QTL nomenclature. Rice Genet Newsl, 1997, 14: 11–13.
16
Shi Y L, Luo Q X, Liu P Y. Effects of CaCl2 on contents of CAM and MDA and permeability of plasma membrane of cucumber seedling under NaCl stress. Plant Physiol Comm, 1995, 31(5): 347–349. (in Chinese)
17
Cheng F Y, Shi H Y, Kao C H. Nitric oxide counteracts the senescence of detached rice leaves induced by dehydration
1
Shen C G. Plant Senescence Physiology and Molecular
and polyethylene glycol but not by sorbitol. Plant Growth
Biology. Beijing: China Agricultural Press, 2001: 30–41. (in Chinese) 2 3
Reg, 2002, 38: 265–272. 18
Cadenas E. Biochemistry of oxygen toxicity. Annu Rev
MDA content during senescence of hybrid rice and three lines
Biochem, 1989, 58: 79–110.
leaves. Acta Bot Bor-Occident Sin, 2003, 23(3): 406–409. (in
Lin Z F, Li S S, Lin G Z, Sun G S, Guo J Y. The relation among leaf senescence, activity of superoxide dismutase and
Chinese with English abstract) 19
Wang H C. Plant hardiness physiology. Plant Physiol Comm,
20
Liang Y C, Hu F, Yang M C, Yu J H. Antioxidative defenses
lipid peroxidation. Acta Bot Sin, 1984, 26(6): 605–615. (in Chinese with English abstract) 4 5
1981, 6: 72–81. (in Chinese )
Bowler C, van Camp W, van Montagu M, Inzé D. Superoxide
and water deficit-induced oxidative damage in rice (Oryza
dismutase in plants. Crit Rev Plant Sci, 1994, 13: 199–218.
sativa L.) growing on non-flooded paddy soils with ground
Duan J, Liang C Y, Huang Y W. Studies of leaf senescence of hybrid rice at flowering and grain formation stages. Acta
6
Hua C, Wang R L. Changes of SOD and CAT activities and
mulching. Plant & Soil, 2003, 257: 407–416. 21
Jiao D M, Li X, Ji B H. Photoprotective effects of high level
Phytophysiol Sin, 1997, 23(2): 139–144. (in Chinese with
expression of C4 phosphoenolpyruvate carboxylase in transgenic
English abstract)
rice during photoinhibition. Photosythetica, 2005, 43(4): 501–
Shen B. Studies on physiology of leaf senescence of
508.