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作物学报 ›› 2021, Vol. 47 ›› Issue (10): 1927-1940.doi: 10.3724/SP.J.1006.2021.03064

• 作物遗传育种·种质资源·分子遗传学 • 上一篇    下一篇

大环内酯类和高表达玉米C4-PEPC基因对水稻耐旱性的影响

宋凝曦1,2(), 李霞1,2,3,*(), 王净1,2, 吴博晗1,4, 曹悦1,5, 杨杰1,3, 谢寅峰2   

  1. 1江苏省农业科学院粮食作物研究所 / 江苏省优质水稻工程技术研究中心 / 国家水稻改良中心南京分中心, 江苏南京 210014
    2南京林业大学生物与环境学院, 江苏南京 210037
    3江苏省粮食作物现代产业技术协同创新中心, 江苏扬州 225009
    4江苏大学环境与安全工程学院, 江苏镇江 212013
    5南京农业大学生命科学学院, 江苏南京 210095
  • 收稿日期:2020-10-25 接受日期:2021-03-19 出版日期:2021-10-12 网络出版日期:2021-04-08
  • 通讯作者: 李霞
  • 作者简介:E-mail: 362600124@qq.com
  • 基金资助:
    国家自然科学基金项目(31571585);国家重点研发计划项目(2016YFD0300501-03)

Effects on drought tolerance by pladienolide B and rice with high expression of C4-PEPC

SONG Ni-Xi1,2(), LI Xia1,2,3,*(), WANG Jin1,2, WU Bo-Han1,4, CAO Yue1,5, YANG Jie1,3, XIE Yin-Feng2   

  1. 1Institute of Food Crops, Jiangsu Academy of Agricultural Sciences, Jiangsu High Quality Rice Engineering Technology Research Center, Nanjing Branch of National Center for Rice Improvement, Nanjing 210014, Jiangsu, China
    2College of Biology and Environment, Nanjing Forestry University, Nanjing 210037, Jiangsu, China
    3Collaborative Innovation Center for Modern Production Technology of Grain Crops of Jiangsu Province, Yangzhou 225009, Jiangsu, China
    4School of the Environment and Safety Engineering, Jiangsu University, Zhenjiang 212013, Jiangsu, China
    5School of Life Sciences, Nanjing Agricultural University, Nanjing 210095, Jiangsu, China
  • Received:2020-10-25 Accepted:2021-03-19 Published:2021-10-12 Published online:2021-04-08
  • Contact: LI Xia
  • Supported by:
    National Natural Science Foundation of China(31571585);National Key Research and Development Program of China(2016YFD0300501-03)

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摘要：

为揭示可变剪接机制参与植物耐旱性的内在机制, 以高表达转玉米C4型磷酸烯醇式丙酮酸羧化酶(phosphoenolpyruvate carboxylase, PEPC)基因(C4-PEPC)水稻(PC)和受体“Kitaake” (WT)为材料, 通过盆栽和水培试验, 研究外施可变剪接抑制剂大环内酯类(pladienolide B, PB)联合干旱处理下, 功能叶片的光合参数、总可溶性糖及其组分、主要抗氧化酶活性以及抗氧化物质含量、Ca2+、NO、H2O2、ABA含量、与蔗糖非发酵1 (sucrose nonfermenting-1, SNF1)相关蛋白激酶(SNF1-related protein kinase 3s, SnRK3s)以及剪接因子基因表达的变化。结果表明: 在盆栽试验中, 与单独自然干旱处理(drought stress, DS)相比, 在孕穗期外施0.5 µmol L-1 PB联合干旱处理(DS+PB), 显著下降了供试水稻的产量及其构成因子的数值, 其中, 在DS+PB处理下, PC的株高、穗数、每穗实粒重和单株产量均显著高于WT。在水培试验中, 与10% PEG-6000模拟干旱处理(PEG)相比, 外施0.5 µmol L -1 PB和10% PEG-6000模拟干旱处理(PEG+PB), 均显著降低了供试水稻功能叶片的净光合速率(Pn)、相对含水量、总可溶性糖含量、脯氨酸含量、SOD酶活性、POD酶活性、CAT酶活性、PEPC酶活性、糖组分(蔗糖、葡萄糖、果糖含量)、Ca2+、NO和H2O2的含量, 其中, PC中3个糖组分以及钙离子含量始终高于WT。与PEG处理相比, PEG+PB处理也导致水稻叶片内糖信号SnRK2s基因(SAPK8和SAPK9)和3个SnRK1基因表达量下降, 其中PC的SAPK8、SAPK10、OsK1a和OsK24表达均高于WT; 进一步10 mmol L-1 EGTA钙离子螯合剂引入实验证明, 钙离子通过调节剪接因子相关基因的表达参与水稻干旱响应。相关性分析也表明, PC中钙离子含量分别与叶片可溶性蛋白含量、ABA含量以及剪接因子RS33的表达水平呈显著或极显著相关。综上, 可变剪接参与水稻干旱响应, 水稻可通过叶内糖信号SnRK1s和SnRK2s基因以及钙离子, 参与调节剪接因子相关基因的表达, 对水稻耐旱起积极的作用。与WT相比, PC的增益效果更强, 这与其内源高钙离子和糖组分含量密切相关。

关键词: 水稻, 可变剪接, 磷酸烯醇式丙酮酸羧化酶, 大环内酯, 干旱

Abstract:

To investigate the intrinsic mechanism of alternative splicing (AS) participated in drought tolerance in plants, the effects of macrolides pladienolide B (PB, one of the AS inhibitors) were studied using the phosphoenolpyruvate carboxylase (C4-PEPC) rice (PC) and “Kitaake” (WT) rice lines in pot experiments and hydroponics experiments, respectively. The changes of photosynthetic parameters, total soluble sugar and sugar components contents, some main antioxidant enzyme activities and antioxidant contents, Ca2+, NO, H2O2, ABA contents, transcript levels of sucrose nonfermenting-1 (SNF1)-related protein kinases (SnRKs), arginine/serine-rich proteins (SR proteins), and PEPC both in C4 and C3 type of the functional leaves in rice lines were measured. Agronomic traits of the WT and PC were recorded in the mature period. In pot experiment, compared with the natural drought treatment alone, the treatment of 0.5 µmol L-1 PB with drought at booting stage had a significant decline on agronomic traits of the tested rice. Among them, plant height, panicle number per plant, filled grain number per panicle, and grain yield per plant in PC were significantly higher than those of WT. In the hydroponics experiment with 0.5 µmol L -1 PB combined with 10% mmol L-1 polyethylene glycol 6000 (PEG-6000) to simulate drought stress, compared with PEG treatment, net photosynthetic rate, relative water content, total soluble sugar content, proline content, SOD activity, POD activity, CAT activity, and PEPC activity were significantly increased in PC than those of WT. Similarly, the contents of sucrose, glucose, fructose, and Ca2+ of leaves in PC lines were significantly higher than those of WT. It was noteworthy that the relative gene expression levels of C4-PEPE, Osppc2a, SnRK2s (SAPK8 and SAPK9), SnRK1s (OsK1a, OsK24, and OsK35), and SR proteins (SR33, SR40, RS29, RS2Z21, and RS2Z38) under PEG+PB treatment were significantly lower than those under PEG treatment. It was further verified by using 10 mmol L-1 EGTA experiments [Ethylene glycolbis (aminoethylether)-tetra-acetic acid, a chelate solution of calcium ions] that Ca2+ were involved in the drought response by regulating the transcript levels of SR proteins genes in rice. In addition, the Ca2+ content in PC lines was significantly correlated with soluble protein content, ABA content, and RS33 transcript level, respectively. In conclusion, AS participated in drought response by regulating the expression of SR related genes through sugar signal both SnRK1s and SnRK2s, and calcium ion as well, which played a positive role in drought tolerance in rice. Compared with WT, PC had a stronger positive effect, which was closely related to its high endogenous Ca 2+ content and the contents of sucrose, glucose, fructose.

Key words: rice, alternative splicing, phosphate phosphoenolpyruvate carboxylase, macrolides pladienolide B, drought

表1

qRT-PCR的基因和引物"

基因名称
Gene name		 正向引物
Forward primer (5′-3′)		 反向引物
Reverse primer (5′-3′)		 基因登录号
Gene accession number
Act CCCTCAAACATCGGTATGGA TTGATCTTCATGCTGCTTGG Os01g4349863
OsK1a AACCAGAGGTAACAGGCAGG AACCAGAGGTAACAGGCAGG Os05g4433941
OsK24 CGTGTTGGCTTCAGTGAAT CCTTCTCTATCTAAGGGCCG Os08g4349863
OsK35 TTGTGTTGGCTTCAGTGAAA CCTTCGCTGTCTAAGGACTG Os03g4332495
C4-PEPC CCCACTATCCTTCGCAAGAC CTAGCCAGTGTTCTGCATGCCGG E17154
Osppc2a CTGGTTGAGATGGTTTTCGC GGTGTGAATTCAGGCACTTC Os01g55350
SAPK8 ATAGATGATAATGTCCAGCG GTTCCTACAGTGGATTTTGG Os03g0764800
SAPK9 CACAGCAACGCCGTCTCC CACACTTCCACCGCTACCAA Os12g0586100
SAPK10 TGCTGATGTGTGGTCGTGTG TGCTGGTATGGTCGCCTCT Os03g0610900
RS29 GGGATCTTTGATTTGCTGCGA CAATTTATGTGTTCCACGCCG Os04g02870
RS33 ACTCCCGGTAAGCACATGAC GGGGCTAGCATGTTTCACTG Os02g03040
SR40 CAATCTGGGGACTGCTTTC TCCTGCTTGGGCTTTTACT Os12g38430
SR33 ATATTGCCTGCTACCCGAAAG CAGAGCAGCACCCAGTTTATTAC Os07g47630
SCL25 AAAGTGCACTCTGCGAACTCTCT GCGGTTCACTGAAAAGGACAA Os07g43950
SCL26 GAAGAGAAAATGAACCAGACCG AAACCCTAGCGAAAAGGAAATC Os03g24890
SCL30 CACGCTGATATGTGGGTCTCAT CCTCCCAACGGAAATCTCTAAC Os12g38430
SCL57 TCCCACACCGATTTATCTTTTT CATGTTCTTTAGCCTGTCCTGA Os11g47830
RSZ21 ATGGTCATTGACAAGTGTGCG CGATAGATCTAATCCCGCAAGG Os06g08840
RS2Z36 TGTCAAAACAGCCCAAGAAATC CCATCCATCGTACACCAATAGC Os05g02880

表2

孕穗期外施PB联合干旱处理对水稻产量及其构成因子的影响"

性状
Trait		 转玉米C4-PEPC水稻 C4-PEPC rice (PC) Kitaake (WT)
CK CK+PB DS DS+PB CK CK+PB DS DS+PB
株高
Plant height (cm)		 87.67 a
100.00%		 84.32 a 96.18% 79.03 b 90.14% 67.83 c 77.37% 87.38 a 100.00% 85.33 a
97.65%		 72.35 bc 82.80% 52.62 d 60.22%
最大分蘖数
The largest tiller number per plant		 10.73 b
100.00%		 9.79 b
91.24%		 8.66 c
80.71%		 8.29 c 77.26% 13.97 a 100.00% 12.22 a
87.47%		 8.23 c 58.91% 7.19 d
51.47%
每株总穗数
Panicle number per plant		 9.33 b
100.00%		 9.18 b
98.39%		 6.33 c 67.85% 5.74 d 61.52% 11.04 a 100.00% 10.57 ab 95.74% 6.29 c 56.97% 5.33 d
48.28%
穗长
Panicle length (cm)		 13.35 a
100.00%		 12.47 a 93.41% 11.04 b 82.70% 8.63 d 64.64% 11.67 ab 100.00% 11.40 ab
97.69%		 10.75 c 92.12% 7.67 d
65.72%
每穗总粒数
Total grain number per panicle		 37.61 a
100.00%		 38.47 a 102.29% 33.63 b 89.42% 28.58 c 75.99% 37.33 a 100.00% 35.87 a
96.09%		 28.83 c 77.23% 27.33 c 73.21%
每穗实粒数
Filled grain number per panicle		 33.48 ab 100.00% 32.87 ab 98.18% 24.58 c 73.42% 19.33 d 57.74% 31.04 b 100.00% 30.12 b
97.04%		 21.38 d 68.88% 18.65 d 60.08%
结实率
Gain filling ratio (%)		 89.34 a
100.00%		 85.44 a 95.63% 80.24 c 89.81% 69.14 e 77.39% 83.24 bc 100.00% 83.97 b 100.88% 74.01 d 88.91% 68.32 e 82.08%
千粒重
1000-grain weight (g)		 25.74 a
100.00%		 24.87 a 96.62% 23.38 b 90.83% 19.95 c 77.51% 25.30 a 100.00% 23.84 ab 94.23% 20.74 c 81.98% 17.87 d 70.63%
每株叶干重
Leaf weight per plant (g)		 3.76 a
100.00%		 3.87 a 102.93% 2.53 c 67.29% 2.45 c 65.16% 3.56 b 100.00% 3.47 b
97.47%		 2.29 c 64.33% 2.03 d 57.02%
每株茎干重
Stem weight per plant (g)		 2.93 a
100.00%		 2.85 a 97.27% 1.23 b 41.98% 0.73 c 24.91% 2.59 a 100.00% 2.44 a
94.21%		 1.51 b 58.30% 0.81 c 31.27%
每株穗干重
Panicle weight per plant (g)		 6.77 a
100.00%		 6.59 a 97.34% 4.95 c 73.12% 2.47 e 36.48% 6.19 b 100.00% 5.93 b
95.80%		 4.12 d 66.56% 2.14 f 34.57%
总干重
Total dry weight per plant (g)		 13.46 a 100.00% 13.31 a 98.89% 8.71 c 64.71% 5.65 d 41.98% 12.34 b 100.00% 11.84 b 95.95% 7.52 c 60.94% 4.98 e 40.36%
单株产量
Yield per plant (g)		 4.13 a
100.00%		 4.05 a 98.06% 2.83 c 68.52% 2.54 d 61.50% 3.82 b 100.00% 3.71 b
97.12%		 2.06 e 53.93% 1.71 f 44.76%

表3

喷施PB联合10% PEG-6000模拟干旱处理对水稻叶片光合参数的变化"

光合参数
Photosynthetic parameters		 转玉米C4-PEPC水稻 C4-PEPC rice (PC) Kitaake (WT)
CK PEG PEG+PB CK PEG PEG+PB
净光合速率
Net photosynthetic rate Pn (μmoL CO2 m-2 s-1)		 20.14 a 100.00% 16.73 c 83.07% 15.60 d 77.46% 18.22 b 100.00% 13.46 c 73.87% 10.68 f
58.62%
气孔导度
Stomatal conductance Gs (mol m-2 s-1)		 0.73 a 100.00% 0.45 b 61.64% 0.46 b 63.01% 0.75 a 100.00% 0.33 c 44.00% 0.31 c
41.33%
胞间CO2浓度
Intercellular CO2 concentration Ci (μmol mol-1)		 366.57 a 100.00% 345.18 ab 94.16% 337.18 b
91.98%		 368.96 a 100.00% 343.04 b 92.97% 354.09 ab
95.97%
蒸腾速率
Transpiration rate Tr (mol H2O m-2 s-1)		 9.06 a 100.00% 6.31 c 69.65% 6.24 c 68.87% 9.46 a 100.00% 7.14 b 75.48% 7.34 b
77.59%
羧化效率
Carboxylation efficiency CE (mol m-2 s-1)		 0.063 a 100.00% 0.048 c 76.19% 0.046 c 73.02% 0.051 b 100.00% 0.039 d 76.47% 0.032 e
62.75%

表4

不同处理对水稻叶片相对含水量、渗透调节物质、抗氧化酶活性以及PEPC酶活性的影响"

生理指标
Physiological indexes		 转玉米C4-PEPC水稻 C4-PEPC rice (PC) Kitaake (WT)
CK PEG PEG+PB CK PEG PEG+PB
相对含水量
Relative water content (%)		 88.43 a
100.00%		 78.43 b 88.69% 73.47 c 83.08% 88.96 a
100.00%		 69.17 d 77.75% 61.42 e 69.04%
总的可溶性蛋白含量
Total soluble protein content (mg g-1)		 14.25 a
100.00%		 12.92 b
90.67%		 9.92 d
69.61%		 14.01 a
100.00%		 11.72 c 83.65% 8.02 e
57.24%
总的可溶性糖含量
Total soluble sugar content (mg g-1)		 21.23 c
100.00%		 28.33 a 133.44% 12.41 e 58.46% 19.02 d
100.00%		 23.04 b 121.14% 9.59 f
50.42%
脯氨酸含量
Proline content (mg g-1)		 63.38 c
100.00%		 75.49 a 119.11% 41.85 d 66.03% 64.15 c
100.00%		 68.04 b 106.06% 38.03 e
59.28%
超氧化物歧化酶活性
Superoxide dismutase activity (U g-1)		 56.78 b
100.00%		 84.54 a 148.89% 33.56 d 59.11% 51.74 c
100.00%		 56.53 b 109.26% 29.78 e
57.56%
过氧化物酶活性
Peroxidase activity (U g-1)		 65.46 c
100.00%		 89.44 a 136.63% 32.73 e 50.01% 59.07 d
100.00%		 76.64 b 129.74% 29.53 f
49.99%
过氧化氢酶活性
Catalase activity (U g-1)		 176.27 a
100.00%		 137.32 c 77.90% 126.27 d 71.63% 160.34 b
100.00%		 130.56 d
81.42%		 96.11 e
59.94%
抗坏血酸含量
Ascorbic acid content (µg g-1)		 11.38 c
100.00%		 16.19 a
142.27%		 7.07 d
62.13%		 12.43 c
100.00%		 14.88 b
119.71%		 6.72 d
54.06%
谷胱甘肽含量
Glutathione content (µmol L-1)		 22.31 a
100.00%		 15.52 c
69.57%		 11.09 e
49.71%		 20.31 b
100.00%		 13.21 d
65.04%		 10.52 e
51.80%
磷酸烯醇式丙酮酸羧化酶活性
PEPC activity (U mg-1 prot)		 60.54 c
100.00%		 90.97 a 150.26% 68.32 b 112.85% 20.03 e
100.00%		 29.44 d 146.98% 21.14 e 105.54%

表5

不同处理对水稻叶片蔗糖、葡萄糖、果糖、钙离子、NO和H2O2含量的影响"

生理指标
Physiological indexes		 转玉米C4-PEPC水稻 C4-PEPC rice (PC) Kitaake (WT)
CK PEG PEG+PB CK PEG PEG+PB
蔗糖含量
Sucrose content (mg g-1)		 9.67 c 100.00% 11.92 a
123.27%		 5.15 d 53.26% 10.19 b 100.00% 10.09 c 99.02% 4.41 e 43.28%
葡萄糖含量
Glucose content (mg g-1)		 8.71 b 100.00% 9.86 a
113.20%		 4.34 c
49.83%		 9.75 a
100.00%		 8.47 b
86.87%		 2.69 d 27.59%
果糖含量
Fructose content (mg g-1)		 3.21 b 100.00% 2.93 d
91.28%		 2.21 e
68.85%		 3.61 a
100.00%		 3.17 c
87.81%		 1.79 f 49.58%
钙离子含量
Ca2+content (mmol g-1)		 1.67 c 100.00% 2.07 a
123.95%		 0.82 d
49.10%		 1.29 b
100.00%		 1.69 c 131.01% 0.43 e 33.33%
一氧化氮含量
NO content (µmol g-1)		 35.61 a 100.00% 22.05 b
61.92%		 18.04 d
50.66%		 36.47 a 100.00% 20.34 c 55.77% 17.92 d 49.14%
过氧化氢含量
H2O2 content (µmol g-1)		 103.07 b 100.00% 107.47 b
104.27%		 82.48 c
80.02%		 102.15 b 100.00% 128.96 a 126.25% 84.11 c 82.34%

表6

不同处理对水稻叶片ABA含量、相对含水量、PEPC以及SnRKs相关基因表达量的影响"

测定指标
Measurement index		 转玉米C4-PEPC水稻 C4-PEPC rice (PC) Kitaake (WT)
CK PEG PEG+PB PEG+PB+EGTA CK PEG PEG+PB PEG+PB+EGTA
ABA 含量
ABA content (μg g-1)		 8.16 d 12.95 a 5.63 e 9.78 b 9.43 c 6.86 b 4.92 f 8.26 d
相对含水量
Relative water content (%)		 87.43 a 76.43 b 73.47 c 59.38 e 89.56 a 68.17 d 62.42 e 51.39 f
C4-PEPC相对表达量
Relative expression of C4-PEPC		 2.27 d 6.44 a 3.27 b 2.53 c
Osppc2a相对表达量
Relative expression of Osppc2a		 0.96 de 1.26 c 0.55 g 1.45 b 1.04 d 1.57 a 0.78 f 1.038 d
SAPK8相对表达量
Relative expression of SAPK8		 1.98 e 10.53 a 1.05 c 0.88 d 1.03 g 5.39 b 2.03 f 0.41 h
SAPK9相对表达量
Relative expression of SAPK9		 3.09 a 2.84 b 1.54 d 0.68 f 1.04 e 1.87 c 0.97 e 1.77 c
SAPK10相对表达量
Relative expression of SAPK10		 0.82 d 3.09 b 2.94 b 0.75 e 1.02 c 5.81 a 0.74 e 0.66 f
OsK1a相对表达量
Relative expression of OsK1a		 1.75 d 14.12 a 10.05 b 1.54 e 1.03 g 10.04 b 5.43 c 1.15 f
OsK24相对表达量
Relative expression of OsK24		 0.97 e 16.99 c 14.41 d 0.74 g 1.01 e 12.89 a 9.06 b 0.25 f
OsK35相对表达量
Relative expression of OsK35		 2.12 g 13.05 a 3.76 f 5.88 d 1.04 h 7.41 b 3.99 e 6.28 c

表7

不同处理对水稻叶片剪接因子相关基因表达的影响"

相对基因的表达
Relative expression level of genes		 转玉米C4-PEPC水稻 C4-PEPC rice (PC) Kitaake (WT)
CK PEG PEG+PB PEG+PB+
EGTA		 CK PEG PEG+PB PEG+PB+EGTA
SR33 2.12 c 2.47 b 3.69 a 1.36 d 1.04 e 0.97 e 2.43 b 0.79 f
SR40 1.65 e 4.57 a 4.15 b 1.17 f 1.03 g 3.36 c 2.11 d 0.86 h
RS29 0.97 e 6.13 a 5.97 a 1.08 d 1.02 d 3.14 b 2.31 c 0.23 f
RS33 1.24 c 0.57 g 0.68 f 2.72 a 1.04 d 0.72 e 0.42 h 1.35 b
SCL25 3.12 b 4.74 a 2.07 d 1.45 e 1.03 g 2.42 c 1.23 f 0.35 h
SCL26 0.76 g 5.13 a 0.95 f 2.41 c 1.01 f 4.56 b 1.24 e 1.38 d
SCL30 0.96 e 0.69 f 2.31 c 2.76 b 1.04 e 1.21 d 4.32 a 4.14 a
SCL57 0.95 e 4.39 a 1.71 c 1.89 c 1.03 d 2.38 b 2.52 b 0.83 f
RS2Z21 5.49 b 10.74 a 9.85 a 1.72 e 1.02 e 5.16 c 3.14 d 0.51 f
RS2Z36 1.89 e 2.19 d 1.97 e 4.27 a 1.01 f 2.37 c 0.96 f 3.87 b
RS2Z38 0.86 e 4.12 a 3.93 b 0.36 f 1.04 d 3.82 b 1.55 c 1.48 c

图1

PC和WT各指标相关性 A: PC各指标相关性; B: WT各指标相关性。* P < 0.05; ** P < 0.01。RWC: 相对含水量; Su: 可溶性糖; Sp: 可溶性蛋白; Suc: 蔗糖; Glu: 葡萄糖; Fru: 果糖。"

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