外源海藻糖增强高表达转玉米C4型PEPC水稻耐旱性的机制

doi:10.11983/CBB20168

植物学报 ›› 2021, Vol. 56 ›› Issue (3): 296-314.DOI: 10.11983/CBB20168

外源海藻糖增强高表达转玉米C₄型PEPC水稻耐旱性的机制

李佳馨¹^,², 李霞¹^,²^,³^,^*(), 谢寅峰¹

¹南京林业大学生物与环境学院, 南京 210037
²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, 南京 210014
³扬州大学农学院, 江苏省粮食作物现代产业技术协同创新中心, 扬州 225009

收稿日期:2020-10-12 接受日期:2021-04-22 出版日期:2021-05-01 发布日期:2021-04-30
通讯作者: 李霞
作者简介:^*E-mail: jspplx@jaas.ac.cn
基金资助:
国家自然科学基金(31571585);国家重点研发计划No(2016YFD0300501-03);江苏省重点研发计划现代农业 No(BE2019377)

Mechanism on Drought Tolerance Enhanced by Exogenous Trehalose in C₄-PEPC Rice

Jiaxin Li¹^,², Xia Li¹^,²^,³^,^*(), Yinfeng Xie¹

¹College of Biology and Environment, Nanjing Forestry University, Nanjing 210037, China
²Nanjing Branch of China National Center for Rice Improvement/Jiangsu High Quality Rice Engineering Technology Research Center/Institute of Food Crops, Jiangsu Academy of Agricultural Sciences, Nanjing 210014, China
³Collaborative Innovation Center for Modern Production Technology of Grain Crops of Jiangsu Province, Agricultural College, Yangzhou University, Yangzhou 225009, China

Received:2020-10-12 Accepted:2021-04-22 Online:2021-05-01 Published:2021-04-30
Contact: Xia Li

1. 附表1 海藻糖处理调控干旱胁迫下水稻叶片内海藻糖、SnRKs 及ABA 相关基因的表达.pdf(227KB)

摘要/Abstract

摘要： 为揭示海藻糖(Tre)调控转玉米(Zea mays) C₄型PEPC基因水稻(Oryza sativa) (PC)的耐旱性机制, 以PC及其野生型Kitaake (WT)为材料, 通过水培试验, 研究了Tre和12% (m/v)聚乙二醇(PEG)单独或联合处理对水稻生理生化特性的影响。结果表明, Tre处理可促进PC和WT水稻幼苗生长, 缓解干旱逆境导致的植株生长抑制, 但对PC的效应更显著。与DS处理相比, Tre+DS联合处理可维持功能叶较高的相对含水量、光化学效率和抗氧化酶活性。在DS处理下, 与WT相比, 外施Tre可使PC的内源Tre和蔗糖含量显著增加, 而葡萄糖含量显著降低, Tre代谢和SnRK1s相关基因表达量增加; 施用Tre也显著促进了ABA合成、信号转导与干旱响应基因的表达, 和维持较稳定的光合能力, 从而使PC表现更强的耐旱性。

关键词: 转C₄-PEPC基因水稻, 干旱胁迫, 磷酸烯醇式丙酮酸羧化酶, 海藻糖, 水稻

Abstract: In order to reveal the mechanism of trehalose (Tre) involved in the drought tolerance of transgenic rice (Oryza sativa) (PC) expressing the C₄-PEPC gene of maize (Zea mays), we analyzed the physiological and biochemistry characteristics of PC and wild-type rice (WT) treated hydroponically with Tre and 12% (m/v) PEG alone or in combination. The results showed that Tre treatment promoted the growth of PC and WT seedlings, and alleviated the inhibition of plant growth caused by drought stress (DS), with the effect being more significant for PC. Compared with DS treatment, Tre+DS treatment maintained functional leaves a higher relative water content, photochemical efficiency and antioxidant enzyme activity. Under DS, compared with WT, PC showed significant increase in the content of Tre and sucrose and decrease in the content of glucose, and up-regulated expression of genes associated with Tre metabolism and SnRK1s after Tre application. Tre application also improved PC the ABA synthesis, and expression of genes related to signal transduction and drought response, and maintained PC a relatively stable photosynthetic capacity, thus possibly conferring stronger drought tolerance of PC.

Key words: C₄-type PEPC transgenic rice, drought stress, phosphate phosphoenolpyruvate carboxylase, trehalose, rice (Oryza sativa)

李佳馨, 李霞, 谢寅峰. 外源海藻糖增强高表达转玉米C₄型PEPC水稻耐旱性的机制. 植物学报, 2021, 56(3): 296-314.

Jiaxin Li, Xia Li, Yinfeng Xie. Mechanism on Drought Tolerance Enhanced by Exogenous Trehalose in C₄-PEPC Rice. Chinese Bulletin of Botany, 2021, 56(3): 296-314.

导出引用管理器 EndNote|Ris|BibTeX

链接本文: https://www.chinbullbotany.com/CN/10.11983/CBB20168

https://www.chinbullbotany.com/CN/Y2021/V56/I3/296

图/表 8

表1 qRT-PCR的基因和引物

Table 1 Genes and primers for qRT-PCR

Gene	Forward primer (5′-3′)	Reverse primer (5′-3′)
Act	CCCTCTTTCATCGGTATGGA	TTGATCTTCATGCTGCTTGG
OsTPP1	CAAATGGATTTGAGCAATAGC	TCACACTGAGTGCTTCTTCCA
OsTPP2	ATGGATTTGAAGACAAGCAAC	TTAAGTGGATTCCTCCTTCCA
OsTPP3	ATGACGAACCACGCCGGC	CTACTTGCCAATCAGCCCTTT
OsTPP7	CCTTCATGAGCGAGACGATG	TCACGAACTCGAACACCTTG
OsTre1	TTGGTACCCCTTACTCCGGCCGATTCA	AAGAGCTCCTGCCTAGCCTAGCCACAT
OsTPS1	AGTTATTATCTGGAAGGAGC	TCAAGAACCTCCTGAATGCC
OsTPS2	ACAAAGATGGGATGAAAGTG	CAGGATTCACAAACAGATTC
OsTPS8	TGAAGAGATAAAATGGCGTG	GAAAAGGTGAATGAATCTGC
OsSnR1a	AACCAGAGGTAACAGGCAGG	CATCTGTCAAGGAATGCAGG
OsSnRK24	CGTGTTGGCTTCAGTGAAT	CCTTCTCTATCTAAGGGCCG
OsSAPK8	ATAGATGATAATGTCCAGCGTGAG	GTTCCTACAGTGGATTTTGGTTG
OsSAPK9	CACAGCAACGCCGTCTCC	CACACTTCCACCGCTACCAA
OsSAPK10	TGCTGATGTGTGGTCGTGTG	TGCTGGTATGGTCGCCTCT
OsABA8ox2	CTACTGCTGATGGTGGCTGA	CCCATGGCCTTTGCTTTAT
OsABA8ox3	AGTACAGCCCATTCCCTGTG	ACGCCTAATCAAACCATTGC
OsNCED3	CCCCTCCCAAACCATCCAAACCGA	TGTGAGCATATCCTGGCGTCGTGA
OsNCED4	TCCATCTCCTTCTCCCTCCTCCCA	CCTCGCACCCTGCTTGATCTTGCC
OsbZIP23	CTCTGATCCCTCGTTGCGTTA	CAACACCCCAGCACCAAACT
OsMYB2	GGGCTGAAACGCACAGGCAAGA	GGGCTGAAACGCACAGGCAAGA
OsRab16b	CAACAACCACCAGCAGCA	GATCTTGTCCATGAATCCC
OsRab21	AGCAGCAGCATGCCATG	TGGTGCCGGTGGTCAT
OsLEA3	TTCCCACCAGGACCAGGCTA	GTCGCCTCCTTGGTATCCT
OsNAC6	CGCTGTACGAGAAGGAG	ACTCGTGCATGATCCAGTTG
C₄-PEPC	GTACCGCGAGTGGCCCGAGG	CGTCCATGAGCTTGCGCCAC
Osppc2a	CAGCTACTCATGCTTAACGC	GCACAGACTACAGCCTGTAC

图1 海藻糖处理缓解干旱胁迫对水稻的生长抑制模拟干旱处理6天后的植株表型(A)、株高(B)、茎粗(C)、鲜重(D)和干重(E)。CK: 正常灌溉; CK+Tre: 正常灌溉+0.5 mmol?L-1海藻糖; DS: 模拟干旱胁迫; DS+Tre: 模拟干旱胁迫+0.5 mmol?L-1海藻糖。图中数值代表来自3个生物学重复的平均值±标准差 (n=9)。不同小写字母的柱值表示差异显著(P<0.05) (Student-Neuman-Keuls)。Bars=1 cm

Figure 1 Trehalose treatments alleviate the growth inhibition of rice under drought stress Plant phenotype (A), plant height (B), stem diameter (C), fresh weight (D) and dry weight (E) after 6 days of simulated drought treatment. CK: Irrigation; CK+Tre: Irrigation and 0.5 mmol?L-1 trehalose; DS: Simulated drought stress; DS+Tre: Simulated drought stress and 0.5 mmol?L-1 trehalose. Values represent means±SD (n=9) from three biological replicates. Bars labeled with different lowercase letters indicate significant differences (P<0.05) (Student-Neuman-Keuls). Bars=1 cm

图2 海藻糖处理提高干旱胁迫下水稻叶片内PEPC的转录及翻译水平模拟干旱处理2小时后C4-PEPC基因的相对表达量(A)、磷酸烯醇式丙酮酸羧化酶(PEPC)活性(B)和Osppc2a基因的相对表达量(C)。缩写同图1。图中数值代表来自3个生物学重复的平均值±标准差(n=6)。不同小写字母的柱值表示差异显著(P<0.05) (Student-Neuman-Keuls)。

Figure 2 Trehalose treatments increase PEPC transcription and translation in rice leaves under drought stress C4-PEPC expression (A), phosphoenolpyruvate carboxylase (PEPC) activity (B) and Osppc2a expression (C) after 2 hours of simulated drought treatment. Abbreviations are the same as those given in Figure 1. Values represent means±SD (n=6) from three biological replicates. Bars labeled with different lowercase letters indicate significant differences (P<0.05) (Student-Neuman-Keuls).

表2 海藻糖处理调节干旱胁迫下水稻叶片的氧化损伤

Table 2 Trehalose treatments regulate the oxidative damage of rice leaves under drought stress

Index	WT				PC
Index	CK	CK+Tre	DS	DS+Tre	CK	CK+Tre	DS	DS+Tre
RWC (%)	91.09 b	92.02 ab	78.05 e	89.21 c	89.68 c	88.30 c	80.81 d	93.00 a
MDA (nmol·mg^-1 prot)	2.26 d	2.22 d	3.39 a	2.52 c	2.40 c	2.18 c	3.03 b	1.89 e
H₂O₂ (μmol·g^-1 FW)	6.87 f	24.84 a	14.59 c	5.09 g	8.01 e	21.68 b	11.96 d	3.63 h
SOD (U·mg^-1 prot)	1087.99 d	1063.79 e	1101.66 c	1126.52 b	1083.80 d	1059.65 e	1102.99 c	1140.24 a
CAT (U·mg^-1 prot)	15.74 e	16.99 c	16.63 d	16.65 d	13.51 f	18.39 a	16.25 d	17.74 b
GR (nmol·g^-1 prot)	1.49 e	2.46 c	2.17 d	0.96 g	1.22 f	3.26 b	3.69 a	2.00 d
APX (U·g^-1 FW)	5.26 c	6.55 b	6.59 b	10.14 a	2.70 f	4.33 d	2.32 g	3.74 e

图3 海藻糖处理维持干旱胁迫下水稻叶片的光合性能模拟干旱处理2小时后PC和WT的最大光化学效率(Fv/Fm) (A)、有效光化学效率(Fv′/Fm′) (B)、实际光化学效率(ΦPSII) (C)、光化学淬灭系数(qP) (D)和非光化学淬灭系数(NPQ) (E)。缩写同图1。图中数值代表来自3个生物学重复的平均值±标准差(n=6)。不同小写字母的柱值表示差异显著(P<0.05) (Student-Neuman-Keuls)。

Figure 3 Trehalose treatment maintain the photosynthetic performance of rice leaves under drought stress Fv/Fm (A), Fv′/Fm′ (B), ΦPSII (C), qP (D) and NPQ (E) of PC and WT after 2 hours of simulated drought treatment. Abbreviations are the same as those given in Figure 1. Values represent means±SD (n=6) from three biological replicates. Bars labeled with different lowercase letters indicate significant differences (P<0.05) (Student-Neuman-Keuls).

表3 海藻糖处理改变干旱胁迫下水稻叶片内可溶性糖的积累与分配

Table 3 Trehalose treatments change the accumulation and distribution of soluble sugars in rice leaves under drought stress

Index (mg·g^-1FW)	WT				PC
Index (mg·g^-1FW)	CK	CK+Tre	DS	DS+Tre	CK	CK+Tre	DS	DS+Tre
Soluble sugar content	16.10 e	16.50 e	29.01 c	34.32 b	14.97 f	19.01 d	35.31 b	41.57 a
Sucrose content	9.40 e	10.78 d	10.34 d	12.36 b	8.51 f	11.18 c	11.61 c	13.81 a
Fructose content	4.01 d	4.09 d	4.95 c	5.81 b	3.86 e	3.88 e	5.49 b	7.66 a
Glucose content	1.64 b	1.28 c	2.35 a	1.62 b	0.88 d	0.78 e	1.32 c	0.91 d
Trehalose content	8.22 f	9.46 e	10.84 d	13.60 b	8.55 f	10.40 d	11.23 c	15.80 a

图4 海藻糖处理影响干旱胁迫下水稻叶片内海藻糖、SnRKs及ABA相关基因的表达 (A) 海藻糖合成与代谢相关基因的表达; (B) SnRKs相关基因的表达; (C) ABA代谢相关基因的表达。缩写同图1。热图显示基因相对表达量对数转换均一化值, 显著性分析表示基因相对表达量之间的差异(附表1)。图中不同小写字母表示差异显著(P<0.05) (Student-Neuman-Keuls)。

Figure 4 Trehalose treatments affect the expression of trehalose, SnRKs and ABA-related genes in rice leaves under drought stress (A) The expression of trehalose biosynthesis and metabolism related genes; (B) The expression of SnRKSs-related genes; (C) The expression of ABA metabolism-related genes. Abbreviations are the same as those given in Figure 1. The heat map shows the log-transformed normalized values of relative gene expression, and the significance analysis showed the difference between relative gene expressions (Appendix Table 1). Different lowercase letters indicate significant differences (P<0.05) (Student-Neuman-Keuls).

图5 海藻糖处理影响干旱胁迫下水稻叶片内信号分子的含量和相关酶活性 (A) 钙离子含量; (B) 一氧化氮含量; (C) 硝酸还原酶活性; (D) 己糖激酶活性。缩写同图1。图中数值代表来自3个生物学重复的平均值±标准差(n=6)。不同小写字母的柱值表示差异显著(P<0.05) (Student-Neuman-Keuls)。

Figure 5 Trehalose treatments affect the content of signal molecules and the activity of related enzymes in rice leaves under drought stress (A) Ca2+ content; (B) NO content; (C) Nitate reductase (NR) activity; (D) Hexokinase (HXK) activity. Abbreviations are the same as those given in Figure 1. Values represent means±SD (n=6) from three biological replicates. Bars labeled with different lowercase letters indicate significant differences (P<0.05) (Student-Neuman-Keuls).

参考文献 99

1	何亚飞, 许梦洁, 李霞 (2018). 干旱条件下DCMU对高表达转C₄-pepc水稻的花青素合成基因及其相关信号的影响. 中国生态农业学报 26, 409-421.
2	李霞, 焦德茂, 戴传超 (2005). 转PEPC基因水稻对光氧化逆境的响应. 作物学报 31, 408-413.
3	刘小龙, 李霞, 钱宝云 (2015). 外源Ca ²+对PEG处理下转C₄型PEPC基因水稻光合生理的调节 . 植物学报 50, 206-216.
4	吴敏怡, 李霞, 何亚飞, 张琛, 严婷 (2017). 脱落酸和己糖激酶抑制剂对高表达C₄-PEPC转基因稻苗耐旱性的影响. 植物研究 37, 402-415.
5	严婷, 李佳馨, 李霞, 谢寅峰 (2019). 转C₄型PEPC基因水稻非生物胁迫耐受性研究进展. 淮阴工学院学报 28, 62-68.
6	杨彩琴, 刘伟娜, 赵志弘, 吴海燕 (1998). 血清钙的甲基百里香酚蓝测定法. 光谱学与光谱分析 18, 485-487.
7	张金飞, 李霞, 何亚飞, 谢寅峰 (2018). 外源葡萄糖增强高表达转玉米C₄型pepc水稻耐旱性的生理机制. 作物学报 44, 82-94.
8	张金飞, 李霞, 谢寅峰 (2017). 植物SnRKs家族在胁迫信号通路中的调节作用. 植物学报 52, 346-357. DOI
9	Akram NA, Waseem M, Ameen R, Ashraf M (2016). Trehalose pretreatment induces drought tolerance in radish (Raphanus sativus L.) plants: some key physio-biochemical traits. Acta Physiol Plant 38, 3. DOI URL
10	Alam MM, Nahar K, Hasanuzzaman M, Fujita M (2014). Trehalose-induced drought stress tolerance: a comparative study among different brassica species. Plant Omics J 7, 271-283.
11	Ambavaram MMR, Basu S, Krishnan A, Ramegowda V, Batlang U, Rahman L, Baisakh N, Pereira A (2014). Coordinated regulation of photosynthesis in rice increases yield and tolerance to environmental stress. Nat Commun 5, 5302. DOI PMID
12	Asami P, Rupasinghe T, Moghaddam L, Njaci I, Roessner U, Mundree S, Williams B (2019). Roots of the resurrection plant tripogon loliiformis survive desiccation without the activation of autophagy pathways by maintaining energy reserves. Front Plant Sci 10, 459. DOI URL
13	Baena-González E, Lunn JE (2020). SnRK1 and trehalose 6-phosphate: two ancient pathways converge to regulate plant metabolism and growth. Curr Opin Plant Biol 55, 52-59. DOI URL
14	Bandyopadhyay A, Datta K, Zhang J, Yang W, Raychaudhuri S, Miyao M, Datta SK (2007). Enhanced photosynthesis rate in genetically engineered indica rice expressing pepc gene cloned from maize. Plant Sci 172, 1204-1209. DOI URL
15	Blázquez MA, Lagunas R, Gancedo C, Gancedo JM (1993). Trehalose-6-phosphate, a new regulator of yeast glycolysis that inhibits hexokinases. FEBS Lett 329, 51-54. PMID
16	Chen PB, Li X, Huo K, Wei XD, Dai CC, Lu CG (2014). Promotion of photosynthesis in transgenic rice over-expressing of maize C₄ phosphoenolpyruvate carboxylase gene by nitric oxide donors. J Plant Physiol 171, 458-466. DOI URL
17	Claeys H, Vi SL, Xu XS, Satoh-Nagasawa N, Eveland AL, Goldshmidt A, Feil R, Beggs GA, Sakai H, Brennan RG, Lunn JE, Jackson D (2019). Control of meristem determinacy by trehalose 6-phosphate phosphatases is uncoupled from enzymatic activity. Nat Plants 5, 352-357. DOI URL
18	Corpas FJ, Barroso JB (2018). Peroxisomal plant metabolism: an update on nitric oxide, Ca ²+ and the NADPH recycling network . J Cell Sci 131, jcs202978.
19	Delorge I, Janiak M, Carpentier S, van Dijck F (2014). Fine tuning of trehalose biosynthesis and hydrolysis as novel tools for the generation of abiotic stress tolerant plants. Front Plant Sci 5, 147. DOI PMID
20	Dey A, Samanta MK, Gayen S, Sen SK, Maiti MK (2016). Enhanced gene expression rather than natural polymorphism in coding sequence of the OsbZIP23 determines drought tolerance and yield improvement in rice genotypes. PLoS One 11, e0150763. DOI URL
21	Ding ZS, Huang SH, Zhou BY, Sun XF, Zhao M (2013). Over-expression of phosphoenolpyruvate carboxylase cDNA from C₄ millet ( Seteria italica) increase rice photosynthesis and yield under upland condition but not in wetland fields. Plant Biotechnol Rep 7, 155-163. DOI URL
22	Ding ZS, Zhou BY, Sun XF, Zhao M (2012). High light tolerance is enhanced by overexpressed PEPC in rice under drought stress. Acta Agron Sin 38, 285-292.
23	Duan JL, Cai WM (2012). OsLEA3-2, an abiotic stress induced gene of rice plays a key role in salt and drought tolerance. PLoS One 7, e45117. DOI URL
24	Durand M, Mainson D, Porcheron B, Maurousset L, Lemoine R, Pourtau N (2018). Carbon source-sink relationship in Arabidopsis thaliana: the role of sucrose transporters. Planta 247, 587-611. DOI URL
25	Ermakova M, Danila FR, Furbank RT, Caemmerer S (2020). On the road to C₄ rice: advances and perspectives. Plant J 101, 940-950. DOI
26	Feng YC, Chen XY, He YL, Kou XH, Xue ZH (2019). Effects of exogenous trehalose on the metabolism of sugar and abscisic acid in tomato seedlings under salt stress. Trans Tianjin Univ 25, 451-471. DOI URL
27	Fichtner F, Lunn JE (2021). The role of trehalose 6-phosphate (Tre6P) in plant metabolism and development. Annu Rev Plant Biol 72, 187-220.
28	Figueroa CM, Feil R, Ishihara H, Watanabe M, Kölling K, Krause U, Höhne M, Encke B, Plaxton WC, Zeeman SC, Li Z, Schu WX, Hoefgen R, Stitt M, Lunn JE (2016). Trehalose 6-phosphate coordinates organic and amino acid metabolism with carbon availability. Plant J 85, 410-423. DOI URL
29	Figueroa CM, Lunn JE (2016). A tale of two sugars: trehalose 6-phosphate and sucrose. Plant Physiol 172, 7-27.
30	Foyer CH, Halliwell B (1976). The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133, 21-25. DOI PMID
31	Ge LF, Chao DY, Shi M, Zhu MZ, Gao JP, Lin HX (2008). Overexpression of the trehalose-6-phosphate phosphatase gene OsTPP1 confers stress tolerance in rice and results in the activation of stress responsive genes. Planta 228, 191-201. DOI URL
32	Giannopolitis CN, Ries SK (1977). Superoxide dismutases I: occurrence in higher plants. Plant Physiol 59, 309-314. PMID
33	Giglioli-Guivarc'h G, Pierre JN, Brown S, Chollet R, Vidal J, Gadal P (1996). The light-dependent transduction pathway controlling the regulatory phosphorylation of C₄ phosphoenolpyruvate carboxylase in protoplasts from digitaria sanguinalis. Plant Cell 8, 573-586. DOI URL
34	Gómez LD, Gilday A, Feil R, Lunn JE, Graham IA (2010). AtTPS1-mediated trehalose 6-phosphate synthesis is essential for embryogenic and vegetative growth and responsiveness to ABA in germinating seeds and stomatal guard cells. Plant J 64, 1-13.
35	Han BY, Fu LL, Zhang D, He XQ, Chen Q, Peng M, Zhang JM (2016). Interspecies and intraspecies analysis of trehalose contents and the biosynthesis pathway gene family reveals crucial roles of trehalose in osmotic-stress tolerance in cassava. Int J Mol Sci 17, 1077. DOI URL
36	He YF, Xie YF, Li X, Yang J (2020). Drought tolerance of transgenic rice overexpressing maize C₄-PEPC gene related to increased anthocyanin synthesis regulated by sucrose and calcium. Biol Plantarum 64, 136-149. DOI URL
37	Hong CY, Chao YY, Yang MY, Cheng SY, Cho SC, Kao CH (2009). NaCl-induced expression of glutathione reductase in roots of rice (Oryza sativa L.) seedlings is mediated through hydrogen peroxide but not abscisic acid. Plant Soil 320, 103-115. DOI URL
38	Hong YB, Zhang HJ, Huang L, Li DY, Song FM (2016). Overexpression of a stress-responsive NAC transcription factor gene ONAC022 improves drought and salt tolerance in rice. Front Plant Sci 7, 4.
39	Huo K, Li X, He YF, Wei XD, Lu W, Zhao CF, Wang CL (2017). Exogenous ATP enhance signal response of suspension cells of transgenic rice ( Oryza sativa L.) expressing maize C₄-pepc encoded phosphoenolpyruvate carboxylase under PEG treatment. Plant Growth Regul 82, 55-67. DOI URL
40	Ilhan S, Ozdemir F, Bor M (2015). Contribution of trehalose biosynthetic pathway to drought stress tolerance of Capparis ovata desf. Plant Biol 17, 402-407. DOI URL
41	Islam MO, Kato H, Shima S, Tezuka D, Matsui H, Imai R (2019). Functional identification of a rice trehalose gene involved in salt stress tolerance. Gene 685, 42-49. DOI URL
42	Izui K, Matsumura H, Furumoto, Kai Y (2004). Phospho enol pyruvate carboxylase: a new era of structural biology. Annu Rev Plant Biol 55, 69-84. DOI URL
43	Jiang DG, Chen WT, Gao J, Yang F, Zhuang CX (2019). Overexpression of the trehalose-6-phosphate phosphatase OsTPP3 increases drought tolerance in rice. Plant Biotechnol Rep 13, 285-292. DOI URL
44	Jiao DM, Ji BH, Li X (2003). Characteristics of chlorophyll fluorescence and membrane-lipid peroxidation during senescence of flag leaf in different cultivars of rice. Photosynthetica 41, 33-41. DOI URL
45	John R, Raja V, Ahmad M, Jan N, Majeed U, Ahmad S, Yaqoob U, Kaul T (2017). Trehalose: metabolism and role in stress signaling in plants. In: Sarwat M, Ahmad A, Abdin M, Ibrahim M, eds. Stress Signaling in Plants: Genomics and Proteomics Perspective, Volume 2. Cham: Springer International Publishing. pp. 261-275.
46	Karki S, Rizal G, Quick WP (2013). Improvement of photosynthesis in rice (Oryza sativa L.) by inserting the C₄ pathway. Rice 6, 28. DOI URL
47	Kim YM, Heinzel N, Giese JO, Koeber J, Melzer M, Rutten T, von Wirén N, Sonnewald U, Hajirezaei MR (2013). A dual role of tobacco hexokinase 1 in primary metabolism and sugar sensing. Plant Cell Environ 36, 1311-1327. DOI URL
48	Kosar F, Akram NA, Sadiq M, Al-Qurainy F, Ashraf M (2019). Trehalose: a key organic osmolyte effectively involved in plant abiotic stress tolerance. J Plant Growth Regul 38, 606-618. DOI URL
49	Kretzschmar T, Pelayo MAF, Trijatmiko KR, Gabunada LFM, Alam R, Jimenez R, Mendioro MS, Slamet- Loedin IH, Sreenivasulu N, Bailey-Serres J, Ismail AM, Mackill DJ, Septiningsih EM (2015). A trehalose-6- phosphate phosphatase enhances anaerobic germination tolerance in rice. Nat Plants 1, 15124. DOI PMID
50	Ku MSB, Agarie S, Nomura M, Fukayama H, Tsuchida H, Ono K, Hirose S, Toki S, Miyao M, Matsuoka M (1999). High-level expression of maize phosphoenolpyruvate carboxylase in transgenic rice plants. Nat Biotechnol 17, 76-80. PMID
51	Latzko E, Kelly GJ (1983). The many-faceted function of phosphoenolpyruvate carboxylase in C₃ plants. Physiol Végét 21, 805-815.
52	Li CX, Shen HY, Wang T, Wang XL (2015). ABA regulates subcellular redistribution of OsABI-LIKE2, a negative regulator in ABA signaling, to control root architecture and drought resistance in Oryza sativa. Plant Cell Physiol 56, 2396-2408. DOI URL
53	Li X, Wang C, Ren CG (2011). Effects of 1-butanol, neomycin and calcium on the photosynthetic characteristics of pepc transgenic rice. Afr J Biotechnol 10, 17466-17476.
54	Li ZW, Zhao Q, Cheng FM (2020). Sugar starvation enhances leaf senescence and genes involved in sugar signaling pathways regulate early leaf senescence in mutant rice. Rice Sci 27, 201-204. DOI URL
55	Liu T, Ye XL, Li M, Li JM, Qi HY, Hu XH (2020). H₂O₂ and NO are involved in trehalose-regulated oxidative stress tolerance in cold-stressed tomato plants. Environ Exp Bot 171, 103961. DOI URL
56	Liu XL, Li X, Dai CC, Zhou JY, Yan T, Zhang JF (2017a). Improved short-term drought response of transgenic rice over-expressing maize C₄ phosphoenolpyruvate carboxylase via calcium signal cascade. J Plant Physiol 218, 206-221. DOI URL
57	Liu XL, Li X, Zhang C, Dai CC, Zhou JY, Ren CG, Zhang JF (2017b). Phosphoenolpyruvate carboxylase regulation in C₄-PEPC expressing transgenic rice during early responses to drought stress. Physiol Plantarum 159, 178-200. DOI URL
58	Livak KJ, Schmittgen TD (2002). Analysis of relative gene expression data using real-time quantitative PCR. Methods 25, 402-408. DOI URL
59	Lunn JE, Delorge I, Figueroa CM, van Dijck P, Stitt M (2014). Trehalose metabolism in plants. Plant J 79, 544-567. DOI URL
60	Mamedov TG, Moellering ER, Chollet R (2005). Identification and expression analysis of two inorganic C- and N- responsive genes encoding novel and distinct molecular forms of eukaryotic phosphoenolpyruvate carboxylase in the green microalga Chlamydomonas reinhardtii. Plant J 42, 832-843. PMID
61	Matsuoka M, Minami EI (1989). Complete structure of the gene for phosphoenolpyruvate carboxylase from maize. Eur J Biochem 181, 593-598. PMID
62	Morales F, Ancín M, Fakhet D, González-Torralba J, Gámez AL, Seminario A, Soba D, Ben Mariem S, Garriga M, Aranjuelo I (2020). Photosynthetic metabolism under stressful growth conditions as a bases for crop breeding and yield improvement. Plants 9, 88. DOI URL
63	Murphy ME, Noack E (1994). Nitric oxide assay using hemoglobin method. Method Enzymol 233, 240. PMID
64	Nakano Y, Asada K (1981). Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22, 867-880.
65	Noctor G, Reichheld JP, Foyer CH (2018). ROS-related redox regulation and signaling in plants. Semin Cell Dev Biol 80, 3-12. DOI URL
66	Oladosu Y, Rafii MY, Samuel C, Fatai A, Magaji U, Kareem I, Kamarudin ZS, Muhammad I, Kolapo K (2019). Drought resistance in rice from conventional to molecular breeding: a review. Intl J Mol Sci 20, 3519. DOI URL
67	Pramanik MHR, Imai R (2005). Functional identification of a trehalose 6-phosphate phosphatase gene that is involved in transient induction of trehalose biosynthesis during chilling stress in rice. Plant Mol Biol 58, 751-762. DOI PMID
68	Qian BY, Li X, Liu XL, Chen PB, Ren CG, Dai CC (2015a). Enhanced drought tolerance in transgenic rice over-expressing of maize C₄ phosphoenolpyruvate carboxylase gene via NO and Ca ²+ . J Plant Physiol 175, 9-20. DOI URL
69	Qian BY, Li X, Liu XL, Wang M (2015b). Improved oxidative tolerance in suspension-cultured cells of C₄-pepc transgenic rice by H₂O₂ and Ca ²+ under PEG-6000. J Integr Plant Biol 57, 534-539. DOI URL
70	Ren CG, Li X, Liu XL, Wei XD, Dai CC (2014). Hydrogen peroxide regulated photosynthesis in C₄-pepc transgenic rice. Plant Physiol Biochem 74, 218-229. DOI URL
71	Sadak MS (2016). Mitigation of drought stress on fenugreek plant by foliar application of trehalose. Int J ChemTech Res 9, 147-155.
72	Samadi S, Habibi G, Vaziri A (2019). Exogenous trehalose alleviates the inhibitory effects of salt stress in strawberry plants. Acta Physiol Plant 41, 112. DOI URL
73	Schaffer AA, Petreikov M (1997). Sucrose-to-starch metabolism in tomato fruit undergoing transient starch accumulation. Plant Physiol 113, 739-746. DOI URL
74	Shahbaz M, Abid A, Masood A, Waraich EA (2017). Foliar-applied trehalose modulates growth, mineral nutrition, photosynthetic ability, and oxidative defense system of rice (Oryza sativa L.) under saline stress. J Plant Nutr 40, 584-599. DOI URL
75	Shi JH, Yi KK, Liu Y, Xie L, Zhou ZJ, Chen Y, Hu ZH, Zheng T, Liu RH, Chen YL, Chen JQ (2015). Phospho enol pyruvate carboxylase in Arabidopsis leaves plays a crucial role in carbon and nitrogen metabolism. Plant Physiol 167, 671-681. DOI URL
76	Simon NML, Kusakina J, Fernández-López Á, Chembath A, Belbin FE, Dodd AN (2018). The energy-signaling hub SnRK1 is important for sucrose-induced hypocotyl elongation. Plant Physiol 176, 1299-1310. DOI URL
77	Smart RE, Bingham GE (1974). Rapid estimates of relative water content. Plant Physiol 53, 258-260. PMID
78	Sun SJ, Qi GN, Gao QF, Wang HQ, Yao FY, Hussain J, Wang YF (2016). Protein kinase OsSAPK8 functions as an essential activator of S-type anion channel OsSLAC1, which is nitrate-selective in rice. Planta 243, 489-500. DOI URL
79	Tachibaana S, Konishi N, Kanda H (1991). Diurnal variation of in vivo and in vitro nitrate reductase activity in cucumber plants. J Jap Soc Hortic Sci 60, 593-599. DOI URL
80	Tang YT, Li X, Lu W, Wei XD, Zhang QJ, Lv CG, Song NX (2018). Enhanced photorespiration in transgenic rice over-expressing maize C₄ phosphoenolpyruvate carboxylase gene contributes to alleviating low nitrogen stress. Plant Physiol Biochem 130, 577-588. DOI URL
81	Theerakulp P, Phongngarm S (2013). Alleviation of adverse effects of salt stress on rice seedlings by exogenous trehalose. Asian J Crop Sci 5, 405-415. DOI URL
82	Tian LF, Xie ZJ, Lu CQ, Hao XH, Wu S, Huang Y, Li DP, Chen LB (2019). The trehalose-6-phosphate synthase TPS5 negatively regulates ABA signaling in Arabidopsis thaliana. Plant Cell Rep 38, 869-882. DOI URL
83	Uzilday B, Turkan I, Ozgur R, Sekmen AH (2014). Strategies of ROS regulation and antioxidant defense during transition from C₃ to C₄ photosynthesis in the genus Flaveria under PEG-induced osmotic stress. J Plant Physiol 171, 65-75. DOI URL
84	Velikova V, Yordanov I, Edreva A (2000). Oxidative stress and some antioxidant systems in acid rain-treated bean plants. Plant Sci 151, 59-66. DOI URL
85	Vishal B, Krishnamurthy P, Ramamoorthy R, Kumar PP (2019). OsTPS8 controls yield-related traits and confers salt stress tolerance in rice by enhancing suberin deposition. New Phytol 221, 1369-1386. DOI URL
86	Wang PC, Zhu JK, Lang ZB (2015). Nitric oxide suppresses the inhibitory effect of abscisic acid on seed germination by S-nitrosylation of SnRK2 proteins. Plant Signal Behav 10, e1031939. DOI URL
87	Wang WJ, Chen QB, Xu SM, Liu WC, Zhu XH, Song CP (2020a). Trehalose-6-phosphate phosphatase E modulates ABA-controlled root growth and stomatal movement inArabidopsis. J Integr Plant Biol 62, 1518-1534. DOI URL
88	Wang Y, Wang LP, Micallef BJ, Tetlow IJ, Mullen RT, Feil R, Lunn JE, Emes MJ (2020b). AKINβ1, a subunit of SnRK1, regulates organic acid metabolism and acts as a global modulator of genes involved in carbon, lipid, and nitrogen metabolism. J Exp Bot 71, 1010-1028.
89	Wingler A (2018). Transitioning to the next phase: the role of sugar signaling throughout the plant life cycle. Plant Physiol 176, 1075-1084. DOI URL
90	Yang A, Dai XY, Zhang WH (2012). A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice. J Exp Bot 63, 2541-2556. DOI URL
91	Yoshida S, Forno DA, Cock J (1971). Laboratory Manual for Physiological Studies of Rice. Los Banos: International Rice Research Institute. pp. 62.
92	Yu WQ, Zhao RR, Wang L, Zhang SJ, Li R, Sheng JP, Shen L (2019). ABA signaling rather than ABA metabolism is involved in trehalose-induced drought tolerance in tomato plants. Planta 250, 643-655. DOI URL
93	Zang BS, Li HW, Li WJ, Deng XW, Wang XP (2011). Analysis of trehalose-6-phosphate synthase (TPS) gene family suggests the formation of TPS complexes in rice. Plant Mol Biol 76, 507-522. DOI URL
94	Zhai ZY, Keereetaweep J, Liu H, Feil R, Lunn JE, Shanklin J (2018). Trehalose 6-phosphate positively regulates fatty acid synthesis by stabilizing WRINKLED. Plant Cell 30, 2616-2627. DOI URL
95	Zhang C, Li X, He YF, Zhang JF, Yan T, Liu XL (2017). Physiological investigation of C₄-phosphoenolpyruvate-carboxylase-introduced rice line shows that sucrose metabolism is involved in the improved drought tolerance. Plant Physiol Biochem 115, 328-342. DOI URL
96	Zhang C, Peng X, Guo XF, Tang GJ, Sun FL, Liu SD, Xi YJ (2018). Transcriptional and physiological data reveal the dehydration memory behavior in switchgrass ( Panicum virgatum L.). Biotechnol Biofuels 11, 91. DOI PMID
97	Zhao RQ (2019). Expression, purification and characterization of the plant Snf1-related protein kinase 1 from Escherichia coli. Protein Expr Purif 162, 24-31. DOI URL
98	Zhong RL, Wang YX, Gai RN, Xi DD, Mao CJ, Feng M (2020). Rice SnRK protein kinase OsSAPK8 acts as a positive regulator in abiotic stress responses. Plant Sci 292, 110373. DOI URL
99	Zhu G, Ye N, Zhang J (2009). Glucose-induced delay of seed germination in rice is mediated by the suppression of ABA catabolism rather than an enhancement of ABA biosynthesis. Plant Cell Physiol 50, 644-651. DOI URL

[1]	龙吉兰蒋铮刘定琴缪宇轩周灵燕冯颖裴佳宁刘瑞强周旭辉伏玉玲. 干旱下植物根系分泌物及其介导的根际激发效应研究进展[J]. 植物生态学报, 2024, 48(预发表): 0-0.
[2]	朱宝, 赵江哲, 张可伟, 黄鹏. 水稻细胞分裂素氧化酶9参与调控水稻叶夹角发育[J]. 植物学报, 2024, 59(1): 0-0.
[3]	方妍力, 田传玉, 苏如意, 刘亚培, 王春连, 陈析丰, 郭威, 纪志远. 水稻抗细菌性条斑病基因的挖掘与初定位[J]. 植物学报, 2024, 59(1): 0-0.
[4]	贾绮玮, 钟芊芊, 顾育嘉, 陆天麒, 李玮, 杨帅, 朱超宇, 胡程翔, 李三峰, 王跃星, 饶玉春. 水稻茎秆细胞壁相关组分含量QTL定位及候选基因分析[J]. 植物学报, 2023, 58(6): 882-892.
[5]	田传玉, 方妍力, 沈晴, 王宏杰, 陈析丰, 郭威, 赵开军, 王春连, 纪志远. 2019-2021年我国南方稻区白叶枯病菌的毒力与遗传多样性调查研究[J]. 植物学报, 2023, 58(5): 743-749.
[6]	张盈川, 吴晓明玉, 陶保龙, 陈丽, 鲁海琴, 赵伦, 文静, 易斌, 涂金星, 傅廷栋, 沈金雄. Bna-miR43介导甘蓝型油菜响应干旱胁迫[J]. 植物学报, 2023, 58(5): 701-711.
[7]	戴若惠, 钱心妤, 孙静蕾, 芦涛, 贾绮玮, 陆天麒, 路梅, 饶玉春. 水稻叶色调控机制及相关基因研究进展[J]. 植物学报, 2023, 58(5): 799-812.
[8]	孙尚, 胡颖颖, 韩阳朔, 薛超, 龚志云. 水稻染色体双链寡核苷酸荧光原位杂交技术[J]. 植物学报, 2023, 58(3): 433-439.
[9]	金佳怡, 罗怿婷, 杨惠敏, 芦涛, 叶涵斐, 谢继毅, 王珂欣, 陈芊羽, 方媛, 王跃星, 饶玉春. 水稻叶绿素含量QTL定位与候选基因表达分析[J]. 植物学报, 2023, 58(3): 394-403.
[10]	严语萍, 俞晓琦, 任德勇, 钱前. 水稻穗粒数遗传机制与育种利用[J]. 植物学报, 2023, 58(3): 359-372.
[11]	刘裕强, 万建民. 寄主监控昆虫唾液蛋白平衡植物抗性与生长发育[J]. 植物学报, 2023, 58(3): 353-355.
[12]	王琪, 吴允哲, 刘学英, 孙丽莉, 廖红, 傅向东. 类受体激酶调控水稻生长发育和环境适应研究进展[J]. 植物学报, 2023, 58(2): 199-213.
[13]	陈图强, 徐贵青, 刘深思, 李彦. 干旱胁迫下梭梭水力性状调整与非结构性碳水化合物动态[J]. 植物生态学报, 2023, 47(10): 1407-1421.
[14]	周洁, 杨晓东, 王雅芸, 隆彦昕, 王妍, 李浡睿, 孙启兴, 孙楠. 梭梭和骆驼刺对干旱的适应策略差异[J]. 植物生态学报, 2022, 46(9): 1064-1076.
[15]	刘晓龙, 季平, 杨洪涛, 丁永电, 付佳玲, 梁江霞, 余聪聪. 脱落酸对水稻抽穗开花期高温胁迫的诱抗效应[J]. 植物学报, 2022, 57(5): 596-610.

外源海藻糖增强高表达转玉米C₄型PEPC水稻耐旱性的机制

Mechanism on Drought Tolerance Enhanced by Exogenous Trehalose in C₄-PEPC Rice

RichHTML

PDF (PC)

补充材料

可视化

被引次数

摘要/Abstract

引用本文

使用本文

图/表 8

参考文献 99

相关文章 15

编辑推荐

Metrics

本文评价