Overexpression of PeAnn1 from Populus euphratica negatively regulates drought resistance in transgenic Arabidopsis thaliana

Wu Xia; Zhang Yinan; Zhao Nan; Zhang Ying; Zhao Rui; Li Jinke; Zhou Xiaoyang; Chen Shaoliang

doi:10.12171/j.1000-1522.20200031

Journal of Beijing Forestry University > 2020 > 42(6): 14-25. > DOI: 10.12171/j.1000-1522.20200031

Wu Xia, Zhang Yinan, Zhao Nan, Zhang Ying, Zhao Rui, Li Jinke, Zhou Xiaoyang, Chen Shaoliang. Overexpression of PeAnn1 from Populus euphratica negatively regulates drought resistance in transgenic Arabidopsis thaliana[J]. Journal of Beijing Forestry University, 2020, 42(6): 14-25. DOI: 10.12171/j.1000-1522.20200031

Citation:

PDF (1603 KB)

Overexpression of PeAnn1 from Populus euphratica negatively regulates drought resistance in transgenic Arabidopsis thaliana

1.
School of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing 100083, China
2.
Public Analysis and Testing Center, Beijing Forestry University, Beijing 100083, China

More Information

Received Date: January 20, 2020
Revised Date: April 27, 2020
Available Online: June 11, 2020
Published Date: June 30, 2020

Graphical Abstract

Abstract

Abstract

ObjectiveAnnexins is a large class of annexin families common in prokaryotes and eukaryotes, and participates in many stress response processes such as oxidative stress, heat stress, drought stress and salt stress. However, the role of Populus euphratica annexin family genes in adapting to adverse conditions is still less known. This paper studies the role of P. euphratica Anneixn1 in osmotic stress and drought resistance.
MethodThe mannitol-induced expression of PeAnn1 was examined in P. euphratica leaves. PeAnn1 sequence was compared with annexin genes from P. tomentosa, Arabidopsis thaliana, Glycine soja, and Oryza sative. Phylogenetic tree of annexins was constructed using MEGA 6 software. PeAnn1-overexpressed A. thaliana (PeAnn1-OE1 and PeAnn1-OE2), Annexin1 mutant (atann1) and wild-type A. thaliana (WT) were used in this study. Plants of each genotype were subjected to increasing osmotic stress caused by different concentrations of mannitol (0, 150, 200, 250, 300 mmol/L), drought, and subsequent water recovery. During the period of water stress, the germination rate, root length, chlorophyll content, and fluorescence parameters, H₂O₂, activity of antioxidant enzymes and expression of encoding genes were examined.
ResultThe short-term mannitol treatment up-regulated the expression of PeAnn1 in P. euphratica leaves. The PeAnn1 sequence displayed higher similarity to P. tomentosa Ann1 (PtAnn1) than other plant species. Phylogenetic analysis revealed that the PeAnn1 was highly homologous to the PtAnn1. The survival rate and root growth of A. thaliana plants were inhibited with increasing concentrations of mannitol, and the inhibition was more pronounced in PeAnn1-overexpressing lines as compared to the WT and mutant (P < 0.05). All the measured photosynthesis parameters, such as chlorophyll content, the maximum photon efficiency of PSⅡ (F_v/F_m), the actual photosynthetic quantum yield (ΦPSⅡ), and the relative electron transfer rate (ETR) were lower in the transgenic plants than in the WT and mutant (P < 0.05). After rehydration, the recovery degree of photosynthetic parameters of PeAnn1-transgenic A. thaliana was also lower than the WT. Under osmotic stress, the activities of antioxidant enzymes, such as SOD, POD, and CAT were significantly lower in PeAnn1-overexpressed plants than those of the WT and mutant. In accordance, the expression of these antioxidant enzyme genes showed a same trend as the activities, which could not remove reactive oxygen species, causing oxidative damage.
ConclusionThe above results indicate that overexpression of PeAnn1 decreases the capacity of A. thaliana in the adaptation to water deficit conditions.
- Populus euphratica,
- annexin protein,
- drought resistance,
- active oxygen,
- transgenic Arabidopsis thaliana

FullText(HTML)

References (38)

References

[1]	Wang W, Vinocur B, Altman A. Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance[J]. Planta, 2003, 218(1): 1−14. doi: 10.1007/s00425-003-1105-5
[2]	Apel K, Hirt H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction[J]. Annual Review of Plant Biology, 2004, 55(1): 373−399. doi: 10.1146/annurev.arplant.55.031903.141701
[3]	Talukdar T, Gorecka K M, De Carvalho-Niebel F, et al. Annexins-calcium and membrane-binding proteins in the plant kingdom: potential role in nodulation and mycorrhization in Medicago truncatula[J]. Acta Biochimica Polonica, 2009, 56(2): 199−210.
[4]	Creutz C E, Pazoles C J, Pollard H B. Identification and purification of an adrenal medulla (synexin) that causes calcium-dependent aggregation of isolated chromamn granules[J]. Journal of Biological Chemistry, 1978, 253(8): 2858−2866.
[5]	Boustead C M, Smallwood M, Small H, et al. Identification of calcium-dependent phospholipid-binding proteins in higher plant cells[J]. FEBS Letters, 1989, 244(2): 456−460. doi: 10.1016/0014-5793(89)80582-4
[6]	Smallwood M P, Keen J N, Bowles D J. Purification and partial sequence analysis of plant annexins[J]. Biochemical Journal, 1990, 270(1): 157−161. doi: 10.1042/bj2700157
[7]	Andrawis A, Solomon M, Delmer D P. Cotton fiber annexins: a potential role in the regulation of callose synthase[J]. Plant Journal, 1993, 3(6): 763−772. doi: 10.1111/j.1365-313X.1993.00763.x
[8]	Seals D F, Parrish M L, Randall S K. A 42-kilodalton annexin-like protein is associated with plant vacuoles[J]. Plant Physiology, 1994, 106(4): 1403−1412. doi: 10.1104/pp.106.4.1403
[9]	Zhou M L, Yang X B, Zhang Q, et al. Induction of annexin by heavy metals and jasmonic acid in Zea mays[J]. Functional and Integrative Genomics, 2013, 13: 241−251.
[10]	Clark G B, Sessions A, Eastburn D J, et al. Differential expression of members of the annexin multigene family in arabidopsis[J]. Plant Physiology, 2001, 126(3): 1072−1084. doi: 10.1104/pp.126.3.1072
[11]	Hashimoto M, Toorchi M, Matsushita K, et al. Proteome analysis of rice root plasma membrane and detection of cold stress responsive proteins[J]. Protein and Peptide Letters, 2009, 16(6): 685−697. doi: 10.2174/092986609788490140
[12]	Yadav D, Boyidi P, Ahmed I, et al. Plant annexins and their involvement in stress responses[J]. Environmental and Experimental Botany, 2018, 155(1): 293−306.
[13]	Kovács I, Ayaydin F, Oberschall A, et al. Immunolocalization of a novel annexin-like protein encoded by a stress and abscisic acid responsive gene in alfalfa[J]. The Plant Journal, 1998, 15(2): 185−197. doi: 10.1046/j.1365-313X.1998.00194.x
[14]	Kreps J A, Wu Y, Chang H S, et al. Transcriptome changes for arabidopsis in response to salt, osmotic, and cold stress[J]. Plant Physiology, 2002, 130(4): 2129−2141. doi: 10.1104/pp.008532
[15]	Cantero A, Barthakur S, Bushart T J, et al. Expression profiling of the arabidopsis annexin gene family during germination, de-etiolation and abiotic stress[J]. Plant Physiology and Biochemistry, 2006, 44(1): 13−24. doi: 10.1016/j.plaphy.2006.02.002
[16]	Lee S, Lee E J, Yang E J, et al. Proteomic identification of annexins, calcium-dependent membrane binding proteins that mediate osmotic stress and abscisic acid signal transduction in arabidopsis[J]. The Plant Cell, 2004, 16(6): 1378−1391. doi: 10.1105/tpc.021683
[17]	Konopka-Postupolska D, Clark G, Goch G, et al. The role of annexin1 in drought stress in arabidopsis[J]. Plant Physiology, 2009, 150(3): 1394−1410. doi: 10.1104/pp.109.135228
[18]	Jami S K, Clark G B, Turlapati S A, et al. Ectopic expression of an annexin from Brassica juncea confers tolerance to abiotic and biotic stress treatments in transgenic tobacco[J]. Plant Physiology and Biochemistry, 2008, 46(12): 1019−1030. doi: 10.1016/j.plaphy.2008.07.006
[19]	Breton G, Vazquez-Tello A, Danyluk J, et al. Two novel intrinsic annexins accumulate in wheat membranes in response to low temperature[J]. Plant and Cell Physiology, 2000, 41(2): 177−184. doi: 10.1093/pcp/41.2.177
[20]	张一南. 胡杨PeAnn1促进转基因拟南芥Cd²⁺内流的分子机制研究[D]. 北京: 北京林业大学, 2018. Zhang Y N. Populus euphratica Annexin1 facilitated Cd²⁺ influx in transgenic arabidopsis under cadmium stress[D]. Beijing: Beijing Forestry University, 2018.
[21]	Zhang H, Deng C, Yao J, et al. Populus euphratica JRL mediates ABA response, ionic and ROS homeostasis in Arabidopsis under salt stress[J/OL]. International Journal of Molecular Sciences, 2019, 20(4): 815 (2019−02−14) [2019−08−20]. https://doi.org/10.3390/ijms20040815.
[22]	Cathcart R, Schwiers E, Ames B N. Detection of picomole levels of hydroperoxides using a fluorescent dichlorofluorescein assay[J]. Analytical Biochemistry, 1983, 134(1): 111−116. doi: 10.1016/0003-2697(83)90270-1
[23]	Trevor E, Kraus R, Austin F. Paclobutrazol protects wheat seedlings from heat and paraquat injury is detoxification of active oxygen involved[J]. Plant and Cell Physiolgy, 1994, 35(1): 45−52.
[24]	Wang R G, Chen S L, Zhou X Y, et al. Ionic homeostasis and reactive oxygen species control in leaves and xylem sap of two poplars subjected to NaCl stress[J]. Tree Physiology, 2008, 28(6): 947−957. doi: 10.1093/treephys/28.6.947
[25]	Wang R G, Chen S L, Deng L, et al. Leaf photosynthesis, fluorescence response to salinity and the relevance to chloroplast salt compartmentation and anti-oxidative stress in two poplars[J]. Trees, 2007, 21(5): 581−591. doi: 10.1007/s00468-007-0154-y
[26]	王瑞, 陈永忠, 陈隆升, 等. 油茶叶片SPAD值与叶绿素含量的相关分析[J]. 中南林业科技大学学报, 2013, 33(2):77−80. Wang R, Chen Y Z, Chen L S, et al. Correlation analysis of SPAD value and chlorophyll content in leaves of Camellia oleifera[J]. Journal of Central South University of Forestry and Technology, 2013, 33(2): 77−80.
[27]	Allan A C, Fluhr R. Two distinct sources of elicited reactive oxygen species in tobacco epidermal cells[J]. The Plant Cell, 1997, 9: 1559−1572. doi: 10.2307/3870443
[28]	Zgallaï H, Steppe K, Lemeur R. Effects of different levels of water stress on leaf water potential, stomatal resistance, protein and chlorophyll content and certain anti-oxidative enzymes in tomato plants[J]. Journal of Integrative Plant Biology, 2006, 48(6): 679−685. doi: 10.1111/j.1744-7909.2006.00272.x
[29]	Wu W M, Li J C, Chen H J, et al. Effects of nitrogen fertilization on chlorophyll fluorescence change in maize (Zea mays L.) under waterlogging at seedling stage[J]. Journal of Food Agriculture and Environment, 2013, 11(1): 545−552.
[30]	Lang Y, Wang M, Zhang G C, et al. Experimental and simulated light responses of photosynthesis in leaves of three tree species under different soil water conditions[J]. Photosynthetica, 2013, 51(3): 370−378. doi: 10.1007/s11099-013-0036-z
[31]	Demmig B, Winter K, Krüger A, et al. Photoinhibition and zeaxanthin formation in intact leaves: a possible role of the xanthophyll cycle in the dissipation of excess light energy[J]. Plant Physiology, 1987, 84(2): 218−224. doi: 10.1104/pp.84.2.218
[32]	Mittler R. Oxidative stress, antioxidants and stress tolerance[J]. Trends in Plant Science, 2002, 7(9): 405−410. doi: 10.1016/S1360-1385(02)02312-9
[33]	张会龙, 武霞, 尧俊, 等. 胡杨PeREM1.3 过表达提高烟草耐盐性的机制[J]. 北京林业大学学报, 2019, 41(1):1−9. Zhang H L, Wu X, Yao J, et al. Overexpression mechanism of PeREM1.3 from Populus euphratica enhancing salt tolerance in transgenic tobacco[J]. Journal of Beijing Forestry University, 2019, 41(1): 1−9.
[34]	陈斌, 王亚男, 马丹炜, 等. 土荆芥化感胁迫对玉米幼根抗氧化酶活性和基因表达的影响[J]. 生态环境学报, 2015, 24(10):1640−1646. Chen B, Wang Y N, Ma D W, et al. The antioxidant enzyme activities and their gene expression in maize radicle under the allelochemical stress from Chenopodium ambrosioides L.[J]. Ecology and Environmental Sciences, 2015, 24(10): 1640−1646.
[35]	Huh S M, Noh E K, Kim H G, et al. Arabidopsis annexins AnnAt1 and AnnAt4 interact with each other and regulate drought and salt stress responses[J]. Plant and Cell Physiology, 2010, 51(9): 1499−1514. doi: 10.1093/pcp/pcq111
[36]	王希, 李勇, 朱延明, 等. 野生大豆胁迫应答膜联蛋白基因的克隆及胁迫耐性分析[J]. 作物学报, 2010, 36(10):1666−1673. Wang X, Li Y, Zhu Y M, et al. Cloning and tolerance analysis of GsANN gene related to response on stress in Glycine soja[J]. The Plant Cell, 2010, 36(10): 1666−1673.
[37]	却志群, 於紫蕾, 沈春修. 水稻膜联蛋白基因OsAnn8干旱和低温条件下表达模式以及CRISPR/Cas9定点编辑[J]. 华北农学报, 2019, 34(1):54−60. Que Z Q, Yu Z L, Shen C X. Expression patterns of Annexin OsAnn8 and CRISPR/Cas9-mediated genome editing of rice under drought and low temperature condition[J]. Acta Agriculturae Boreali-Sinica, 2019, 34(1): 54−60.
[38]	Liao C, Zheng Y, Guo Y. MYB30 transcription factor regulates oxidative and heat stress responses through ANNEXIN-mediated cytosolic calcium signaling in arabidopsis[J]. New Phytologist, 2017, 216(1): 163−177. doi: 10.1111/nph.14679

Cited By

Cited by

Periodical cited type(3)

1.	马思圆，尧俊，李静，安珂悦，赵瑞，赵楠，周晓阳，陈少良. 胡杨PeMAX2调控拟南芥耐旱性. 北京林业大学学报. 2024(06): 106-117 . 本站查看
2.	高鹏飞，高冰，冯郑红，吴建慧. 绢毛委陵菜PsWRKY40的克隆与耐镉功能分析. 园艺学报. 2023(06): 1269-1283 .
3.	侯思源，张会龙，尧俊，张莹，赵楠，赵瑞，周晓阳，陈少良. 胡杨PeREM6.5调控拟南芥水分胁迫耐受机制. 北京林业大学学报. 2022(09): 40-51 . 本站查看

Other cited types(1)

Get Citation

PDF

XML

Article views (1951) PDF downloads (81) Cited by(4)

Turn off MathJax

Article Contents

Abstract

References

Overexpression of PeAnn1 from Populus euphratica negatively regulates drought resistance in transgenic Arabidopsis thaliana

Abstract

References

Cited by

Periodical cited type(3)

Other cited types(1)

Catalog

Export File

Citation

Format

Content