SUPEROXIDE DISMUTASE FAMILY GENES IN WATERMELON AND THEIR RESPONSES TO DIFFERENT ABIOTIC STRESSES

doi:10.15302/J-FASE-2020350

Front. Agr. Sci. Eng.

2021, Vol. 8

Issue (4) : 645-658 https://doi.org/10.15302/J-FASE-2020350

RESEARCH ARTICLE

SUPEROXIDE DISMUTASE FAMILY GENES IN WATERMELON AND THEIR RESPONSES TO DIFFERENT ABIOTIC STRESSES

Yong ZHOU, Linjuan OUYANG, Dahu ZHOU, Yicong CAI, Haohua HE(

)

Key Laboratory of Crop Physiology, Ecology and Genetic Breeding (Ministry of Education), Jiangxi Agricultural University, Nanchang 330045, China.

Download: PDF(2057 KB) HTML
Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks

Abstract

• A total of 8 SOD genes from watermelon were identified and bioinformatically analyzed.

• The SOD proteins from watermelon and other different plant species can be classified into five groups consistent with their metal cofactors.

• ClSOD genes exhibited distinctive tissue-specific and abiotic stress responsive expression patterns.

Superoxide dismutase (SOD) is an important enzyme in the antioxidant system of plants and plays a vital role in stress responses by maintaining the dynamic balance of reactive oxygen species (ROS) concentrations. Genome-wide analysis of the SOD gene family in various plant species has been conducted but little is known about this gene family in watermelon (Citrullus lanatus). Here, eight SOD genes were identified in the watermelon genome and are designated ClCSD1-5, ClFSD1-2 and ClMSD according to their metal cofactors. Phylogenetic analysis shows that SOD proteins from various plant species can be classified into five groups and members in the same group possess the same metal cofactor and similar subcellular localizations. Expression analysis of the ClSOD genes indicates that they had tissue-specific expression patterns with high expression in different tissues including the leaves, flowers and fruit. In addition, the expression of ClSOD genes differed appreciably under salinity, drought and abscisic acid (ABA) treatments, indicating that they may be involved in ROS scavenging under different abiotic stresses via an ABA-dependent signaling pathway. These results lay the foundation for elucidating the function of ClSOD genes in stress tolerance and fruit development in watermelon.

Keywords abiotic stress expression analysis phylogeny SOD superoxide dismutase watermelon

Corresponding Author(s): Haohua HE

Just Accepted Date: 28 June 2020 Online First Date: 02 December 2020 Issue Date: 19 November 2021

Cite this article:

Yong ZHOU,Linjuan OUYANG,Dahu ZHOU, et al. SUPEROXIDE DISMUTASE FAMILY GENES IN WATERMELON AND THEIR RESPONSES TO DIFFERENT ABIOTIC STRESSES[J]. Front. Agr. Sci. Eng. , 2021, 8(4): 645-658.

URL:

https://academic.hep.com.cn/fase/EN/10.15302/J-FASE-2020350
https://academic.hep.com.cn/fase/EN/Y2021/V8/I4/645

Tab.1 Features of SOD family genes identified in watermelon

Fig.1 Phylogenetic analysis of SOD proteins in watermelon and other plant species. The phylogenetic tree was constructed using Clustal Omega and MEGA 7.0 by the neighbor-joining method with 1000 bootstrap repeats. The protein sequences used for creation of the phylogenetic tree are listed in Table S2. Cl, Citrullus lanatus; At, Arabidopsis thaliana; Sl, Solanum lycopersicum; Cs, Cucumis sativus; Mt, Medicago truncatula; Sb, Sorghum bicolor; Bd, Brachypodium distachyon.

Fig.2 (a) Phylogenetic relationships, (b) structures and (c) conserved motifs of watermelon SOD proteins. Multiple alignments were conducted with Clustal Omega using full-length watermelon SOD protein sequences, and the phylogenetic tree was created with MEGA 7.0 using the NJ method with bootstrap tests repeated 1000 times. The colored boxes indicate different conserved motifs, and their positions in each watermelon SOD protein sequence are displayed proportionally.

Fig.3 Multiple sequence alignment of ClSOD protein sequences. Two conserved Cu/ZnSOD signatures (GFH[VLI]H[AES][LY]GDTT and GNAG[EGA]R[ILV][CAG]CG) are indicated with the red box. The metal binding sites of Cu/ZnSODs for Cu²⁺ and Zn²⁺ are indicated with red arrows. The conserved FeSOD signature (AQ[VI]WNHDF[FL]WES) and metal binding domain (D[MV]WEHAYY) are boxed with blue and brown, respectively. Two conserved His residues in FeSODs are indicated with blue, while six conserved residues (His, Phe, Gln and Asp) are indicated with blue boxes.

Fig.4 Exon-intron structure of watermelon SOD genes based on the phylogenetic relationship. Exons and introns are indicated by blue boxes and black lines, respectively, and their lengths in each gene are displayed proportionally.

Fig.5 Chromosomal locations of the watermelon SOD genes. Segmentally duplicated SOD genes are indicated in red.

Fig.6 Distribution of stress- and hormone-responsive elements in 1-kb promoter regions of ClSOD genes. LTR, low temperature-responsive element; MBS, MYB binding site involved in drought-inducibility; W-box, WRKY binding site involved in abiotic stress and defense response; ARE, cis-element essential for the anaerobic induction; WUN-motif, wound-responsive element; TC-rich repeats, cis-element involved in defense and stress responsiveness; ABRE, ABA-responsive element; ERE, ethylene-responsive element; CGTCA-motif, MeJA-responsive element; TCA-element, salicylic acid-responsive element; TGA-element, auxin-responsive element; P-box and TATC-box, gibberellin-responsive element.

Fig.7 Expression patterns of selected ClSOD genes (a) in watermelon tissues and (b) during fruit development. L, leaves; R, roots; S, stems; Fr, fruits; F, flowers; FF and FR are fruit flesh and fruit rind at 10, 18, 26, and 34 days after pollination, respectively. For transcriptome analysis the gene expression levels were calculated with the logarithmic method involving log₂(RPKM+ 1).

Fig.8 Expression pattern analysis of ClSOD genes in response to salinity stress. Mean values with the same letters above the bars are not significantly different (Tukey’s multiple range tests, P<0.05) for different treatment elapsed times.

Fig.9 Expression patterns of ClSOD genes under drought treatment determined by qRT-PCR. Mean values with the same letter above the bars are not significantly different (Tukey’s multiple range tests, P<0.05) between different treatment elapsed times.

Fig.10 Expression pattern analysis of ClSOD genes in response to ABA treatment. Different mean values with the same letter above the bars are not significantly different (Tukey’s multiple range tests, P<0.05) between different treatment elapsed times.

1	Y Zhou, L F Hu, S F Ye, L W Jiang, S Q Liu. Molecular cloning and functional characterization of a Cu/Zn superoxide dismutase gene (CsCSD1) from Cucumis sativus. Plant Cell, Tissue and Organ Culture, 2018, 135(2): 309–319 https://doi.org/10.1007/s11240-018-1465-y
2	G R Cramer, K Urano, S Delrot, M Pezzotti, K Shinozaki. Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biology, 2011, 11(1): 163 https://doi.org/10.1186/1471-2229-11-163 pmid: 22094046
3	C Waszczak, M Carmody, J Kangasjärvi. Reactive oxygen species in plant signaling. Annual Review of Plant Biology, 2018, 69(1): 209–236 https://doi.org/10.1146/annurev-arplant-042817-040322 pmid: 29489394
4	F K Choudhury, R M Rivero, E Blumwald, R Mittler. Reactive oxygen species, abiotic stress and stress combination. Plant Journal, 2017, 90(5): 856–867 https://doi.org/10.1111/tpj.13299 pmid: 27801967
5	P Ahmad, C A Jaleel, M A Salem, G Nabi, S Sharma. Roles of enzymatic and nonenzymatic antioxidants in plants during abiotic stress. Critical Reviews in Biotechnology, 2010, 30(3): 161–175 https://doi.org/10.3109/07388550903524243 pmid: 20214435
6	J Zhang, B Li, Y Yang, W Hu, F Chen, L Xie, L Fan. Genome-wide characterization and expression profiles of the superoxide dismutase gene family in Gossypium. International Journal of Genomics, 2016, 2016: 8740901 https://doi.org/10.1155/2016/8740901 pmid: 27660755
7	A Mhamdi, F Van Breusegem. Reactive oxygen species in plant development. Development, 2018, 145(15): dev164376 https://doi.org/10.1242/dev.164376 pmid: 30093413
8	S S Gill, N A Anjum, R Gill, S Yadav, M Hasanuzzaman, M Fujita, P Mishra, S C Sabat, N Tuteja. Superoxide dismutase--mentor of abiotic stress tolerance in crop plants. Environmental Science and Pollution Research International, 2015, 22(14): 10375–10394 https://doi.org/10.1007/s11356-015-4532-5 pmid: 25921757
9	J B Song, L M Zeng, R R Chen, Y H Wang, Y Zhou. In silico identification and expression analysis of superoxide dismutase (SOD) gene family in Medicago truncatula. 3 Biotech, 2018, 8(8): 348
10	Y Sheng, I A Abreu, D E Cabelli, M J Maroney, A F Miller, M Teixeira, J S Valentine. Superoxide dismutases and superoxide reductases. Chemical Reviews, 2014, 114(7): 3854–3918 https://doi.org/10.1021/cr4005296 pmid: 24684599
11	R G Alscher, N Erturk, L S Heath. Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. Journal of Experimental Botany, 2002, 53(372): 1331–1341 https://doi.org/10.1093/jexbot/53.372.1331 pmid: 11997379
12	M Pilon, K Ravet, W Tapken. The biogenesis and physiological function of chloroplast superoxide dismutases. Biochimica et Biophysica Acta, 2011, 1807(8): 989–998 https://doi.org/10.1016/j.bbabio.2010.11.002 pmid: 21078292
13	K Feng, J Yu, Y Cheng, M Ruan, R Wang, Q Ye, G Zhou, Z Li, Z Yao, Y Yang, Q Zheng, H Wan. The SOD gene family in tomato: identification, phylogenetic relationships, and expression patterns. Frontiers in Plant Science, 2016, 7: 1279 https://doi.org/10.3389/fpls.2016.01279 pmid: 27625661
14	W Wang, X Zhang, F Deng, R Yuan, F Shen. Genome-wide characterization and expression analyses of superoxide dismutase (SOD) genes in Gossypium hirsutum. BMC Genomics, 2017, 18(1): 376 https://doi.org/10.1186/s12864-017-3768-5 pmid: 28499417
15	Y Zhou, L Hu, H Wu, L Jiang, S Liu. Genome-wide identification and transcriptional expression analysis of cucumber superoxide dismutase (SOD) family in response to various abiotic stresses. International Journal of Genomics, 2017, 2017: 7243973 https://doi.org/10.1155/2017/7243973 pmid: 28808654
16	T Wang, H Song, B H Zhang, Q W Lu, Z Liu, S L Zhang, R L Guo, C Wang, Z L Zhao, J R Liu, R H Peng. Genome-wide identification, characterization, and expression analysis of superoxide dismutase (SOD) genes in foxtail millet (Setaria italica L.). 3 Biotech, 2018, 8(12): 486
17	L B Wang, L Wang, Z Zhang, M Ma, R Z Wang, M Qian, S L Zhang. Genome-wide identification and comparative analysis of the superoxide dismutase gene family in pear and their functions during fruit ripening. Postharvest Biology and Technology, 2018, 143: 68–77 https://doi.org/10.1016/j.postharvbio.2018.04.012
18	X M Han, Q X Chen, Q Yang, Q Y Zeng, T Lan, Y J Liu. Genome-wide analysis of superoxide dismutase genes in Larix kaempferi. Gene, 2019, 686: 29–36 https://doi.org/10.1016/j.gene.2018.10.089 pmid: 30389562
19	C Zhou, C Zhu, H Fu, X Li, L Chen, Y Lin, Z Lai, Y Guo. Genome-wide investigation of superoxide dismutase (SOD) gene family and their regulatory miRNAs reveal the involvement in abiotic stress and hormone response in tea plant (Camellia sinensis). PLoS One, 2019, 14(10): e0223609 https://doi.org/10.1371/journal.pone.0223609 pmid: 31600284
20	W Jiang, L Yang, Y He, H Zhang, W Li, H Chen, D Ma, J Yin. Genome-wide identification and transcriptional expression analysis of superoxide dismutase (SOD) family in wheat (Triticum aestivum). PeerJ, 2019, 7: e8062 https://doi.org/10.7717/peerj.8062 pmid: 31763072
21	Q Zhou, Q Cai. The superoxide dismutase genes might be required for appropriate development of the ovule after fertilization in Xanthoceras sorbifolium. Plant Cell Reports, 2018, 37(5): 727–739 https://doi.org/10.1007/s00299-018-2263-z pmid: 29387898
22	G Bresciani, I B da Cruz, J González-Gallego. Manganese superoxide dismutase and oxidative stress modulation. Advances in Clinical Chemistry, 2015, 68: 87–130 https://doi.org/10.1016/bs.acc.2014.11.001 pmid: 25858870
23	S Tounsi, K Feki, Y Kamoun, M N Saïdi, S Jemli, M Ghorbel, C Alcon, F Brini. Highlight on the expression and the function of a novel MnSOD from diploid wheat (T. monococcum) in response to abiotic stress and heavy metal toxicity. Plant Physiology and Biochemistry, 2019, 142: 384–394 https://doi.org/10.1016/j.plaphy.2019.08.001 pmid: 31401434
24	H Wu, R Li, Y Liu, X Zhang, J Zhang, E Ma. A second intracellular copper/zinc superoxide dismutase and a manganese superoxide dismutase in Oxya chinensis: molecular and biochemical characteristics and roles in chlorpyrifos stress. Ecotoxicology and Environmental Safety, 2020, 187: 109830 https://doi.org/10.1016/j.ecoenv.2019.109830 pmid: 31648074
25	J H Wu, J Zhang, X Li, J J Xu, L Wang. Identification and characterization of a PutCu/Zn-SOD gene from Puccinellia tenuiflora (Turcz.) Scribn. et Merr. Plant Growth Regulation, 2016, 79(1): 55–64 https://doi.org/10.1007/s10725-015-0110-6
26	Q Guan, X Liao, M He, X Li, Z Wang, H Ma, S Yu, S Liu. Tolerance analysis of chloroplast OsCu/Zn-SOD overexpressing rice under NaCl and NaHCO3 stress. PLoS One, 2017, 12(10): e0186052 https://doi.org/10.1371/journal.pone.0186052 pmid: 29020034
27	Y Yang, G J Ahammed, C Wan, H Liu, R Chen, Y Zhou. Comprehensive analysis of TIFY transcription factors and their expression profiles under jasmonic acid and abiotic stresses in watermelon. International Journal of Genomics, 2019, 2019: 6813086 https://doi.org/10.1155/2019/6813086 pmid: 31662958
28	H Li, Y Mo, Q Cui, X Yang, Y Guo, C Wei, J Yang, Y Zhang, J Ma, X Zhang. Transcriptomic and physiological analyses reveal drought adaptation strategies in drought-tolerant and-susceptible watermelon genotypes. Plant Science, 2019, 278: 32–43 https://doi.org/10.1016/j.plantsci.2018.10.016 pmid: 30471727
29	H Li, J Chang, H Chen, Z Wang, X Gu, C Wei, Y Zhang, J Ma, J Yang, X Zhang. Exogenous melatonin confers salt stress tolerance to watermelon by improving photosynthesis and redox homeostasis. Frontiers in Plant Science, 2017, 8: 295 https://doi.org/10.3389/fpls.2017.00295 pmid: 28298921
30	D J Kliebenstein, R A Monde, R L Last. Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization. Plant Physiology, 1998, 118(2): 637–650 https://doi.org/10.1104/pp.118.2.637 pmid: 9765550
31	K Nath, S Kumar, R S Poudyal, Y N Yang, R Timilsina, Y S Park, J Nath, P S Chauhan, B Pant, C H Lee. Developmental stage-dependent differential gene expression of superoxide dismutase isoenzymes and their localization and physical interaction network in rice (Oryza sativa L.). Genes & Genomics, 2014, 36(1): 45–55 https://doi.org/10.1007/s13258-013-0138-9
32	C J Chen, R Xia, H Chen, Y H He. TBtools, a Toolkit for Biologists integrating various biological data handling tools with a user-friendly interface. bioRxiv, 2018, 289660 https://doi.org/10.1101/289660
33	F Sievers, D G Higgins. Clustal Omega for making accurate alignments of many protein sequences. Protein Science, 2018, 27(1): 135–145 https://doi.org/10.1002/pro.3290 pmid: 28884485
34	S Kumar, G Stecher, K Tamura. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 2016, 33(7): 1870–1874 https://doi.org/10.1093/molbev/msw054 pmid: 27004904
35	Y Wang, H Tang, J D Debarry, X Tan, J Li, X Wang, T H Lee, H Jin, B Marler, H Guo, J C Kissinger, A H Paterson. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Research, 2012, 40(7): e49 https://doi.org/10.1093/nar/gkr1293 pmid: 22217600
36	Y Ren, S Guo, J Zhang, H He, H Sun, S Tian, G Gong, H Zhang, A Levi, Y Tadmor, Y Xu. A tonoplast sugar transporter underlies a sugar accumulation QTL in watermelon. Plant Physiology, 2018, 176(1): 836–850 https://doi.org/10.1104/pp.17.01290 pmid: 29118248
37	E Filiz, I Koc, I I Ozyigit. Comparative analysis and modeling of superoxide dismutases (SODs) in Brachypodium distachyon L. Applied Biochemistry and Biotechnology, 2014, 173(5): 1183–1196 https://doi.org/10.1007/s12010-014-0922-2 pmid: 24781980
38	E Filiz, H Tombuloğlu. Genome-wide distribution of superoxide dismutase (SOD) gene families in Sorghum bicolor. Turkish Journal of Biology, 2015, 39(1): 49–59 https://doi.org/10.3906/biy-1403-9
39	D L Guo, X R Ji, Q Li, G H Zhang, Y H Yu. Genome-wide characterisation of superoxide dismutase genes in grape and their expression analyses during berry development process. Journal of Horticultural Science & Biotechnology, 2020, 95(1): 53–64 https://doi.org/10.1080/14620316.2019.1647799
40	K H Lin, S C Sei, Y H Su, C M Chiang. Overexpression of the Arabidopsis and winter squash superoxide dismutase genes enhances chilling tolerance via ABA-sensitive transcriptional regulation in transgenic Arabidopsis. Plant Signaling & Behavior, 2019, 14(12): 1685728 https://doi.org/10.1080/15592324.2019.1685728 pmid: 31680612

[1]		Download
[2]		Download
[3]		Download
[4]		Download

[1]	Tonglu WEI, Dalong GUO, Jihong LIU. *OVEREXPRESSION OF PTRLEA7, A LATE EMBRYOGENESIS ABUNDANT FAMILY GENE FROM PONCIRUS TRIFOLIATA, CONFERS ENHANCED DROUGHT TOLERANCE BY ENHANCING ANTIOXIDANT CAPACITY*[J]. Front. Agr. Sci. Eng. , 2021, 8(2): 236-246.
[2]	Alexey MORGOUNOV, Fatih OZDEMIR, Mesut KESER, Beyhan AKIN, Thomas PAYNE, Hans-Joachim BRAUN. International Winter Wheat Improvement Program: history, activities, impact and future[J]. Front. Agr. Sci. Eng. , 2019, 6(3): 240-250.
[3]	Shilei ZHENG, Jingru ZHU, Jiao LI, Shuang ZHANG, Yunfei MA. Leonurine protects ischemia-induced brain injury via modulating SOD, MDA and GABA levels[J]. Front. Agr. Sci. Eng. , 2019, 6(2): 197-205.
[4]	Yu WANG,Jie ZHOU,Jingquan YU. The critical role of autophagy in plant responses to abiotic stresses[J]. Front. Agr. Sci. Eng. , 2017, 4(1): 28-36.
[5]	Hongxia MIAO,Peiguang SUN,Yulu MIAO,Juhua LIU,Jianbin ZHANG,Caihong JIA,Jingyi WANG,Zhuo WANG,Zhiqiang JIN,Biyu XU. Genome-wide identification and expression analysis of the β-amylase genes strongly associated with fruit development, ripening, and abiotic stress response in two banana cultivars[J]. Front. Agr. Sci. Eng. , 2016, 3(4): 346-356.
[6]	Yang SONG,Chen ZHU,Waseem RAZA,Dongsheng WANG,Qiwei HUANG,Shiwei GUO,Ning LING,Qirong SHEN. Coupling of the chemical niche and microbiome in the rhizosphere: implications from watermelon grafting[J]. Front. Agr. Sci. Eng. , 2016, 3(3): 249-262.

Viewed

Full text

Abstract

Cited

Shared

Discussed