Transcriptomic and physiological evidence for the relationship between unsaturated fatty acid and salt stress in peanut

Frontiers in Plant Science

Volumn 9, Issue , 2018, Pages

  Sui, Na ^a   Wang, Yu ^a   Liu, Shanshan ^a   Yang, Zhen ^a   Wang, Fang ^b   Wan, Shubo ^c  

^a SHANDONG NORMAL UNIVERSITY   (China)

^b SHANDONG AGRICULTURAL UNIVERSITY   (China)

^c SHANDONG PEANUT RESEARCH INSTITUTE   (China)

Author keywords

Peanut; Salt stress; Transcriptomic profile; Unsaturated fatty acid; 3 fatty acid desaturase

Indexed keywords

EID: 85043394162     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2018.00007     Document Type: Article

References (75)

1. Allakhverdiev, S. I., Kinoshita, M., Inaba, M., Suzuki, I., and Murata, N. (2001). Unsaturated fatty acids in membrane lipids protect the photosynthetic machinery against salt-induced damage in Synechococcus. Plant Physiol. 125, 1842–1853. doi: 10.1104/pp.125.4.1842
2. Allakhverdiev, S. I., Nishiyama, Y., Suzuki, I., Tasaka, Y., and Murata, N. (1999). Genetic engineering of the unsaturation of fatty acids in membrane lipids alters the tolerance of Synechocystis to salt stress. Proc. Natl. Acad. Sci. U.S.A. 96, 5562–5567. doi: 10.1073/pnas.96.10.5862
3. Apel, K., and Hirt, H. (2004). Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373–399. doi: 10.1146/annurev.arplant.55.031903.141701
4. Apweiler, R., Bairoch, A., Wu, C. H., Barker, W. C., Boeckmann, B., Ferro, S., et al. (2004). UniProt: the universal protein knowledgebase. Nucleic Acids Res. 32, 115–119. doi: 10.1093/nar/gkh131
5. Bhunia, R. K., Chakraborty, A., Kaur, R., Maiti, M. K., and Sen, S. K. (2016). Enhancement of α-linolenic acid content in transgenic tobacco seeds by targeting a plastidial ω-3 fatty acid desaturase (fad7) gene of Sesamum indicum to ER. Plant Cell Rep. 35, 213–226. doi: 10.1007/s00299-015-1880-z
6. Carillo, P., Annunziata, M. G., Pontecorvo, G., Fuggi, A., and Woodrow, P. (2011). “Salinity stress and salt tolerance,” in Abiotic Stress in Plants - Mechanisms and Adaptations, eds A. Shanker and B. Venkateswarlu (INTECH). doi: 10.5772/22331
7. Chen, H. X., Li, W. J., An, S. Z., and Gao, H. Y. (2004). Characterization of PSII photochemistry and thermostability in salt-treated Rumex leaves. J. Plant Physiol. 161, 257–226. doi: 10.1078/0176-1617-01231
8. Chen, M., Song, J., and Wang, B. S. (2010). NaCl increases the activity of the plasma membrane H+-ATPase in C3 halophyte Suaeda salsa callus. Acta Physiol. Plant 32, 27–36. doi: 10.1007/s11738-009-0371-7
9. Chen, Z. B., Wang, M. L., Barkley, N. A., and Pittman, R. N. (2010). A simple allele-specific PCR assay for detecting FAD2 alleles in both A and B genomes of the cultivated peanut for high-oleatetraitselection. Plant Mol. Biol. Rep. 28, 542–548. doi: 10.1007/s11105-010-0181-5
10. Chen, Z., Xu, C., Chen, M., Xu, L., Wang, K., Lin, S., et al. (1994). Effect of chilling acclimation on thylakoid membrane protein of wheat. Acta Bot. Sin. 36, 423–429.
11. Cheng, S., Yang, Z., Wang, M. J., Song, J., Sui, N., and Fan, H. (2014). Salinity improves chilling resistance in Suaeda salsa. Acta Physiol. Plant 36, 1823–1830. doi: 10.1007/s11738-014-1555-3
12. Chi, X., Hu, R., Yang, Q., Zhang, X., Pan, L., Chen, N., et al. (2012). Validation of reference genes for gene expression studies in peanut by quantitative real-time RT-PCR. Mol. Genet. Genomics 287, 167–176. doi: 10.1007/s00438-011-0665-5
13. Chi, X., Yang, Q., Pan, L., Chen, M., He, Y., Yang, Z., et al. (2011). Isolation and characterization of fatty acid desaturase genes from peanut (Arachishypogaea, L.). Plant Cell Rep. 30, 1393–1404. doi: 10.1007/s00299-011-1048-4
14. Cooke, D. T., and Burden, R. S. (1990). Lipid modulation of plasma membrane-bound ATPases. Physiol. Plant. 78, 152–159. doi: 10.1111/j.1399-3054.1990.tb08730.x
15. Deng, Y., Feng, Z., Yuan, F., Guo, J., Suo, S., and Wang, B. (2015). Identification and functional analysis of the autofluorescent substance in Limonium bicolor salt glands. Plant Physiol. Biochem. 97, 20–27. doi: 10.1016/j.plaphy.2015.09.007
16. Deng, Y. Y., Li, J. Q., Wu, S. F., Zhu, Y. P., Chen, Y. W., and He, F. C. (2006). Integrated nr database in protein annotation systemand its localization. Comput. Eng. 32, 71–74. Available online at: en.cnki.com.cn/Article_en/ CJFDTOTAL-JSJC200605025.htm
17. Deuticke, B., and Haest, C. W. (1987). Lipid modulation of transport proteins in vertebrate cell membranes. Annu. Rev. Physiol. 49, 221–235. doi: 10.1146/annurev.ph.49.030187.001253
18. Dietz, K. J., Jacob, S., Oelze, M. L., Laxa, M., Tognetti, V., de Miranda S. M., et al. (2006). The function of peroxiredoxins in plant organelle redox metabolism. J. Exp. Bot. 57, 1697–1709. doi: 10.1093/jxb/erj160
19. Feng, J., Dong, Y., Liu, W., He, Q., Daud, M. K., Chen, J., et al. (2017). Genome-wide identification of membrane-bound fatty acid desaturase genes in Gossypium hirsutum and their expressions during abiotic stress. Sci. Rep. 7:45711. doi: 10.1038/srep45711
20. Giannopolitis, C. N., and Ries, S. K. (1977). Superoxide dismutases I. occurrence in higher plants. Plant Physiol. 59, 309–314. doi: 10.1104/pp.59.2.309
21. Gibson, S., Arondel, V., Iba, K., and Somerville, C. (1994). Cloning of a temperature-regulated gene encoding a chloroplast ω-3 desaturase from Arabidopsis thaliana. Plant Physiol. 106, 1615–1621. doi: 10.1104/pp.106.4.1615
22. Graham, D., and Patterson, B. D. (1982). Responses of plants to low, non-freezing temperatures: proteins, metabolism, and acclimation. Annu. Rev. Plant Physiol. 33, 347–372. doi: 10.1146/annurev.pp.33.060182.0 02023
23. 2 S production is involved in OsSE5-promoted ammonium tolerance in roots of Oryza sativa. Plant Cell Environ. 40, 1777–1790. doi: 10.1111/pce.12982
24. Guo, J., Shi, G., Guo, X., Zhang, L., Xu, W., Wang, Y., et al. (2015). Transcriptome analysis reveals that distinct metabolic pathways operate in salt-tolerant and salt-sensitive upland cotton varieties subjected to salinity stress. Plant Sci. 238, 33–45. doi: 10.1016/j.plantsci.2015.05.013
25. Huang, C., He, W., Guo, J., Chang, X., Su, P., and Zhang, L. (2005). Increased sensitivity to salt stress in an ascorbate-deficient Arabidopsis mutant. J. Exp. Bot. 56, 3041–3049. doi: 10.1093/jxb/eri301
26. Huflejt, M., Tremolieres, A., Pineau, B., Lang, J., Hatheway, J., and Packer, L. (1990). Changes in membrane lipid composition during saline growth of the freshwater Cyanobacterium Synechococcus 6311. Plant Physiol. 94, 1512–1521. doi: 10.1104/pp.94.4.1512
27. Jimenez, A., Hernandez, J. A., Del Rio, L. A., and Sevilla, F. (1997). Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Physiol. 114, 275–284. doi: 10.1104/pp.114.1.275
28. Kanehisa, M., Goto, S., Kawashima, S., Okuno, Y., and Hattori, M. (2004). The KEGG resource for deciphering the genome. Nucleic Acids Res. 32, 277–280. doi: 10.1093/nar/gkh063
29. Kayani, S. A., Naqvi, H. H., Ting, P. I., and Kumamoto, J. (1990). Effect of salinity on fatty acid and fatty alcohol composition during the germination of jojoba (Simmondsiachinensis) seeds. J. Agric. Food Chem. 38, 1269–1271. doi: 10.1021/jf00095a025
30. Khamutov, G., Fry, I. V., Huflejt, M. E., and Packer, L. (1990). Membrane lipid composition, fluidity, and surface charge changes in response to growth of the freshwater Cyanobacterium synechococcus 6311 under high salinity. Arch. Biochem. Biophys. 277, 263–267. doi: 10.1016/0003-9861(90)90577-L
31. Klett, E. L., Chen, S., Yechoor, A., Lih, F. B., and Coleman, R. A. (2017). Long-chain acyl-CoAsynthetase isoforms differ in preferences for eicosanoid species and long-chain fatty acids. J. Lipid Res. 58, 884–894. doi: 10.1194/jlr.M072512
32. Klinkenberg, J., Faist, H., Saupe, S., Lambertz, S., Krischke, M., Stingl, N., et al. (2014). Two fatty acid desaturases, stearoyl-acyl carrier protein ∆9-desaturase6 and fatty acid desaturase3, are involved in drought and hypoxia stress signaling in Arabidopsis crown galls. Plant Physiol. 164, 570–583. doi: 10.1104/pp.113.230326
33. Kooten, O., and Snel, J. F. (1990). The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosyn. Res. 25, 147–150. doi: 10.1007/BF00033156
34. Liu, X. Y., Yang, J. H., Li, B., and Meng, Q. W. (2006). Antisense-mediated depletion of tomato chloroplast omega-3 fatty acid desaturase enhances thermal tolerance. J. Integr. Plant Biol. 48, 1096–1107. doi: 10.1111/j.1744-7909.2006.00335.x
35. Mahajan, S., and Tuteja, N. (2005). Cold, salinity and drought stresses: anoverview. Arch. Biochem. Biophys. 444, 139–158. doi: 10.1016/j.abb.2005.10.018
36. Manan, S., Chen, B., She, G., Wan, X., and Zhao, J. (2017). Transport and transcriptional regulation of oil production in plants. Crit. Rev. Biotechnol. 37, 641–655. doi: 10.1080/07388551.2016.1212185
37. Mata-Pérez, C., Sánchez-Calvo, B., Padilla, M. N., Begara-Morales, J. C., Luque, F., Melguizo, M., et al. (2016). Nitro-fatty acids in plant signaling: nitro-linolenicacid induces the molecular chaperone network in Arabidopsis. Plant Physiol. 170, 686–701. doi: 10.1104/pp.15.01671
38. McConn, M., Hugly, S., Browse, J., and Somerville, C. A. (1994). Mutation at the FAD8 locus of Arabidopsis identifies a second chloroplast x-3 desaturase. Plant Physiol. 106, 1609–1614. doi: 10.1104/pp.106.4.1609
39. Menard, G. N., Moreno, J. M., Bryant, F. M., Munoz-Azcarate, O., Kelly, A. A., Hassani-Pak, K., et al. (2017). Genome wide analysis of fatty acid desaturation and its response to temperature. Plant Physiol. 173, 1594–1605. doi: 10.1104/pp.16.01907
40. Mikami, K., and Murata, N. (2003). Membrane fluidity and the perception of environmental signals in cyanobacteria and plants. Prog. Lipid Res. 42, 527–543. doi: 10.1016/S0163-7827(03)00036-5
41. Mittler, R., Vanderauwera, S., Gollery, M., and Van Breusegem, F. (2004). Reactive oxygen gene network of plants. Trends Plant Sci. 9, 490–498. doi: 10.1016/j.tplants.2004.08.009
42. Nishiuchi, T., and Iba, K. (1998). Roles of plastid ω-3 fatty acid desaturases in defence response of higher plants. J. Plant Res. 111, 481–486. doi: 10.1007/BF02507782
43. Qin, L. Q., Li, L., Bi, C., Zhang, Y. L., Wan, S. B., Meng, J. J., et al. (2011). Damaging mechanisms of chilling-and salt stress to Arachishypogaea, L. leaves. Photosynthetica 49, 37–42. doi: 10.1007/s11099-011-0005-3
44. Ritter, D., and Yopp, J. H. (1993). Plasma membrane lipid composition of the halophilic cyanobacterium Aphanothece halophytica. Arch. Microbiol. 159, 435–439. doi: 10.1007/BF00288590
45. Sairam, R., and Srivastava, G. (2002). Changes in antioxidant activity in sub-cellular fractions of tolerant and susceptible wheat genotypes in response to long term salt stress. Plant Sci. 162, 897–904. doi: 10.1016/S0168-9452(02)00037-7
46. Schansker, G., Srivastava, A., and Strasser, R. J. (2003). Characterization of the 820-nmtransmission signal paralleling the chlorophyll a fluorescence rise (OJIP) in pea leaves. Funct. Plant Biol. 30, 785–796. doi: 10.1071/FP03032
47. Schöffl, F., Prandl, R., and Reindl, A. (1999). Molecular Responses to Cold, Drought, Heat and Salt Stress in Higher Plants. Austin, TX: R. G. Landes Company.
48. Shi, J., Lang, C., Wang, F., Wu, X., Liu, R., Zheng, T., et al. (2017). Depressed expression of FAE1 and FAD2 genes modifies fatty acid profiles and storage compounds accumulation in Brassica napus seeds. Plant Sci. 263, 177–182. doi: 10.1016/j.plantsci.2017.07.014
49. Shockey, J. M., and Fulda, M. S. (2002). Arabidopsis contains nine long-chain acyl-coenzyme a synthetase genes that participate in fatty acid and glycerolipid metabolism1. Plant Physiol. 129, 1710–1722. doi: 10.1104/pp.003269
50. Siegenthaler, P. A., and Eichenberger, W. (1984). “Structure, function, and metabolism of plant lipids,” in International Symposium on the Structure, Function, and Metabolism of Plant Lipids 1984 (Neuchâtel: Elsevier Science Publishers).
51. Singh, S. C., Sinha, R. P., and Hader, D. P. (2002). Role of lipids and fatty acids in stress tolerance in cyanobacteria. Acta Protozool. 41, 297–308.
52. Song, J., and Wang, B. (2015). Using euhalophytes to understand salt tolerance and to develop saline agriculture - Suaeda salsa as a promising model. Ann. Bot. 115, 541–553. doi: 10.1093/aob/mcu194
53. Sui, N. (2015). Photoinhibition of Suaeda salsa to chilling stress is related to energy dissipation and water-water cycle. Photosynthetica 53, 207–212. doi: 10.1007/s11099-015-0080-y
54. Sui, N., Li, M., Li, K., Song, J., and Wang, B. S. (2010). Increase in unsaturated fatty acids in membrane lipids of Suaeda salsa L. enhances protection of photosystem II under high salinity. Photosynthetica 48, 623–629. doi: 10.1007/s11099-010-0080-x
55. Sui, N., Li, M., Liu, X. Y., Wang, N., Fang, W., and Meng, Q. W. (2007). Response of xanthophyll cycle and chloroplastic antioxidant enzymes to chilling stress in tomato over-expressing glycerol-3-phosphate acyltransferase gene. Photosynthetica 45, 447–454. doi: 10.1007/s11099-007-0074-5
56. Sui, N., Tian, S. S., Wang, W. Q., Wang, M. J., and Fan, H. (2017). Overexpression of glycerol-3-phosphate acyltransferase from Suaeda salsa improves salt stress in Arabidopsis. Front. Plant Sci. 8:1337. doi: 10.3389/fpls.2017.01337
57. Sui, N., Yang, Z., Liu, M., and Wang, B. (2015). Identification and transcriptomic profiling of genes involved in increasing sugar content during salt stress in sweet sorghum leaves. BMC Genomics 16:534. doi: 10.1186/s12864-015-1760-5
58. Tarazona, S., García-Alcalde, F., Dopazo, J., Ferrer, A., and Conesa, A. (2011). Differential expression in RNA-seq: a matter of depth. Genome Res. 21, 2213–2223. doi: 10.1101/gr.124321.111
59. Tasaka, Y., Gombos, Z., Nishiyama, Y., Mohanty, Y., Ohba, T., Ohki, K., et al. (1996). Targeted mutagenesis of acyl-lipid desaturases in Synechocystis: evidence for the important roles of polyunsaturated membrane lipids in growth, respiration and photosynthesis. EMBOJ. 15, 6416–6425.
60. Tatusov, R. L., Galperin, M. Y., Natale, D. A., and Koonin, E. V. (2000). The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res. 28, 33–36. doi: 10.1093/nar/28.1.33
61. Teixeira, M. C., Carvalho, I. S., and Brodelius, M. (2010). ω-3 fatty acid desaturase genes isolated from purslane (Portulacaoleracea, L.): expression in different tissues and response to cold and woundstress. J. Agric. Food Chem. 58, 1870–1877. doi: 10.1021/jf902684v
62. Teodoro, B. G., Sampaio, I. H., Bomfim, L. H., Queiroz, A. L., Silveira, L. R., Souza, A. O., et al. (2017). Long-chain acyl-CoA synthetase 6 regulates lipid synthesis and mitochondrial oxidative capacity in human and rat skeletal muscle. J Physiol. 595, 677–693. doi: 10.1113/JP272962
63. Thakur, S., Singh, L., Zularisam, A. W., Sakinah, M., and Din, M. F. M. (2017). Lead induced oxidative stress and alteration in the activities of antioxidative enzymes in rice shoots. Biol. Plant. 61, 595–598. doi: 10.1007/s10535-016-0680-9
64. Vuleta, A., Manitašević Jovanović, S., and Tucić, B. (2016). Adaptive flexibility of enzymatic antioxidants SOD, APX and CAT to high light stress: the clonal perennial monocot Iris pumila as a study case. Plant Physiol. Biochem. 100, 166–173. doi: 10.1016/j.plaphy.2016.01.011
65. Wang, A. G., and Luo, G. H. (1990). Quantitative relation between the reaction of hydroxylamine and superoxide anion radicals in plants. Plant Physiol. Comm. 6, 55–57.
66. Wang, H. S., Yu, C., Tang, X. F., Zhu, J., Ma, N. N., and Meng, Q. W. (2014). A tomato endoplasmic reticulum (ER)-type omega-3 fatty acid desaturase (LeFAD3) functions in early seedling tolerance to salinity stress. Plant Cell Rep. 33, 131–142. doi: 10.1007/s00299-013-1517-z
67. Wicke, B., Sikkema, R., Dornburg, V., and Faaij, A. (2011). Exploring land use changes and the role of palm oil production in Indonesia and Malaysia. Land Use Policy 28, 193–206. doi: 10.1016/j.landusepol.2010. 06.001
68. Xu, Y., and Siegenthaler, P. A. (1997). Low temperature treatments induce an increase in the relative content of both linolenic and λ3-hexadecenoic acids in thylakoid membrane phosphatidylglycerol of squash cotyledons. Plant Cell Physiol. 38, 611–618. doi: 10.1093/oxfordjournals.pcp. a029211
69. Yadav, N. S., Wierzbicki, A., Aegerter, M., Caster, C. S., Perez-Grau, L., Kinney, A. J., et al. (1993). Cloning of higher plant [omega]-3 fatty acid desaturases. Plant Physiol. 103, 467–476. doi: 10.1104/pp.103.2.467
70. Yang, Z., Wang, Y., Wei, X. C., Zhao, X., Wang, B. S., and Sui, N. (2017). Transcription profiles of genes related to hormonal regulations under salt stress in sweet sorghum. Plant Mol. Biol. Report. 8, 1–14. doi: 10.1007/s11105-017-1047-x
71. Yu, C., Wang, H. S., Yang, S., Tang, X. F., Duan, M., and Meng, Q. W. (2009). Overexpression of endoplasmic reticulum omega-3 fatty acid desaturase gene improves chilling tolerance in tomato. Plant Physiol. Biochem. 47, 1102–1112. doi: 10.1016/j.plaphy.2009.07.008
72. Yuan, F., Lyu, M. J. A., Leng, B. Y., Zheng, G. Y., Feng, Z. T., Li, P. H., et al. (2015). Comparative transcriptome analysis of developmental stages of the Limonium bicolor leaf generates insights into salt gland differentiation. Plant Cell Environ. 38, 1637–1657. doi: 10.1111/pce.12514
73. Zhang, M., Barg, R., Yin, M., Yardena, G. D., Alicia, L. F., Salts, Y., et al. (2005). Modulated fatty acid desaturation via overexpression of two distinct x-3 desaturases differentially alters tolerance to various abiotic stresses in transgenic tobacco cells and plants. Plant J. 44, 361–371. doi: 10.1111/j.1365-313X.2005.02536.x
74. Zhong, S., Joung, J. G., Zheng, Y., Chen, Y. R., Liu, B., Shao, Y., et al. (2011). High-throughput illumina strand-specific RNAsequencing library preparation. Cold Spring Harbor Protoc. 2011, 940–949. doi: 10.1101/pdb.prot5652
75. Zhou, J. C., Fu, T. T., Sui, N., Guo, J. R., Feng, G., Fan, J. L., et al. (2016). The role of salinity in seed maturation of the euhalophyte Suaeda salsa. Plant Biosyst. 150, 83–90. doi: 10.1080/11263504.2014.976294