Research Advances on Molecular Mechanism of Salt Tolerance in Suaeda
Abstract
:Simple Summary
Abstract
1. Introduction
2. Ion Regulation and Compartmentation
3. Osmotic Adjustment of Organic Solutes
4. Antioxidant Capacity Regulation
5. Secretion of Plant Hormones
6. Changes in the Pathway of Photosynthetic System
7. Omics Approaches
7.1. Transcriptomics
7.2. Proteomics
7.3. Metabolomics
8. Conclusions and Perspectives
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Song, J.; Shi, W.; Liu, R.; Xu, Y.; Sui, N.; Zhou, J.; Feng, G. The role of the seed coat in adaptation of dimorphic seeds of the euhalophyte Suaeda salsa to salinity. Plant Species Biol. 2017, 32, 107–114. [Google Scholar] [CrossRef]
- Flowers, T.J.; Colmer, T.D. Salinity tolerance in halophytes. New Phytol. 2008, 179, 945–963. [Google Scholar] [CrossRef] [PubMed]
- Song, J.; Wang, B.S. Using euhalophytes to understand salt tolerance and to develop saline agriculture: Suaeda salsa as a promising model. Ann. Bot. 2015, 115, 541–553. [Google Scholar] [CrossRef] [PubMed]
- Guo, J.; Li, Y.; Han, G.; Song, J.; Wang, B. NaCl markedly improved the reproductive capacity of the euhalophyte Suaeda salsa. Funct. Plant Biol. 2018, 45, 350–361. [Google Scholar] [CrossRef]
- Wang, X.; Shao, X.; Zhang, W.; Sun, T.; Ding, Y.; Lin, Z.; Li, Y. Genus Suaeda: Advances in phytology, chemistry, pharmacology and clinical application. Pharmacol. Res. 2022, 106203, 1895–2021. [Google Scholar]
- He, Q.; Altieri, A.H.; Cui, B.S. Herbivory drives zonation of stress-tolerant marsh plant. Ecology 2015, 96, 1318–1328. [Google Scholar] [CrossRef] [PubMed]
- Zhao, Y.; Ma, Y.; Duan, H.; Liu, R.; Song, J. Traits of fatty acid accumulation in dimorphic seeds of the euhalophyte Suaeda salsa in saline conditions. Plant Biosyst. 2019, 153, 514–520. [Google Scholar] [CrossRef]
- Zhao, H.L. Study on edible value of Suaeda salsa l. pall. J. Anhui Agricul. Sci. 2010, 38, 14350–14351. [Google Scholar]
- Zhang, J.Y.; Li, M.H.; Xu, L.M.; Wang, Z.J. Effect of Suaeda seed oil on blood-fat and immunologic function of mouse. Occup. Health 2008, 24, 1529–1530. [Google Scholar]
- Guo, J.; Du, M.; Tian, H.; Wang, B. Exposure to high salinity during seed development markedly enhances seedling emergence and fitness of the progeny of the extreme halophyte Suaeda salsa. Front. Plant Sci. 2020, 11, 1291. [Google Scholar] [CrossRef]
- Huang, W.; Li, Z.; Qiao, H.; Li, C.; Liu, X. Interactive effect of sodium chloride and drought on growth and osmotica of Suaeda salsa. Chin. J. Eco-Agric. 2008, 16, 173–178. [Google Scholar] [CrossRef]
- Guo, F.; Tang, Z. Enhanced H+ transport activity of tonoplast vesicles isolated from roots of salt-tolerant mutant of wheat under NaCl stress. Chin. Sci. Bull. 1999, 44, 1198–1201. [Google Scholar] [CrossRef]
- Qiu, N.; Chen, M.; Guo, J.; Bao, H.; Ma, X.; Wang, B. Coordinate up–regulation of V-H+-ATPase and vacuolar Na+/H+ antiporter as a response to NaCl treatment in a C3 halophyte Suaeda salsa. Plant Sci. 2007, 172, 1218–1225. [Google Scholar] [CrossRef]
- Guo, J.; Dong, X.; Han, G.; Wang, B. Salt-enhanced reproductive development of Suaeda salsa L. coincided withion transporter gene upregulation in flowers and increased pollen K+ content. Front. Plant Sci. 2019, 10, 333. [Google Scholar] [CrossRef]
- Gharat, S.A.; Parmar, S.; Tambat, S.; Vasudevan, M.; Shaw, B.P. Transcriptome analysis of the response to NaCl in Suaeda maritima provides an insight into salt tolerance mechanisms in halophytes. PLoS ONE 2016, 119, e0163485. [Google Scholar] [CrossRef]
- Shrikanth, K.S.; Parida, A.K.; Girivasan, K.P. Differentially expressed long-term salinity responsive sequences in halophyte Suaeda maritima L. Dumort. Eur. J. Biol. Biotechnol. 2022, 31, 59–67. [Google Scholar] [CrossRef]
- Diray-Arce, J.; Clement, M.; Gul, B.; Khan, M.A.; Nielsen, B.L. Transcriptome assembly, profiling and differential gene expression analysis of the halophyte Suaeda fruticosa provides insights into salt tolerance. BMC Genom. 2015, 16, 353. [Google Scholar] [CrossRef]
- Wang, B.; Lüttge, U.; Ratajczak, R. Effects of salt treatment and osmotic stress on V-ATPase and V-PPase in leaves of the halophyte Suaeda salsa. J. Exp. Bot. 2001, 52, 2355–2365. [Google Scholar] [CrossRef]
- Liu, L.; Wang, Y.; Wang, N.; Dong, Y.; Fan, X.; Liu, X.; Yang, J.; Li, H. Cloning of a vacuolar H+-pyrophosphatase gene from the halophyte Suaeda corniculata whose heterologous overexpression improves salt, saline-alkali and drought tolerance in Arabidopsis. J. Integr. Plant Biol. 2011, 53, 731–742. [Google Scholar] [CrossRef]
- Guo, S.; Yin, H.; Zhang, X.; Zhao, F.; Li, P.; Chen, S.; Zhao, Y.; Zhang, H. Molecular cloning and characterization of a Vacuolar H+-pyrophos-phatase gene, SsVP, from the halophyte Suaeda salsa and its overexpression increases salt and drought tolerance of Arabidopsis. Plant Mol. Biol. 2006, 60, 41–50. [Google Scholar] [CrossRef]
- Wang, W.; Liu, Y.; Duan, H.; Yin., X.; Cui, Y.; Chai, W.; Song, X.; Flowers, T.; Wang, S. SsHKT1;1 is coordinated with SsSOS1 and SsNHX1 to regulate Na+ homeostasis in Suaeda salsa under saline conditions. Plant Soil 2020, 449, 117–131. [Google Scholar] [CrossRef]
- Hasegawa, P.M. Sodium Na+ homeostasis and salt tolerance of plants. Environ. Exp. Bot. 2013, 92, 19–31. [Google Scholar] [CrossRef]
- Huang, Y.; Zhang, X.; Li, Y.; Ding, J.; Du, H.; Zhao, Z.; Zhou, L.; Liu, C.; Gao, S.; Cao, M.; et al. Overexpression of the Suaeda salsa SsNHX1 gene confers enhanced salt and drought tolerance to transgenic Zea mays. J. Integr. Agric. 2018, 17, 2612–2623. [Google Scholar] [CrossRef] [Green Version]
- Li, X.; Wang, F.; Sun, D.; Wang, N.; Dong, Y.; Liu, W.; Liu, X.; Yao, N.; Chen, H.; Chi, M.; et al. Cloning and characterization of SucNHX1, a novel vacular Na+/H+ antiporter from the halophyte Suaeda corniculata that enhances the saline-alkali tolerance in Arabidopsis by its overexpression. Plant Cell Tissue Organ Cult. 2018, 134, 395–407. [Google Scholar] [CrossRef]
- Zhao, F.; Wang, Z.; Zhang, Q.; Zhao, Y.; Zhang, H. Analysis of the physiological mechanism of salt-tolerant transgenic rice carrying a vacuolar Na+/H+ antiporter gene from Suaeda salsa. J. Plant Res. 2006, 119, 95–104. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.; Li, P.; Wang, B. Cloning and expression of subunit H of V-H+-ATPase in vacuole membrane in the leaves of the halophyte Suaeda salsa under salt stress. Acta. Bot. Boreal. Occident. Sin. 2006, 26, 63–67. [Google Scholar]
- Liu, Q.; Liu, R.; Ma, Y.; Song, J. Physiological and molecular evidence for Na+ and Cl− exclusion in the roots of two Suaeda salsa populations. Aquat. Bot. 2018, 146, 1–7. [Google Scholar] [CrossRef]
- Khan, M.A.; Ungar, I.A.; Showalter, A.M. The effect of salinity on the growth, water status, and ion content of a leaf succulent perennial halophyte, Suaeda fruticosa L. Forssk. J. Arid. Environ. 2000, 451, 73–84. [Google Scholar] [CrossRef]
- Mori, S.; Suzuki, K.; Oda, R.; Higuchi, K.; Maeda, Y.; Yoshiba, M.; Tadano, T. Characteristics of Na+ and K+ absorption in Suaeda salsa L. Pall. Soil Sci. Plant Nutr. 2011, 573, 377–386. [Google Scholar] [CrossRef]
- Mori, S.; Akiya, M.; Yamamura, K.; Murano, H.; Arao, T.; Kawasaki, A.; Higuchi, K.; Maeda, Y.; Yoshiba, M.; Tadano, T. Physiological role of sodium in the growth of the halophyte Suaeda salsa (L.) Pall. under high-sodium conditions. Crop Sci. 2010, 50, 2492–2498. [Google Scholar] [CrossRef]
- Song, J.; Chen, M.; Feng, G.; Jia, Y.H.; Wang, B.S.; Zhang, F.S. Effect of salinity on growth, ion accumulation and the roles of ions in osmotic adjustment of two populations of Suaeda salsa. Plant Soil 2009, 314, 133–141. [Google Scholar] [CrossRef]
- Wang, S.M.; Zhang, J.L.; Flowers, T.J. Low-affinity Na+ uptake in the halophyte Suaeda maritima. Plant Physiol. 2007, 1452, 559–571. [Google Scholar] [CrossRef] [PubMed]
- Yang, C.; Shi, D.; Wang, D. Comparative effects of salt and alkali stresses on growth, osmotic adjustment and ionic balance of an alkali-resistant halophyte Suaeda glauca Bge. Plant Growth Regul. 2008, 562, 179–190. [Google Scholar] [CrossRef]
- Yeo, A.R. Salt tolerance in the halophyte Suaeda maritima L. Dum.: Intracellular compartmentation of ions. J. Exp. Bot. 1981, 32, 487–497. [Google Scholar] [CrossRef]
- Yeo, A.R.; Flowers, T.J. Salt tolerance in the halophyte Suaeda maritima L. Dum.: Evaluation of the effect of salinity upon growth. J. Exp. Bot. 1980, 31, 1171–1183. [Google Scholar] [CrossRef]
- Shao, Q.; Han, N.; Ding, T.; Zhou, F.; Wang, B. SsHKT1;1 is a potassium transporter of the C3 halophyte Suaeda salsa that is involved in salt tolerance. Funct. Plant Biol. 2014, 41, 790–802. [Google Scholar] [CrossRef]
- Lebaudy, A.; Véry, A.A.; Sentenac, H. K+ channel activity in plants: Genes, regulations and functions. FEBS. Lett. 2007, 581, 2357–2366. [Google Scholar] [CrossRef]
- Corratgé-Faillie, C.; Jabnoune, M.; Zimmermann, S.; Véry, A.A.; Fizames, C.; Sentenac, H. Potassium and sodium transport in non-animal cells: The Trk/Ktr/HKT transporter family. Cell Mol. Life Sci. 2010, 67, 2511–2532. [Google Scholar] [CrossRef]
- Cuéllar, T.; Pascaud, F.; Verdeil, J.L.; Torregrosa, L.; Adam-Blondon, A.F.; Thibaud, J.B.; Sentenac, H.; Gaillard, I. A grapevine Shaker inward K+ channel activated by the calcineurin B-like calcium sensor 1-protein kinase CIPK23 network is expressed in grape berries under drought stress conditions. Plant J. 2010, 51, 58–69. [Google Scholar] [CrossRef]
- Duan, H.; Ma, Q.; Zhang, J.; Hu, J.; Bao, A.; Wei, L.; Wang, Q.; Luan, S.; Wang, S. The inward-rectifying K+ channel SsAKT1 is a candidate involved in K+ uptake in the halophyte Suaeda salsa under saline condition. Plant Soil 2015, 395, 173–187. [Google Scholar] [CrossRef]
- Jin, H.; Dong, D.; Yang, Q.; Zhu, D. Salt responsive transcriptome profiling of Suaeda glauca via RNA sequencing. PLoS ONE 2016, 11, e0150504. [Google Scholar] [CrossRef] [PubMed]
- Nedelyaeva, O.I.; Popova, L.G.; Volkov, V.S.; Balnokin, Y.V. Molecular cloning and characterization of SaCLCd, SaCLCf, and SaCLCg, novel proteins of the chloride channel family CLC from the halophyte Suaeda altissima L. Pall. Plants 2022, 11, 409. [Google Scholar] [CrossRef] [PubMed]
- Nedelyaeva, O.I.; Shuvalov, A.V.; Mayorova, O.V.; Yurchenko, A.A.; Popova, L.G.; Balnokin, Y.V.; Karpichev, I.V. Cloning and functional analysis of SaCLCc1, a gene belonging to the chloride channel family (CLC), from the halophyte Suaeda altissima (L.) Pall. Dokl. Biochem. Biophys. 2018, 481, 186–189. [Google Scholar] [CrossRef] [PubMed]
- Gong, Z.; Loescher, W.H. Expression of a celery mannose 6-phosphate reductase in Arabidopsis thaliana enhances salt tolerance and induces biosynthesis of both mannitol and aglucosyl-mannitol dimer. Plant Cell Environ. 2003, 26, 275–283. [Google Scholar]
- Moghaieb, R.E.A.; Saneoka, H.; Fujita, K. Effect of salinity on osmotic adjustment, glycine betaine accumulation and the betaine aldehyde dehydrogenase gene expression in two halophytic plants, Salicornia europaea and Suaeda maritime. Plant Sci. 2004, 166, 1345–1349. [Google Scholar] [CrossRef]
- Liu, J.R.; Yi, Y.J.; Zhao, K.F. Effects of salinity onion contents, betaine level and betaine-aldehyde dehydrogenase activity in seepweed Suaeda salsa seedlings. J. Integr. Plant Biol. 1994, 36, 622–626. [Google Scholar]
- Flowers, T.J.; Hall, J.L. Salt tolerance in the halophyte, Suaeda rnaritima L. Dum.: The influence of the salinity of the culture solution on the content of various organic compounds. Ann. Bot. 1978, 42, 1057–1063. [Google Scholar] [CrossRef]
- Park, J.; Okita, T.W.; Edwards, G.E. Salt tolerant mechanismsin single-cell C4 species Bienertia sinuspersici and Suaeda aralocaspica Chenopodiaceae. Plant Sci. 2009, 176, 616–626. [Google Scholar] [CrossRef]
- Song, J.; Ding, X.D.; Feng, G.; Zhang, F.S. Nutritional and osmotic roles of nitrate in a euhalophyte and xerophyte in saline conditions. New Phytol. 2006, 171, 357–366. [Google Scholar] [CrossRef]
- Zhang, H.Y.; Zhao, K.F. Effects of salt and water stresses on osmotic adjustment of Suaeda salsa seedlings. Acta. Bot. Sin. 1998, 40, 56–61. [Google Scholar]
- Tipirdamaz, R.; Gagneul, D.; Duhaze, C.; Aïnouche, A.; Monnier, C.; Özkum, D.; Larher, F. Clustering of halophytes from an inland salt marsh in Turkey according to their ability to accumulate sodium and nitrogenous osmolytes. Environ. Exp. Bot. 2006, 57, 139–153. [Google Scholar] [CrossRef]
- Anbarasi, G.; Somasundaram, S.T. Growth regulation and proteomic approaches of exogenous abscisic acid induced changes on salt tolerance factors in Suaeda maritima. Plant Physiol. Rep. 2020, 25, 33–50. [Google Scholar] [CrossRef]
- Greenway, H.; Osmond, C.B. Salt responses of enzymes from species differing in salt tolerance. Plant Physiol. 1972, 49, 256–259. [Google Scholar] [CrossRef] [PubMed]
- Jin, H.; Dong, D.; Yang, C.; Yuan, F.; Yu, X.; Fu, X.; Zhu, D. Cloning and analysis of PEAMT gene in Suaeda Glauca. Chin. Agric. Sci. Bull. 2015, 31, 178–183. [Google Scholar]
- Li, W.; Zhang, C.Y.; Lu, Q.T.; Wen, X.G.; Lu, C.M. The combined effect of salt stress and heat shock on proteome profiling in Suaeda salsa. J. Plant Physiol. 2011, 168, 1743–1752. [Google Scholar] [CrossRef]
- Wu, H.; Liu, X.; You, L.; Zhang, L.; Zhou, D.; Feng, J.; Zhao, J.; Yu, J. Effects of salinity on metabolic profiles, gene expressions, and antioxidant enzymes in halophyte Suaeda salsa. J. Plant Growth Regul. 2012, 31, 332–341. [Google Scholar] [CrossRef]
- Askari, H.; Edqvist, J.; Hajheidari, M.; Kafi, M.; Salekdeh, G.H. Effects of salinity levels on proteome of Suaeda aegyptiaca leaves. Proteomics 2006, 6, 2542–2554. [Google Scholar] [CrossRef]
- Li, Q.; Gao, X.; Yu, X.; Wang, X.; An, L. Molecular cloning and characterization of betaine aldehyde dehydrogenase gene from Suaeda liaotungensis and its use in improved tolerance to salinity in transgenic tobacco. Biotechnol. Lett. 2003, 25, 1431–1436. [Google Scholar] [CrossRef] [PubMed]
- Li, Q.; Liu, D.; Gao, X.; Su, Q.; Jia, A. Cloning of cDNA encoding choline monooxygenase from Suaeda liaotungensis and salt tolerance of transgenic tobacco. J. Integr. Plant Biol. 2003, 45, 242–247. [Google Scholar]
- Wang, F.; Wang, M.; Guo, C.; Wang, N.; Li, X.; Chen, H.; Dong, Y.; Chen, X.; Wang, Z.; Li, H. Cloning and characterization of a novel betaine aldehyde dehydrogenase gene from Suaeda corniculata. Genet. Mol. Res. 2016, 15, gmr15027848. [Google Scholar] [CrossRef]
- Wang, P.; Ma, C.; Zhao, K.; Zhao, Y.; Zhang, H. Isolation and characterizing of a Δ1-pyrroline-5-carboxylate synthase gene in Suaeda salsa under salinity stress. J. Shandong Norm. Univ. Nat. Sci. 2002, 17, 59–62. [Google Scholar]
- Wang, P.; Ma, C.; Cao, Z.; Zhao, Y.; Zhang, H. Molecular cloning and differential expression of amyo-inositol-1-phosphate synthase gene in Suaeda salsa under salinity stress. J. Plant Physiol. Mol. Biol. 2002, 28, 175–180. [Google Scholar]
- Li, Q.; Song, J. Analysis of widely targeted metabolites of the euhalophyte Suaeda salsa under saline conditions provides new insights into salt tolerance and nutritional value in halophytic species. BMC Plant Biol. 2019, 19, 388. [Google Scholar] [CrossRef]
- Pang, Q.; Zhang, A.; Zang, W.; Wei, L.; Yan, X. Integrated proteomics and metabolomics for dissecting the mechanism of global responses to salt and alkali stress in Suaeda corniculata. Plant Soil 2016, 402, 379–394. [Google Scholar] [CrossRef]
- Zang, W.; Miao, R.; Zhang, Y.; Yuan, Y.; Pang, Q.; Zhou, Z. Metabolic and molecular basis for the salt and alkali responses of Suaeda corniculate. Environ. Exp. Bot. 2021, 192, 104643. [Google Scholar] [CrossRef]
- Xu, Y.; Liu, R.; Sui, N.; Shi, W.; Wang, L.; Tian, C.; Song, J. Changes in endogenous hormones and seed-coat phenolics during seed storage of two Suaeda salsa populations. Aust. J. Bot. 2016, 64, 325–332. [Google Scholar] [CrossRef]
- Wang, B.; Luttge, U.; Ratajczak, R. Specific regulation of SOD isoforms by NaCl and osmotic stress in leaves of the C3 halophyte Suaeda salsa L. J. Plant Physiol. 2004, 161, 285–293. [Google Scholar] [CrossRef]
- Guan, B.; Yu, J.; Lu, Z.; Zhang, Y.; Wang, X. Effects of water-salt stresses on seedling growth and activities of antioxidative enzyme of Suaeda salsa in coastal wetlands of the Yellow River Delta. Environ. Sci. 2011, 32, 2422–2429. [Google Scholar]
- Pang, C.; Zhang, S.; Gong, Z.; Wang, B. NaCl treatment markedly enhances H2O2-scavenging system in leaves of halophyte Suaeda salsa. Physiol. Plantarum 2005, 125, 490–499. [Google Scholar]
- Mohamed, E.; Matsuda, R.; El-Khatib, A.A.; Takechi, K.; Takano, H.; Takio, S. Characterization of the superoxide dismutase genes of the halophyte Suaeda maritima in Japan and Egypt. Plant Cell Rep. 2015, 34, 2099–2110. [Google Scholar] [CrossRef]
- Li, H.; Wang, H.; Wen, W.; Yang, G. The antioxidant system in Suaeda salsa under salt stress. Plant Signal Behav. 2020, 15, 1771939. [Google Scholar] [CrossRef] [PubMed]
- Sahu, B.B.; Shaw, B.P. Isolation, identification and expression analysis of salt induced genes in Suaeda maritima, a natural halophyte, using PCR-based suppression subtractive hybridization. BMC Plant Biol. 2009, 9, 69. [Google Scholar] [CrossRef] [PubMed]
- Hameed, A.; Hussain, T.; Gulzar, S.; Aziz, I.; Gul, B.; Khan, M.A. Salt tolerance of a cash crop halophyte Suaeda fruticosa: Biochemical responses to salt and exogenous chemical treatments. Acta Physiol. Plant. 2012, 34, 2331–2340. [Google Scholar] [CrossRef]
- Qi, Y.; Zhang, S.; Wang, L.; Wang, M.; Zhang, H. Overexpression of GST gene accelerates the growth of transgenic Arabidopsis under salt stress. J. Plant Physiol. Mol. Biol. 2004, 30, 517–522. [Google Scholar]
- Hara, M.; Fujinaga, M.; Kuboi, T. Metal binding by citrus dehydrin with histidine–rich domains. J. Exp. Bot. 2005, 56, 2695–2703. [Google Scholar] [CrossRef]
- Tiwari, P.; Chakrabarty, D. Dehydrin in the past four decades: From chaperones to transcription co-regulators in regulating abiotic stress response. Curr. Res. Biotech. 2021, 3, 249–259. [Google Scholar] [CrossRef]
- Ma, H.; Sun, H.; Li, H.; Deng, S.; Wang, X.; Chen, S.; Chen, L.; Zhang, L.; Zhong, M. Functional analysis of the SsDHN of Suaeda salsa L. Pall. Mol. Plant Breed. 2021, 19, 827–832. [Google Scholar]
- Ayarpadikannan, S.; Chung, E.; Cho, C.W.; So, H.A.; Kim, S.O.; Jeon, J.M.; Kwak, M.H.; Lee, S.W.; Lee, J.H. Exploration for the salt stress tolerance genes from a salt-treated halophyte, Suaeda asparagoides. Plant Cell Rep. 2012, 31, 35–48. [Google Scholar] [CrossRef]
- Ma, C.; Wang, P.; Cao, Z.; Zhao, Y.; Zhang, H. cDNA cloning and gene expression of APX in Suaeda salsa in response to salt stress. J. Plant Physiol. Mol. Biol. 2002, 28, 261–266. [Google Scholar]
- Ma, C.; Wang, P.; Cao, Z.; Zhao, Y.; Zhang, H. Cloning and differential gene expression of two catalases in Suaeda salsa in response to salt stress. J. Integr. Plant Biol. 2003, 45, 93–97. [Google Scholar]
- Li, K.; Pang, C.H.; Ding, F.; Sui, N.; Feng, Z.T.; Wang, B.S. Overexpression of Suaeda salsa stroma ascorbate peroxidase in Arabidopsis. S. Afr. J. Bot. 2012, 78, 235–245. [Google Scholar] [CrossRef]
- Behera, L.M.; Hembram, P. Advances on plant salinity stress responses in the post-genomic era: A review. J. Crop Sci. Biotech. 2021, 24, 117–126. [Google Scholar] [CrossRef]
- Yu, Z.; Duan, X.; Luo, L.; Dai, S.; Ding, Z.; Xia, G. How plant hormones mediate salt stress responses. Trends Plant Sci. 2020, 25, 1117–1130. [Google Scholar] [CrossRef]
- Li, W.; Liu, X.; Ajmal Khan, M.; Yamaguchi, S. The effect of plant growth regulators, nitric oxide, nitrate, nitrite and light on the germination of dimorphic seeds of Suaeda salsa under saline conditions. J. Plant Res. 2005, 118, 207–214. [Google Scholar] [CrossRef] [PubMed]
- Li, W.; Yamaguchi, S.; Khan, M.; An, P.; Liu, X.; Tran, L.S. Roles of gibberellins and abscisic acid in regulating germination of Suaeda salsa dimorphic seeds under salt stress. Front. Plant Sci. 2016, 6, 1235. [Google Scholar] [CrossRef] [PubMed]
- Boucaud, J.; Ungar, I.A. Hormonal control of germination under saline conditions of three halophytic taxa in the genus Suaeda. Physiol. Plant. 1976, 37, 143–148. [Google Scholar] [CrossRef]
- Guo, J.; Lu, C.; Zhao, F.; Gao, S.; Wang, B. Improved reproductive growth of euhalophyte Suaeda salsa under salinity is correlated with altered phytohormone biosynthesis and signal transduction. Funct. Plant Biol. 2020, 47, 170–183. [Google Scholar] [CrossRef]
- Fisher, D.D.; Schenk, H.J.; Thorsch, J.A.; Ferren, W.R., Jr. Leaf anatomy and subgeneric affiliations of C3 and C4 species of Suaeda Chenopodiaceae in North America. Am. J. Bot. 1997, 849, 1198–1210. [Google Scholar] [CrossRef]
- Li, Q.; Liu, R.; Li, Z.; Fan, H.; Song, J. Positive effects of NaCl on the photoreaction and carbon assimilation efficiency in Suaeda salsa. Plant Physiol. Bioch. 2022, 177, 32–37. [Google Scholar] [CrossRef]
- Ibraheem, F.; Al-Zahrani, A.; Mosa, A. Physiological adaptation of three wild halophytic Suaeda species: Salt tolerance strategies and metal accumulation capacity. Plants 2022, 11, 537. [Google Scholar] [CrossRef]
- Wei, L.; Pang, Q.; Zhang, A.; Guo, J.; Yan, X. Effects of salt and alkali stresses on photosynthetic characteristics of Suaeda corniculata seedlings. J. Northeast. For. Univ. 2012, 40, 32–35. [Google Scholar]
- Lu, C.; Qiu, N.; Wang, B.; Zhang, J. Salinity treatment shows no effects on photosystem II photochemistry, but increases the resistance of photosystem II to heat stress in halophyte Suaeda salsa. J. Exp. Bot. 2003, 54, 851–860. [Google Scholar] [CrossRef] [PubMed]
- Hao, X.; Li, J.; Gao, S.; Tuerxun, Z.; Chang, X.; Hu, W.; Chen, G.; Huang, Q. SsPsaH, a H subunit of the photosystem I reaction center of Suaeda salsa, confers the capacity of osmotic adjustment in tobacco. Genes Genom. 2020, 42, 1455–1465. [Google Scholar] [CrossRef] [PubMed]
- Sui, N.; Tian, S.; Wang, W.; Wang, M.; Fan, H. Overexpression of glycerol-3-phosphate acyltransferase from Suaeda salsa improves salt tolerance in Arabidopsis. Front. Plant Sci. 2017, 8, 1337. [Google Scholar] [CrossRef] [PubMed]
- Jha, U.C.; Bohra, A.; Jha, R.; Parida, S.K. Salinity stress response and ‘omics’ approaches for improving salinity stress tolerance in major grain legumes. Plant Cell Rep. 2019, 38, 255–277. [Google Scholar] [CrossRef]
- Lawlor, D. Abiotic stress adaptation in plants. Physiological, Molecular and Genomic Foundation. Ann. Bot. 2011, 107, vii–ix. [Google Scholar] [CrossRef]
- Zhang, X.; Yao, Y.; Li, X.; Zhang, L.; Fan, S. Transcriptomic analysis identifies novel genes and pathways for salt stress responses in Suaeda salsa leaves. Sci. Rep. 2020, 10, 4236. [Google Scholar] [CrossRef]
- Guo, S.; Tan, Y.; Chu, H.; Sun, M.; Xing, J. Transcriptome sequencing revealed molecular mechanisms underlying tolerance of Suaeda salsa to saline stress. PLoS ONE 2019, 14, e0219979. [Google Scholar] [CrossRef] [Green Version]
- Han, Z.J.; Sun, Y.; Zhang, M.; Zhai, J.T. Transcriptomic profile analysis of the halophyte Suaeda rigida response and tolerance under NaCl stress. Sci. Rep. 2020, 10, 15148. [Google Scholar] [CrossRef]
- Wang, M.; Ren, T.; Marowa, P.; Du, H.; Xu, Z. Identification and selection of reference genes for gene expression analysis by quantitative real-time PCR in Suaeda glauca’s response to salinity. Sci. Rep. 2021, 11, 8569. [Google Scholar] [CrossRef]
- Diray-Arce, J.; Knowles, A.; Suvorov, A.; O’Brien, J.; Hansen, C.; Bybee, S.M.; Gul, B.; Ajmal Khan, M.; Nielsen, B.L. Identification and evolutionary characterization of salt-responsive transcription factors in the succulent halophyte Suaeda fruticosa. PLoS ONE 2019, 14, e0222940. [Google Scholar] [CrossRef] [PubMed]
- Li, X.; Yang, X.; Hu, Y.; Yu, X.; Li, Q. A novel NAC transcription factor from Suaeda liaotungensis K. enhanced transgenic Arabidopsis drought, salt, and cold stress tolerance. Plant Cell Rep. 2014, 33, 767–778. [Google Scholar] [CrossRef] [PubMed]
- Yang, X.; Hu, Y.; Li, X.; Yu, X.; Li, Q. Molecular characterization and function analysis of SlNAC2 in Suaeda liaotungensis K. Gene 2014, 543, 190–197. [Google Scholar] [CrossRef]
- Wu, D.; Sun, Y.; Wang, H.; Shi, H.; Su, M.; Shan, H.; Li, T.; Li, Q. The SlNAC8 gene of the halophyte Suaeda liaotungensis enhances drought and salt stress tolerance in transgenic Arabidopsis thaliana. Gene 2018, 662, 10–20. [Google Scholar] [CrossRef]
- Wang, H.F.; Shan, H.Y.; Shi, H.; Wu, D.D.; Li, T.T.; Li, Q.L. Characterization of a transcription factor SlNAC7 gene from Suaeda liaotungensis and its role in stress tolerance. J. Plant Res. 2021, 134, 1105–1120. [Google Scholar] [CrossRef] [PubMed]
- Liu, X.; Sun, X.; Wang, X.; MA, H. Cloning and expression analysis of SsDREB gene from Suaeda salsa L. J. Nucl. Agric. Sci. 2011, 25, 684–691. [Google Scholar]
- Sun, X.; Ma, H.; Jia, X.; Chen, Y.; Ye, X. Molecular cloning and characterization of two novel DREB genes encoding dehydration-responsive element binding proteins in halophyte Suaeda salsa. Genes Genom. 2015, 37, 199–212. [Google Scholar] [CrossRef]
- Sun, X.; Su, J.; Jia, X.; Liang, L.; Xiao, Z.; Deng, Y. Cloning and expression analysis of two DREB1/CBF genes in Suaeda salsa L. Sci. Agric. Sin. 2016, 49, 2418–2429. [Google Scholar]
- Liu, X.; Wu, H.; Ji, C.; Wei, L.; Zhao, J.; Yu, J. An integrated proteomic and metabolomic study on the chronic effects of mercury in Suaeda salsa under an environmentally relevant salinity. PLoS ONE 2013, 8, e64041. [Google Scholar]
- Fernandez-Garcia, N.; Hernandez, M.; Casado-vela, J.; Bru, R.; Elortza, F.; Hedden, P.; Olmos, E. Changes to the proteome and targeted metabolites of xylem sap in Brassica oleracea in response to salt stress. Plant Cell Environ. 2011, 34, 821–836. [Google Scholar] [CrossRef]
- Zhang, H.; Han, B.; Wang, T.; Chen, S.X.; Li, H.Y. Mechanisms of plant salt response: Insights from proteomics. J. Proteome Res. 2012, 11, 49–67. [Google Scholar] [CrossRef] [PubMed]
- Benjamin, J.J.; Miras-Moreno, B.; Araniti, F.; Salehi, H.; Bernardo, L.; Parida, A.; Lucini, L. Proteomics revealed distinct responses to salinity between the halophytes Suaeda maritima L. Dumort and Salicornia brachiata Roxb. Plants 2020, 9, 227. [Google Scholar] [CrossRef] [PubMed]
- Qi, C.H.; Chen, M.; Song, J.; Wang, B.S. Increase in aquaporin activity is involved in leaf succulence of the euhalophyte Suaeda salsa, under salinity. Plant Sci. 2009, 176, 200–205. [Google Scholar] [CrossRef]
- Tao, J.; Chen, H.; Ma, B.; Zhang, W.; Chen, S.; Zhang, J. The role of ethylene in plants under salinity stress. Front. Plant Sci. 2015, 6, 1059. [Google Scholar] [CrossRef]
- Benjamin, J.J.; Lucini, L.; Jothiramshekar, S.; Parida, A. Metabolomic insights into the mechanisms underlying tolerance to salinity in different halophytes. Plant Physiol. Biochem. 2019, 135, 528–545. [Google Scholar] [CrossRef]
- Kumari, A.; Parida, A.K. Metabolomics and network analysis reveal the potential metabolites and biological pathways involved in salinity tolerance of the halophyte Salvadora persica. Environ. Exp. Bot. 2018, 148, 85–99. [Google Scholar] [CrossRef]
- Yadav, S.; Elansary, H.O.; Mattar, M.A.; Elhindi, K.M.; Alotaibi, M.A.; Mishra, A. Differential accumulation of metabolites in Suaeda species provides new insights into abiotic stress tolerance in C4-halophytic species in elevated CO2 conditions. Agronomy 2021, 11, 131. [Google Scholar] [CrossRef]
Suaeda Species | Gene | Function | Reference |
---|---|---|---|
Suaeda salsa | SsVP | Encoding V-H+-ATPase | [20] |
SsNHX1 | Na+/H+ antiporter | [23] | |
SsSOS1 | Na+/H+ antiporter | [27] | |
SsHKT1;1 | K+ uptake under salt stress | [21] | |
SsHKT1 | K+ uptake under salt stress | [36] | |
SsAKT1 | K+ uptake under salt stress | [40] | |
SsCMO | Encoding choline monooxygenase | [56] | |
SsBADH | Encoding betaine aldehyde dehydrogenase | [56] | |
SsP5CS | Encoding D1-pyrroline-5-carboxylate synthase | [61] | |
SsINPS | Encoding myo-inositol-1-phosphate (I-1-P) synthase | [62] | |
Sscat1 | Encoding catalase | [80] | |
SsAPX | Encoding ascorbate peroxidase | [79] | |
SsGST | Encoding glutathione S-transferase | [74] | |
SsDHN | Encoding betaine aldehyde dehydrogenase | [77] | |
SsFNR | Encoding carbon-assimilation-related enzymes | [63] | |
SsRbcl | Encoding carbon-assimilation-related enzymes | [63] | |
SsRbcs | Encoding carbon-assimilation-related enzymes | [63] | |
SsRCA | Encoding carbon-assimilation-related enzymes | [63] | |
SsPGK | Encoding carbon-assimilation-related enzymes | [63] | |
SsGAPDH | Encoding carbon-assimilation-related enzymes | [63] | |
SsGPAT | Encoding glycerol3-phosphate acyltransferase | [95] | |
SsCBF1 | CBF/DREB transcription factor | [109] | |
ERF1/2 | ERF transcription factor | [88] | |
S. corniculate | ScVP | Encoding V-H+-ATPase | [19] |
SucNHX1 | Na+/H+ antiporter | [24] | |
ScBADH | Encoding betaine aldehyde dehydrogenase | [60] | |
S. liaotungensis | SlCMO | Encoding choline monooxygenase | [59] |
SlBADH | Encoding betaine aldehyde dehydrogenase | [57] | |
SlPEAMT | Encoding phosphoethanolamine methyltransferase | [54] | |
SlNAC1 | NAC transcription factor | [102] | |
SlNAC2 | NAC transcription factor | [102] | |
SlNAC7 | NAC transcription factor | [105] | |
SlNAC8 | NAC transcription factor | [102] | |
S. maritima | SmGST | Encoding glutathione S-transferase | [72] |
CMO | Encoding choline monooxygenase | [15] | |
BADH | Encoding betaine aldehyde dehydrogenase | [15] | |
S. glauca | SgDHN | Encoding betaine aldehyde dehydrogenase | [78] |
AP2 | AP2 transcription factor | [100] | |
S. altissima | SaCLCc1 | Encoding chloride channel protein | [43] |
SaCLCd | Encoding chloride channel protein | [42] | |
SaCLCf | Encoding chloride channel protein | [42] | |
SaCLCg | Encoding chloride channel protein | [42] | |
S. aegyptiaca | CMO | Encoding choline monooxygenase | [58] |
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Yu, W.; Wu, W.; Zhang, N.; Wang, L.; Wang, Y.; Wang, B.; Lan, Q.; Wang, Y. Research Advances on Molecular Mechanism of Salt Tolerance in Suaeda. Biology 2022, 11, 1273. https://doi.org/10.3390/biology11091273
Yu W, Wu W, Zhang N, Wang L, Wang Y, Wang B, Lan Q, Wang Y. Research Advances on Molecular Mechanism of Salt Tolerance in Suaeda. Biology. 2022; 11(9):1273. https://doi.org/10.3390/biology11091273
Chicago/Turabian StyleYu, Wancong, Wenwen Wu, Nan Zhang, Luping Wang, Yiheng Wang, Bo Wang, Qingkuo Lan, and Yong Wang. 2022. "Research Advances on Molecular Mechanism of Salt Tolerance in Suaeda" Biology 11, no. 9: 1273. https://doi.org/10.3390/biology11091273
APA StyleYu, W., Wu, W., Zhang, N., Wang, L., Wang, Y., Wang, B., Lan, Q., & Wang, Y. (2022). Research Advances on Molecular Mechanism of Salt Tolerance in Suaeda. Biology, 11(9), 1273. https://doi.org/10.3390/biology11091273