Reshifting Na+ from Shoots into Long Roots Is Associated with Salt Tolerance in Two Contrasting Inbred Maize (Zea mays L.) Lines
Abstract
:1. Introduction
2. Results
2.1. Salt Tolerance Differences between QXN233 and QXH0121 Inbred Lines
2.2. Na+ and K+ Changes in QXN233 and QXH0121
2.3. Alterations in Compatible Solutes in QXN233 and QXH0121
2.4. Expression Patterns of Na+ and K+ Ion Transporter Genes in QXN233 and QXH0121
2.5. Expression Patterns of Some Salt-Responsive Genes in QXN233 and QXH0121
3. Discussion
4. Materials and Methods
4.1. Plant Growth and NaCl Treatments
4.2. Growth Parameters, Chlorophyll, and Malondialdehyde (MDA) Content
4.3. Na+ and K+ Contents
4.4. Proline, Soluble Sugar, Soluble Protein Content and Superoxide Dismutase (SOD) Activity
4.5. Quantitative Real-Time PCR (qRT-PCR) Analysis
4.6. Statistical Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
- Machado, R.U.A.; Serralheiro, R.P. Soil salinity: Effect on vegetable crop growth. Management practices to prevent and mitigate soil salinization. Horticulturae 2017, 3, 30. [Google Scholar] [CrossRef]
- Munns, R. Genes and salt tolerance: Bringing them together. New Phytol. 2005, 167, 645–663. [Google Scholar] [CrossRef]
- Tester, M.; Davenport, R. Na+ tolerance and Na+ transport in higher plants. Ann. Bot. 2003, 91, 503–527. [Google Scholar] [CrossRef]
- Munns, R.; Tester, M. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 2008, 59, 651–681. [Google Scholar] [CrossRef]
- Shabala, S.; Cuin, T.A. Potassium transport and plant salt tolerance. Physiol. Plant. 2008, 133, 651–669. [Google Scholar] [CrossRef] [PubMed]
- Farooq, M.; Park, J.R.; Jang, Y.H.; Kim, E.G.; Kim, M.K. Rice cultivars under salt stress show differential expression of genes related to the regulation of Na+/K+ balance. Front. Plant Sci. 2021, 12, 680131. [Google Scholar] [CrossRef] [PubMed]
- Sun, Y.; Kong, X.; Li, C.; Liu, Y.; Ding, Z. Potassium retention under salt stress is associated with natural variation in salinity tolerance among Arabidopsis accessions. PLoS ONE 2015, 10, e0124032. [Google Scholar] [CrossRef] [PubMed]
- Mansour, M.M.F.; Ali, E.F. Evaluation of proline functions in saline conditions. Phytochemistry 2017, 140, 52–68. [Google Scholar] [CrossRef] [PubMed]
- Gao, Y.; Lu, Y.; Wu, M.; Liang, E.; Li, Y.; Zhang, D.; Yin, Z.; Ren, X.; Dai, Y.; Deng, D.; et al. Ability to remove Na+ and retain K+ correlates with salt tolerance in two maize inbred lines seedlings. Front. Plant Sci. 2016, 7, 1716. [Google Scholar] [CrossRef]
- Mansour, M.M.F.; Hassan, F.A.S. How salt stress responsive proteins regulate plant adaptation to saline conditions. Plant Mol. Biol. 2022, 108, 175–224. [Google Scholar] [CrossRef] [PubMed]
- Shabala, S.; Wu, H.H.; Bose, J. Salt stress sensing and early signalling events in plant roots: Current knowledge and hypothesis. Plant Sci. 2015, 241, 109–119. [Google Scholar] [CrossRef]
- Hernández, J.A.; Almansa, M.S. Short-term effects of salt stress on antioxidant systems and leaf water relations of pea leaves. Physiol. Plant. 2002, 115, 251–257. [Google Scholar] [CrossRef]
- Feng, J.P.; Ma, W.Y.; Ma, Z.B.; Ren, Z.Y.; Zhou, Y.; Zhao, J.J.; Li, W.; Liu, W. GhNHX3D, a vacuolar-localized Na+/H+ antiporter, positively regulates salt response in upland cotton. Int. J. Mol. Sci. 2021, 22, 4047. [Google Scholar] [CrossRef]
- Jabeen, Z.; Irshad, F.; Hussain, N.; Han, Y.; Zhang, G.P. NHX-type Na+/H+ antiporter gene expression under different salt levels and allelic diversity of HvNHX in wild and cultivated barleys. Front. Genet. 2022, 12, 809–988. [Google Scholar] [CrossRef]
- Zhang, M.; Li, Y.D.; Liang, X.Y.; Lu, M.H.; Lai, J.S.; Song, W.B.; Jiang, C.F. A teosinte-derived allele of an HKT1 family sodium transporter improves salt tolerance in maize. Plant Biotechnol. J. 2022, 21, 97–108. [Google Scholar] [CrossRef]
- Pandolfi, C.; Azzarello, E.; Mancuso, S.; Shabala, S. Acclimation improves salt stress tolerance in Zea mays plants. J. Plant Physiol. 2016, 201, 1–8. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Z.B.; Zhang, J.W.; Chen, Y.J.; Li, R.F.; Wang, H.Z.; Wei, J.H. Genome wide analysis and identification of HAK potassium transporter gene family in maize (Zea mays L.). Mol. Biol. Rep. 2012, 39, 846573. [Google Scholar] [CrossRef]
- Qin, Y.J.; Wu, W.H.; Wang, Y. ZmHAK5 and ZmHAK1 function in K+ uptake and distribution in maize under low K+ conditions. J. Integr. Plant Biol. 2019, 61, 691–705. [Google Scholar] [CrossRef]
- Zhang, M.; Liang, X.Y.; Wang, L.M.; Cao, Y.B.; Song, W.B.; Shi, J.P.; Lai, J.S.; Jiang, C.F. A HAK family Na+ transporter confers natural variation of salt tolerance in maize. Nat. Plants 2019, 5, 12971308. [Google Scholar] [CrossRef] [PubMed]
- Riedelsberger, J.; Miller, J.K.; Valdebenito-Maturana, B.; Piñeros, M.A.; González, W.; Dreyer, I. Plant HKT channels: An updated view on structure, function and gene regulation. Int. J. Mol. Sci. 2021, 22, 1892. [Google Scholar] [CrossRef]
- Hussain, S.; Zhang, R.; Liu, S.L.; Li, R.K.; Zhou, Y.C.; Chen, Y.L.; Hou, H.Y.; Dai, Q.G. Transcriptome-wide analysis revealed the potential of the high-affinity potassium transporter (HKT) gene family in rice salinity tolerance via ion homeostasis. Bioengineering 2022, 9, 410. [Google Scholar] [CrossRef]
- Jiang, Z.L.; Song, G.S.; Shan, X.H.; Wei, Z.Y.; Liu, Y.Z.; Jiang, C.; Jiang, Y.; Jin, F.X.; Li, Y.D. Association analysis and identification of ZmHKT1;5 variation with salt stress tolerance. Front. Plant Sci. 2018, 9, 1485. [Google Scholar] [CrossRef]
- Venkataraman, G.; Shabala, S.; Véry, A.A.; Hariharan, G.N.; Somasundaram, S.; Pulipati, S.; Sellamuthu, G.; Harikrishnan, M.; Kumari, K.; Shabala, L.; et al. To exclude orto accumulate? Revealing the role of the sodium HKT1;5 transporter in plant adaptive responses to varying soil salinity. Plant Physiol. Biochem. 2021, 169, 333–342. [Google Scholar] [CrossRef]
- Zhang, M.; Cao, Y.B.; Wang, Z.P.; Wang, Z.Q.; Shi, J.P.; Liang, X.Y.; Song, W.B.; Chen, Q.J.; Lai, J.S.; Jiang, C.F. A retrotransposon in an HKT1 family sodium transporter causes variation of leaf Na+ exclusion and salt tolerance in maize. New Phytol. 2018, 217, 1161–1176. [Google Scholar] [CrossRef]
- Cao, Y.B.; Liang, X.Y.; Yin, P.; Zhang, M.; Jiang, C.F. A domestication-associated reduction in K+-preferring HKT transporter activity underlies maize shoot K+ accumulation and salt tolerance. New Phytol. 2019, 222, 301–317. [Google Scholar] [CrossRef]
- Paul, A.; Chatterjee, A.; Subrahmanya, S.; Shen, G.X.; Mishra, N. NHX gene family Camellia sinensis: In-silico Genome-wide identification, expression profiles, and regulatory network analysis. Front. Plant Sci. 2021, 12, 777884. [Google Scholar] [CrossRef]
- Sun, Y.L.; Mu, C.H.; Liu, X. Key factors identified by proteomic analysis in maize (Zea mays L.) seedlings’ response to long-term exposure to different phosphate levels. Proteome Sci. 2018, 16, 19. [Google Scholar] [CrossRef]
- Sun, Y.L.; Mu, C.H.; Zheng, H.X.; Lu, S.H.; Zhang, H.; Zhang, X.C.; Liu, X. Exogenous Pi supplementation improved the salt tolerance of maize (Zea mays L.) by promoting Na+ exclusion. Sci. Rep. 2018, 8, 16203. [Google Scholar] [CrossRef]
- Sun, Y.L.; Zheng, H.X. Divergent molecular and physiological response of two maize breeding lines under phosphate deficiency. Plant Mol. Biol. Rep. 2022, 40, 197–207. [Google Scholar] [CrossRef]
- Rady, M.M.; Elrys, A.S.; Abo El-Maati, M.F.; Desoky, E.M. Interplaying roles of silicon and proline effectively improve salt and cadmium stress tolerance in Phaseolus vulgaris plant. Plant Physiol. Biochem. 2019, 139, 558–568. [Google Scholar] [CrossRef]
- Quan, R.D.; Shang, M.; Zhang, H.; Zhao, Y.X.; Zhang, J.R. Improved chilling tolerance by transformation with betA gene for the enhancement of glycine betaine synthesis in maize. Plant Sci. 2004, 166, 141–149. [Google Scholar] [CrossRef]
- Gavaghan, C.L.; Li, J.V.; Hadfield, S.T.; Hole, S.; Nicholson, J.K.; Wilson, I.D.; Howe, P.W.A.; Stanley, P.D.; Holmes, E. Application of NMR-based metabolomics to the investigation of salt stress in maize (Zea mays). Phytochem. Anal. 2010, 22, 214–224. [Google Scholar] [CrossRef]
- Henry, C.; Bledsoe, S.W.; Griffiths, C.A.; Kollman, A.; Paul, M.J.; Sakr, S.; Lagrimini, L.M. Differential role for trehalose metabolism in salt-stressed maize. Plant Physiol. 2015, 169, 10721089. [Google Scholar] [CrossRef]
- Chen, F.; Fang, P.; Zeng, W.; Ding, Y.; Zhuang, Z.; Peng, Y. Comparing transcriptome expression profiles to reveal the mechanisms of salt tolerance and exogenous glycine betaine mitigation in maize seedlings. PLoS ONE 2020, 15, e0233616. [Google Scholar] [CrossRef]
- Zhu, M.; Li, Q.; Zhang, Y.; Zhang, M.; Li, Z. Glycine betaine increases salt tolerance in maize (Zea mays L.) by regulating Na+ homeostasis. Front. Plant Sci. 2022, 13, 978304. [Google Scholar] [CrossRef]
- Rohman, M.M.; Islam, M.R.; Monsur, M.B.; Amiruzzaman, M.; Fujita, M.; Hasanuzzaman, M. Trehalose protects maize plants from salt stress and phosphorus deficiency. Plants 2019, 8, 568. [Google Scholar] [CrossRef]
- Rady, M.M.; Hemida, K.A. Sequenced application of ascorbate-proline-glutathione improves salt tolerance in maize seedlings. Ecotoxicol. Environ. Saf. 2016, 133, 252–259. [Google Scholar] [CrossRef]
- Sandhu, D.; Pudussery, M.V.; Kumar, R.; Pallete, A.; Markley, P.; Bridges, W.C.; Sekhon, R.S. Characterization of natural genetic variation identifies multiple genes involved in salt tolerance in maize. Funct. Integr. Genom. 2019, 20, 261–275. [Google Scholar] [CrossRef]
- Zhang, X.; Liu, P.; Qing, C.; Yang, C.; Shen, Y.; Ma, L. Comparative transcriptome analyses of maize seedling root responses to salt stress. Peer J. 2021, 9, e10765. [Google Scholar] [CrossRef]
- Luo, M.J.; Zhao, Y.X.; Wang, Y.D.; Shi, Z.; Zhang, P.P.; Zhang, Y.X.; Song, W.; Zhao, J.R. Comparative proteomics of contrasting maize genotypes provides insights into salt stress tolerance mechanisms. J. Proteome Res. 2018, 17, 141–153. [Google Scholar] [CrossRef]
- Chen, F.; Fang, P.; Peng, Y.; Zeng, W.; Zhao, X.; Ding, Y.; Zhuang, Z.; Gao, Q.; Ren, B. Comparative proteomics of salt-tolerant and salt-sensitive maize inbred lines to reveal the molecular mechanism of salt tolerance. Int. J. Mol. Sci. 2019, 20, 4725. [Google Scholar] [CrossRef] [PubMed]
- Zhao, X.Y.; Bai, X.; Jiang, C.F.; Li, Z. Phosphoproteomic analysis of two contrasting maize inbred lines provides insights into the mechanism of salt-stress tolerance. Int. J. Mol. Sci. 2019, 20, 1886. [Google Scholar] [CrossRef] [PubMed]
- Weng, Q.Y.; Zhao, Y.M.; Zhao, Y.N.; Song, X.Q.; Yuan, J.C.; Liu, Y.H. Identification of salt stress responsive proteins in maize (Zea may) seedlings using iTRAQ Based proteomic technique. Iran. J. Biotechnol. 2021, 19, e2512. [Google Scholar] [CrossRef] [PubMed]
- Richter, J.A.; Erban, A.; Kopka, J.; Zörb, C. Metabolic contribution to salt stress in two maize hybrids with contrasting resistance. Plant Sci. 2015, 233, 107–115. [Google Scholar] [CrossRef]
- Liang, X.Y.; Liu, S.Y.; Wang, T.; Li, F.R.; Cheng, J.K.; Lai, J.S.; Qin, F.; Li, Z.; Wang, X.F.; Jiang, C.F. Metabolomics driven gene mining and genetic improvement of tolerance to salt-induced osmotic stress in maize. New Phytol. 2021, 23, 2355–2370. [Google Scholar] [CrossRef]
- Luo, X.; Wang, B.C.; Gao, S.; Zhang, F.; Terzaghi, W.; Dai, M.Q. Genome-wide association study dissects the genetic bases of salt tolerance in maize seedlings. J. Integr. Plant Biol. 2019, 61, 658–674. [Google Scholar] [CrossRef]
- Liu, P.; Zhang, Y.C.; Zou, C.Y.; Yang, C.; Pan, G.T.; Ma, L.L.; Shen, Y.O. Integrated analysis of long noncoding RNAs and mRNAs reveals the regulatory network of maize seedling root responding to salt stress. BMC Genom. 2022, 23, 50. [Google Scholar] [CrossRef]
- Liu, P.; Zhu, Y.X.; Liu, H.; Liang, Z.J.; Zhang, M.Y.; Zou, C.Y.; Yuan, G.S.; Shibin Gao, S.B.; Pan, G.T.; Shen, Y.O.; et al. A combination of a genome-wide association study and a transcriptome analysis reveals circRNAs as new regulators involved in the response to salt stress in maize. Int. J. Mol. Sci. 2022, 23, 9755. [Google Scholar] [CrossRef]
- Kotula, L.; Caparros, G.P.; Zörb, C.; Colmer, T.D.; Flowers, T.J. Improving crop salt tolerance using transgenic approaches: An update and physiological analysis. Plant Cell Environ. 2020, 43, 2932–2956. [Google Scholar] [CrossRef]
- Steppuhn, H.; Asay, K.H. Emergence, height, and yield of tall, NewHy, and green wheatgrass forage crops grown in saline root zones. Can. J. Plant Sci. 2005, 85, 863–875. [Google Scholar] [CrossRef]
- Omoto, E.; Iwasaki, Y.; Miyake, H.; Taniguchi, M. Salinity induces membrane structure and lipid changes in maize mesophyll and bundle sheath chloroplasts. Physiol. Plant. 2016, 157, 13–23. [Google Scholar] [CrossRef]
- Fu, L.B.; Shen, Q.F.; Kuang, L.H.; Yu, J.H.; Wu, D.Z.; Zhang, G.P. Metabolite profiling and gene expression of Na+/K+ transporter analyses reveal mechanisms of the difference in salt tolerance between barley and rice. Plant Physiol. Biochem. 2018, 130, 248–257. [Google Scholar] [CrossRef] [PubMed]
- Wang, H.; An, T.T.; Huang, D.; Liu, R.J.; Xu, B.C.; Zhang, S.Q.; Deng, X.P.; Siddique, K.H.M.; Chen, Y.L. Arbuscular mycorrhizal symbioses alleviating salt stress in maize is associated with a decline in root-to-leaf gradient of Na+/K+ ratio. BMC Plant Biol. 2021, 21, 457. [Google Scholar] [CrossRef]
- Aleman, F.; Nieves-Cordones, M.; Martinez, V.; Rubio, F. Root K+ acquisition in plants: The Arabidopsis thaliana model. Plant Cell Physiol. 2011, 52, 1603–1612. [Google Scholar] [CrossRef]
- Ma, W.; Ren, Z.; Zhou, Y.; Zhao, J.; Zhang, F.; Feng, J.; Liu, W.; Ma, X. Genome-Wide Identification of the Gossypium hirsutum NHX genes reveals that the endosomal-type GhNHX4A is critical for the salt tolerance of cotton. Int. J. Mol. Sci. 2020, 21, 7712. [Google Scholar] [CrossRef] [PubMed]
- Hayat, S.; Hayat, Q.; Alyemeni, M.N.; Wani, A.S.; Pichtel, J.; Ahmad, A. Role of proline under c hanging environments: A review. Plant Signal Behav. 2012, 7, 1456–1466. [Google Scholar] [CrossRef] [PubMed]
- Arias-Baldrich, C.; Bosch, N.; Begines, D.; Feria, A.B.; Monreal, J.A.; García-Mauriño, S.J. Proline synthesis in barley under iron deficiency and salinity. Plant Physiol. 2015, 183, 121–129. [Google Scholar] [CrossRef]
- Wang, M.Q.; Wang, Y.F.; Zhang, Y.F.; Li, C.X.; Gong, S.C.; Yan, S.Q.; Li, G.L.; Hu, G.H.; Ren, H.L.; Yang, J.F.; et al. Comparative transcriptome analysis of salt-sensitive and salt-tolerant maize reveals potential mechanisms to enhance salt resistance. Genes Genom. 2019, 41, 781801. [Google Scholar] [CrossRef]
- Sun, Y.L.; Mu, C.H.; Chen, Y.; Kong, X.P.; Xu, Y.C.; Zheng, H.X.; Zhang, H.; Wang, Q.C.; Xue, Y.F.; Li, Z.X.; et al. Comparative transcript profiling of maize inbreds in response to long-term phosphorus deficiency stress. Plant Physiol. Biochem. 2016, 109, 467481. [Google Scholar] [CrossRef]
- Liu, X.; Su, S. Growth and physiological response of Viola tricolor L. to NaCl and NaHCO3 stress. Plants 2023, 12, 178. [Google Scholar] [CrossRef]
Plants | Treatments | Plant Height (cm) | Leaf Width (cm) | Leaf Length (cm) | Root Length (cm) |
---|---|---|---|---|---|
QXN233 | Control | 59.75 ± 0.30 a | 2.65 ± 0.30 a | 50.75 ± 0.30 a | 41.00 ± 0.90 b |
200 mM NaCl | 37.25 ± 5.50 c | 1.85 ± 0.10 b | 43.00 ± 5.00 b | 18.25± 1.50 d | |
QXH0121 | Control | 46.00 ± 4.20 b | 1.95 ± 0.07 ab | 56.00 ± 1.40 a | 60.00± 4.50 a |
200 mM NaCl | 34.25 ± 0.30 c | 1.80 ± 0.04 b | 43.00 ± 1.70 b | 40.00 ± 2.40 c | |
QXN233 | Control | 58.95 ± 0.34 a | 2.75 ± 0.36 a | 51.75 ± 0.26 a | 40.00 ± 0.67 b |
400 mM NaCl | 35.15 ± 3.40 c | 1.60 ± 0.14 b | 40.12 ± 4.90 b | 17.85 ± 1.34 d | |
QXH0121 | Control | 45.69 ± 3.68 b | 1.97 ± 0.11 ab | 55.79 ± 1.10 a | 59.46± 4.34 a |
400 mM NaCl | 34.75 ± 0.29 c | 1.67 ± 0.13 b | 42.19 ± 1.15 b | 39.14 ± 3.16 c |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Zhao, Z.; Zheng, H.; Wang, M.; Guo, Y.; Wang, Y.; Zheng, C.; Tao, Y.; Sun, X.; Qian, D.; Cao, G.; et al. Reshifting Na+ from Shoots into Long Roots Is Associated with Salt Tolerance in Two Contrasting Inbred Maize (Zea mays L.) Lines. Plants 2023, 12, 1952. https://doi.org/10.3390/plants12101952
Zhao Z, Zheng H, Wang M, Guo Y, Wang Y, Zheng C, Tao Y, Sun X, Qian D, Cao G, et al. Reshifting Na+ from Shoots into Long Roots Is Associated with Salt Tolerance in Two Contrasting Inbred Maize (Zea mays L.) Lines. Plants. 2023; 12(10):1952. https://doi.org/10.3390/plants12101952
Chicago/Turabian StyleZhao, Zhenyang, Hongxia Zheng, Minghao Wang, Yaning Guo, Yingfei Wang, Chaoli Zheng, Ye Tao, Xiaofeng Sun, Dandan Qian, Guanglong Cao, and et al. 2023. "Reshifting Na+ from Shoots into Long Roots Is Associated with Salt Tolerance in Two Contrasting Inbred Maize (Zea mays L.) Lines" Plants 12, no. 10: 1952. https://doi.org/10.3390/plants12101952