Salt tolerance in Brassicaceae crops: physiological responses and molecular mechanisms
Tenghui Wang
A , Xuyan Yang A , Zhenyu Fan A B and Yushu Wang A B *
A College of Life Sciences, Agriculture and Forestry, Qiqihar University,
B Heilongjiang Provincial Key Laboratory of Resistance Gene Engineering and Protection of Biodiversity in Cold Areas, College of Life Sciences, Agriculture and Forestry, Qiqihar University, Qiqihar, China.
Abstract
Soil salinisation is a growing threat to global agriculture, reducing crop yields. Brassicaceae crops are vital vegetables and cash crops. Salt stress significantly affects the growth and development of Brassicaceae crops. A better understanding of the molecular and physiological mechanisms of salt tolerance is of theoretical and practical importance to improve Brassicaceae crop’s salt tolerance and crop quality. Combined with previous research results, we discuss recent advances in research on salt stress response and salt tolerance in Brassicaceae crops. We summarised recent research progress on the physiological and molecular mechanisms of ionic homeostasis, antioxidant regulation, hormonal regulation and accumulation of osmotic-adjustment substances. We also discussed the molecular mechanism of Brassicaceae crop salt tolerant varieties from the perspective of differentially expressed genes, differentially expressed proteins and metabolites through transcriptome, proteome and metabonomic analysis methods. This paper summarises the molecular mechanisms in the perspective of differentially expressed genes, differentially expressed proteins, and metabolites through transcriptomic, proteome and metabolomics analysis. The review provides abundant data for accelerating the breeding of salt-tolerant Brassicaceae and laid a foundation for understanding the mechanism of salt tolerance of Brassicaceae crops and breeding salt-tolerance varieties.
Keywords: abiotic stress, Brassicaceae crop, hormone regulation, omics analysis, physiological alterations, salt stress, sodium, stress response.
References
Acosta-Motos JR, Hernández JA, Álvarez S, Barba-Espín G, Sánchez-Blanco MJ (2017) The long-term resistance mechanisms, critical irrigation threshold and relief capacity shown by Eugenia myrtifolia plants in response to saline reclaimed water. Plant Physiology and Biochemistry 111, 244-256.
| Crossref | Google Scholar |
Adetunji AE, Sershen , Varghese B, Pammenter NW (2020) Effects of inorganic salt solutions on vigour, viability, oxidative metabolism and germination enzymes in aged cabbage and lettuce seeds. Plants 9, 1164 PMID:.
| Crossref | Google Scholar | PubMed |
Ahmed NU, Park J-I, Jung H-J, et al. (2012) Molecular characterization of stress resistance-related chitinase genes of Brassica rapa. Plant Physiology and Biochemistry 58, 106-115 PMID:.
| Crossref | Google Scholar | PubMed |
Ali S, Mir ZA, Tyagi A, et al. (2017) Identification and comparative analysis of Brassica juncea pathogenesis-related genes in response to hormonal, biotic and abiotic stresses. Acta Physiologiae Plantarum 39, 268.
| Crossref | Google Scholar |
Ashraf M, Harris PJC (2004) Potential biochemical indicators of salinity tolerance in plants. Plant Science 166, 3-16.
| Crossref | Google Scholar |
Bandurska H (2004) Free proline accumulation in leaves of cultivated plant species under water deficit conditions. Acta Agrobotanica 57, 57-67.
| Crossref | Google Scholar |
Ben Rejeb K, Benzarti M, Debez A, et al. (2015) NADPH oxidase-dependent H2O2 production is required for salt-induced antioxidant defense in Arabidopsis thaliana. Journal of Plant Physiology 174, 5-15 PMID:.
| Crossref | Google Scholar | PubMed |
Chakraborty K, Bose J, Shabala L, et al. (2016a) Evaluating relative contribution of osmotolerance and tissue tolerance mechanisms toward salinity stress tolerance in three Brassica species. Physiologia Plantarum 158, 135-151 PMID:.
| Crossref | Google Scholar | PubMed |
Chakraborty K, Bose J, Shabala L, et al. (2016b) Difference in root K+ retention ability and reduced sensitivity of K+-permeable channels to reactive oxygen species confer differential salt tolerance in three Brassica species. Journal of Experimental Botany 67, 4611-4625 PMID:.
| Crossref | Google Scholar | PubMed |
Chen K, Li G-J, Bressan RA, et al. (2020) Abscisic acid dynamics, signaling, and functions in plants. Journal of Integrative Plant Biology 62, 25-54 PMID:.
| Crossref | Google Scholar | PubMed |
Chevilly S, Dolz-Edo L, Morcillo L, et al. (2021) Identification of distinctive physiological and molecular responses to salt stress among tolerant and sensitive cultivars of broccoli (Brassica oleracea var. Italica). BMC Plant Biology 21, 488.
| Crossref | Google Scholar |
Chini A, Fonseca S, Fernández G, Adie B, Chico JM, Lorenzo O, García-Casado G, López-Vidriero I, Lozano FM, Ponce MR, Micol JL, Solano R (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448((7154)), 666-671.
| Crossref | Google Scholar |
Cleland J (2013) World population growth; past, present and future. Environmental and Resource Economics 55, 543-554.
| Crossref | Google Scholar |
Cui F, Sui N, Duan G, et al. (2018) Identification of metabolites and transcripts involved in salt stress and recovery in peanut. Frontiers in Plant Science 9, 217 PMID:.
| Crossref | Google Scholar | PubMed |
Damaris RN, Lin Z, Yang P, et al. (2019) The rice alpha-amylase, conserved regulator of seed maturation and germination. International Journal of Molecular Sciences 20, 450 PMID:.
| Crossref | Google Scholar | PubMed |
Di Martino C, Delfine S, Pizzuto R, et al. (2003) Free amino acids and glycine betaine in leaf osmoregulation of spinach responding to increasing salt stress. New Phytologist 158, 455-463 PMID:.
| Crossref | Google Scholar | PubMed |
Du X, Yu R, Shi C, et al. (2021) Comparative transcriptomics reveals osmotic and ionic stress key genes contributing to the difference in the salinity tolerance of two pak choi cultivars. Environmental and Experimental Botany 191, 104621.
| Crossref | Google Scholar |
Duan X, Dai C, Li Z, et al. (2016) Ectopic over-expression of BoHO1, a cabbage heme oxygenase gene, improved salt tolerance in Arabidopsis: a case study on proteomic analysis. Journal of Plant Physiology 196–197, 1-13 PMID:.
| Crossref | Google Scholar | PubMed |
El Moukhtari A, Cabassa-Hourton C, Farissi M, et al. (2020) How does proline treatment promote salt stress tolerance during crop plant development? Frontiers in Plant Science 11, 1127 PMID:.
| Crossref | Google Scholar | PubMed |
Fang Y, Li J, Jiang J, et al. (2017) Physiological and epigenetic analyses of Brassica napus seed germination in response to salt stress. Acta Physiologiae Plantarum 39, 128.
| Crossref | Google Scholar |
Fernie AR, Schauer N (2009) Metabolomics-assisted breeding: a viable option for crop improvement? Trends in Genetics 25, 39-48 PMID:.
| Crossref | Google Scholar | PubMed |
Fiehn O (2002) Metabolomics – the link between genotypes and phenotype. Plant Molecular Biology 48(1–2), 155-71.
| Google Scholar |
Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytologist 179, 945-963 PMID:.
| Crossref | Google Scholar | PubMed |
Gavaghan CL, Li JV, Hadfield ST, et al. (2011) Application of NMR-based metabolomics to the investigation of salt stress in maize (Zea mays). Phytochemical Analysis 22, 214-224 PMID:.
| Crossref | Google Scholar | PubMed |
Gogna M, Bhatla SC (2019) Biochemical mechanisms regulating salt tolerance in sunflower. Plant Signaling & Behavior 14, 1670597 PMID:.
| Crossref | Google Scholar | PubMed |
Habibi G (2015) Contrastive response of Brassica napus L. to exogenous salicylic acid, selenium and silicon supplementation under water stress. Archives of Biological Sciences 67, 397-404.
| Crossref | Google Scholar |
Hadiarto T, Tran L-SP (2011) Progress studies of drought-responsive genes in rice. Plant Cell Reports 30, 297-310 PMID:.
| Crossref | Google Scholar | PubMed |
Hajiboland R, Bahrami-Rad S, Akhani H, et al. (2018) Salt tolerance mechanisms in three Irano-Turanian Brassicaceae halophytes relatives of Arabidopsis thaliana. Journal of Plant Research 131, 1029-1046 PMID:.
| Crossref | Google Scholar | PubMed |
Hajiboland R, Bahrami-Rad S, Zeinalzade N, et al. (2020) Differential functional traits underlying the contrasting salt tolerance in Lepidium species. Plant and Soil 448, 315-334.
| Crossref | Google Scholar |
Halliwell B (1987) Oxidative damage, lipid peroxidation and antioxidant protection in chloroplasts. Chemistry and Physics of Lipids 44, 327-340.
| Crossref | Google Scholar |
He X-J, Mu R-L, Cao W-H, et al. (2005) AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. The Plant Journal 44, 903-916 PMID:.
| Crossref | Google Scholar | PubMed |
He L, Li J, Shi L, et al. (2021) Exogenous metabolites spray, which identified from metabolomics analysis and transcriptomic analysis, can improve salt tolerance of Chinese cabbages (Brassica rapa L. ssp pekinensis). Journal of Plant Interactions 16, 452-461.
| Crossref | Google Scholar |
Ishikawa A, Tanaka H, Kato C, et al. (2005) Molecular characterization of the ZKT gene encoding a protein with PDZ, K-Box, and TPR motifs in Arabidopsis. Bioscience, Biotechnology, and Biochemistry 69, 972-978 PMID:.
| Crossref | Google Scholar | PubMed |
Jan SA, Shinwari ZK, Rabbani MA (2016) Agro-morphological and physiological responses of Brassica rapa ecotypes to salt stress. Pakistan Journal of Botany 48, 1379-1384.
| Google Scholar |
Jia H, Shao M, He Y, et al. (2015) Proteome dynamics and physiological responses to short-term salt stress in Brassica napus leaves. PLoS ONE 10, e0144808 PMID:.
| Crossref | Google Scholar | PubMed |
Jia K, Yan C, Yan H, et al. (2020) Physiological responses of turnip (Brassica rapa L. subsp. rapa) seedlings to salt stress. HortScience 55, 1567-1574.
| Crossref | Google Scholar |
Kazan K, Manners JM (2012) JAZ repressors and the orchestration of phytohormone crosstalk. Trends in Plant Science 17, 22-31 PMID:.
| Crossref | Google Scholar | PubMed |
Khalid M, Saeed-ur-Rahman , Ali M, et al. (2021) Salicylic acid mediated protection of Brassica campestris sp. chinensis from saline stress via SA receptor NPR1 dependent transcriptional regulation and biosynthesis of related biochemicals. Environmental Technology & Innovation 24, 101950.
| Crossref | Google Scholar |
Kusuda H, Koga W, Kusano M, et al. (2015) Ectopic expression of myo-inositol 3-phosphate synthase induces a wide range of metabolic changes and confers salt tolerance in rice. Plant Science 232, 49-56 PMID:.
| Crossref | Google Scholar | PubMed |
Liang W, Cui W, Ma X, et al. (2014) Function of wheat Ta-UnP gene in enhancing salt tolerance in transgenic Arabidopsis and rice. Biochemical and Biophysical Research Communications 450, 794-801 PMID:.
| Crossref | Google Scholar | PubMed |
Lodeyro AF, Carrillo N (2015) Salt stress in higher plants: mechanisms of toxicity and defensive responses. In ‘Stress responses in plants’. (Eds B Tripathi, M Müller) pp. 1–33. (Springer: Cham, Switzerland). doi:10.1007/978-3-319-13368-3_1
Long W, Zou X, Zhang X (2015) Transcriptome analysis of canola (Brassica napus) under salt stress at the germination stage. PLoS ONE 10, e0116217 PMID:.
| Crossref | Google Scholar | PubMed |
Lu H, Chandrasekar B, Oeljeklaus J, et al. (2015) Subfamily-specific fluorescent probes for cysteine proteases display dynamic protease activities during seed germination. Plant Physiology 168, 1462-1475 PMID:.
| Crossref | Google Scholar | PubMed |
Luo J, Tang S, Peng X, et al. (2015) Elucidation of cross-talk and specificity of early response mechanisms to salt and PEG-simulated drought stresses in Brassica napus using comparative proteomic analysis. PLoS ONE 10, e0138974 PMID:.
| Crossref | Google Scholar | PubMed |
Mahajan S, Pandey GK, Tuteja N (2008) Calcium- and salt-stress signaling in plants: shedding light on SOS pathway. Archives of Biochemistry and Biophysics 471, 146-158 PMID:.
| Crossref | Google Scholar | PubMed |
Martin JA, Wang Z (2011) Next-generation transcriptome assembly. Nature Reviews Genetics 12, 671-682 PMID:.
| Crossref | Google Scholar | PubMed |
Misra BB, Langefeld C, Olivier M, et al. (2019) Integrated omics: tools, advances and future approaches. Journal of Molecular Endocrinology 62, R21-R45.
| Crossref | Google Scholar |
Morgenthal K, Weckwerth W, Steuer R (2006) Metabolomic networks in plants: transitions from pattern recognition to biological interpretation. Biosystems 83, 108-117 PMID:.
| Crossref | Google Scholar | PubMed |
Muchate NS, Nikalje GC, Rajurkar NS, et al. (2016) Plant Salt Stress: Adaptive Responses, Tolerance Mechanism and Bioengineering for Salt Tolerance. The Botanical Review 82, 371-406.
| Crossref | Google Scholar |
Munns R (2002) Comparative physiology of salt and water stress. Plant, Cell & Environment 25, 239-250.
| Crossref | Google Scholar |
Munns R (2005) Genes and salt tolerance: bringing them together. New Phytologist 167, 645-663 PMID:.
| Crossref | Google Scholar | PubMed |
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annual Review of Plant Biology 59, 651-681 PMID:.
| Crossref | Google Scholar | PubMed |
Mustafa G, Komatsu S (2021) Plant proteomic research for improvement of food crops under stresses: a review. Molecular omics 17(6), 860-880.
| Crossref | Google Scholar |
Oomen RJFJ, Benito B, Sentenac H, et al. (2012) HKT2;2/1, a K+-permeable transporter identified in a salt-tolerant rice cultivar through surveys of natural genetic polymorphism. The Plant Journal 71, 750-762 PMID:.
| Crossref | Google Scholar | PubMed |
Pan Y-J, Liu L, Lin Y-C (2016) Ethylene antagonizes salt-induced growth retardation and cell death process via transcriptional controlling of ethylene-, BAG- and senescence-associated genes in Arabidopsis. Frontiers in Plant Science 7, 696.
| Crossref | Google Scholar |
Pan J, Zhang L, Chen M, et al. (2022) Identification and charactering of APX genes provide new insights in abiotic stresses response in Brassica napus. PeerJ 10, e13166 PMID:.
| Crossref | Google Scholar | PubMed |
Pavlović I, Pěnčík A, Novák O, et al. (2018) Short-term salt stress in Brassica rapa seedlings causes alterations in auxin metabolism. Plant Physiology and Biochemistry 125, 74-84 PMID:.
| Crossref | Google Scholar | PubMed |
Per TS, Khan NA, Reddy PS, et al. (2017) Approaches in modulating proline metabolism in plants for salt and drought stress tolerance: phytohormones, mineral nutrients and transgenics. Plant Physiology and Biochemistry 115, 126-140 PMID:.
| Crossref | Google Scholar | PubMed |
Pittman JK (2012) Multiple transport pathways for mediating intracellular pH homeostasis: the contribution of H+/ion exchangers. Frontiers in Plant Science 3,.
| Crossref | Google Scholar |
Postiglione AE, Muday GK (2020) The role of ROS homeostasis in ABA-induced guard cell signaling. Frontiers in Plant Science 11, 968 PMID:.
| Crossref | Google Scholar | PubMed |
Prasad K, Sharmila P, Kumar PA, et al. (2000) Transformation of Brassica juncea (L.) Czern with bacterial codA gene enhances its tolerance to salt stress. Molecular Breeding 6, 489-499.
| Crossref | Google Scholar |
Qin H, Huang R (2020) The phytohormonal regulation of Na+/K+ and reactive oxygen species homeostasis in rice salt response. Molecular Breeding 40, 47.
| Crossref | Google Scholar |
Qiu N, Liu Q, Li J, et al. (2017) Physiological and transcriptomic responses of Chinese cabbage (Brassica rapa L. ssp. Pekinensis) to salt stress. International Journal of Molecular Sciences 18, 1953 PMID:.
| Crossref | Google Scholar | PubMed |
Richter JA, Erban A, Kopka J, et al. (2015) Metabolic contribution to salt stress in two maize hybrids with contrasting resistance. Plant Science 233, 107-115 PMID:.
| Crossref | Google Scholar | PubMed |
Rodríguez-Rosales MP, Gálvez FJ, Huertas R, et al. (2009) Plant NHX cation/proton antiporters. Plant Signaling & Behavior 4, 265-276 PMID:.
| Crossref | Google Scholar | PubMed |
Roy SJ, Negrão S, Tester M (2014) Salt resistant crop plants. Current Opinion in Biotechnology 26, 115-124 PMID:.
| Crossref | Google Scholar | PubMed |
Sadughi M, Sharifan H, Pessarakli M (2015) Effects of Caspian Sea Water on Sugar Beet Seed Germination. Journal of Plant Nutrition 38(11), 1685-1693.
| Crossref | Google Scholar |
Seo YJ, Park J-B, Cho Y-J, et al. (2010) Overexpression of the ethylene-responsive factor gene BrERF4 from Brassica rapa increases tolerance to salt and drought in Arabidopsis plants. Molecules and Cells 30, 271-277 PMID:.
| Crossref | Google Scholar | PubMed |
Shabala S, Cuin TA (2008) Potassium transport and plant salt tolerance. Physiologia Plantarum 133, 651-669 PMID:.
| Crossref | Google Scholar | PubMed |
Shabala S, Pottosin II (2010) Potassium and potassium-permeable channels in plant salt tolerance. In ‘Ion channels and plant stress responses’. (Eds V Demidchik, F Maathuis) pp. 87–110. (Springer: Berlin, Heidelberg, Germany) doi:10.1007/978-3-642-10494-7_5
Shahzad B, Rehman A, Tanveer M, et al. (2022) Salt stress in brassica: effects, tolerance mechanisms, and management. Journal of Plant Growth Regulation 41, 781-795.
| Crossref | Google Scholar |
Sharma A, Li X, Lim YP (2014) Comparative genomics of Brassicaceae crops. Breeding Science 64, 3-13 PMID:.
| Crossref | Google Scholar | PubMed |
Shi H, Quintero FJ, Pardo JM, et al. (2002) The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. The Plant Cell 14, 465-477 PMID:.
| Crossref | Google Scholar | PubMed |
Shi H, Lee B-H, Wu S-J, et al. (2003) Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nature Biotechnology 21, 81-85 PMID:.
| Crossref | Google Scholar | PubMed |
Shu J, Ma X, Ma H, et al. (2022) Transcriptomic, proteomic, metabolomic, and functional genomic approaches of Brassica napus L. during salt stress. PLoS ONE 17, e0262587 PMID:.
| Crossref | Google Scholar | PubMed |
Singh J, Singh V, Dutt V, et al. (2022) Insights into salt tolerance of mustard (Brassica juncea L. Czern&Coss): a metabolomics perspective. Environmental and Experimental Botany 194, 104760.
| Crossref | Google Scholar |
Slama I, Abdelly C, Bouchereau A, et al. (2015) Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress. Annals of Botany 115, 433-447 PMID:.
| Crossref | Google Scholar | PubMed |
Sun J, Wang MJ, Ding MQ, et al. (2010) H2O2 and cytosolic Ca2+ signals triggered by the PM H+-coupled transport system mediate K+/Na+ homeostasis in NaCl-stressed Populus euphratica cells. Plant, Cell & Environment 33, 943-958 PMID:.
| Crossref | Google Scholar | PubMed |
Sun X, Xu L, Wang Y, et al. (2016) Transcriptome-based gene expression profiling identifies differentially expressed genes critical for salt stress response in radish (Raphanus sativus L.). Plant Cell Reports 35, 329-346 PMID:.
| Crossref | Google Scholar | PubMed |
Sun X, Wang Y, Xu L, et al. (2017) Unraveling the root proteome changes and its relationship to molecular mechanism underlying salt stress response in radish (Raphanus sativus L.). Frontiers in Plant Science 8, 1192 PMID:.
| Crossref | Google Scholar | PubMed |
Tang X, Mu X, Shao H, et al. (2015) Global plant-responding mechanisms to salt stress: physiological and molecular levels and implications in biotechnology. Critical Reviews in Biotechnology 35, 425-437 PMID:.
| Crossref | Google Scholar | PubMed |
Tanou G, Molassiotis A, Diamantidis G (2009) Induction of reactive oxygen species and necrotic death-like destruction in strawberry leaves by salinity. Environmental and Experimental Botany 65, 270-281.
| Crossref | Google Scholar |
Tanveer M, Ahmed HAI (2020) ROS signalling in modulating salinity stress tolerance in plants//Salt and drought stress tolerance in plants. In ‘Salt and drought stress tolerance in plants: signaling networks and adaptive mechanisms’. (Eds M Hasanuzzaman, M Tanveer) pp. 299–314. (Springer: Cham, Switzerland) doi:10.1007/978-3-030-40277-8_11
Taïbi K, Taïbi F, Ait Abderrahim L, et al. (2016) Effect of salt stress on growth, chlorophyll content, lipid peroxidation and antioxidant defence systems in Phaseolus vulgaris L. South African Journal of Botany 105, 306-312.
| Crossref | Google Scholar |
Tohda R, Tanaka H, Mutoh R, et al. (2021) Crystal structure of higher plant heme oxygenase-1 and its mechanism of interaction with ferredoxin. Journal of Biological Chemistry 296, 100217 PMID:.
| Crossref | Google Scholar | PubMed |
Ton J, Flors V, Mauch-Mani B (2009) The multifaceted role of ABA in disease resistance. Trends in Plant Science 14, 310-317.
| Crossref | Google Scholar |
van Zelm E, Zhang Y, Testerink C (2020) Salt tolerance mechanisms of plants. Annual Review of Plant Biology 71, 403-433 PMID:.
| Crossref | Google Scholar | PubMed |
Verma D, Upadhyay SK, Singh K (2022) Characterization of APX and APX-R gene family in Brassica juncea and B. rapa for tolerance against abiotic stresses. Plant Cell Reports 41, 571-592 PMID:.
| Crossref | Google Scholar | PubMed |
Wan H, Qian J, Zhang H, et al. (2022) Combined transcriptomics and metabolomics analysis reveals the molecular mechanism of salt tolerance of Huayouza 62, an elite cultivar in rapeseed (Brassica napus L.). International Journal of Molecular Sciences 23, 1279 PMID:.
| Crossref | Google Scholar | PubMed |
Wang X, Hou C, Zheng K, et al. (2017) Overexpression of ERF96, a small ethylene response factor gene, enhances salt tolerance in Arabidopsis. Biologia Plantarum 61, 693-701.
| Crossref | Google Scholar |
Wang J, Qiu N, Wang P, Zhang W, Yang X, Chen M, Wang B, Sun J (2019) Na+ compartmentation strategy of Chinese cabbage in response to salt stress. Plant Physiology and Biochemistry 140, 151-157.
| Crossref | Google Scholar |
Wang W, Pang J, Zhang F, et al. (2022) Transcriptomic and metabolomics-based analysis of key biological pathways reveals the role of lipid metabolism in response to salt stress in the root system of Brassica napus. Plant Growth Regulation 97, 127-141.
| Crossref | Google Scholar |
Wani AS, Ahmad A, Hayat S, et al. (2013) Salt-induced modulation in growth, photosynthesis and antioxidant system in two varieties of Brassica juncea. Saudi Journal of Biological Sciences 20, 183-193 PMID:.
| Crossref | Google Scholar | PubMed |
Widodo , Patterson JH, Newbigin E, et al. (2009) Metabolic responses to salt stress of barley (Hordeum vulgare L.) cultivars, Sahara and Clipper, which differ in salinity tolerance. Journal of Experimental Botany 60, 4089-4103.
| Crossref | Google Scholar |
Wishart DS (2007) Current progress in computational metabolomics. Briefings in Bioinformatics 8, 279-293 PMID:.
| Crossref | Google Scholar | PubMed |
Xu F-F, Xu X-F (2012) Effects of NaCl stress on seed germination of radish. Journal of Jilin Agricultural Sciences 7, 48-50.
| Crossref | Google Scholar |
Yan M (2016) Hydro-priming increases seed germination and early seedling growth in two cultivars of Napa cabbage (Brassica rapa subsp. pekinensis) grown under salt stress. The Journal of Horticultural Science and Biotechnology 91, 421-426.
| Crossref | Google Scholar |
Yang Y, Guo Y (2018) Elucidating the molecular mechanisms mediating plant salt-stress responses. New Phytologist 217, 523-539 PMID:.
| Crossref | Google Scholar | PubMed |
Yong H-Y, Zou Z, Kok E-P, et al. (2014) Comparative transcriptome analysis of leaves and roots in response to sudden increase in salinity in Brassica napus by RNA-seq. BioMed Research International 2014, 467395.
| Crossref | Google Scholar |
You J, Chan Z (2015) ROS regulation during abiotic stress responses in crop plants. Frontiers in Plant Science 6, 1092 PMID:.
| Crossref | Google Scholar | PubMed |
Yousuf PY, Ahmad A, Ganie AH, et al. (2017) Antioxidant response and proteomic modulations in Indian mustard grown under salt stress. Plant Growth Regulation 81, 31-50.
| Crossref | Google Scholar |
Zhao S, Zhang Q, Liu M, et al. (2021) Regulation of plant responses to salt stress. International Journal of Molecular Sciences 22, 4609 PMID:.
| Crossref | Google Scholar | PubMed |
Zhu J-K (2016) Abiotic stress signaling and responses in plants. Cell 167, 313-324 PMID:.
| Crossref | Google Scholar | PubMed |
Zhu K, Jin Q, Samma MK, et al. (2014) Molecular cloning and characterization of a heme oxygenase1 gene from sunflower and its expression profiles in salinity acclimation. Molecular Biology Reports 41, 4109-4121 PMID:.
| Crossref | Google Scholar | PubMed |
