Adaptative Mechanisms of Halophytic Eutrema salsugineum Encountering Saline Environment

Abstract

Salt cress (Eutrema salsugineum), an Arabidopsis-related halophyte, can naturally adapt to various harsh climates and soil conditions; thus, it is considered a desirable model plant for deciphering mechanisms of salt and other abiotic stresses. Accumulating evidence has revealed that compared with Arabidopsis, salt cress possesses stomata that close more tightly and more succulent leaves during extreme salt stress, a noticeably higher level of proline, inositols, sugars, and organic acids, as well as stress-associated transcripts in unstressed plants, and they are induced rapidly under stress. In this review, we systematically summarize the research on the morphology, physiology, genome, gene expression and regulation, and protein and metabolite profile of salt cress under salt stress. We emphasize the latest advances in research on the genome adaptive evolution encountering saline environments, and epigenetic regulation, and discuss the mechanisms underlying salt tolerance in salt cress. Finally, we discuss the existing questions and opportunities for future research in halophytic Eutrema. Together, the review fosters a better understanding of the mechanism of plant salt tolerance and provides a reference for the research and utilization of Eutrema as a model extremophile in the future. Furthermore, the prospects for salt cress applied to explore the mechanism of salt tolerance provide a theoretical basis to develop new strategies for agricultural biotechnology.

Keywords: Arabidopsis relative model system; antioxidant system; gene expression; ion homeostasis; osmo-adaptation; saline adaptation; salt cress; salt stress tolerance.

Figure 1

Growth comparison of Eutrema salsugineum (Shandong) and Arabidopsis thaliana plants in the control (CK) and stress treatment conditions. (A) Growth comparison of Eutrema and Arabidopsis plants in the control and NaCl treatment (100, 200, 300, and 400 mM NaCl) conditions. Eutrema seeds germinated 10 days, and Arabidopsis seeds germinated for 7 days in 1/2 MS medium, then the seedlings of uniform growth moved to 1/2 MS medium containing 0 (CK), 100, 200, 300, and 400 mM NaCl for growing for about 5 days. (B) Growth comparison of the 50-day-old Eutrema and 30-day-old Arabidopsis plants that grow in a mixture of vermiculite, perlite and peat moss (1:1:1), with a photoperiod of 16 h light/22°C and 8 h dark/18°C. (C) Growth comparison of the 60-day-old Eutrema and 40-day-old Arabidopsis plants. The surface sterilized Eutrema seeds planted in 1/2 MS medium, was firstly stratified treatment (4°C for 13 days) to synchronize the germination, then moved into the growth chamber for 7 days; the seedlings were transplanted in nutrient soil for 34 days, followed by 6 day-salt treatment using 200 mM NaCl. The surface sterilized Arabidopsis seeds planted in 1/2 MS medium, was firstly stratified treatment in 4°C for 3 days, then moved into a growth chamber for 7 days; the seedlings were transplanted in nutrient soil containing vermiculite, perlite, and peat moss (1:1:1) for 24 days, followed by 6-day salt treatment using 200 mM NaCl. (D) Phenotype comparison of Eutrema plants under salt, drought, and cold stresses. Eutrema seeds were planted in a mixture of vermiculite, perlite, and peat moss (1:1:1) in a greenhouse for 60 days with a photoperiod of 16 h light/22°C and 8 h dark/18°C, followed by stress treatments using 300 mM NaCl (Salt), no watering (Drought) and low temperature of 4–6°C (Cold) for 2 weeks, respectively, or kept in normal growth condition (CK).

Figure 2

Adaptative mechanisms of halophytic Eutrema salsugineum encountering saline environment. The adaptative mechanisms of Eutrema plants to saline stress are mainly including: (1) The adaptive evolution endowing E. salsugineum plants with the expanded defense related genes and/or gene family members to facilitate plants more flexibility in response to salinity stress; (2) The constitutive higher expression of stress defense genes such as P5CS and SOS1 in the absence of salt stress; (3) Anticipatory prepared osmolytes such as proline and secondary compounds, and a higher efficience to activate the existed enzymatic machinery as well as the adjustment of metabolism; (4) The halophytic E. salsugineum possessing exceptional control over Na⁺ influx and export mechanisms, the superior ability to coordinate its distribution to various tissues, and the efficient sequestration of Na⁺ into vacuoles; (5) A constitutively upregulated antioxidative protection system, and the effective regulation of redox status in halophytic Eutrema; (6) The succulent-like leaves, an extra endodermis and cortex cell layer in root tissues, and higher density of stomata exhibitting a more tightly closing when responding to salt stress, as well as an almost unaffected net photosynthetic rate, in the lower or even moderate concentration of salinity. SOS1, salt overly sensitive 1 (plasma membrane Na⁺/H⁺ antiporter); NHX, vacuolar Na⁺/H⁺ antiporter; V-ATPase, vacuolar H⁺-ATPase; VP1 (V-Ppase), vacuolar H⁺-translocating inorganic pyrophosphatase (vacuolar H⁺-pyrophosphatase); HKT1, group 1 high-affinity K⁺ transporter; GPX, glutathione peroxidases; PSII, photosystem II; PQ, plastoquinone.

Figure 3

Major transporters regulating Na⁺/K⁺ homeostasis in Eutrema under salinized tissues. Plasma membrane Na⁺/H⁺ antiporter SOS1 functions in the regulation of ion homeostasis by extruding excessive Na⁺ out of cells, facilitating Na⁺ loading into the xylem in roots and shoots, and reducing the transfer of Na⁺ from roots to shoots, to counterbalance the uptake of Na⁺. Tonoplast-localized Na⁺/H⁺ exchanger NHX1 driven by vacuole H⁺-PPase (VP1) and/or H⁺-ATPase (V-ATPase) proton pumps is responsible for the sequestration of Na⁺ into the vacuole, to reduce the concentration of Na⁺ in the cytosol. The halophytic Eutrema HKT1;2 (EsHKT1;2 and EpHKT1;2) is considered as the Na⁺/K⁺ co-transporter, that function in Na⁺ retrieval from the xylem vessels under salt stress, and helps sequester ions into xylem parenchyma cells to protect photosynthetic tissues. SOS1, salt overly sensitive 1 (a plasma membrane Na⁺/H⁺ antiporter); NHX, vacuolar Na⁺/H⁺ antiporter; V-ATPase, vacuolar H⁺-ATPase; V-PPase, vacuolar H⁺-translocating inorganic pyrophosphatase (vacuolar H⁺-pyrophosphatase); HKT1, group 1 high-affinity K⁺ transporter.

Figure 4

Overview of the constitutively higher expressed antioxidative protection system and effective regulation of redox status in halophytic Eutrema. The plasma membrane ROS produced through NADPH oxidases (NOXs), the important components of signal transduction, encoded by RBOHD and RBOHF genes, is associated with the regulation of Na⁺/K⁺ homeostasis and increased accumulation of proline involved in salt tolerance. The enhanced antioxidant tolerance of Eutrema is associated with: (1) A constitutively enhanced H₂O₂ generated to keep the antioxidant system up-regulated to preadapted plant to salinity stress, as well as a chloroplastic production of H₂O₂ inducing the accumulation of glucosinolates to activate the stress defense system, (2) Antioxidative enzymes such as GPX, and non-enzymatic antioxidants such as ascorbate and glutathione facilitating ROS homeostasis and alleviating damage of singlet oxygen (¹O₂) to PSII under salt stress, (3) A higher expression level of thioredoxin CDSP32 regulating redox status of target proteins and highly reduced states of PQ pool and P700 facilitating redox homeostasis and lower photoinhibition under salt stress. NOXs, NADPH oxidases; GPX, glutathione peroxidases; PSII, photosystem II; PQ, plastoquinone.