Salt Stress Inhibits Photosynthesis and Destroys Chloroplast Structure by Downregulating Chloroplast Development–Related Genes in Robinia pseudoacacia Seedlings

Abstract

Soil salinization is an important factor limiting food security and ecological stability. As a commonly used greening tree species, Robinia pseudoacacia often suffers from salt stress that can manifest as leaf yellowing, decreased photosynthesis, disintegrated chloroplasts, growth stagnation, and even death. To elucidate how salt stress decreases photosynthesis and damages photosynthetic structures, we treated R. pseudoacacia seedlings with different concentrations of NaCl (0, 50, 100, 150, and 200 mM) for 2 weeks and then measured their biomass, ion content, organic soluble substance content, reactive oxygen species (ROS) content, antioxidant enzyme activity, photosynthetic parameters, chloroplast ultrastructure, and chloroplast development-related gene expression. NaCl treatment significantly decreased biomass and photosynthetic parameters, but increased ion content, organic soluble substances, and ROS content. High NaCl concentrations (100–200 mM) also led to distorted chloroplasts, scattered and deformed grana lamellae, disintegrated thylakoid structures, irregularly swollen starch granules, and larger, more numerous lipid spheres. Compared to control (0 mM NaCl), the 50 mM NaCl treatment significantly increased antioxidant enzyme activity while upregulating the expression of the ion transport-related genes Na+/H+ exchanger 1(NHX 1) and salt overly sensitive 1 (SOS 1) and the chloroplast development-related genes psaA, psbA, psaB, psbD, psaC, psbC, ndhH, ndhE, rps7, and ropA. Additionally, high concentrations of NaCl (100–200 mM) decreased antioxidant enzyme activity and downregulated the expression of ion transport- and chloroplast development-related genes. These results showed that although R. pseudoacacia can tolerate low concentrations of NaCl, high concentrations (100–200 mM) can damage chloroplast structure and disturb metabolic processes by downregulating gene expression.

Thirteen complete chloroplast genomes of the costaceae family: insights into genome structure, selective pressure and phylogenetic relationships

“…The psbD encodes the core protein D2 of the photosynthesis complex PSII, which is an important factor affecting photosynthetic efficiency during salt stress [ 43 ]. The clpP encodes caseinolytic protease (Clp) complex, which plays essential roles in maintaining protein homeostasis and comprises both plastid-encoded and nuclear-encoded subunits [ 44 ]. Rapid clpP sequence evolution is associated with genetic incompatibilities [ 45 ].…”

Sensitivity and responses of chloroplasts to salt stress in plants

“…The most important physiological process occurring in chloroplasts is photosynthesis, which is the energy source for plant growth and development and plays crucial roles in plant productivity ( Yang et al., 2020 ; Zahra et al., 2022 ; Lu et al., 2023 ). Photosynthesis comprises light reaction and dark reaction phases.…”

“…The negative effect of salt stress on photoreaction is mainly reflected in electron transport chain (ETC) and photosystems ( Huang et al., 2019 ). High salinity blocks electron transport chain, resulting in excessive accumulation of ROS which cause oxidative damage to thylakoid membrane proteins, lipids, membranes, and photosynthetic enzymes ( Lu et al., 2023 ). The inhibition of electron transport and the oxidative damage to photosynthetic apparatus under salt stress resulted in photoinhibition to photosystems.…”

“…The excess accumulation of Na + and Cl - ions inside chloroplasts not only affects photosynthetic components ( Davenport et al., 2005 ), but also inhibits the uptake of K + and Ca 2+ ions, which disrupts ion homeostasis ( Hu and Schmidhalter, 2005 ; Bose et al., 2017 ). In addition, when plants are exposed to salt stress, the decline of carbon assimilation and the reduced photosynthetic electron transport rate will increase reactive oxygen species (ROS) production, that leads to oxidative stress ( Munns and Tester, 2008 ; Huang et al., 2019 ; Lu et al., 2023 ). Thus, salt stress induces osmotic stress, ionic stress and oxidative stress to chloroplasts and negatively affects the function of chloroplasts ( Figure 1 ).…”

Application of a Bi-Directional Gated Recurrent Unit Combined with a Recurrent Neural Network Model Based on Fusion Attention Mechanism in Estimating Soil Salinity

“…Soil salinization refers to the accumulation of a large amount of salt and alkali components on the surface of soil under the combined action of natural and human factors, resulting in reduced agricultural production and ecological environment deterioration, leading to large-scale waste of land resources, and has become one of the thorny ecological problems worldwide [1]. According to statistics, over 100 countries and regions worldwide have an area of nearly 1 billion hm2 of land affected by soil salinization [2], accounting for approximately 25% of the total land area of the world [3]. Soil salinization has seriously affected the water absorption capacity of crop roots and soil structure [4], resulting in large-scale farmland degradation and crop yield reduction [5], resulting in a loss of global income of over 32 billion US dollars per year [6].…”