Here, for the first time, we aimed to identify in rice the key mechanisms and processes underlying tolerance to high-temperature (HT) or salt stress (SS) alone, the co-occurrence of both stresses, and recovery using physiological and biochemical measurements and gene expression analysis. We also investigated whether recovery from the two stressors depended on the relative intensities/relief of each stressor. Wild type (‘Yukinkomai’) rice plants were found to be more susceptible to salinity or heat applied individually. SS leads to a depletion of cellular water content, higher accumulation of Na⁺, and alterations in photosynthetic pigments. The stress-tolerant cultivar ‘YNU31-2-4’ (YNU) displayed a lower Na⁺/K⁺ ratio, higher water content in cells and improved photosynthetic traits, antioxidant system, and expression of defence genes. Strikingly, the SS + HT combination provided a significant level of protection to rice plants from the effects of SS alone. The expression pattern of a selected set of genes showed a specific response and dedicated pathways in plants subjected to each of the different stresses, while other genes were explicitly activated when the stresses were combined. Aquaporin genes were activated by SS, while stress-related (P5CS, MSD1, HSPs, and ions transporters) genes were shaped by HT. Hierarchical clustering and principal component analyses showed that several traits exhibited a gradually aggravating effect as plants were exposed to the combined stresses and identified heat as a mitigating factor, clearly separating heat + salt-stressed from salt-non-heat-stressed plants. Furthermore, seedling recovery was far more dependent on the relative intensities of stressors and cultivars, demonstrating the influence of one stressor over another upon stress-release. Taken together, our data show the uniqueness and complexity of the physiological and molecular network modules used by rice plants to respond to single and combined stresses and recovery.

The yield-reduction effect of abiotic stressors such as salinity and heat stresses with the growing world population threatens food security. Although adverse effects of salinity and heat stress on plant growth and production parameters have been documented, in nature, abiotic stresses occur sequentially or simultaneously. In this study, the stress tolerance and yield capacity of Yukinkomai, YNU31-2-4, and YNU SL rice genotypes tested under control (26 °C, 0 mM NaCl), salinity (26 °C, 75 mM NaCl), heat (31 °C, 0 mM NaCl), and heat and salinity (31 °C, 75 mM NaCl) stress combinations at vegetative and reproductive stages with six different scenarios. The results show that salinity and the heat and salinity combination stresses highly reduce plant growth performance and yield capacity. Heat stress during reproduction does not affect the yield but reduces the grain quality. The YNU31-2-4 genotype performs better under heavy salt and heat and salinity stress then the Yukinkomai and YNU SL genotypes. YNU31-2-4 genotypes accumulate less Na⁺ and more K⁺ under salt and multiple stresses. In the YNU31-2-4 genotype, low Na⁺ ion accumulation increases photosynthetic activity and pigment deposition, boosting the yield. Stress lowers the glucose accumulation in dry seeds, but the YNU31-2-4 genotype has a higher glucose accumulation.

Transgenerational plasticity in plants enables rapid adaptation to environmental changes, allowing organisms and their offspring to adapt to the environment without altering their underlying DNA. In this study, we investigated the transgenerational plasticity in salinity tolerance of rice plants using a reciprocal transplant experimental strategy. Our aim was to assess whether non-genetic environment-induced phenotypic modifications and transgenerational salinity affect the salinity tolerance of progeny while excluding nuclear genomic factors for two generations. Using salt-tolerant and salt-sensitive rice genotypes, we observed that the parentally salt-stressed salt-sensitive genotype displayed greater growth performance, photosynthetic activity, yield performance, and transcriptional responses than the parentally non-stressed salt-sensitive plants under salt stress conditions. Surprisingly, salt stress-exposed salt-tolerant progeny did not exhibit as much salinity tolerance as salt stress-exposed salt-sensitive progeny under salt stress. Our findings indicate that the phenotypes of offspring plants differed based on the environment experienced by their ancestors, resulting in heritable transgenerational phenotypic modifications in salt-sensitive genotypes via maternal effects. These results elucidated the mechanisms underlying transgenerational plasticity in salinity tolerance, providing valuable insights into how plants respond to changing environmental conditions.