How plants adapt to combined and sequential abiotic stresses: A transcriptomics approach

Abstract

In nature, plants are exposed to a variety of stresses to which they must adapt to survive. With the changing climate, the stress experienced by plants is likely to be exacerbated. In recent years, we have observed an increased number of extreme weather events, such as flooding, heat waves, and drought. Moreover, these stresses rarely occur in isolation, often appearing simultaneously or sequentially. For example, high temperatures can lead to drought, or a period of flooding may be followed by an extended drought. Even when stress levels are low, combined or sequential sublethal stresses can significantly impair plant health, reducing vegetative and reproductive growth (Balfagón et al. 2019). Therefore, it is essential to understand how plants respond to combined or sequential sublethal stresses to improve their resilience and performance in a changing climate. In plant biology, we have accumulated a great knowledge of how plants respond and adapt to various abiotic stresses. However, most of our knowledge focuses on individual stresses rather than combinations of stresses. This gap likely arises from the challenges of conducting combined stress experiments in laboratory settings, as well as the complex nature of stress responses at the molecular and cellular levels (Zandalinas et al. 2021). Despite these challenges, recent studies provided valuable insights into plant responses to stress combinations (Sinha et al. 2023; Zandalinas and Mittler 2022). One early finding from these studies is that stress combinations often act synergistically rather than additively, meaning that combined stresses can harm plants more severely than a single stress itself (Zandalinas and Mittler 2022). Understanding the molecular mechanisms of these synergic interactions remains complex and is still an active area of research. A recent work by Zhang Jiang and colleagues published in Plant Physiology (Jiang et al. 2024) addresses this critical question of how plants acclimate to sublethal combined and sequential abiotic stresses, using the model plant Arabidopsis thaliana. The researchers designed their experimental setup to reveal the specific responses triggered by complex stress conditions (Fig.). Plants were exposed to 6 different treatments: a control, progressive drought (by withholding water), high temperature (27 °C), 5-day submergence, and 2 combined stress conditions—high temperature with progressive drought (HTD) and 5-day submergence followed by progressive drought (PSD). The study measured 15 different physiological and morphological traits, including dry biomass as a indicator of vegetative growth under both single and combined stress conditions. Consistent with previous studies in the field (Suzuki et al. 2014), the combined sublethal stresses had a synergistic negative impact on plant morphology and physiology beyond the effects of individual stresses. To decode the molecular mechanisms underlying these synergistic effects, the authors performed transcriptomic analysis on plants exposed to single and combined stress conditions. Interestingly, they identified sets of differentially expressed genes unique to each combined stress condition (HTD and PSD), suggesting that unique molecular responses are activated by specific stress combinations. Some of the implicated key molecular pathways include ABA signaling, photo-acclimation, and plastid–nucleus communication (Jiang et al. 2024). Schematic representation of the experimental setup used in Jiang et al. (2024). A) Control conditions: plants maintained at 21 °C with regular watering. B) Submergence: plants were submerged for 5 days, then returned to control conditions. C) High temperature stress: plants were watered but kept at 27 °C. D) Progressive drought: water was gradually withheld to induce drought conditions. E) Sequential stress: a 5-day submergence followed by progressive drought. F) Combined stress: high temperature (27 °C) coupled with progressive drought. Created with BioRender.com. Among the differentially expressed genes, 48 transcription factors were upregulated by combined stresses, with 8 of these shared between the HTP and PSD treatments. To validate the role of these transcription factors in stress response, the authors employed a reverse genetics approach. Testing over 40 A. thaliana mutants, they validated 39 genes as potential regulators of multi-stress responses. Notably, EARLY FLOWERING 6 (ELF6) was identified as a negative regulator of phenotypic acclimation to heat and drought, while ARABIDOPSIS TÓXICOS EN LEVADURA 80 (ATL80) appeared to act as a positive regulator for sequential flooding and drought stress. The discovery of a unique set of genes responding specifically to combined stresses aligns with previous literature, which suggests that exposure to one type of stress has influence the response to subsequent stresses (Guo et al. 2021). Addressing how plants respond to combination of stresses is essential to increase stress resilience of crops and ensure food security for our future. By deciphering the complex responses to combined stresses, Jiang and colleagues (Jiang et al. 2024) take a crucial step toward developing plants that can better withstand the increasingly challenging environmental conditions brought about by climate change. Understanding the unique transcriptomic responses to combined stresses can facilitate the development of more targeted strategies for crop improvement. Future research could focus on examining the set of downregulated genes under combined stresses and further investigate the precise molecular mechanisms involved. The identified genes and molecular pathways could also be studied in other, agriculturally important plants, providing valuable insights for breeding programs aimed at enhancing tolerance to multiple stresses. Nonetheless, there are still a couple of important research gaps in the field of stress combinations. What kind of signaling mechanisms are involved in sensing and responding to a combination of stresses? In the case of multiple stresses occurring simultaneously, which stress plants would need to respond first, particularly if those stresses involve different molecular and cellular strategies to deal with? Are there common mechanisms in plants that would allow them to gain tolerance against both abiotic and biotic stresses? Certainly, future research is necessary to get a full picture of how plants respond and handle multiple stresses; and we are in exiting times when the technology is allowing us to study this complex, yet exciting, world of plant stress response. B.A. and A.B.K. wish to thank Plant Physiology for the opportunity to act as an Assistant Features Editors. No new data were generated or analyzed in support of this research.

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