Stress memory in plants: key aspects (review)

Plants are constantly exposed to the destructive effects of unfavorable environmental conditions, both abiotic and biotic. In the case of crops, this negatively affects yields. Numerous laboratory studies have focused on the effects of various stress factors on plant growth and development. The results of attempts to transfer the obtained data to field cultivation conditions indicate the presence of critical aspects of the plant-stress interaction. In this review, we consider some of these aspects. Thus, most studies are focused on the analysis of molecular responses of plants to single-factor stresses (Y. Saijo, et al., 2020). The natural environment is characterized by multifactorial effects in various combinations. Therefore, recently there has been an increasing number of publications analyzing the response of plants to two- and three-factor stress combinations of abiotic factors with abiotic (T. Obata et al., 2015; N. Suzuki et al., 2016; S.I. Zandalinas et al., 2022) and biotic (S. Rasmussen et al., 2013; N. Suzuki et al., 2014; A.R. Devireddy et al., 2020) stressors. It has been shown that the mechanism of plant response under combinatorial influence arises as a result of integration and modulation of responses to individual stress components (N. Suzuki et al., 2014), which can be neutral, antagonistic or unrelated to each other, and is often unpredictable and requires experimental confirmation (S. Rasmussen et al., 2013). Responses to abiotic and biotic factors are controlled by different, sometimes conflicting signaling pathways, which under combinatorial stress can interact and/or inhibit each other (S. Rasmussen et al., 2013; N. Suzuki et al., 2014). The quality of the plant stress response depends not only on the genotype, but also on the epigenetic regulation of the expression of the corresponding genes and the accumulation of the necessary metabolites (Z.H. Chen et al., 2020), known as “stress memory” (A. Weinhold, 2018). In the natural environment of plant growth, recurrent events of the same type and combinatorial stresses are not uncommon. The formation of reversible heritable stress memory occurs as a result of the plant experiencing a primary stress effect (priming). The plant remembers its defense reaction by introducing epigenetic changes into the genome and, when the stress is repeated, triggers the remembered reactions to the previous experience (M. Hilker et al., 2016; J. Lämke et al, 2017). A distinction is made between cis-priming, when the type of primary and repeated stresses coincides, and trans-priming, when the priming memory is triggered in response to a stimulus of a different type (M. Hilker et al., 2016; A.U. Nair et al., 2022). The set of epigenetic marks that arise after priming constitutes the plant's memory of the stressful event and is aimed at regulating the expression of specific genes (M. Hilker et al., 2016; L. Virlouvet et al., 2018; A. Nishad, A.K. Nandi, 2021; C. Jacques et al., 2021). Stress memory can be short-term (mitotically inherited) and long-term (meiotically inherited) (M. Hilker et al., 2016; J. Lämke et al., 2017). In the absence of repeated stressful events, forgetting occurs when the plant activates epigenetic regulatory mechanisms that reset stress memory marks (A. Wibowo et al., 2016). The plant's defense response to individual stressors and their combination during priming and repeated events is expressed in significant modulation of gene expression and the content of various metabolites (A. Aharoni et al., 2011; S.I. Zandalinas et al., 2022). Transcripts and metabolites with a differential response to stress can serve as biomarkers of stress memory (Aina et al., 2024). A characteristic feature of biomarkers (genes, metabolites) is considered to be significant differences in fluctuations in expression (genes) and content (metabolites) during priming, repeated stresses and returns to normal conditions (Y. Ding et al., 2013, 2014; C. Jacques et al., 2021). Putative biomarker genes may be associated with the metabolism of various compounds, including components of plant antioxidant defense, phytohormones, pathogenesis-associated PR proteins, etc. (O.K. Anisimova et al., 2021; S.I. Zandalinas et al., 2022; O. Aina et al., 2024), as well as with the regulation of gene expression (transcription factors, non-coding RNAs, circadian oscillators, etc.) (H. Wei et al., 2022; W. Cao et al., 2024). Based on the presented material, it is assumed that studies of plant defense/adaptive responses, especially cultivated plants, aimed at increasing stress resistance, should be carried out taking into account the aspects discussed in the review. The result of such studies may be the identification of key biomarkers of plant memory about the effects of various stress factors and their combinations, and, as a consequence, the identification of donors of epialleles/epimutations associated with inherited stress memory.