Stress memory induced transcriptional and metabolic changes of perennial ryegrass (Lolium perenne) in response to salt stress

Abstract

Preexposure to a stress could induce stable signals and reactions on plant physiology and gene expression during future encounters as a 'stress memory'. In this study, we found that two trainable genes, BPSP encoding putative brown plant hopper susceptibility protein and sucs encoding sucrose synthase displayed transcriptional memory for their considerably higher transcript levels during two or more subsequent stresses (S3, S4) relative to the initial stress (S0), and their expression returning to basal transcript levels (non-stressed) during the recovery states (R1, R2 and R3). Removing the repetitive stress/recovery exercise, activated transcriptional memory from two trainable genes persisted for at least 4 days in perennial ryegrass. The pretrainable genes with stress memory effort had higher response to the subsequent elevated NaCl concentration treatment than the non-trainable plants, which was confirmed by lower electrolyte leakage and minimum H2 O2 and O2 (-) accumulation. Salt stress elevated the content of 41 metabolites in perennial ryegrass leaves, and sugars and sugar alcohol accounted for more than 74.1% of the total metabolite content. The salt stress memory was associated with higher contents of 11 sugars and 1 sugar alcohol in the pretrainable grass leaves. Similarly, six sugars showed greater content in the pretrainable grass roots. These novel phenomena associated with transcriptional memory and metabolite profiles could lead to new insights into improving plant salinity acclimation process.

Pivotal roles of environmental sensing and signaling mechanisms in plant responses to climate change

“…Alternatively, plants may indirectly sense eCO 2 -related factors, such as soluble sugars, which are sensed through various signaling pathways (Baena-González & Sheen, 2008), and which play central roles, not only in carbon and energy metabolism, but also in plant tolerance to environmental stresses (Couée, Sulmon, Gouesbet, & Amrani, 2006). Besides eCO 2 (Noctor & Mhamdi, 2017), various climate change-related factors, especially temperature variations (Riikonen et al, 2012), and salinity (Hu, Jin, Li, Amombo, & Fu, 2016), lead to increased levels of soluble sugars, whereas nutrient shortage, ozone, high light, heavy metals, and chemical pollutions (Rosa et al, 2009;Serra et al, 2013) lead to decreased levels of soluble sugars (Figure 4a). Besides eCO 2 (Noctor & Mhamdi, 2017), various climate change-related factors, especially temperature variations (Riikonen et al, 2012), and salinity (Hu, Jin, Li, Amombo, & Fu, 2016), lead to increased levels of soluble sugars, whereas nutrient shortage, ozone, high light, heavy metals, and chemical pollutions (Rosa et al, 2009;Serra et al, 2013) lead to decreased levels of soluble sugars (Figure 4a).…”

“…For instance, global changes in sugar levels, re-orientation of carbon metabolism, involvement in stress tolerance, and sugar-mediated transcriptome reprogramming determine long-term changes and modify developmental programs according to metabolic status. Increases in soluble sugar levels under salt stress or low temperature are respectively linked to salt stress memory (Hu et al, 2016) and cold hardening (Riikonen et al, 2012). Increases in soluble sugar levels under salt stress or low temperature are respectively linked to salt stress memory (Hu et al, 2016) and cold hardening (Riikonen et al, 2012).…”

“…Soluble sugars are highly sensitive to environmental fluctuations, especially when carbon partitioning between sources and sinks is affected. Besides eCO 2 (Noctor & Mhamdi, 2017), various climate change-related factors, especially temperature variations (Riikonen et al, 2012), and salinity (Hu, Jin, Li, Amombo, & Fu, 2016), lead to increased levels of soluble sugars, whereas nutrient shortage, ozone, high light, heavy metals, and chemical pollutions (Rosa et al, 2009;Serra et al, 2013) lead to decreased levels of soluble sugars (Figure 4a). Variations of sugar levels are sensed by the SnRK1 (Snf1-related protein kinase 1) sensor, which is involved in stress tolerance.…”

“…and of long-term modifications may lead to mechanisms of stress defense priming, whereby plants show increased stress tolerance after pre-exposures to other stresses or to stress-related regulators that induce shifts of metabolic, hormonal, or physiological status (Horváth et al, 2015;Hu et al, 2016;Noctor & Mhamdi, 2017;Riikonen et al, 2012;Savvides, Ali, Tester, & Fotopoulos, 2016). Such processes of training or hardening involve various biochemical pathways and compounds (Horváth et al, 2015;Hu et al, 2016;Savvides et al, 2016) that are able to induce, prior to stress exposure, chemical priming against subsequent abiotic stresses (Savvides et al, 2016). For instance, global changes in sugar levels, re-orientation of carbon metabolism, involvement in stress tolerance, and sugar-mediated transcriptome reprogramming determine long-term changes and modify developmental programs according to metabolic status.…”

“…Pre-stress levels of soluble sugars determine the capacity to withstand subsequent abiotic stresses (Ramel, Sulmon, Gouesbet, & Couée, 2009). Increases in soluble sugar levels under salt stress or low temperature are respectively linked to salt stress memory (Hu et al, 2016) and cold hardening (Riikonen et al, 2012).…”