Tomato plants increase their tolerance to low temperature in a chilling acclimation process entailing comprehensive transcriptional and metabolic adjustments

Abstract

Low temperature is a major environmental stress that seriously compromises plant development, distribution and productivity. Most crops are from tropical origin and, consequently, chilling sensitive. Interestingly, however, some tropical plants, are able to augment their chilling tolerance when previously exposed to suboptimal growth temperatures. Yet, the molecular and physiological mechanisms underlying this adaptive process, termed chilling acclimation, still remain practically unknown. Here, we demonstrate that tomato plants can develop a chilling acclimation response, which includes comprehensive transcriptomic and metabolic adjustments leading to increased chilling tolerance. More important, our results reveal strong resemblances between this response and cold acclimation, the process whereby plants from temperate regions raise their freezing tolerance after exposure to low, non-freezing temperatures. Both chilling and cold acclimation are regulated by a similar set of transcription factors and hormones, and share common defence mechanisms, including the accumulation of compatible solutes, the mobilization of antioxidant systems and the rearrangement of the photosynthetic machinery. Nonetheless, we have found some important divergences that may account for the freezing sensitivity of tomato plants. The data reported in this manuscript should foster new research into the chilling acclimation response with the aim of improving tomato tolerance to low temperature.

Rootstock Sub-Optimal Temperature Tolerance Determines Transcriptomic Responses after Long-Term Root Cooling in Rootstocks and Scions of Grafted Tomato Plants

“…This was unexpected since the accumulation of flavonoids and anthocyanins involved in ROS scavenging is an important adjustment during cold acclimation (Ruelland et al, 2009; Schulz et al, 2016). Several genes encoding enzymes involved in flavonol and anthocyanin biosynthesis were up-regulated during cold treatment in tomato leaves together with numerous genes coding for enzymes with antioxidant activity, in agreement with increased anthocyanin levels (Barrero-Gil et al, 2016). Whereas no corresponding data are available for tomato roots, expression of genes encoding enzymes involved in secondary metabolism, especially phenylpropanoid and lignin biosynthesis, is increased in the roots of a cold-tolerant compared to a sensitive rice cultivar after a short-term cold stress (Yang et al, 2015).…”

“…In contrast, analysis of DEG detected in leaves of ‘Moneymaker’ during an exposure to 10°C for 3 h indicated that transcription factor activity dominated the early response together with GO terms for stress response and hormone biosynthesis and signaling (Barrero-Gil et al, 2016). In addition, metabolism was adjusted by accumulation of compatible solutes, activation of antioxidants systems and rearrangement of the photosynthetic machinery (Barrero-Gil et al, 2016).…”

“…In this study shoots or roots did not accumulate sugars or amino acids indicating that the low temperature treatment applied only to the rootstocks was not sufficiently severe or that after 22 days of sub-optimal temperature treatment concentrations of these compounds returned to control values. Another study on leaves of ‘Moneymaker’ subjected to 10°C for up to 48 h also did not observe a significant accumulation of compatible sugars and suggested that the accumulation of amino acids and polyamines might play a relevant role in tomato chilling acclimation (Barrero-Gil et al, 2016). …”

“…The early transcriptomic response in leaves of 3-week-old ‘Moneymaker’ plants to 3, 24, and 48 h at 10°C revealed 1537, 4404, and 4600 DEGs, respectively, with more up- than down-regulated genes (Barrero-Gil et al, 2016). No studies on the influence of sub-optimal root temperature on roots of tomato are available for a direct comparison.…”

“…In addition, metabolism was adjusted by accumulation of compatible solutes, activation of antioxidants systems and rearrangement of the photosynthetic machinery (Barrero-Gil et al, 2016). These early stress responses were not found in the present study, indicating that after a cold treatment of 10°C for 22 days no acute stress responses can be observed anymore and that the plants have probably reached a new homeostasis.…”