Abstract
High-temperature (HT) stress is a major environmental stress that limits plant growth and development. MAPK cascades play key roles in plant growth and stress signaling, but their involvement in the HT stress response is poorly understood. Here, we describe a 47-kD MBP-phosphorylated protein (p47-MBPK) activated in tomato (Solanum lycopersicum) leaves under HT and identify it as SlMPK1 by tandem mass spectrometry analysis. Silencing of SlMPK1 in transgenic tomato plants resulted in enhanced tolerance to HT, while overexpression resulted in reduced tolerance. Proteomic analysis identified a set of proteins involved in antioxidant defense that are significantly more abundant in RNA interference-SlMPK1 plants than nontransgenic plants under HT stress. RNA interference-SlMPK1 plants also showed changes in membrane lipid peroxidation and antioxidant enzyme activities. Furthermore, using yeast two-hybrid screening, we identified a serine-proline-rich protein homolog, SlSPRH1, which interacts with SlMPK1 in yeast, in plant cells, and in vitro. We demonstrate that SlMPK1 can directly phosphorylate SlSPRH1. Furthermore, the serine residue serine-44 of SlSPRH1 is a crucial phosphorylation site in the SlMPK1-mediated antioxidant defense mechanism activated during HT stress. We also demonstrate that heterologous expression of SlSPRH1 in Arabidopsis (Arabidopsis thaliana) led to a decrease in thermotolerance and lower antioxidant capacity. Taken together, our results suggest that SlMPK1 is a negative regulator of thermotolerance in tomato plants. SlMPK1 acts by regulating antioxidant defense, and its substrate SlSPRH1 is involved in this pathway.
Highlights
High-temperature (HT) stress is a major environmental stress that limits plant growth and development
The results suggest that p47-MBPK is a MAPK-like protein
Our results show that the expression of both genes did not change significantly in SlMPK1 RNA interference (RNAi) lines when compared with the wild type at normal growth temperature or HT stress (Supplemental Fig. S2C)
Summary
High-temperature (HT) stress is a major environmental stress that limits plant growth and development. Recent studies showed that the silencing of tomato MPK1/2 by virus-induced gene silencing (VIGS) abolishes plant tolerance to heat, cold, and oxidative stress (Nie et al, 2013; Zhou et al, 2014; Lv et al, 2017) These results suggest an opposite function to AtMPK6, a close homolog to SlMPK1, under HT or cold stress in Arabidopsis (Li et al, 2012, 2017; Evrard et al, 2013; Zhao et al, 2017). Analysis of the proteome using isobaric tags for relative and absolute quantification (iTRAQ) revealed that several proteins involved in antioxidant defense were significantly up-regulated in RNAi-SlMPK1 plants under HT stress. Our results reveal a potential involvement of SlMPK1 as part of the HT response in tomato and unravel the molecular mechanisms by which SlMPK1 negatively regulates the HT response
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