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Phylogenetic and expression dynamics of tomato ClpB/Hsp100 gene under heat stress.

ABSTRACT: Heat shock proteins (Hsps) are stress-responsive molecular chaperones, which uphold proper protein folding in response to external and internal stresses. The Hsp100 gene family plays a substantial role in thermos-tolerance of plants. This study investigated evolutionary relationship and expression of ClpB/Hsp100 gene family in tomato under heat stress. Six SlHsp100 genes were identified using bioinformatics tools. In silico sub-cellular localization indicated that of these 6 ClpB/Hsp100 members, 4 are found in chloroplast, 1 in mitochondria and 1 in the cytoplasm. For evolutionary study, 36 SlHsp100 genes were included in the phylogenetic tree showing a hierarchical clustering shared by the members of the kingdoms Plantae, Archaea, Chromista, Fungi and Bacteria. A total 4 pairs of orthologous and 5 pairs of paralogous genes were identified. Functional divergence between different Hsp100 clusters showed considerable functional homology. Thermo-tolerance measured in terms of cell viability, cell membrane stability and pollen viability indicated that it was paralleled by thermal resistance of Hsps. Reverse transcriptase polymerase chain reaction was used to analyze gene expression in leaves of five-week-old tomato seedlings following exposure to heat stress (45°C) and control (25°C). Chloroplastic LeHSP110/ClpB gene was upregulated in all tomato genotypes after exposure to heat stress highlighting the crucial role of this gene family in acquired thermo-tolerance.

SUBMITTER: Gul S

PROVIDER: S-EPMC8363017 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundClpB-cyt/HSP100 protein acts as chaperone, mediating disaggregation of denatured proteins. Previous studies have shown that ClpB-cyt/HSP100 gene belongs to the group class I Clp ATPase proteins and ClpB-cyt/HSP100 transcript is regulated by heat stress and developmental cues.ResultsNine ORFs were noted to constitute rice class I Clp ATPases in the following manner: 3 ClpB proteins (ClpB-cyt, Os05g44340; ClpB-m, Os02g08490; ClpB-c, Os03g31300), 4 ClpC proteins (ClpC1, Os04g32560; ClpC2, Os12g12580; ClpC3, Os11g16590; ClpC4, Os11g16770) and 2 ClpD proteins (ClpD1, Os02g32520; ClpD2, Os04g33210). Using the respective signal sequences cloned upstream to GFP/CFP reporter proteins and transient expression studies with onion epidermal cells, evidence is provided that rice ClpB-m and Clp-c proteins are indeed localized to their respective cell locations mitochondria and chloroplasts, respectively. Associated with their diverse cell locations, domain structures of OsClpB-c, OsClpB-m and OsClpB-cyt proteins are noted to possess a high-level conservation. OsClpB-cyt transcript is shown to be enriched at milk and dough stages of seed development. While expression of OsClpB-m was significantly less as compared to its cytoplasmic and chloroplastic counterparts in different tissues, this transcript showed highest heat-induced expression amongst the 3 ClpB proteins. OsClpC1 and OsClpC2 are predicted to be chloroplast-localized as is the case with all known plant ClpC proteins. However, the fact that OsClpC3 protein appears mitochondrial/chloroplastic with equal probability and OsClpC4 a plasma membrane protein reflects functional diversity of this class. Different class I Clp ATPase transcripts were noted to be cross-induced by a host of different abiotic stress conditions. Complementation assays of Deltahsp104 mutant yeast cells showed that OsClpB-cyt, OsClpB-m, OsClpC1 and OsClpD1 have significantly positive effects. Remarkably, OsClpD1 gene imparted appreciably high level tolerance to the mutant yeast cells.ConclusionsRice class I Clp ATPase gene family is constituted of 9 members. Of these 9, only 3 belonging to ClpB group are heat stress regulated. Distribution of ClpB proteins to different cell organelles indicates that their functioning might be critical in different cell locations. From the complementation assays, OsClpD1 appears to be more effective than OsClpB-cyt protein in rescuing the thermosensitive defect of the yeast ScDeltahsp104 mutant cells.

Project description:Climate change is causing temperature increment in crop production areas worldwide, generating conditions of heat stress that negatively affect crop productivity. Tomato (Solanum lycopersicum), a major vegetable crop, is highly susceptible to conditions of heat stress. When tomato plants are exposed to ambient day/night temperatures that exceed 32 °C/20 °C, respectively, during the reproductive phase, fruit set and fruit weight are reduced, leading to a significant decrease in yield. Processing tomato cultivars are cultivated in open fields, where environmental conditions are not controlled; therefore, plants are exposed to multiple abiotic stresses, including heat stress. Nonetheless, information on stress response in processing tomatoes is very limited. Understanding the physiological response of modern processing tomato cultivars to heat stress may facilitate the development of thermotolerant cultivars. Here, we compared two tomato processing cultivars, H4107 and H9780, that we found to be constantly differing in yield performance. Using field and temperature-controlled greenhouse experiments, we show that the observed difference in yield is attributed to the occurrence of heat stress conditions. In addition, fruit set and seed production were significantly higher in the thermotolerant cultivar H4107, compared with H9780. Despite the general acceptance of pollen viability as a measure of thermotolerance, there was no difference in the percentage of viable pollen between H4107 and H9780 under either of the conditions tested. In addition to observations of similar pollen germination and bud abscission rates, our results suggest that processing tomato cultivars may present a particular case, in which pollen performance is not determining reproductive thermotolerance. Our results also demonstrate the value of combining controlled and uncontrolled experimental settings, in order to validate and identify heat stress-related responses, thus facilitating the development of thermotolerant processing tomato cultivars.

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Phylogenetic and expression dynamics of tomato ClpB/Hsp100 gene under heat stress.

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