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Dynamics of the Transcriptome Response to Heat in the Moss, Physcomitrella patens.

ABSTRACT: Thermal stress negatively impacts crop yields, and as the overall temperature of the earth's atmosphere is gradually increasing, the identification of the temperature transduction pathway of the heat signal is essential in developing new strategies in order to adapt plant breeding to warmer climates. Heat stress damages the molecular structures and physiological processes in plants in proportion to the level and duration of the stress, which leads to different types of responses. In general, plants respond more efficiently when they are first subjected to a moderate temperature increase before being subjected to a higher temperature stress. This adaptive response is called the acclimation period and has been investigated in several plant species. However, there is a lack of information on the dynamic of the Heat Shock Response (HSR) over a continuous period of temperature rise without an acclimation period. In this paper, we investigated the effects of mild (30 °C) and high (37 °C) continuous heat stress over a 24-h period. Through RNA-Seq analysis, we assessed the remodeling of the transcriptome in the moss Physcomitrella patens. Our results showed that the 30 °C treatment particularly affected the expression of a few genes at 1 and 24 h, suggesting a biphasic response. Up-regulated genes at 1 h encode mainly HSR proteins (protein folding and endoplasmic reticulum stress), indicating an early heat response; while the up-regulated genes at 24 h belong to the thiamine biosynthesis pathway. In contrast, the genes involved in photosynthesis and carbon partitioning were repressed by this treatment. Under a higher temperature stress (37 °C), the induction of the HSR occurred rapidly (1 h) and was then attenuated throughout the time points investigated. A network approach (Weighted Gene Correlation Network Analysis, WGCNA) was used to identify the groups of genes expressing similar profiles, highlighting a HsfA1E binding motif within the promoters of some unrelated genes which displayed rapid and transient heat-activation. Therefore, it could be suggested that these genes could be direct targets of activation by a HsfA1E transcription factors.

SUBMITTER: Elzanati O

PROVIDER: S-EPMC7073223 | biostudies-literature | 2020 Feb

REPOSITORIES: biostudies-literature

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Dynamics of the Transcriptome Response to Heat in the Moss, Physcomitrella patens.

Elzanati Osama O Mouzeyar Said S Roche Jane J

International journal of molecular sciences 20200222 4

Thermal stress negatively impacts crop yields, and as the overall temperature of the earth's atmosphere is gradually increasing, the identification of the temperature transduction pathway of the heat signal is essential in developing new strategies in order to adapt plant breeding to warmer climates. Heat stress damages the molecular structures and physiological processes in plants in proportion to the level and duration of the stress, which leads to different types of responses. In general, pla ...[more]

PMID: 32098429

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Project description:BACKGROUND: Hexokinase catalyzes the phosphorylation of glucose and fructose, but it is also involved in sugar sensing in both fungi and plants. We have previously described two types of hexokinases in the moss Physcomitrella. Type A, exemplified by PpHxk1, the major hexokinase in Physcomitrella, is a soluble protein that localizes to the chloroplast stroma. Type B, exemplified by PpHxk2, has an N-terminal membrane anchor. Both types are found also in vascular plants, and localize to the chloroplast stroma and mitochondrial membranes, respectively. RESULTS: We have now characterized all 11 hexokinase encoding genes in Physcomitrella. Based on their N-terminal sequences and intracellular localizations, three of the encoded proteins are type A hexokinases and four are type B hexokinases. One of the type B hexokinases has a splice variant without a membrane anchor, that localizes to the cytosol and the nucleus. However, we also found two new types of hexokinases with no obvious orthologs in vascular plants. Type C, encoded by a single gene, has neither transit peptide nor membrane anchor, and is found in the cytosol and in the nucleus. Type D hexokinases, encoded by three genes, have membrane anchors and localize to mitochondrial membranes, but their sequences differ from those of the type B hexokinases. Interestingly, all moss hexokinases are more similar to each other in overall sequence than to hexokinases from other plants, even though characteristic sequence motifs such as the membrane anchor of the type B hexokinases are highly conserved between moss and vascular plants, indicating a common origin for hexokinases of the same type. CONCLUSIONS: We conclude that the hexokinase gene family is more diverse in Physcomitrella, encoding two additional types of hexokinases that are absent in vascular plants. In particular, the presence of a cytosolic and nuclear hexokinase (type C) sets Physcomitrella apart from vascular plants, and instead resembles yeast, where all hexokinases localize to the cytosol. The fact that all moss hexokinases are more similar to each other than to hexokinases from vascular plants, even though both type A and type B hexokinases are present in all plants, further suggests that the hexokinase gene family in Physcomitrella has undergone concerted evolution.

Dataset Information

Dynamics of the Transcriptome Response to Heat in the Moss, Physcomitrella patens.

Publications

Dynamics of the Transcriptome Response to Heat in the Moss, Physcomitrella patens.

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