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Comparative physiology and transcriptional networks underlying the heat shock response in Populus trichocarpa, Arabidopsis thaliana and Glycine max Public

David J. Weston, Abhijit A. Karve, Lee E. Gunter, Sara S. Jawdy, Xiaohan Yang, Sara M. Allen and Stan D. Wullschleger. 2011 September 01 Plant, Cell & Environment Volume 34, Issue 9, pages 1488-1506, September 2011
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Abstract

The heat shock response continues to be layered with additional complexity as interactions and crosstalk among heat shock proteins (HSPs), the reactive oxygen network and hormonal signalling are discovered. However, comparative analyses exploring variation in each of these processes among species remain relatively unexplored. In controlled environment experiments, photosynthetic response curves were conducted from 22 to 42 °C and indicated that temperature optimum of light-saturated photosynthesis was greater for Glycine max relative to Arabidopsis thaliana or Populus trichocarpa. Transcript profiles were taken at defined states along the temperature response curves, and inferred pathway analysis revealed species-specific variation in the abiotic stress and the minor carbohydrate raffinose/galactinol pathways. A weighted gene co-expression network approach was used to group individual genes into network modules linking biochemical measures of the antioxidant system to leaf-level photosynthesis among P. trichocarpa, G. max and A. thaliana. Network-enabled results revealed an expansion in the G. max HSP17 protein family and divergence in the regulation of the antioxidant and heat shock modules relative to P. trichocarpa and A. thaliana. These results indicate that although the heat shock response is highly conserved, there is considerable species-specific variation in its regulation.

Highlights


The estimated proportion of electrons passing through PSII (ETR) as measured by chlorophyll a fluorescence showed a similar, yet slightly more robust response to temperature than that observed for Asat. The optimum for ETR was again greatest for soybean (37.2 °C, SE = 0.43), followed by poplar (34.8 °C, SE = 0.67) and Arabidopsis (33.2 °C, SE = 0.89; Fig. 1b). The ratio of intercellular to ambient CO2 (Ci/Ca) was plotted against temperature and showed little evidence for stomatal limitation (Fig. 1c). Dark respiration showed the typical rise in respiration as leaf temperature increased (Fig. 1d). Increasing and decreasing leaf temperature from 22 to 42 °C indicated no hysteresis in the response of gas exchange or chlorophyll fluorescence parameters (data not shown).


Comparison of differentially expressed transcripts at distinct physiological states of photosynthetic thermoinhibition. (a) Photosynthetic temperature response curves were taken and samples were collected at physiological states of growth temperature (baseline), photosynthetic optimum, 20% inhibition of optimum and 30% inhibition of optimum. Physiological states were analysed as three contrasts (optimum versus baseline, 20% inhibition versus optimum, 30% inhibition versus 20% inhibition) for the determination of differential gene expression. (b) Venn diagrams showing the intersections of total numbers of transcripts induced for the three contrasts of poplar, Arabidopsis and soybean. Note that physiological states were calculated separately for each species and subsequent sampling temperatures are provided in Supporting Information Table S13.


PageMan display of selected gene categories for stress-related, and secondary and primary metabolism pathways. An unpaired Wilcoxon rank sum test was used to determine if the median fold change within a particular ontological group is the same as the median fold change of all genes not in that group. Multiple testing was corrected with Bengermani Hochberg. Resultant P values were transformed to z values with P = 0.05 set to 0. False colours are used to distinguish among over-(yellow) and under-(blue) represented categories.


Weighted gene co-expression network construction and module correlation to physiological state. (a) (Arabidopsis), (c) (soybean) and (e) (poplar) are multi-dimensional scaling plots of the gene co-expression network. Each circle represents a single gene and the colour of the circle corresponds to module designation. The distance between circles is a function of topological overlap and provides a visual representation of gene and module relationships within network. (b) (Arabidopsis), (d) (soybean) and (f) (poplar) report the positive (+) and negative (−) Spearman correlation of the module eigenvalue (y-axis) with the physiological state (x-axis). Symbols indicate ratio was significantly different than zero at P < 0.001 (***), P < 0.01 (**), P < 0.05 (*).





Citation

WESTON, D. J., KARVE, A. A., GUNTER, L. E., JAWDY, S. S., YANG, X., ALLEN, S. M. and WULLSCHLEGER, S. D. (2011), Comparative physiology and transcriptional networks underlying the heat shock response in Populus trichocarpa, Arabidopsis thaliana and Glycine max. Plant, Cell & Environment, 34: 1488-1506. doi: 10.1111/j.1365-3040.2011.02347.x