Ambient temperature and genotype differentially affect developmental and phenotypic plasticity in Arabidopsis thaliana

Abstract

Background: Global increase in ambient temperatures constitute a significant challenge to wild and cultivated plant species. Forward genetic analyses of individual temperature-responsive traits have resulted in the identification of several signaling and response components. However, a comprehensive knowledge about temperature sensitivity of different developmental stages and the contribution of natural variation is still scarce and fragmented at best.

Results: Here, we systematically analyze thermomorphogenesis throughout a complete life cycle in ten natural Arabidopsis thaliana accessions grown under long day conditions in four different temperatures ranging from 16 to 28 °C. We used Q₁₀, GxE, phenotypic divergence and correlation analyses to assess temperature sensitivity and genotype effects of more than 30 morphometric and developmental traits representing five phenotype classes. We found that genotype and temperature differentially affected plant growth and development with variing strengths. Furthermore, overall correlations among phenotypic temperature responses was relatively low which seems to be caused by differential capacities for temperature adaptations of individual accessions.

Conclusion: Genotype-specific temperature responses may be attractive targets for future forward genetic approaches and accession-specific thermomorphogenesis maps may aid the assessment of functional relevance of known and novel regulatory components.

Keywords: Arabidopsis; Natural variation; Phenotypic plasticity; Phenotyping; Thermomorphogenesis.

Fig. 1

Phenotypic profiling approach. Schematic representation of the accessions, cultivation temperatures (°C) and phenotype classes used in the phenotypic profiling approach. Numbers indicate individual traits listed and color-coded according to the corresponding phenotype class. Blue squares indicate phenotypes sorted into ‘morphometric phenotypes’. Their position is indicative for the developmental stage at time of assessment. Further information on trait values and specific time of assessments are shown in Additional file 1

Fig. 2

Col-0 growth and development in response to different ambient temperatures. a Quantification of phenotypic traits recorded at different growth temperatures. Box plots show median and interquartile ranges (IQR), outliers (> 1.5 times IQR) are shown as circles. Units for each trait are specified in Additional file 16. Different letters denote statistical differences (P > 0.05) among samples as assessed by one-factorial ANOVA and Tukey HSD. b Summary of temperature effects on developmental timing. Circles denote medians, bars denote IQRs (n > 15). Times of phenotypic assessment for selected traits in (a) are indicated by asterisks

Fig. 3

Natural variation in temperature sensitivity of phenotypic traits (Q₁₀). Mean log₂Q₁₀ values for each accession (a) summarized in box plots for each phenotype class and (b) presented as a heatmap for all individual phenotypes. a Box plots show median and interquartile ranges (IQR), whiskers range from min. to max. Values. b positive (increasing) and negative (decreasing) log₂Q₁₀ values are shown in yellow and blue, respectively with a log₂Q₁₀ cut-off value of 2 for better resolution. Missing data are denoted in light gray

Fig. 4

Genotype and temperature effects on phenotypic variation. a Genotype ($P_{\mathrm{st}}^{\mathrm{gen}}$, black) and temperature ($P_{\mathrm{st}}^{\text{temp}}$, green) contribution to variation. Solid lines show mean P_st values and shaded areas indicate standard deviations. b Scatter plot of mean $P_{\mathrm{st}}^{\mathrm{gen}}$ and $P_{\mathrm{st}}^{\text{temp}}$ values over all temperatures and accessions, respectively. Phenotypes are color-coded according to the phenotype classes shown in Fig. 1 and described in Additional file 1. A heatmap of individual $P_{\mathrm{st}}^{\mathrm{gen}}$ and $P_{\mathrm{st}}^{\text{temp}}$ values and a scatter plot including standard deviations are shown in Additional file 16

Fig. 5

Principle component and correlation analyses. a Phenotypic data of all temperatures and genotypes were subjected to principle component analysis (PCA). b-c Correlation analysis of temperature responses among individual traits or trait groups of all analyzed genotypes (b) or in selected individual accessions (c). Spearmann correlation coefficients were tested for significance and coefficients with P < 0.05 and P < 0.1 are presented in (b) and (c), respectively. Phenotype correlations for all accessions individually are shown in Additional file 18