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. 2020 Mar 9;15(3):e0229843.
doi: 10.1371/journal.pone.0229843. eCollection 2020.

Effects of Day Length- And Temperature-Regulated Genes on Annual Transcriptome Dynamics in Japanese Cedar (Cryptomeria Japonica D. Don), a Gymnosperm Indeterminate Species

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Free PMC article

Effects of Day Length- And Temperature-Regulated Genes on Annual Transcriptome Dynamics in Japanese Cedar (Cryptomeria Japonica D. Don), a Gymnosperm Indeterminate Species

Mine Nose et al. PLoS One. .
Free PMC article

Abstract

Seasonal phenomena in plants are primarily affected by day length and temperature. The shoot transcriptomes of trees grown in the field and a controlled-environment chamber were compared to characterize genes that control annual rhythms and the effects of day length- and temperature-regulated genes in the gymnosperm Japanese cedar (Cryptomeria japonica D. Don), which exhibits seasonally indeterminate growth. Annual transcriptome dynamics were clearly demonstrated by principal component analysis using microarray data obtained under field-grown conditions. Analysis of microarray data from trees grown in a controlled chamber identified 2,314 targets exhibiting significantly different expression patterns under short-day (SD) and long-day conditions, and 2,045 targets exhibited significantly different expression patterns at 15°C (LT; low temperature) versus 25°C. Interestingly, although growth was suppressed under both SD and LT conditions, approximately 80% of the SD- and LT-regulated targets differed, suggesting that each factor plays a unique role in the annual cycle. The top 1,000 up-regulated targets in the growth/dormant period in the field coincided with more than 50% of the SD- and LT-regulated targets, and gene co-expression network analysis of the annual transcriptome indicated a close relationship between the SD- and LT-regulated targets. These results indicate that the respective effects of day length and temperature interact to control annual transcriptome dynamics. Well-known upstream genes of signaling pathways responsive to environmental conditions, such as the core clock (LHY/CjLHYb and CCA1/CjLHYa) and PEBP family (MFT) genes, exhibited unique expression patterns in Japanese cedar compared with previous reports in other species, suggesting that these genes control differences in seasonal regulation mechanisms between species. The results of this study provide new insights into seasonal regulation of transcription in Japanese cedar.

Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. PCA of microarray data.
The first two principal components obtained from PCA of annual time series samples of microarray data are shown (gray circles). The seasonal conditions of Japanese cedar grown in a controlled-environment chamber were estimated by plotting microarray data against the PCA results of annual time series samples. (A) Red and green circles indicate samples collected from cuttings grown under LD and SD conditions, respectively. (B) Orange and blue circles indicate samples collected from cuttings grown under HT and LT conditions, respectively.
Fig 2
Fig 2. Annual expression pattern of the top-scoring targets of principal component 1.
Annual expression patterns of the targets with the top 1,000 positive and negative scores for principal component 1 (blue and orange, respectively). Each line represents the average normalized intensity value of an individual transcript.
Fig 3
Fig 3. Expression pattern of a cluster of targets regulated by day length and temperature.
(A) Median profile of four clusters of SD-regulated targets under LD and SD conditions (red and green, respectively). (B) Median profile of four clusters of LT-regulated targets under HT and LT conditions (orange and blue, respectively).
Fig 4
Fig 4. Comparison of genes regulated under SD and LT conditions and top 1,000 positive and negative scoring targets of principal component 1.
Expression of targets with positive scores for principal component 1 increased in winter, and expression of targets with negative scores increased in summer; refer to Fig 2.
Fig 5
Fig 5. Co-expression gene network of annual transcriptome dynamics.
The gene network was estimated based on correlation coefficients of the expression value between genes using the microarray data of annual time series samples, and 1,953 targets were connected. Dot colors indicate the results of experimental time series samples; “SD-regulated” indicates targets that were up- or down-regulated under SD conditions, “LT-regulated” indicates targets that were up- or down-regulated under LT conditions, and “SD- and LT-regulated” indicates targets that were up- or down-regulated under both SD and LT conditions. This result demonstrated a close relationship between SD- and LT-regulated genes in the annual transcriptome dynamics.
Fig 6
Fig 6. Annual expression patterns of starch-related genes.
Each line represents the average normalized intensity value of an individual transcript of a gene involved in starch synthesis (A) or starch degradation (B), as listed in Table 5. Broken lines and solid lines indicate transcripts up-regulated by SD and LT conditions, respectively. Double lines indicate transcripts up-regulated by both SD and LT conditions. Dotted lines indicate transcripts not up-regulated by either SD or LT conditions in this study.
Fig 7
Fig 7. Annual expression pattern of clock-related genes and PEBP family-related genes under field conditions.

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Grant support

This study is a part of the project on “Development of mitigation and adaptation techniques to global warming in the sectors of agriculture, forestry, and fisheries” and “Development of adaptation techniques to the climate change in the sectors of agriculture, forestry, and fisheries” supported by the Ministry of Agriculture, Forestry and Fisheries, Japan, and the Japan Society for the Promotion of Science KAKENHI (grant no.: 15K18716).
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