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.

Highlights

  • Day length and temperature, which exhibit large annual changes, have a marked influence on seasonal phenomena, such as bud flush and formation, growth pattern, and dormancy induction [1,2,3,4,5,6]

  • This study provides considerable insight into the control of phenology in Japanese cedar, a gymnosperm indeterminate species

  • The co-expression network of annual transcriptome dynamics revealed a close relationship between SD- and low temperature (LT)-regulated genes

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Summary

Introduction

Day length and temperature, which exhibit large annual changes, have a marked influence on seasonal phenomena, such as bud flush and formation, growth pattern, and dormancy induction [1,2,3,4,5,6]. A number of previous reports have described how annual cycles are controlled at the transcript level and the effects of day length and temperature in the model tree, Populus [5,6,7,8,9]. The expression of core clock genes, which play roles in adaptation to day length and temperature changes and the regulation of seasonal phenomena [15, 16], was shown to be arrested under conditions of continuous light or dark in gymnosperm conifers, in contrast to angiosperms [17, 18]. Differences in diurnal rhythms of clock genes between Arabidopsis and Pseudotsuga menziesii (Douglas-fir) have been reported [19]. These data suggest the importance of studying gymnosperms to understand their unique seasonal regulatory mechanisms

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