Molecular phenology in plants: in natura systems biology for the comprehensive understanding of seasonal responses under natural environments

Summary Phenology refers to the study of seasonal schedules of organisms. Molecular phenology is defined here as the study of the seasonal patterns of organisms captured by molecular biology techniques. The history of molecular phenology is reviewed briefly in relation to advances in the quantification technology of gene expression. High‐resolution molecular phenology ( HMP ) data have enabled us to study phenology with an approach of in natura systems biology. I review recent analyses of FLOWERING LOCUS C ( FLC ), a temperature‐responsive repressor of flowering, along the six steps in the typical flow of in natura systems biology. The extensive studies of the regulation of FLC have made this example a successful case in which a comprehensive understanding of gene functions has been progressing. The FLC ‐mediated long‐term memory of past temperatures creates time lags with other seasonal signals, such as photoperiod and short‐term temperature. Major signals that control flowering time have a phase lag between them under natural conditions, and hypothetical phase lag calendars are proposed as mechanisms of season detection in plants. Transcriptomic HMP brings a novel strategy to the study of molecular phenology, because it provides a comprehensive representation of plant functions. I discuss future perspectives of molecular phenology from the standpoints of molecular biology, evolutionary biology and ecology. Contents Summary 399 I. Introduction 400 II. Definition and methodological advance of molecular phenology 401 III. In natura systems biology using high‐resolution molecular phenology (HMP) data 402 IV. Predicting properties of a temperature‐responding machinery (Step 1) 402 V. FLC as a candidate gene regulatory system for past temperature memory (Step 2) 404 VI. In natura quantification of past temperature memory by HMP (Step 3) 405 VII. Development of a molecular phenology‐based mechanistic model (Step 4) 406 VIII. New insight into and analysis of the mechanism: digital repression of FLC (Step 5) 406 IX. New insight into and analysis of natural signals: phase lag calendar hypotheses (Step 6) 407 X. Transcriptomic HMP (revolution in Step 3) 409 XI. Perspectives: circles of in natura systems biology 409 Acknowledgements 410 References 410