Plants distinguish different photoperiods to independently control seasonal flowering and growth

• 成果类型: Article
• 署名作者: Wang, Qingqing; Liu, Wei; Leung, Chun Chung; Tarte, Daniel A.; Gendron, Joshua M.
• 署名单位: Yale University
• 刊物名称: SCIENCE
• ISSN/ISSBN: 0036-10219
• DOI: 10.1126/science.adg9196
• 发表日期: 2024-02-09
• 关键词: arabidopsis-thaliana; starch turnover; salicylic-acid; cell-death; circadian clock; protein; light; deficient; daylength; responses

摘要

INTRODUCTION Daylength, or photoperiod, is a stable indicator of the season, and organisms can measure photoperiods to predict seasonal changes in climate. In plants, flowering and growth are often regulated by photoperiod, and the photoperiodic flowering pathway is well understood. By contrast, much less is known about how photoperiod regulates growth, including the measurement system and genes that are required. RATIONALE Studies of photoperiodic flowering have benefitted from mutants with obvious defects in seasonal flowering time, and genes whose expression is controlled by photoperiod and can be tracked under different daylengths. We hypothesized that similar tools would allow for increased understanding of the genes and measurement systems that participate in photoperiodic growth, potentially revealing a different mechanism than is used for seasonal flowering. RESULTS Arabidopsis thaliana grows faster in long days, so we mined transcriptomic data for genes that are induced in long days and required for proper vegetative growth. We identified MYO-INOSITOL-1-PHOSPHATE SYNTHASE 1 (MIPS1), which encodes a gene necessary for plants to produce myo-inositol, a sugar required for a variety of important cellular processes that control growth. We then showed that MIPS1 expression is induced during long but not short days and that a mips1 mutant plant has growth defects in long but not short days. Because the flowering photoperiod measurement system has been characterized in plants, we tested whether our growth mutants were in the same pathway. We found that the mips1 mutant has no flowering defect, and photoperiodic flowering mutants have no growth defect, results that were confirmed by double mutants with mips1 and photoperiodic flowering mutantions. These experiments showed that photoperiodic flowering and growth are genetically separable and that the photoperiod measurement system governing flowering is not controlling photoperiodic growth. Further experiments showed that MIPS1 expression and function are regulated by a circadian clock-controlled metabolic daylength measurement system. By changing light intensities over the course of a day while maintaining the integrated intensity, we demonstrated that photoperiodic growth and MIPS1 function are controlled by the photosynthetic period and that flowering is controlled by a wholly different photoperiod. CONCLUSION Our results show that plants can measure two different photoperiods in natural day cycles. They can detect an absolute photoperiod with low light-detecting photoreceptor systems to control flowering time. In parallel, they can measure the photosynthetic period as a metabolic daylength to control growth. This allows plants to independently coordinate seasonal developmental processes. This work opens the possibility that several photoperiod measurement systems can operate in parallel in organisms to precisely regulate a variety of seasonal processes. Plants detect two different daylengths to control seasonal flowering and growth. In natural day cycles, photoperiodic flowering and photoperiodic growth operate through different measuring systems. Photoperiodic flowering detects an absolute photoperiod that is sensed by photoreceptors activated at low light intensities. For flowering during long-day seasons, the photoperiod extends into the light-sensitive portion of the day, which activates expression of the florigen gene (FT) to promote flowering. Photoperiodic growth detects the photosynthetic period, which is defined as the duration of time that light is above the photosynthetic compensation point. For growth during long-day seasons, the photosynthetic period extends into the light-sensitive portion of the day, activating MYO-INOSITOL-1-PHOSPHATE SYNTHASE 1 (MIPS1) expression to support rapid growth. Hence, parallel photoperiod measurement systems allow different photoperiodic processes to be coordinated independently across the year.