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The phenology of temperate perennials, including the timing of vegetative growth and flowering, is well known to be controlled by seasonal dormancy cycles. Dormant structures are known as buds and have specialized covering structures, symplastic isolation from the plant, and often autonomous stores of carbon and nitrogen reserves. In contrast, in annual plants, our current understanding of the control of the timing of flowering focuses on the mechanisms affecting floral initiation, the transition from a vegetative apical meristem to a inflorescence meristem producing flower primordia in place of leaves. Recently we revealed that annual crops in Brassicaceae exhibit chilling-responsive growth control in a manner closely resembling bud dormancy breakage in perennial species. Here I discuss evidence that vernalization in autumn is widespread and further discuss its role in inducing flower bud set prior to winter. I also review evidence that flower bud dormancy has a more widespread role in annual plant flowering time control than previously appreciated., (© The Author(s) 2024. Published by Oxford University Press on behalf of the Society for Experimental Biology.)

Winter annual life history is conferred by the requirement for vernalization to promote the floral transition and control the timing of flowering. Here we show using winter oilseed rape that flowering time is controlled by inflorescence bud dormancy in addition to vernalization. Winter warming treatments given to plants in the laboratory and field increase flower bud abscisic acid levels and delay flowering in spring. We show that the promotive effect of chilling reproductive tissues on flowering time is associated with the activity of two FLC genes specifically silenced in response to winter temperatures in developing inflorescences, coupled with activation of a BRANCHED1-dependent bud dormancy transcriptional module. We show that adequate winter chilling is required for normal inflorescence development and high yields in addition to the control of flowering time. Because warming during winter flower development is associated with yield losses at the landscape scale, our work suggests that bud dormancy activation may be important for effects of climate change on winter arable crop yields.

Plants with winter annual life history germinate in summer or autumn and require a period of prolonged winter cold to initiate flowering, known as vernalization. In the Brassicaceae, the requirement for vernalization is conferred by high expression of orthologs of the FLOWERING LOCUS C (FLC) gene, the expression of which is known to be silenced by prolonged exposure to winter-like temperatures [1]. Based on a wealth of vernalization experiments, typically carried out in the range of 5°C-10°C, we would expect field environments during winter to induce flowering in crops with winter annual life history. Here, we show that, in the case of winter oilseed rape, expression of multiple FLC orthologs declines not during winter but predominantly during October when the average air temperature is 10°C-15°C. We further demonstrate that plants proceed through the floral transition in early November and overwinter as inflorescence meristems, which complete floral development in spring. To validate the importance of pre-winter temperatures in flowering time control, we artificially simulated climate warming in field trial plots in October. We found that increasing the temperature by 5°C in October results in raised FLC expression and delays the floral transition by 3 weeks but only has a mild effect on flowering date the following spring. Our work shows that winter annuals overwinter as a floral bud in a manner that resembles perennials and highlights the importance of studying signaling events in the field for understanding how plants transition to flowering under real environmental conditions., (Copyright © 2019 The Authors. Published by Elsevier Ltd.. All rights reserved.)

Pleiotropy occurs when one gene influences more than one trait, contributing to genetic correlations among traits. Consequently, it is considered a constraint on the evolution of adaptive phenotypes because of potential antagonistic selection on correlated traits, or, alternatively, preservation of functional trait combinations. Such evolutionary constraints may be mitigated by the evolution of different functions of pleiotropic genes in their regulation of different traits. Arabidopsis thaliana flowering-time genes, and the pathways in which they operate, are among the most thoroughly studied regarding molecular functions, phenotypic effects, and adaptive significance. Many of them show strong pleiotropic effects. Here, we review examples of pleiotropy of flowering-time genes and highlight those that also influence seed germination. Some genes appear to operate in the same genetic pathways when regulating both traits, whereas others show diversity of function in their regulation, either interacting with the same genetic partners but in different ways or potentially interacting with different partners. We discuss how functional diversification of pleiotropic genes in the regulation of different traits across the life cycle may mitigate evolutionary constraints of pleiotropy, permitting traits to respond more independently to environmental cues, and how it may even contribute to the evolutionary divergence of gene function across taxa., (© 2019 The Authors. New Phytologist © 2019 New Phytologist Trust.)

Plants integrate seasonal signals, including temperature and day length, to optimize the timing of developmental transitions. Seasonal sensing requires the activity of two proteins, FLOWERING LOCUS C (FLC) and FLOWERING LOCUS T (FT), that control certain developmental transitions in plants. During reproductive development, the mother plant uses FLC and FT to modulate progeny seed dormancy in response to temperature. We found that for regulation of seed dormancy, FLC and FT function in opposite configuration to how those same genes control time to flowering. For seed dormancy, FT regulates seed dormancy through FLC gene expression and regulates chromatin state by activating antisense FLC transcription. Thus, in Arabidopsis the same genes controlled in opposite format regulate flowering time and seed dormancy in response to the temperature changes that characterize seasons., (Copyright © 2018 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.)

Climate change is accelerating plant developmental transitions coordinated with the seasons in temperate environments. To understand the importance of these timing advances for a stable life history strategy, we constructed a full life cycle model of Arabidopsis thaliana. Modelling and field data reveal that a cryptic function of flowering time control is to limit seed set of winter annuals to an ambient temperature window which coincides with a temperature-sensitive switch in seed dormancy state. This coincidence is predicted to be conserved independent of climate at the expense of flowering date, suggesting that temperature control of flowering time has evolved to constrain seed set environment and therefore frequency of dormant and non-dormant seed states. We show that late flowering can disrupt this bet-hedging germination strategy. Our analysis shows that life history modelling can reveal hidden fitness constraints and identify non-obvious selection pressures as emergent features.

Clock-regulated pathways coordinate the response of many developmental processes to changes in photoperiod and temperature. We model two of the best-understood clock output pathways in Arabidopsis, which control key regulators of flowering and elongation growth. In flowering, the model predicted regulatory links from the clock to cycling DOF factor 1 (CDF1) and flavin-binding, KELCH repeat, F-box 1 (FKF1) transcription. Physical interaction data support these links, which create threefold feed-forward motifs from two clock components to the floral regulator FT. In hypocotyl growth, the model described clock-regulated transcription of phytochrome-interacting factor 4 and 5 (PIF4, PIF5), interacting with post-translational regulation of PIF proteins by phytochrome B (phyB) and other light-activated pathways. The model predicted bimodal and end-of-day PIF activity profiles that are observed across hundreds of PIF-regulated target genes. In the response to temperature, warmth-enhanced PIF4 activity explained the observed hypocotyl growth dynamics but additional, temperature-dependent regulators were implicated in the flowering response. Integrating these two pathways with the clock model highlights the molecular mechanisms that coordinate plant development across changing conditions., (© 2015 The Authors. Published under the terms of the CC BY 4.0 license.)