A negative feedback loop between TERMINAL FLOWER1 and LEAFY protects inflorescence indeterminacy.

Inflorescences of flowering plants adopt diverse genetically programmed and environmentally tuned architectures. By contrast, continued maintenance of the stem cell pool within the apical meristem is unresponsive to environmental cues. Through a combination of modeling and experimentation in Arabidopsis, we reveal a negative feedback loop that buffers environmental signals. This loop comprises the determinacy-promoting pioneer transcription factor LEAFY (LFY) and the indeterminacy-promoting transcriptional corepressor TERMINAL FLOWER1 (TFL1). At the transition to the flower-producing reproductive phase, LFY directly and quantitatively up-regulates expression of TFL1. TFL1 in turn negatively feeds back on LFY to prevent LFY overaccumulation. This blocks inflorescence termination even under strong florally inductive signals. Our work uncovers a mechanism for robust environmental buffering involving differential responses of two cell populations to the same environmental stimulus. Editor's summary: Plant meristems contain a pool of self-renewing stem cells that produce new organs such as leaves and flowers. Although much of plant development continuously iterates, some plants terminate their meristems, for example, when they produce a flower. Huang et al. studied how Arabidopsis inflorescence meristems maintain the stem cell pool to allow continuous development despite environmental cues to promote flowering. Using spatial expression analysis, investigation of cis-regulatory sequences, and computational modeling, the authors found that two stem cell regulators mutually regulate each other in a negative feedback loop. Although one of these signals is regulated by floral induction cues, the negative feedback loop maintains regulation of expression levels in tissues where the stem cell pool must be retained. —Madeleine Seale INTRODUCTION: Stem cell–containing meristems of plant shoots give rise to new organs after embryogenesis with input from environmental cues. Many inflorescence shoots, including that of Arabidopsis thaliana, are indeterminate, maintaining their stem cells and producing new lateral meristems until the plant dies. The role and identity of the organs produced by the lateral meristems changes from resource production, in leaves and side shoots termed branches, to resource allocation to the next generation, in the seeds formed by flowers. This life history trait underpins food security and is triggered by seasonal cue–dependent increases in the level of systemic florigen protein FLOWERING LOCUS T (FT), which directs lateral meristems to produce determinate flowers instead of indeterminate branches. The adjacent inflorescence meristem does not respond to this systemic cue. It is not known what controls the robustness of the inflorescence meristem fate nor how the differential response to FT in the inflorescence and lateral meristems is achieved. RATIONALE: A central problem in developmental biology is how adjacent cell populations decode the same systemic cue into opposite fates and how robustness to environmental noise is programmed. Addressing these questions informs principles of developmental buffering and fate specification and uncovers levers for tuning shoot architecture. RESULTS: Using cell biological, genetic, and computer modeling approaches, we revealed that the differential responses in the inflorescence meristem and lateral meristems rely on the interactions between the flower-promoting pioneer transcription factor LEAFY (LFY) and the branch- or indeterminacy-promoting transcriptional corepressor TERMINAL FLOWER1 (TFL1). We show that floral cues and FT activate LFY expression in the inflorescence meristem and lateral meristems. Specifically in the inflorescence meristem, LFY directly up-regulates the opposite-acting TFL1. We found that LFY cannot initiate this indeterminacy program in lateral meristems and instead activates floral fate and determinacy. That LFY activates TFL1 transcription in the inflorescence meristem is unexpected, given the opposite roles of LFY and TFL1 in meristem indeterminacy. This paradox is explained by our demonstration that LFY and TFL1 act in a negative feedback loop. Based on computer simulations and experimental data, the role of the negative feedback loop is to ensure that TFL1 is up-regulated in inflorescence meristems in a manner that is proportional to inductive cue intensity (FT levels) through LFY. Only when this condition is met can TFL1 effectively block LFY overaccumulation to prevent conversion of the inflorescence meristem to flower fate. Computational modeling further points to a role of factors that counteract activation of TFL1 by LFY. Their preferential accumulation in the lateral meristems can enable context dependent responses to the same systemic signal. CONCLUSION: Computational simulations, together with experimental data, identified the negative feedback loop as an ideal mechanism for buffering of developmental pathways against strong and fluctuating environmental signals. Our work explains how Arabidopsis inflorescences can simultaneously exhibit environmental responsive plasticity and fate switching in the lateral meristems and phenotypic robustness and fate buffering in the inflorescence meristem. This enables both early and continued production of flowers, a likely adaptation for reproductive success in fluctuating environments. LFY-TFL1 negative feedback loop buffers seasonal cues.: Seasonal cues trigger florigen (FT) production and LFY up-regulation in all shoot meristems. In the inflorescence meristem, LFY forms a negative feedback loop with the indeterminacy factor TFL1, which buffers LFY levels, thereby preserving indeterminacy. In lateral meristems, where buffering is restricted, LFY instead triggers a fate switch from production of branches to that of flowers. [ABSTRACT FROM AUTHOR]