skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: The biology of time: dynamic responses of cell types to developmental, circadian and environmental cues
SUMMARY As sessile organisms, plants are finely tuned to respond dynamically to developmental, circadian and environmental cues. Genome‐wide studies investigating these types of cues have uncovered the intrinsically different ways they can impact gene expression over time. Recent advances in single‐cell sequencing and time‐based bioinformatic algorithms are now beginning to reveal the dynamics of these time‐based responses within individual cells and plant tissues. Here, we review what these techniques have revealed about the spatiotemporal nature of gene regulation, paying particular attention to the three distinct ways in which plant tissues are time sensitive. (i) First, we discuss how studying plant cell identity can reveal developmental trajectories hidden in pseudotime. (ii) Next, we present evidence that indicates that plant cell types keep their own local time through tissue‐specific regulation of the circadian clock. (iii) Finally, we review what determines the speed of environmental signaling responses, and how they can be contingent on developmental and circadian time. By these means, this review sheds light on how these different scales of time‐based responses can act with tissue and cell‐type specificity to elicit changes in whole plant systems.  more » « less
Award ID(s):
2042159
PAR ID:
10446286
Author(s) / Creator(s):
 ;  ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
The Plant Journal
Volume:
109
Issue:
4
ISSN:
0960-7412
Page Range / eLocation ID:
p. 764-778
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract Plant roots navigate the soil ecosystem with each cell type uniquely responding to environmental stimuli. Below ground, the plant's response to its surroundings is orchestrated at the cellular level, including morphological and molecular adaptations that shape root system architecture as well as tissue and organ functionality. Our understanding of the transcriptional responses at cell type resolution has been profoundly enhanced by studies of the model plant Arabidopsis thaliana. However, both a comprehensive view of the transcriptional basis of these cellular responses to single and combinatorial environmental cues in diverse plant species remains elusive. In this review, we highlight the ability of root cell types to undergo specific anatomical or morphological changes in response to abiotic and biotic stresses or cues and how they collectively contribute to the plant's overall physiology. We further explore interconnections between stress and the temporal nature of developmental pathways and discuss examples of how this transcriptional reprogramming influences cell type identity and function. Finally, we highlight the power of single-cell and spatial transcriptomic approaches to refine our understanding of how environmental factors fine tune root spatiotemporal development. These complex root system responses underscore the importance of spatiotemporal transcriptional mapping, with significant implications for enhanced agricultural resilience. 
    more » « less
  2. Dubrovsky, Joseph (Ed.)
    Abstract A fundamental question in developmental biology is how the progeny of stem cells become differentiated tissues. The Arabidopsis root is a tractable model to address this question due to its simple organization and defined cell lineages. In particular, the zone of dividing cells at the root tip—the root apical meristem—presents an opportunity to map the gene regulatory networks underlying stem cell niche maintenance, tissue patterning, and cell identity acquisition. To identify molecular regulators of these processes, studies over the last 20 years employed global profiling of gene expression patterns. However, these technologies are prone to information loss due to averaging gene expression signatures over multiple cell types and/or developmental stages. Recently developed high-throughput methods to profile gene expression at single-cell resolution have been successfully applied to plants. Here, we review insights from the first published single-cell mRNA sequencing and chromatin accessibility datasets generated from Arabidopsis roots. These studies successfully reconstruct developmental trajectories, phenotype cell identity mutants at unprecedented resolution, and reveal cell type-specific responses to environmental stimuli. The experimental insight gained from Arabidopsis paves the way to profile roots from additional species. 
    more » « less
  3. SUMMARY Daily rhythms in physiology are obvious and widespread. While for millennia it was thought that these cycles represent passive responses to environmental cycles, we now recognize that many of them are governed by circadian oscillators. In plants, these cell‐autonomous oscillators regulate daily processes such as photosynthesis, organ growth, and hormone production, as well as seasonal transitions like flowering. Furthermore, the circadian system gates plant responses to biotic and abiotic stresses, modulating susceptibility to pathogens and environmental extremes in a time‐of‐day‐dependent manner. Variants of circadian clock genes have been repeatedly selected during crop domestication and improvement, highlighting the importance of the circadian system to plants and its relevance for agriculture. Here, I review the history of circadian studies in plants and summarize our current understanding of the molecular nature of the circadian oscillator. I also discuss how this complex network both responds to and is buffered against changes in the environment. Next, I examine how circadian oscillators differ between various tissues and how their activities are coordinated throughout the plant body. Finally, I discuss emerging directions, such as ways in which this understanding can be applied to crop improvement in the face of climate change. 
    more » « less
  4. Single-cell genomics technologies are ushering in a new research era. In this review, we summarize the benefits and current challenges of using these technologies to probe the transcriptional regulation of plant development. In addition to profiling cells at a single snapshot in time, researchers have recently produced time-resolved datasets to map cell responses to stimuli. Live-imaging and spatial transcriptomic techniques are rapidly being adopted to link a cell's transcriptional profile with its spatial location within a tissue. Combining these technologies is a powerful spatiotemporal approach to investigate cell plasticity and developmental responses that contribute to plant resilience. Although there are hurdles to overcome, we conclude by discussing how single-cell genomics is poised to address developmental questions in the coming years. 
    more » « less
  5. Abstract Plant cells communicate information for the regulation of development and responses to external stresses. A key form of this communication is transcriptional regulation, accomplished via complex gene networks operating both locally and systemically. To fully understand how genes are regulated across plant tissues and organs, high resolution, multi-dimensional spatial transcriptional data must be acquired and placed within a cellular and organismal context. Spatial transcriptomics (ST) typically provides a two-dimensional spatial analysis of gene expression of tissue sections that can be stacked to render three-dimensional data. For example, X-ray and light-sheet microscopy provide sub-micron scale volumetric imaging of cellular morphology of tissues, organs, or potentially entire organisms. Linking these technologies could substantially advance transcriptomics in plant biology and other fields. Here, we review advances in ST and 3D microscopy approaches and describe how these technologies could be combined to provide high resolution, spatially organized plant tissue transcript mapping. 
    more » « less