Biology subjects

Birnbaum, K. D.

Publications and source records attributed to Birnbaum, K. D..

7 recordsLinked to original sources

bioRxiv2024

A temporal map of division, chromatin modification, and identity specification in the regenerating Arabidopsis root.

The widespread regenerative capacity of plants is mediated by the ability of specialized cells to reprogram their fate, but the sequential cellular states of regenerating plant cells remain an open question. Here, we characterize the trajectory of cellular reprogramming using single-cell RNA/ATAC-seq, imaging, and mutant analysis. The earliest events were dependent on repressive chromatin modification, where Multiome and genetic analysis showed that Class I histone deacetylases (HDACs) HDA9 and HDA19 were needed to shut down old identities and to prevent a runaway stress response. Cell division mediates a second step needed for the acquisition of many new identity markers, where division rates were tuned by DOF transcription factor OBP1 accelerating and SMR5, 7, and 10 decelerating division rates hours later. The results show how plants actively mediate the loss of remnant identities within hours of injury and then tune cell division rates to rapidly reprogram cells to new identities.

developmental biology↗

bioRxiv2023

A common regulatory switch controls a suite of C4 traits in multiple cell types

The C4 photosynthetic pathway provided a major advantage to plants growing in hot, dry environments, including the ancestors of our most productive crops. Two traits were essential for the evolution of this pathway: increased vein density and the functionalization of bundle sheath cells for photosynthesis. Although GRAS transcriptional regulators, including SHORT ROOT (SHR), have been implicated in mediating leaf patterning in both C3 and C4 species, little is known about what controls the specialized features of the cells that mediate C4 metabolism and physiology. We show in the model monocot, Setaria viridis, that SHR regulates components of multiple cell identities, including chloroplast biogenesis and photosynthetic gene expression in bundle sheath cells, a central feature of C4 plants. Furthermore, we found that it also contributes to the two-cell compartmentalization of the characteristic four-carbon shuttle pathway. Disruption of SHR function clearly reduced photosynthetic capacity and seed yield in mutant plants under heat stress. Together, these results show how cell identities are remodeled by SHR to host the suite of traits characteristic of C4 regulation, which are a main engineering target in non-C4 crops to improve climate resilience.

plant biology↗

bioRxiv2023

Nuclear GSH import precedes coordinated cell cycle changes during regeneration

The plasticity of plant cells underlies their wide capacity to regenerate, with increasing evidence in plants and animals implicating cell cycle dynamics in cellular reprogramming. To investigate the cell cycle during cellular reprogramming, we developed a comprehensive set of cell cycle phase markers in the Arabidopsis root. Using single-cell RNA-seq profiles and live imaging during regeneration, we found that a subset of cells near an ablation injury dramatically increases division rate by truncating G1. Cells in G1 undergo a transient nuclear peak of glutathione (GSH) prior to coordinated entry into S phase followed by rapid divisions and cellular reprogramming. A symplastic block of the ground tissue impairs regeneration, which is rescued by exogenous GSH. We propose a model in which GSH from the outer tissues is released upon injury licensing an exit from G1 near the wound to induce rapid cell division and reprogramming.

plant biology↗

bioRxiv2022

Stem cell regulators control a G1 duration gradient in the plant root meristem

In meristems, where new plant organs initiate, key stem cell regulators have been identified, but their link to cell cycle progression remains unclear. Here, we show that the root meristem has a positional gradient of G1 duration that ranges from [~]2 h near the meristem boundary to more than 20 h in stem cells and early derivatives. Mutants in the PLETHORA (PLT) genes shortened G1 length and flattened its gradient. Computer modeling of an incoherent feed-forward loop (IFFL) predicted the inference of a negative regulatory pathway. We propose that PLT genes play opposing roles, maintaining meristem and stem cell activity and inhibiting G1 progression through the CDK inhibitor KRP5, a PLT target, and RBR1. This establishes a previously undescribed proximal-distal feature of the root meristem in which a G1 duration gradient is shaped by stem cell and meristem maintenance regulators.

plant biology↗

bioRxiv2021

Ground tissue circuitry regulates organ complexity in cereal roots

Most plant roots have multiple cortex layers that make up the bulk of the organ and play key roles in physiology, such as flood tolerance and symbiosis. However, little is known about the formation of cortical layers outside of the highly reduced anatomy of the model Arabidopsis. Here we use single-cell RNAseq to rapidly generate a cell resolution map of the maize root, revealing an alternative configuration of the tissue formative SHORT-ROOT (SHR) signaling pathway adjacent to an expanded cortex. We show that maize SHR protein is hypermobile, moving at least eight cell layers into the cortex. Higher-order SHR mutants in both maize and Setaria have reduced numbers of cortical layers, showing that the SHR pathway controls expansion of cortical tissue in grasses that sets up anatomical complexity and a host of key traits. One sentence summarySingle-cell RNA-seq maps the maize root transcriptome uncovering a mechanism that regulates cortex layer number.

genomics↗

bioRxiv2021

Analysis of phloem trajectory links tissue maturation to cell specialization.

The mechanisms that allow cells in the plant meristem to coordinate tissue-wide maturation gradients with specialized cell networks are critical for indeterminate growth. Here, we reconstructed the protophloem developmental trajectory of 19 cells from cell birth to terminal differentiation at single cell resolution in the Arabidopsis root. We found that cellular specification is mediated near the stem cell niche by PHLOEM EARLY DOF (PEAR) transcription factors. However, the PEAR dependent differentiation program is repressed by a broad gradient of PLETHORA (PLT) transcription factors, which directly inhibit PEARs own direct target ALTERED PHLOEM DEVELOPMENT (APL). The dissipation of PLT gradient around 7 cells from the stem cell activates APL expression, and a subsequent transitional network that results in a "seesaw" pattern of mutual inhibition over developmental time. Together, we provide a mechanistic understanding of how morphogen-like maturation gradients interface with cell-type specific transcriptional regulators to stage cellular differentiation.

plant biology↗

bioRxiv2018

Week-long imaging of cell divisions in the Arabidopsis root meristem

Characterizing the behaviors of dynamic systems requires capturing them with high temporal and spatial resolution. Owing to its transparency and genetic tractability, the Arabidopsis thaliana root lends itself well to live imaging when combined with cell and tissue-specific fluorescent reporters. We developed a novel 4D imaging method that utilizes simple confocal microscopy and readily available components to track cell divisions in the root stem cell niche and surrounding region for up to one week. This new setup allows us to finely analyze meristematic cell division rates that lead to patterning. Using this method, we performed a direct measurement of cell division intervals within and around the root stem cell niche. The results reveal a short, steep gradient of cell division in proximal stem cells, with progressively more rapid cell division rates from QC, to cells in direct contact with the QC (initials), to their immediate daughters, after which division rates appear to become more homogeneous. These results provide a baseline to study how perturbations in signaling could affect cell division patterns in the root meristem.

developmental biology↗