CAREER: Spatiotemporal Coordination of Growth and Differentiation Across Tissues

Roots are essential for plant growth and agricultural productivity because they anchor plants and absorb the water and nutrients needed to sustain development. Root growth and development require neighboring tissues to divide, expand, and mature in a coordinated manner; if this coordination fails, because plants are surrounded by interconnected cell walls, organs tear themselves apart as they grow and normal root growth breaks down. More broadly, understanding how distinct tissues communicate during organ growth remains a major unresolved question in developmental biology. This project will determine how plants coordinate growth and differentiation across tissues, using Arabidopsis thaliana roots as a model. Recent work has shown that disrupting hormone signaling in a single cell layer of the root can dramatically reshape the growth of neighboring layers and halt root growth, confirming that developing tissues must communicate with each other to remain coordinated. To examine this communication, broad manipulation of plant hormone pathways in the whole plant often produces undesirable side effects, therefore understanding tissue-specific signaling, proposed here, is crucial for the precise engineering of crops. By uncovering the signals that maintain this coordination, the project will advance fundamental understanding of how multicellular plant organs grow and lay the foundation for precision plant engineering strategies to improve crop productivity, essential for food security. The project will also expand training in plant biology through a new undergraduate research course, a high school outreach project in plant genome engineering, and a training workshop on single-cell and spatial methods in plant biology. The project will test the hypothesis that organ development depends on molecular and mechanical feedback between neighboring tissues, such that perturbing hormone signaling in one cell layer dynamically reprograms both local and adjacent cell behaviors. Roots provide a tractable system for these studies because concentric tissue layers and rigid cell walls allow chemical and mechanical signals to be tracked across layers. The project focuses on brassinosteroid signaling; tissue-specific disruption of a hormone receptor leads to exaggerated expansion in neighboring cells and loss of inter-tissue coordination. Combining tissue-specific perturbations with single-cell, spatial, and live-imaging approaches, the project will identify coordination-responsive cell states, track how signaling outputs propagate across neighboring cell layers, and discover candidate factors that mediate developmental integration between tissues. Quantitative imaging, mechanical assays, and artificial intelligence-enabled mechano-biochemical modeling will link these molecular changes to root cell geometry, growth dynamics, and tissue mechanics. Finally, inducible perturbation systems will be used to define spatial and temporal windows in which coordination is established and maintained, testing when and where signaling is required, whether coordination can be restored after it has been disrupted, and how many cells must be affected to trigger breakdown. These studies will generate a multiscale framework for how molecular and mechanical signals integrate across tissues to build a multicellular organ. Combining AI with single-cell and spatial approaches, the project advances plant biotechnology while producing publicly available datasets, code, computational models, and molecular resources for the larger research community. This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria. NSF Award ID: 2544734 | Program: 01003031DB NSF RESEARCH & RELATED ACTIVIT,01002627DB NSF RESEARCH & RELATED ACTIVIT | Principal Investigator: Trevor Nolan | Institution: California Institute of Technology, PASADENA, CA | Award Amount: $1,225,440 View on NSF Award Search: https://www.nsf.gov/awardsearch/show-award/?AWD_ID=2544734 View on Research.gov: https://www.research.gov/awardapi-service/v1/awards/2544734.html