Single-cell and spatial multiomics identifies heterogeneous xylem development driven by mechanical stress in Populus

Area of Science:

• Plant Biology
• Wood Formation
• Biotechnology

Background:

• Xylem provides structural support and forms tension wood under mechanical stress.
• Key questions about tension wood fiber distinctness, lineage, and genetic control remained unanswered for over a century.

Purpose of the Study:

• To determine if tension wood fibers are morphologically distinct from normal wood fibers.
• To investigate the lineage of tension wood fibers.
• To identify key genes regulating tension wood formation.

Main Methods:

• Single-cell RNA sequencing (scRNA-seq) of normal, tension, and opposite xylem.
• Spatial transcriptomics and metabolomics for validating differential developmental speed and cell-type ratios.
• Phosphoproteomics to analyze conserved mechanical sensing mechanisms.

Main Results:

• Fibers in normal and tension wood are the same cell type and originate from the same lineage.
• Differential developmental speed and cell-type ratios in tension and opposite xylem were confirmed.
• Mechanical sensing mechanisms are conserved across angiosperm stems and roots.
• A set of genes involved in cell fate transition during tension wood formation was identified.

Conclusions:

• Tension wood formation does not involve distinct cell types or lineages.
• Identified genes provide targets for understanding and manipulating wood formation.
• Insights into cell development heterogeneity can optimize biomass production and bioenergy yield.