A cell wall-associated gene network shapes leaf boundary domains

Abstract

Boundary domains delimit and organize organ growth throughout plant development almost relentlessly building plant architecture and morphogenesis. Boundary domains display reduced growth and orchestrate development of adjacent tissues in a non-cell autonomous manner. How these two functions are achieved remains elusive despite the identification of several boundary-specific genes. Here, we show using morphometrics at the organ and cellular levels that leaf boundary domain development requires SPINDLY (SPY), an O-fucosyltransferase, to act as cell growth repressor. Further we show that SPY acts redundantly with the CUP-SHAPED COTYLEDON transcription factors (CUC2 and CUC3), which are major determinants of boundaries development. Accordingly at the molecular level, CUC2 and SPY repress a common set of genes involved in cell wall loosening providing a molecular framework for the growth repression associated with boundary domains. Atomic force microscopy (AFM) confirmed that young leaf boundary domain cells have stiffer cell walls than marginal outgrowth. This differential cell wall stiffness was reduced in spy mutant. Taken together our data reveal a concealed CUC2 cell wall associated gene network linking tissue patterning with cell growth and mechanics.Summary statementDecreased cell-wall loosening gene expression contributes to the coordination of cell growth and mechanics with tissue patterning thus driving boundary development.

The maize preligule band is subdivided into distinct domains with contrasting cellular properties prior to ligule outgrowth

“…Cell wall-modifying genes are enriched among the transcriptional targets of BRs, and BR signaling is known to affect cell wall composition and structure, suggesting that cell wall biophysical properties are a component of boundary function (Bai et al, 2012;Graeff et al, 2021;Sun et al, 2010). Consistent with this, cell wallrelated gene ontology terms are also significantly enriched among the transcriptional targets of LOB, while CUC2 represses many genes associated with cell wall loosening (Bell et al, 2012;Bouré et al, 2022;Cucinotta et al, 2018). Other experiments show that cell wall-related genes are enriched among highly translated transcripts in the boundary (Tian et al, 2014).…”

“…Cell fate, as well as differences in the rate and direction of cell division and expansion, are patterned along these axes. The boundary is maintained at the base of the organ throughout development and can be recapitulated at other locations on the developing organ (Bouré et al, 2022;Johnston et al, 2014;Nahar et al, 2012;Xiao et al, 2022).…”

“…Other experiments show that cell wall-related genes are enriched among highly translated transcripts in the boundary (Tian et al, 2014). Additionally, cells in boundary domains have more rigid cell walls, as measured with atomic force microscopy (AFM) (Bouré et al, 2022;Sampathkumar et al, 2019). Changes in cell wall composition or remodeling activity could contribute to the decreased rate of cell expansion in boundary domains, but more experiments are needed to determine how the boundary function modulates growth.…”