Real-time conversion of tissue-scale mechanical forces into an interdigitated growth pattern

Abstract

The leaf epidermis is a dynamic biomechanical shell that integrates growth across spatial scales to influence organ morphology. Pavement cells, the fundamental unit of this tissue, morph irreversibly into highly lobed cells that drive planar leaf expansion. Here we define how tissue-scale cell wall tensile forces and the microtubule-cellulose synthase systems pattern interdigitated growth in real-time. A morphologically potent subset of cortical microtubules span the periclinal and anticlinal cell faces to pattern cellulose fibers that generate a patch of anisotropic wall. The result is local polarized growth that is mechanically coupled to the adjacent cell via a pectin-rich middle lamella, and this drives lobe formation. Finite element pavement cell models revealed cell wall tensile stress as an upstream patterning element that links cell- and tissue-scale biomechanical parameters to interdigitated growth. Cell lobing in leaves is evolutionarily conserved, occurs in multiple cell types, and is associated with important agronomic traits. Our general mechanistic models of lobe formation provide a foundation to analyze the cellular basis of leaf morphology and function.

Cell shape: A ROP regulatory tug-of-war in pavement cell morphogenesis

“…Notably, PHGAPs preferentially accumulate in the anticlinal face on the indentation side, where they form stripes at the plasma membrane 7 . This localization pattern strikingly resembles that of the microtubules that populate the cortical anticlinal face in the indentation and then extend to the outer periclinal face of the cell (i.e., transfacial, Figure 1) 9 . Indeed, PHGAPs largely colocalize with microtubules and are dependent on microtubules for their association with the anticlinal face in the indentation region 7 .…”

“…Transfacial microtubule bundles connect the indentation regions of pavement cells, which correspond to zones of predicted maximal tensile stresses 9,14 . This co-alignment of microtubules with mechanical stress patterns is dependent on the microtubule severing enzyme Katanin (KTN1) 14 , which is itself regulated by ROP6 15 .…”

Probing stress-regulated ordering of the plant cortical microtubule array via a computational approach

“…The observed anticlinal wall alignment of microtubules is strongly correlated with the magnitude and direction of tensile forces in the wall predicted by finite element (FE) modeling (8).…”

“…Tensile force patterns in cell wall are sensitive to the geometry of the cell or tissue organization (25, 36, 48, 49). Therefore, we tested if stress patterns obtained from the validated FE model of a polarized plant cell (25) could bias the cellular scale organization of the microtubule array.…”

“…Microtubules are highly dynamic polymers in the cell, with individual microtubules and the entire microtubule network turning over on the time scale of minutes (6)(7)(8). The underlying dynamic instability of microtubules mediates these unpredictable behaviors (6,7,9,10).…”