A HAT7/ATHB13/brassinosteroid signaling module mediates growth of laticifer cells in Euphorbia lathyris.

Abstract

Laticifers, the coenocytic cells responsible for latex production, represent one of the most extreme examples of continuous and polarized growth in plants. Their unique architecture, extending over large distances, requires tight coordination between wall extensibility, cytoplasmic organization, and hormonal control. Here, we characterized the poor in latex 13 (pil13) mutant of Euphorbia lathyrism, which, similar to the previously described pil1 and pil6 mutants, is defective in laticifer expansion during post-embryonic phases of plant growth. Through comparative transcriptomic analyses of these 3 pil mutants, we identified a core set of 266 differentially expressed genes (DEGs) that define a transcriptomic signature associated with laticifers. We further identified a regulatory network linking 2 HD-Zip I transcription factors, HAT7 and ATHB13, with brassinosteroid (BR) signaling in the mediation of laticifer growth. This HAT7/ATHB13-BR module regulates the expression of laticifer DEGs involved in cell wall remodeling. Consequently, we found that laticifer cell walls are highly enriched in low-esterified homogalacturonan (HG) and branched rhamnogalacturonan-I (RG-I) pectins. Whole-mount immunolocalization revealed that laticifer cell walls exhibit a peculiar spatial segregation of pectic polysaccharides. These pectins follow a characteristic complementary, non-overlapping deposition pattern along the laticifer longitudinal axis, presumably conferring both elasticity and mechanical integrity. This modular pectin assembly appears compatible with the high flexibility and mechanical sinuosity required for growing laticifers through host tissues, while accommodating internal turgor pressure changes derived from latex accumulation. Our findings define the laticifer as a cellular model in which wall remodeling, cell growth, turgor pressure, and hormonal signaling are mechanistically coupled.