A GhSnRK10-GhRopGEF5-GhROP10 signaling pathway regulates cotton fiber cell growth.

Directional cell growth is central to cellular morphogenesis and is regulated by intra- and extracellular signaling pathways. Cotton fiber, the most important natural textile material, exemplifies a linear unidirectional cell growth that combines diffuse and polar growth patterns. However, the molecular mechanisms that govern polar growth of cotton fibers remain poorly understood. In this study, we identified a novel signaling pathway in which a guanine nucleotide exchange factor (GhRopGEF5) functions as a negative regulator of fiber polar growth. GhRopGEF5 is phosphorylated at threonine 398 by the SNF1-related protein kinase GhSnRK10, which in turn activates the fiber tip-localized GhROP10 to regulate reactive oxygen species and free Ca²⁺ levels for repressing polar growth of cotton fibers. Transcriptome analysis showed that GhRopGEF5 modulates microtubule- and cytoskeleton-related genes and affects hormone regulatory pathways, including auxin and ABA signaling, as well as small G-protein networks, ultimately regulating fiber elongation. Gene-edited transgenic cotton lines targeting GhRopGEF5 and its interaction partners, GhSnRK10 and GhROP10, consistently exhibited enhanced fiber length, revealing an evolutionarily adapted growth-restraining mechanism distinct from the typical Rho-of-plants (ROP)-mediated growth promotion in other tip-growing cells. This work reveals a GhRopGEF5-centered regulatory pathway that significantly affects the polar growth of cotton fibers, addressing a critical knowledge gap in the molecular mechanisms underlying this process. These findings provide valuable genetic resources for the development of superior cotton varieties with improved fiber quality.