A GhSnRK10–GhRopGEF5–GhROP10 signaling pathway regulates cotton fiber cell growth

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