Microtubule (MT)-dependent MT nucleation by γ-tubulin is required for interphase plant cells to establish a highly dynamic cortical MT network underneath the plasma membrane, which influences the deposition of cell wall materials and consequently governs patterns of directional cell expansion. Newly formed MTs either assume 40° angles or are parallel to the extant ones. To date, it has been enigmatic how the γ-tubulin complex is recruited to the sidewall of cortical MTs and initiates MT nucleation. Here, we discovered that the augmin complex was recruited to cortical MTs and initiated MT nucleation in both branching and parallel forms. The augmin complex overwhelmingly colocalized with the γ-tubulin complex. When the function of the augmin complex was compromised, MT nucleation frequency was drastically reduced, most obviously for the branching nucleation. Consequently, the augmin knockdown cells displayed highly parallel and bundled MTs, replacing the fine and mesh-like MT network in the wild-type cells. Our findings uncovered a mechanism by which the augmin complex functions in recruiting the γ-tubulin complex to cortical MTs and initiating MT nucleation, and they shifted the paradigm of the commonly perceived mitotic-specific function of augmin and established its crucial function in MT-dependent MT nucleation in interphase plant cells.

Microtubules (MTs) and actin filaments (F-actin) function cooperatively to regulate plant cell morphogenesis. However, the mechanisms underlying the crosstalk between these two cytoskeletal systems, particularly in cell shape control, remain largely unknown. In this study, we show that introduction of the MyTH4-FERM tandem into KCBP (kinesin-like calmodulin-binding protein) during evolution conferred novel functions. The MyTH4 domain and the FERM domain in the N-terminal tail of KCBP physically bind to MTs and F-actin, respectively. During trichome morphogenesis, KCBP distributes in a specific cortical gradient and concentrates at the branching sites and the apexes of elongating branches, which lack MTs but have cortical F-actin. Further, live-cell imaging and genetic analyses revealed that KCBP acts as a hub integrating MTs and actin filaments to assemble the required cytoskeletal configuration for the unique, polarized diffuse growth pattern during trichome cell morphogenesis. Our findings provide significant insights into the mechanisms underlying cytoskeletal regulation of cell shape determination.DOI: http://dx.doi.org/10.7554/eLife.09351.001