Reprogramming of Stem Cell Activity to Convert Thorns into Branches

Thorns arise from axillary shoot apical meristems that proliferate for a time and then terminally differentiate into a sharp tip. Like other meristems, thorn meristems contain stem cells but, in the case of thorns, these stem cells undergo a programmed cessation of proliferative activity. Using Citrus, we characterize a gene network necessary for thorn development. We identify two Citrus genes, THORN IDENTITY1 (TI1) and THORN IDENTITY2 (TI2), encoding TCP transcription factors, as necessary for stem cell quiescence and thorn identity. Disruption of TI1 and TI2 function results in reactivation of stem cells and concomitant conversion of thorns to branches. Expression of WUSCHEL (WUS) defines the shoot stem cell niche in the apical meristems of many angiosperm species; we show that TI1 binds to the Citrus WUS promoter and negatively regulates its expression to terminate stem cell proliferation. We propose that shifts in the timing and function of components of this gene network can account for the evolution of Citrus thorn identity. Modulating this pathway can significantly alter plant architecture and could be leveraged to improve crop yields. [Display omitted] •Citrus thorn primordia express meristematic markers but then terminally differentiate•TI1 and TI2 encode TCP transcription factors and are required for thorn identity•TI1 and TI2 negatively regulate CsWUS expression and TI1 binds to the CsWUS promoter•Mutations of TI1, TI2, or the CsWUS promoter result in increased branching Zhang et al. identify THORN IDENTITY1 (TI1) and TI2 as necessary for specifying thorn identity in Citrus. Mutation of TI1 and TI2 releases repression of the stem cell regulator WUSCHEL in thorn meristems, resulting in continued cell proliferation and concomitant conversion of thorns into branches.