ARF10, ARF16, and ARF17 are involved in cytokinesis during pollen development in Arabidopsis

Pollen formation involves several cell divisions: meiosis I/II and pollen mitosis I/II. Auxin response factors (ARFs) are essential transcription factors in the auxin signaling pathway. While ARFs have been implicated in pollen wall patterning and pollen maturation, their roles in cell division during pollen formation remain unclear. Here, we characterize the essential roles of ARF10, ARF16, and ARF17 in the cytokinesis processes of meiosis and PMI. In the arf10arf16arf17^+/- mutant, the cell plate is abnormally deposited during PMI cytokinesis, resulting in irregular cell identity and pollen degeneration. These phenotypes are consistent with ARF10 and ARF16 being expressed primarily in the vegetative cell of bicellular pollen. The phenotypes of the arf10arf16arf17^+/- mutant are similar to those of glucan synthase-like 10 (gsl10), a loss-of-function mutant of a member of the callose synthesis family. GSL10 is expressed in the vegetative cell of bicellular pollen, and its transcript is reduced in the arf10arf16arf17^+/- mutant. We confirmed that these three ARFs can directly bind to the GSL10 promoter. Thus, we reveal an ARF10, ARF16, and ARF17-GSL10 pathway that is specifically activated in the vegetative cell for pollen development. Moreover, we discovered that in the arf17 single mutant, the cell plate was abnormally formed after meiosis I, resulting in cytokinesis defects in the tetrads. Collectively, our results indicate that ARF17 alone is involved in meiotic cytokinesis and that ARF10, ARF16, and ARF17 are redundantly required for PMI cytokinesis. Our research thus provides insights into the key auxin signaling pathways involved in cell division during pollen development.