Phytochrome-Interacting Factors Regulate Katanin-Mediated Microtubule Severing to Control Hypocotyl/Mesocotyl Elongation During Skotomorphogenesis

Abstract The ability of plant seeds to emerge from the soil is achieved either by mesocotyl elongation in monocots or by hypocotyl elongation in dicots. Phytochrome-interacting factors (PIFs) are required for skotomorphogenesis, and microtubule remodeling plays a key driving role in cell elongation. However, the underlying cellular mechanisms in which PIFs act in concert with microtubule remodeling to control cell elongation during skotomorphogenesis remain unknown. Here, we demonstrate that in S. italica, the microtubule-severing defective mutant Siktn1 exhibits shortened mesocotyls and disorganized microtubule arrays. Similarly, in Arabidopsis, the microtubule-severing defective mutants lue1 and ktn80.1234 show shortened hypocotyls and abnormal microtubule arrays, which are caused by impaired microtubule severing. Intriguingly, pifq mutants exhibit shortened hypocotyls with reduced KTN1 and KTN80 expression, prompting us to investigate the relationship between PIFs and microtubule severing. Importantly, we found that PIFs transcriptionally activate KTN1 expression either in Arabidopsis or in S. italica. Further live-cell imaging confirmed that pifq mutants show reduced severing frequency and dwell time of the katanin complex. Taken together, these findings uncover a mechanism that PIFs orchestrate microtubule dynamics by regulating katanin activity, thereby fine-tuning cell elongation of hypocotyls/mesocotyls during skotomorphogenesis.