Data-Driven Modeling of Intracellular Auxin Fluxes Indicates a Dominant Role of the ER in Controlling Nuclear Auxin Uptake

• Published in: Cell reports (Cambridge) 2018-03, Vol.22 (11), p.3044-3057
• Main Authors: Middleton, Alistair M., Dal Bosco, Cristina, Chlap, Phillip, Bensch, Robert, Harz, Hartmann, Ren, Fugang, Bergmann, Stefan, Wend, Sabrina, Weber, Wilfried, Hayashi, Ken-ichiro, Zurbriggen, Matias D., Uhl, Rainer, Ronneberger, Olaf, Palme, Klaus, Fleck, Christian, Dovzhenko, Alexander
• Format: Article
• Language: English
• Subjects: auxin; auxin flux; auxin sensor; endoplasmic reticulum; Endoplasmic Reticulum - metabolism; fluorescent aux; Humans; Indoleacetic Acids - metabolism; mathematical modeling; microscopy; Nuclear Proteins - metabolism; nucleus; Plant Proteins - genetics; Plant Proteins - metabolism; protoplasts; Signal Transduction; single cells
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2018.02.074

In plants, the phytohormone auxin acts as a master regulator of developmental processes and environmental responses. The best characterized process in the auxin regulatory network occurs at the subcellular scale, wherein auxin mediates signal transduction into transcriptional programs by triggering the degradation of Aux/IAA transcriptional repressor proteins in the nucleus. However, whether and how auxin movement between the nucleus and the surrounding compartments is regulated remain elusive. Using a fluorescent auxin analog, we show that its diffusion into the nucleus is restricted. By combining mathematical modeling with time course assays on auxin-mediated nuclear signaling and quantitative phenotyping in single plant cell systems, we show that ER-to-nucleus auxin flux represents a major subcellular pathway to directly control nuclear auxin levels. Our findings propose that the homeostatically regulated auxin pool in the ER and ER-to-nucleus auxin fluxes underpin auxin-mediated downstream responses in plant cells. [Display omitted] •Auxin transport probe NBD-NAA does not enter the nucleus by simple diffusion•Modulation of auxin transport at the ER affects auxin-mediated responses•Model of nuclear auxin fluxes interconnects short- and long-term auxin responses•The ER is the main conduit for nuclear auxin uptake Middleton et al. study how the plant phytohormone auxin enters the nucleus by using quantitative phenotyping in single plant cell systems and bespoke mathematical models that relate controlled perturbations to experimentally measurable responses. Their findings show that auxin predominantly enters the nucleus via the endoplasmic reticulum.