Root gravitropism is regulated by a transient lateral auxin gradient controlled by a tipping-point mechanism

Leah R. Band*, Darren M. Wells*, Antoine Larrieu*, Jianyong Sun*, Alistair M. Middleton*, Andrew P. French, Géraldine Brunoud, Ethel Mendocilla Sato, Michael H. Wilson, Benjamin Péret, Marina Oliva, Ranjan Swarup, Ilkka Sairanen, Geraint Parry, Karin Ljung, Tom Beeckman, Jonathan M. Garibaldi, Mark Estelle#, Markus R. Owen, Kris Vissenberg, T. Charlie Hodgman, Tony P. Pridmore, John R. King, Teva Vernoux# & Malcolm J. Bennett#

Gravity profoundly influences plant growth and development. Plants respond to changes in orientation by using gravitropic responses to modify their growth. Cholodny and Went hypothesized over 80 years ago that plants bend in response to a gravity stimulus by generating a lateral gradient of a growth regulator at an organ’s apex, later found to be auxin. Auxin regulates root growth by targeting Aux/IAA repressor proteins for degradation. We used an Aux/IAA-based reporter, domain II (DII)-VENUS, in conjunction with a mathematical model to quantify auxin redistribution following a gravity stimulus. Our multidisciplinary approach revealed that auxin is rapidly redistributed to the lower side of the root within minutes of a 90° gravity stimulus. Unexpectedly, auxin asymmetry was rapidly lost as bending root tips reached an angle of 40° to the horizontal. We hypothesize roots use a “tipping point” mechanism that operates to reverse the asymmetric auxin flow at the midpoint of root bending. These mechanistic insights illustrate the scientific value of developing quantitative reporters such as DII-VENUS in conjunction with parameterized mathematical models to provide high-resolution kinetics of hormone redistribution.

Proceedings of the National Academy of Sciences 109 (12), 4668-4673