Tradeoff Between Speed and Robustness in Primordium Initiation Mediated by Auxin-CUC1 Interaction

Abstract

ABSTRACTRobustness is the reproducible development of a phenotype despite stochastic noise. It often involves tradeoffs with other performance metrics, but the mechanisms underlying such tradeoffs were largely unknown. AnArabidopsisflower robustly develops four sepals from four precisely positioned auxin maxima. Thedevelopment related myb-like 1(drmy1)mutant generates stochastic noise in auxin signaling that disrupts both the robust position and number of sepal primordia. Here, we found that increased expression ofCUP-SHAPED COTYLEDON1(CUC1), a boundary specification transcription factor, in thedrmy1mutant underlies this loss of robustness. CUC1 surrounds and amplifies stochastic auxin patches indrmy1to form variably positioned auxin maxima and sepal primordia. RemovingCUC1fromdrmy1provides time for the noise in auxin signaling to resolve into four precisely positioned auxin maxima, restoring robust sepal initiation. However, removing CUC1 decreases auxin maxima intensity and slows down sepal initiation. Thus, CUC1 increases morphogenesis speed but impairs robustness against auxin noise. Further, using a computational model, we found that the observed phenotype can be explained by the effect of CUC1 in repolarizing PIN FORMED1 (PIN1), a polar auxin transporter. Thus, our study illustrates a tradeoff between speed and robustness during development.