Weill Institute for Cell and Molecular Biology, Cornell University, Ithaca, NY, 14853, USA.
Section of Plant Biology, School of Integrative Plant Science, Cornell University, Ithaca, NY, 14853, USA.
Nat Commun. 2024 Jul 13;15(1):5911. doi: 10.1038/s41467-024-50172-9.
Robustness 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. An Arabidopsis flower robustly develops four sepals from four precisely positioned auxin maxima. The development related myb-like 1 (drmy1) mutant generates noise in auxin signaling that disrupts robustness in sepal initiation. Here, we find that increased expression of CUP-SHAPED COTYLEDON1 (CUC1), a boundary specification transcription factor, in drmy1 underlies this loss of robustness. CUC1 surrounds and amplifies stochastic auxin noise in drmy1 to form variably positioned auxin maxima and sepal primordia. Removing CUC1 from drmy1 provides time for noisy auxin signaling to resolve into four precisely positioned auxin maxima, restoring robust sepal initiation. However, removing CUC1 decreases the intensity of auxin maxima and slows down sepal initiation. Thus, CUC1 increases morphogenesis speed but impairs robustness against auxin noise. Further, using a computational model, we find that the observed phenotype can be explained by the effect of CUC1 in repolarizing PIN FORMED1 (PIN1), a polar auxin transporter. Lastly, our model predicts that reducing global growth rate improves developmental robustness, which we validate experimentally. Thus, our study illustrates a tradeoff between speed and robustness during development.
稳健性是指表型在随机噪声下可重复发育。它通常涉及与其他性能指标的权衡，但这些权衡的机制在很大程度上是未知的。拟南芥花从四个精确定位的生长素最大值中稳健地发育出四个萼片。与发育相关的 myb 样 1（drmy1）突变体在生长素信号中产生噪声，从而破坏了萼片起始的稳健性。在这里，我们发现 drmy1 中 CUP-SHAPED COTYLEDON1（CUC1）的表达增加，CUC1 是一个边界指定转录因子，是稳健性丧失的基础。CUC1 包围并放大了 drmy1 中的随机生长素噪声，形成了位置可变的生长素最大值和萼片原基。从 drmy1 中去除 CUC1 为嘈杂的生长素信号提供了时间，使其能够解析为四个精确定位的生长素最大值，从而恢复了稳健的萼片起始。然而，去除 CUC1 会降低生长素最大值的强度并减缓萼片起始。因此，CUC1 提高了形态发生速度，但损害了对生长素噪声的稳健性。此外，我们使用计算模型发现，CUC1 可以通过重新极化极性生长素转运蛋白 PIN FORMED1（PIN1）来解释观察到的表型。最后，我们的模型预测，降低全局生长速率可以改善发育稳健性，我们通过实验验证了这一点。因此，我们的研究说明了在发育过程中速度和稳健性之间的权衡。
