A subset of group S1 bZIP transcription factors controls resource management during starvation and recovery in Arabidopsis

Theresa Wildenhain, Cezary Smaczniak, Alexander Marsell, Jan Draken, Daniel Maag, Philipp Kreisz, Markus Krischke, Martin J Müller, Kerstin Kaufmann, Christoph Weiste, Wolfgang Dröge-Laser
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Abstract

Plants exhibit considerable phenotypic plasticity, allowing them to adapt their metabolism to the fluctuating energy supply in a natural environment. Using dark-induced senescence (DIS) as an experimental system, a mutant study combining phenotypic, transcriptomic and chromatin immunoprecipitation sequencing (ChIP-seq) approaches identified distinct members of the Arabidopsis thaliana group S1 basic leucine zipper (bZIP) transcription factors that orchestrate the starvation response. Whereas excluding bZIP2, bZIP11 and bZIP44 to play a major role in DIS, bZIP1 and bZIP53 act partially redundantly to control a co-expression network governing amino acid catabolism and transport, gluconeogenesis and energy homeostasis. Moreover, bZIP1 and bZIP53 regulate genes involved in the asparagine–glutamine balance, two amino acids critical for carbon and nitrogen homeostasis. This transcriptional reprogramming in resource management is required for survival during starvation and regaining meristematic activity during the recovery from stress. Thus, our findings provide insights into the transcriptional control of plant resource and energy management during starvation. Overall, this work sheds light on the discrepancy between in vitro DNA binding and overexpression studies versus mutant analyses and in vivo DNA binding, providing a critical view on how to define specific transcription factor functions within large families.
S1组bZIP转录因子的一个子集控制着拟南芥在饥饿和恢复期间的资源管理
植物表现出相当大的表型可塑性,使它们能够适应自然环境中波动的能量供应。利用黑暗诱导衰老(DIS)作为实验系统,一项结合表型、转录组学和染色质免疫沉淀测序(ChIP-seq)方法的突变研究发现了拟南芥群S1碱性亮氨酸拉链(bZIP)转录因子的不同成员,这些转录因子协调饥饿反应。虽然bZIP2、bZIP11和bZIP44在DIS中不起主要作用,但bZIP1和bZIP53在控制氨基酸分解代谢和运输、糖异生和能量稳态的共表达网络中起部分冗余作用。此外,bZIP1和bZIP53调节与天冬酰胺-谷氨酰胺平衡有关的基因,这两种氨基酸对碳和氮的稳态至关重要。这种资源管理中的转录重编程是在饥饿期间生存和在应激恢复期间恢复分生组织活动所必需的。因此,我们的研究结果为饥饿期间植物资源和能量管理的转录控制提供了见解。总的来说,这项工作揭示了体外DNA结合和过表达研究与突变分析和体内DNA结合之间的差异,为如何在大家族中定义特定的转录因子功能提供了批判性的观点。
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