An RNA helicase coordinates with iron signal regulators to alleviate chilling stress in Arabidopsis

Chilling stress is one of the major environmental stresses that restrains plant development and growth. Our previous study showed that a potential iron sensor BTS (BRUTUS) was involved in temperature response in Arabidopsis plants. However, whether plant iron homeostasis is involved in plant response to temperature fluctuation is not known. In this study, we discover that BTS mutant bts-2 is sensitive to chilling stress, and the sensitivity is attributed to the accumulation of iron. The suppressor screening of bts-2 led to the discovery of RH24, a DEAD-box RNA helicase, that fully suppresses bts-2 sensitivity to low temperatures. RH24 is accumulated under low temperatures, where it unwinds the key transcription factor ILR3 (IAA-leucine resistant 3) mRNA and increases the ILR3 protein levels. ILR3 acts downstream of BTS to activate iron uptake. Intriguingly, RH24 sequesters ILR3 in phase-separated condensates to reduce ILR3-mediated iron overload, and BTS or cold treatments further facilitated the condensate formation. Therefore, RH24 and BTS coordinately control ILR3 to reduce iron uptake under chilling stress. Our findings reveal that the RNA helicase RH24 and BTS finetunes ILR3 to maintain plant iron homeostasis in response to temperature fluctuations.

低温胁迫是限制植物生长发育的主要环境胁迫之一。本团队前期研究发现，潜在铁感受器（iron sensor）BTS（BRUTUS）参与拟南芥的温度响应过程，但植物铁稳态是否参与植物对温度波动的应答尚不清楚。本研究发现，BTS突变体bts-2对低温胁迫敏感，且该敏感表型由铁积累所介导。通过对bts-2进行抑制子筛选，我们鉴定到DEAD盒RNA解旋酶（DEAD-box RNA helicase）RH24，其可完全恢复bts-2的低温敏感表型。RH24在低温条件下积累，通过解旋关键转录因子ILR3（IAA-亮氨酸抗性3）的信使RNA（mRNA）提升ILR3的蛋白水平。ILR3位于BTS的下游，可激活铁吸收过程。有趣的是，RH24会将ILR3隔离在相分离凝聚体中，以削弱ILR3介导的铁过载，而BTS处理或低温处理可进一步促进该凝聚体的形成。因此，RH24与BTS协同调控ILR3，以在低温胁迫下减少铁吸收。本研究揭示，RNA解旋酶RH24与BTS通过精细调控ILR3，维持植物在温度波动下的铁稳态。