Ca(2+)-dependent phosphorylation of NRAMP1 by CPK21 and CPK23 facilitates manganese uptake and homeostasis in Arabidopsis.

Ca(2+)-dependent phosphorylation of NRAMP1 by CPK21 and CPK23 facilitates manganese uptake and homeostasis in Arabidopsis.
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CPK21 和 CPK23 对 NRAMP1 的 Ca2 依赖性磷酸化促进拟南芥中的锰吸收和稳态

DOI:
10.1073/pnas.2204574119
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发表时间:
2022-10-04
影响因子:
11.1
通讯作者:
Wang, Cun
Wang, Cun
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Fu, Dali;Zhang, Zhenqian;Wallrad, Lukas;Wang, Zhangqing;Hoeller, Stefanie;Ju, ChuanFeng;Schmitz-Thom, Ina;Huang, Panpan;Wang, Lei;Peiter, Edgar;Kudla, Joerg;Wang, Cun

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锰(Mn)缺乏是碱性和石灰性土壤中作物营养的一种严重且普遍的紊乱情况。然而,人们很大程度上仍不清楚锰供应的波动是如何被感知和传递信号的,以及锰转运蛋白的活性是如何被调控的。在此我们发现,锰缺乏会在拟南芥根部一个特定的“低锰感知微环境”中引发时空限定的多细胞Ca2+振荡。我们确定Ca2+信号解码激酶CPK21和CPK23可调控锰吸收转运蛋白NRAMP1。我们将NRAMP1中的苏氨酸498定义为这两种激酶的靶点,以及从机制上决定NRAMP1活性的关键。这些发现描绘出一个Ca2+-CPK21/23 - NRAMP1轴,它是植物建立对有限锰供应耐受性的关键机制。 必需微量营养素锰(Mn)的体内平衡在所有生物体中关键取决于其可利用性和吸收效率。植物的锰缺乏尤其发生在碱性和石灰性土壤中,严重限制了作物产量。然而,锰可利用性的感知和信号传递以及锰吸收调控的潜在机制仍有待阐明。在此,我们揭示锰缺乏会在拟南芥根部引发时空限定的持久Ca2+振荡。这些Ca2+信号从单个细胞产生,在细胞间扩展和增强,转变为更高层次的多细胞振荡。此外,通过相互作用筛选,我们确定Ca2+依赖的蛋白激酶CPK21和CPK23为Ca2+信号解码成分,它们将这些信号转化为对高亲和力锰转运蛋白天然抗性相关巨噬细胞蛋白1(NRAMP1)吸收活性的调控。相应地,cpk21/23双突变体在锰限制条件下表现出生长和根系发育受损,而激酶过表达使植物对低锰供应的耐受性增强。此外,我们通过生化分析以及酵母锰吸收和拟南芥nramp1突变体的互补实验表明,将NRAMP1内的苏氨酸498磷酸化定义为从机制上决定NRAMP1活性的关键。总之,这些发现描绘出Ca2+-CPK21/23 - NRAMP1轴是维持植物锰体内平衡的关键。
Manganese (Mn) deficiency represents a serious and widespread disturbance of crop nutrition in alkaline and calcareous soils. However, it has remained largely unknown how fluctuations in Mn supply are sensed and signaled and how the activity of Mn transporters is regulated. Here we discovered that Mn depletion triggers spatiotemporally defined multicellular Ca2+ oscillations in a specific “low Mn-sensing niche” in Arabidopsis roots. We identified the Ca2+ signal-decoding kinases CPK21 and CPK23 as regulating the Mn uptake transporter NRAMP1. We defined Thr498 in NRAMP1 as a target of both kinases and as a pivot mechanistically determining NRAMP1 activity. These findings delineate a Ca2+-CPK21/23-NRAMP1 axis as key mechanism for establishing plant resilience to limited Mn supply. Homeostasis of the essential micronutrient manganese (Mn) is crucially determined through availability and uptake efficiency in all organisms. Mn deficiency of plants especially occurs in alkaline and calcareous soils, seriously restricting crop yield. However, the mechanisms underlying the sensing and signaling of Mn availability and conferring regulation of Mn uptake await elucidation. Here, we uncover that Mn depletion triggers spatiotemporally defined long-lasting Ca2+ oscillations in Arabidopsis roots. These Ca2+ signals initiate in individual cells, expand, and intensify intercellularly to transform into higher-order multicellular oscillations. Furthermore, through an interaction screen we identified the Ca2+-dependent protein kinases CPK21 and CPK23 as Ca2+ signal-decoding components that bring about translation of these signals into regulation of uptake activity of the high-affinity Mn transporter natural resistance associated macrophage proteins 1 (NRAMP1). Accordingly, a cpk21/23 double mutant displays impaired growth and root development under Mn-limiting conditions, while kinase overexpression confers enhanced tolerance to low Mn supply to plants. In addition, we define Thr498 phosphorylation within NRAMP1 as a pivot mechanistically determining NRAMP1 activity, as revealed by biochemical assays and complementation of yeast Mn uptake and Arabidopsis nramp1 mutants. Collectively, these findings delineate the Ca2+-CPK21/23-NRAMP1 axis as key for mounting plant Mn homeostasis.
DOI: 10.1104/pp.15.01194
发表时间: 2016-02-01
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影响因子: 7.4
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