Emerging roles of the CBL-CIPK calcium signaling network as key regulatory hub in plant nutrition

Plant physiology and development essentially depend on sufficient uptake of various essential nutritive ions via their roots and their appropriate transport and distribution within the organism. Many of these essential nutrients are heterogeneously distributed in the soil or are available in fluctuating concentrations. This natural situation requires constant regulatory adjustment and balancing of nutrient uptake and homeostasis. Here, we review recent findings on the role of Ca2+ signals and Ca2+-dependent regulation via the CBL-CIPK Ca2+ sensor-protein kinase network in these processes. We put special emphasis on Ca2+ controlled processes that contribute to establishing the homeostasis of macro-nutrients like potassium (K+), nitrogen (N), and magnesium (Mg2+) and on the micro-nutrient iron (Fe). Increasing experimental evidence indicates the occurrence of nutrient-specific, spatially and temporally defined cytoplasmic Ca2+ elevations as early responses to nutrient fluctuations. Specific CBL-CIPK complexes translate these signals into phosphorylation regulation of important channels and transporters like AKT1, NPF6.3/NRT1.1, AMT1, SLAC1, TPK1 and IRT1. We discuss a crucial and coordinating role for these Ca2+ signaling mechanisms in regulating the sensing, uptake, distribution and storage of various ions. Finally, we reflect on the emerging multifaceted and potentially integrating role of the nutrient kinase CIPK23 in regulating multiple nutrient responses. From this inventory, we finally deduce potential mechanisms that can convey the coordinated regulation of distinct steps in the transport of one individual ion and mechanisms that can bring about the integration of adaptive responses to fluctuations of different ions to establish a faithfully balanced plant nutrient homeostasis.

Automated summary

Plant physiology and development rely on the uptake and distribution of essential nutritive ions via roots, with recent findings highlighting the importance of Ca2+ signals and the CBL-CIPK Ca2+ sensor-protein kinase network in regulating nutrient uptake and homeostasis. Nutrient-specific cytoplasmic Ca2+ elevations are observed as early responses to fluctuations, with CBL-CIPK complexes translating these signals into phosphorylation regulation of key channels and transporters. These Ca2+ signaling mechanisms play a coordinating role in regulating the sensing, uptake, distribution, and storage of ions, with potential implications for establishing plant nutrient homeostasis.