Cross-talk between plasma membrane (PM) and subcellular organelles is essential for cellular Ca²⁺ homeostasis. Emptying the endoplasmic reticulum (ER) calcium stores increases Ca²⁺ entry though PM (store operated Ca²⁺ entry, SOCE). STIM1 and Orai1 are the principal players in SOCE. STIM senses the Ca²⁺ content inside ER, and, when it decreases, activates Orai1, a PM store-operated calcium channel (SOC) that promotes Ca²⁺ entry and increases cytosolic Ca²⁺. We have studied here the role of cytoplasmic organelles. We monitored the fate of Ca²⁺ entering through SOC and its redistribution among different organelles (ER, mitochondria, nucleus, cytosol) using selectively targeted Ca²⁺ probes. On depletion of the ER Ca²⁺ stores SERCA colocalizes with STIM1 and Orai1 at puncta. ER Ca²⁺ refilling is tightly coupled to SOCE when the proportions of STIM1, Orai1 and SERCA are adequate, and little Ca²⁺ reaches the cell core under these conditions. The tightness of this calcium entry-calcium refilling (CECR) coupling, as measured by the slope of the stimulus-signal strength function, was comparable to classic excitation-response coupling mechanisms. Mitochondrial Ca²⁺ uptake was very minor. SERCA is the third element of SOCE. It colocalizes with STIM1 and Orai1 at puncta, where it is tightly coupled to plasma membrane SOC. This allows extremely efficient refilling of the ER stores. Whereas ER takes up most of the SOCE calcium load, mitochondria take very little. These differences in behaviour depend on: i) spatial positioning with regard to SOC, ii) amplitude of the high Ca²⁺ microdomains, and iii) differences in the Ca²⁺ affinity of the uptake mechanisms present in both organelles.