A Review of Nuclear-Organellar Communication in Response to Heat Stress

Plants coordinate their growth and developmental programs through dynamic communication in the core of the nucleus, enabling them to adapt to persistently high-temperature environments. Upon heat stress, plants primarily perceive and transduce thermal signals between the nucleus and other organelles, a process defined as nuclear-organellar communication. The published research on plants in response to heat environments mainly focuses on sensing heat physical signals from the plasma membrane (PM)/cytosol to the nucleus, eliciting nuclear transcriptional reprogramming and decoding organelle-derived retrograde signals to the nucleus. Consequently, plants have evolved sophisticated systems to decode adverse temperature signals relying on efficient nuclear-organellar coordination. This review summarizes how plants maintain cellular homeostasis via nuclear crosstalk. Heat signals are initially perceived, which triggers the production of secondary messengers including phosphatidic acid (PA), calcium ions (Ca²⁺) and reactive oxygen species (ROS). In addition, proteins also deliver thermal signals to the nucleus. As the central signaling hub, the nucleus orchestrates global transcriptional reprogramming predominantly through the Heat Shock Transcriptional Factors (HSFs)-heat shock proteins (HSPs) regulatory module, and sends instructions to the endoplasmic reticulum (ER), chloroplasts and mitochondria. Conversely, organelle-derived retrograde signals coordinate stress adaptation: the unfolded protein response relieves ER stress, and heat stress activates ROS-mediated chloroplast-to-nucleus and mitochondria-to-nucleus feedback pathways. We further outline candidate thermosensing proteins residing in different organelles, and highlight major unsolved issues. Critical knowledge gaps include the intrinsic thermosensing capacity of chloroplasts and mitochondria, inter-organellar coordination of second-messenger dynamics, specific organelle functions, and the biological roles of membrane contact sites. Further mechanistic insights will facilitate the application of genome editing, synthetic biology and artificial-intelligence-aided design to breed heat-tolerant crops without yield penalties.