<p>Phosphorus (P) is an essential macronutrient for plant growth and development, yet its limited availability in soil severely constrains crop productivity.&#xa0;To cope with phosphate (Pi) deficiency, plants have evolved a sophisticated signaling network centered on SPX domain proteins, which serve as central regulators of Pi homeostasis. Recent breakthrough structural studies have revolutionized our understanding of these proteins, revealing their function as cellular Pi sensors through binding of the inositol pyrophosphate InsP<sub>8</sub>.&#xa0;This review synthesizes current knowledge of SPX protein molecular structures, evolution, and functions within the Pi signaling network. We detail their sensing mechanism, focusing on inositol pyrophosphate binding and the subsequent control of PHR activity and phosphate starvation response (PSR) gene expression. Recent cryo-electron microscopy structures of rice SPX1-PHR2, <i>Arabidopsis</i> PHO1;H1, and human XPR1 have provided unprecedented insights into phosphate transport mechanisms and SPX domain regulation. We also discuss emerging functions of SPX proteins in coordinating arbuscular mycorrhizal symbiosis, plant immunity, nitrogen-phosphorus balance, and cold stress responses, highlighting their broad significance in plant biology. Finally, we discuss key challenges and future research directions crucial for translating these mechanistic insights into innovative strategies to enhance phosphorus use efficiency (PUE) in crops, including structure-guided protein engineering approaches.</p>

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The SPX protein family in plants: from phosphate sensors to multifunctional signaling hubs

  • Shenghong Ge,
  • Kai Yuan,
  • Mingguang Lei

摘要

Phosphorus (P) is an essential macronutrient for plant growth and development, yet its limited availability in soil severely constrains crop productivity. To cope with phosphate (Pi) deficiency, plants have evolved a sophisticated signaling network centered on SPX domain proteins, which serve as central regulators of Pi homeostasis. Recent breakthrough structural studies have revolutionized our understanding of these proteins, revealing their function as cellular Pi sensors through binding of the inositol pyrophosphate InsP8. This review synthesizes current knowledge of SPX protein molecular structures, evolution, and functions within the Pi signaling network. We detail their sensing mechanism, focusing on inositol pyrophosphate binding and the subsequent control of PHR activity and phosphate starvation response (PSR) gene expression. Recent cryo-electron microscopy structures of rice SPX1-PHR2, Arabidopsis PHO1;H1, and human XPR1 have provided unprecedented insights into phosphate transport mechanisms and SPX domain regulation. We also discuss emerging functions of SPX proteins in coordinating arbuscular mycorrhizal symbiosis, plant immunity, nitrogen-phosphorus balance, and cold stress responses, highlighting their broad significance in plant biology. Finally, we discuss key challenges and future research directions crucial for translating these mechanistic insights into innovative strategies to enhance phosphorus use efficiency (PUE) in crops, including structure-guided protein engineering approaches.