April 8, 2024 | Jiaqi Xiao, Yijie Zhou, Yunyun Xie, Taotao Li, Xingguo Su, Junxian He, Yueming Jiang, Hong Zhu, Hongxia Qu
ATP is the primary energy source for plants, and a shortage of ATP can threaten plant growth, stress resistance, and crop quality. The processes that contribute to the ATP pool, including production, dissipation, transport, and elimination, have been extensively studied. ATP not only provides energy but also acts as a signaling molecule to regulate global metabolic responses. The identification of the eATP receptor DORN1 has improved understanding of how plants cope with ATP homeostasis disruption and the key points where ATP signaling pathways intersect. SnRK1α, the master regulator of the energy management network, has been shown to restore ATP pool balance and mediate a complex metabolic network to adapt to fluctuating environments. This review summarizes recent advances in understanding the regulatory control of the cellular ATP pool and discusses possible interactions among key regulators of ATP-pool homeostasis and crosstalk between iATP/eATP signaling pathways. The physiological and molecular levels of ATP deficit perception and SnRK1α-mediated cellular ATP homeostasis modulation are discussed. Future research directions for modulating plant cellular ATP homeostasis are suggested.
Key words: ATP, DORN1, SnRK1α, ATP homeostasis and signaling
ATP homeostasis and signaling in plants are crucial for plant life, as energy supply limitations rapidly block growth and initiate senescence and death. While the roles of iATP and eATP in the cellular metabolic network have been well studied at both physiological and molecular levels, the points of intersection among ATP signaling pathways and the interactions between SnRK1α and key regulators of ATP homeostasis remain largely uncharacterized. The role of iATP/eATP homeostasis in plant survival and the function of SnRK1α in redistributing cellular carbohydrate resources in response to starvation have been recognized. However, a comprehensive understanding of how plants cope with energy deficits and respond to changing environments through global and complex manipulation of ATP pool homeostasis at the whole-cell level is still lacking. Additionally, how SnRK1α, the central energy sensor, mediates cellular metabolic reprogramming in response to fluctuations in the ATP pool and possible links between SnRK1α activation and eATP signals remain to be clarified.
This review provides a comprehensive summary of the metabolic processes that contribute to the ATP pool, including production, dissipation, transport, and elimination of iATP/eATP, and illustrates the proposed regulatory system of ATP homeostasis in Figure 1. Recent advances in the understanding of components that regulate ATP signal transduction and homeostasis of the ATP pool are discussed. In addition, we focus on regulatory circuits around the master energy regulator SnRK1α, covering not only the perception of energy-deficit signals but also ATP signaling cascades. We summarize the current understanding of the diverse functions of SnRK1α, including its extensive regulatory effects on growth and development, stress resistance, and crop quality (Figure 2;ATP is the primary energy source for plants, and a shortage of ATP can threaten plant growth, stress resistance, and crop quality. The processes that contribute to the ATP pool, including production, dissipation, transport, and elimination, have been extensively studied. ATP not only provides energy but also acts as a signaling molecule to regulate global metabolic responses. The identification of the eATP receptor DORN1 has improved understanding of how plants cope with ATP homeostasis disruption and the key points where ATP signaling pathways intersect. SnRK1α, the master regulator of the energy management network, has been shown to restore ATP pool balance and mediate a complex metabolic network to adapt to fluctuating environments. This review summarizes recent advances in understanding the regulatory control of the cellular ATP pool and discusses possible interactions among key regulators of ATP-pool homeostasis and crosstalk between iATP/eATP signaling pathways. The physiological and molecular levels of ATP deficit perception and SnRK1α-mediated cellular ATP homeostasis modulation are discussed. Future research directions for modulating plant cellular ATP homeostasis are suggested.
Key words: ATP, DORN1, SnRK1α, ATP homeostasis and signaling
ATP homeostasis and signaling in plants are crucial for plant life, as energy supply limitations rapidly block growth and initiate senescence and death. While the roles of iATP and eATP in the cellular metabolic network have been well studied at both physiological and molecular levels, the points of intersection among ATP signaling pathways and the interactions between SnRK1α and key regulators of ATP homeostasis remain largely uncharacterized. The role of iATP/eATP homeostasis in plant survival and the function of SnRK1α in redistributing cellular carbohydrate resources in response to starvation have been recognized. However, a comprehensive understanding of how plants cope with energy deficits and respond to changing environments through global and complex manipulation of ATP pool homeostasis at the whole-cell level is still lacking. Additionally, how SnRK1α, the central energy sensor, mediates cellular metabolic reprogramming in response to fluctuations in the ATP pool and possible links between SnRK1α activation and eATP signals remain to be clarified.
This review provides a comprehensive summary of the metabolic processes that contribute to the ATP pool, including production, dissipation, transport, and elimination of iATP/eATP, and illustrates the proposed regulatory system of ATP homeostasis in Figure 1. Recent advances in the understanding of components that regulate ATP signal transduction and homeostasis of the ATP pool are discussed. In addition, we focus on regulatory circuits around the master energy regulator SnRK1α, covering not only the perception of energy-deficit signals but also ATP signaling cascades. We summarize the current understanding of the diverse functions of SnRK1α, including its extensive regulatory effects on growth and development, stress resistance, and crop quality (Figure 2;