<p>Land plants have evolved strategies to survive water deficiency. Among these adaptations, the “drying without dying” strategy evolved in early land plants and is maintained in the desiccated seeds of angiosperms. This process is regulated by a family of ABA receptors known as the PYR/PYL/RCAR (PYL) family, which can bind to clade A protein phosphatases 2Cs (PP2Cs) and suppress their inhibition of water stress responses. ABA-independent PYLs first emerged in an aquatic algal lineage; however, their evolutionary origins and the mechanistic basis of ABA-independent PYL variants in land plants remain poorly characterized. Here, we characterize ABA-independent PYL-like proteins from bacteria, algae, and land plants that retain constitutive PP2C binding but lack ABA-enhanced inhibitory activity, supporting their putative bacterial origin via horizontal gene transfer. We identified a bacterial PYL homolog (PrPYL) in <i>Paraburkholderia rhynchosiae</i> with PP2C-binding ability, three PP2C-inhibiting PYL homologs in Zygnematales algae, and ABA-independent PYL-like proteins in seed plants (e.g., AtPYL13 and AtPYL13-like proteins). <i>AtPYL13</i>-like genes in dicots exhibited high expression during seed maturation and in desiccated seeds, suggesting a functional shift from canonical ABA receptors to ABA-independent PYL-like proteins following gene family expansion. Two invariant residues underlie ABA dependence in canonical PYL receptors. Transcription factor ABI3 mediates <i>AtPYL13</i> expression during the mature seed stage, thereby locally restricting constitutively activated stress signaling. Our findings indicate that ABA-independent <i>PYL</i>-like genes likely originated via horizontal transfer from bacteria and function in basal stress signaling in seed plants.</p>

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ABA-independent PP2C-binding in PYLs traces to bacterial origins and persists in land plants

  • Tianjiao Lu,
  • Qingzhong Li,
  • Tao Hu,
  • Wenqi Li,
  • Yafei Lu,
  • Huiling Huang,
  • Yang Zhao

摘要

Land plants have evolved strategies to survive water deficiency. Among these adaptations, the “drying without dying” strategy evolved in early land plants and is maintained in the desiccated seeds of angiosperms. This process is regulated by a family of ABA receptors known as the PYR/PYL/RCAR (PYL) family, which can bind to clade A protein phosphatases 2Cs (PP2Cs) and suppress their inhibition of water stress responses. ABA-independent PYLs first emerged in an aquatic algal lineage; however, their evolutionary origins and the mechanistic basis of ABA-independent PYL variants in land plants remain poorly characterized. Here, we characterize ABA-independent PYL-like proteins from bacteria, algae, and land plants that retain constitutive PP2C binding but lack ABA-enhanced inhibitory activity, supporting their putative bacterial origin via horizontal gene transfer. We identified a bacterial PYL homolog (PrPYL) in Paraburkholderia rhynchosiae with PP2C-binding ability, three PP2C-inhibiting PYL homologs in Zygnematales algae, and ABA-independent PYL-like proteins in seed plants (e.g., AtPYL13 and AtPYL13-like proteins). AtPYL13-like genes in dicots exhibited high expression during seed maturation and in desiccated seeds, suggesting a functional shift from canonical ABA receptors to ABA-independent PYL-like proteins following gene family expansion. Two invariant residues underlie ABA dependence in canonical PYL receptors. Transcription factor ABI3 mediates AtPYL13 expression during the mature seed stage, thereby locally restricting constitutively activated stress signaling. Our findings indicate that ABA-independent PYL-like genes likely originated via horizontal transfer from bacteria and function in basal stress signaling in seed plants.