In ancestors of modern-day streptophyte algae, cell division has undergone a switch from a cleavage-like mode to an inside-out mechanism, in which new cell walls are inserted at the cell center and expand centrifugally, eventually fusing with the maternal cell wall at a specific cortical region, termed cortical division zone (CDZ) 1-3. This switch in cell division involved the stepwise evolution of two novel cytoskeleton arrays, the phragmoplast and preprophase band (PPB). The PPB/phragmoplast system possibly provided basis for tunable cell division orientation, which enabled 3D development and morphological adaptations required for successful colonization of terrestrial habitats4. How the cytoskeleton acquired its novel functions, however, is still largely enigmatic. Our previous work identified IQ67-DOMAIN8 (IQD8) of Arabidopsis thaliana as an important determinant of PPB formation and division plane positioning5,6. IQD8 is an intrinsically disordered scaffold protein that interacts with core components of the CDZ7. Here, through phylogenetic and functional analyses, we show that IQDs emerged in the last common ancestor of Klebsormidiophyceae and Phragmoplastophyta algae. Gradual changes in motif composition and acquisition likely facilitated functional diversification of IQDs in terms of subcellular localization and protein-protein interactions. Cross-complementation studies in Arabidopsis mutants provide evidence for evolutionarily conserved functions of land-plant IQDs as key regulators of PPB formation and division plane control. In summary, our work establishes IQDs as plant-specific scaffold proteins, which likely played a role in rewiring and neofunctionalization of protein-protein interaction networks at distinct subcellular sites to facilitate evolutionary adaptations of the cell division apparatus and microtubule cytoskeleton in general.

In ancestors of modern-day streptophyte algae, cell division has undergone a switch from a cleavage-like mode to an inside-out mechanism, in which new cell walls are inserted at the cell center and expand centrifugally, eventually fusing with the maternal cell wall at a specific cortical region, termed cortical division zone (CDZ) 1-3. This switch in cell division involved the stepwise evolution of two novel cytoskeleton arrays, the phragmoplast and preprophase band (PPB). The PPB/phragmoplast system possibly provided basis for tunable cell division orientation, which enabled 3D development and morphological adaptations required for successful colonization of terrestrial habitats4. How the cytoskeleton acquired its novel functions, however, is still largely enigmatic. Our previous work identified IQ67-DOMAIN8 (IQD8) of Arabidopsis thaliana as an important determinant of PPB formation and division plane positioning5,6. IQD8 is an intrinsically disordered scaffold protein that interacts with core components of the CDZ7. Here, through phylogenetic and functional analyses, we show that IQDs emerged in the last common ancestor of Klebsormidiophyceae and Phragmoplastophyta algae. Gradual changes in motif composition and acquisition likely facilitated functional diversification of IQDs in terms of subcellular localization and protein-protein interactions. Cross-complementation studies in Arabidopsis mutants provide evidence for evolutionarily conserved functions of land-plant IQDs as key regulators of PPB formation and division plane control. In summary, our work establishes IQDs as plant-specific scaffold proteins, which likely played a role in rewiring and neofunctionalization of protein-protein interaction networks at distinct subcellular sites to facilitate evolutionary adaptations of the cell division apparatus and microtubule cytoskeleton in general.

The preprophase band (PPB) is a transient cytokinetic structure that marks the future division plane at the onset of mitosis. The PPB forms a dense cortical ring of mainly microtubules, actin filaments, endoplasmic reticulum, and associated proteins that encircles the nucleus of mitotic cells. After PPB disassembly, the positional information is preserved by the cortical division zone (CDZ). The formation of the PPB and its contribution to timely CDZ set-up involves activities of functionally distinct microtubule-associated proteins (MAPs) that interact physically and genetically to support robust division plane orientation in plants. Recent studies identified two types of plant-specific MAPs as key regulators of PPB formation, the TON1 RECRUITMENT MOTIF (TRM) and IQ67 DOMAIN (IQD) families. Both families share hallmarks of disordered scaffold proteins. Interactions of IQDs and TRMs with multiple binding partners, including the microtubule severing KATANIN1, may provide a molecular framework to coordinate PPB formation, maturation, and disassembly.

In ancestors of modern-day streptophyte algae, cell division has undergone a switch from a cleavage-like mode to an inside-out mechanism, in which new cell walls are inserted at the cell center and expand centrifugally, eventually fusing with the maternal cell wall at a specific cortical region, termed cortical division zone (CDZ) 1-3. This switch in cell division involved the stepwise evolution of two novel cytoskeleton arrays, the phragmoplast and preprophase band (PPB). The PPB/phragmoplast system possibly provided basis for tunable cell division orientation, which enabled 3D development and morphological adaptations required for successful colonization of terrestrial habitats4. How the cytoskeleton acquired its novel functions, however, is still largely enigmatic. Our previous work identified IQ67-DOMAIN8 (IQD8) of Arabidopsis thaliana as an important determinant of PPB formation and division plane positioning5,6. IQD8 is an intrinsically disordered scaffold protein that interacts with core components of the CDZ7. Here, through phylogenetic and functional analyses, we show that IQDs emerged in the last common ancestor of Klebsormidiophyceae and Phragmoplastophyta algae. Gradual changes in motif composition and acquisition likely facilitated functional diversification of IQDs in terms of subcellular localization and protein-protein interactions. Cross-complementation studies in Arabidopsis mutants provide evidence for evolutionarily conserved functions of land-plant IQDs as key regulators of PPB formation and division plane control. In summary, our work establishes IQDs as plant-specific scaffold proteins, which likely played a role in rewiring and neofunctionalization of protein-protein interaction networks at distinct subcellular sites to facilitate evolutionary adaptations of the cell division apparatus and microtubule cytoskeleton in general.