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.

Treatment of potato plants with the pathogen-associated molecular pattern Pep-13 leads to the activation of more than 1200 genes. One of these, StPIP1_1, encodes a protein of 76 amino acids with sequence homology to PAMP-induced secreted peptides (PIPs) from Arabidopsis thaliana. Expression of StPIP1_1 is also induced in response to infection with Phytophthora infestans, the causal agent of late blight disease. Apoplastic localization of StPIP1_1-mCherry fusion proteins is dependent on the presence of the predicted signal peptide. A synthetic peptide corresponding to the last 13 amino acids of StPIP1_1 elicits the expression of the StPIP1_1 gene itself, as well as that of pathogenesis related genes. The oxidative burst induced by exogenously applied StPIP1_1 peptide in potato leaf disks is dependent on functional StSERK3A/B, suggesting that StPIP1_1 perception occurs via a receptor complex involving the co-receptor StSERK3A/B. Moreover, StPIP1_1 induces expression of FRK1 in Arabidopsis in an RLK7-dependent manner. Expression of an RLK from potato with high sequence homology to AtRLK7 is induced by StPIP1_1, by Pep-13 and in response to infection with P. infestans. These observations are consistent with the hypothesis that, upon secretion, StPIP1_1 acts as an endogenous peptide required for amplification of the defense response.

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.

This contribution reports on a meeting of plant cytoskeleton scientists-the European Plant Cytoskeletal Club 2023 conference.

Tomato (Solanum lycopersicum) fruit shape is related to microtubule organization and the activity of microtubule-associated proteins (MAPs). However, insights into the mechanism of fruit shape formation from a cell biology perspective remain limited. Analysis of the tissue expression profiles of different microtubule regulators revealed that functionally distinct classes of MAPs, including members of the plant-specific MICROTUBULE-ASSOCIATED PROTEIN 70 (MAP70) and IQ67 DOMAIN (IQD, also named SUN in tomato) families, are differentially expressed during fruit development. SlMAP70-1–3 and SlIQD21a are highly expressed during fruit initiation, which relates to the dramatic microtubule pattern rearrangements throughout this developmental stage of tomato fruits. Transgenic tomato lines overexpressing SlMAP70-1 or SlIQD21a produced elongated fruits with reduced cell circularity and microtubule anisotropy, while their loss-of-function mutants showed the opposite phenotype, harboring flatter fruits. Fruits were further elongated in plants coexpressing both SlMAP70-1 and SlIQD21a. We demonstrated that SlMAP70s and SlIQD21a physically interact and that the elongated fruit phenotype is likely due to microtubule stabilization induced by the SlMAP70–SlIQD21a interaction. Together, our results identify SlMAP70 proteins and SlIQD21a as important regulators of fruit elongation and demonstrate that manipulating microtubule function during early fruit development provides an effective approach to alter fruit shape.

Leaf epidermis pavement cells form highly complex shapes with interlocking lobes and necks at their anticlinal walls. The microtubule cytoskeleton plays essential roles in pavement cell morphogenesis, in particular at necks. Vice versa, shape generates stress patterns that regulate microtubule organization. Genetic or pharmacological perturbations that affect pavement cell shape often affect microtubule organization. Pavement cell shape and microtubule organization are therefore closely interconnected. Here, we present commonly used approaches for the quantitative analysis of pavement cell shape characteristics and of microtubule organization. In combination with ablation experiments, these methods can be applied to investigate how different genotypes (or treatments) affect the organization and stress responsiveness of the microtubule cytoskeleton.

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.