Developmental innovations of stomatal form and function in grasses

• Applicant: Professor Dr. Michael Raissig
• Subject Area: Plant Cell and Developmental Biology ; Plant Genetics and Genomics ; Plant Physiology
• Term: from 2018 to 2024
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 394575017

• Final Report Year: 2024

Final Report Abstract

How biological form is generated through coordination of cell division patterns and acquisition of distinct cell fates and how a specific form affects its function are some of the most fundamental questions in biology. Plant stomata—small, adjustable cellular valves at the plant-environment interface that balance photosynthetic carbon dioxide uptake with water vapour release—offer an outstanding developmental, evolutionary and physiological model system to link development, morphology and physiological function. Unlike most other plants, grasses form morphologically innovative stomatal complexes, which feature dumbbell-shaped rather than kidney-shaped guard cells (GCs) that are flanked by two lateral subsidiary cells (SCs). This derived form accelerates opening and closing kinetics and enhances water-use efficiency, which might contribute to the grass family’s evolutionary success and to the fact that domesticated grasses like rice, maize and wheat provide more than half of human caloric intake. In this project, we used the model grass and wheat relative Brachypodium distachyon to dissect the developmental mechanisms of how grasses build their innovative stomatal form and how this contributes to superior gas exchange dynamics in grasses. We used comparative (single-cell) transcriptomics, gene editing and mutant analysis, and transgenic reporter lines and confocal microscopy to identify and characterize novel developmental modules. We (a) identified a novel polarity program that controls the formative SC division, (b) found a hair-cell-specific regulator that indirectly affects stomatal size and gas exchange, (c) quantitatively determined gas exchange dynamics in B. distachyon, (d) comprehensively described grass leaf development using single-cell-resolution transcriptomics, (e) further deciphered how the core transcription factor BdMUTE coordinates the GC and SC lineages, (f) identified novel mutants using forward genetics and (g) started to genetically dissect how succulents make ontogenetically distinct SCs. In conclusion, this Emmy Noether grant enabled significant progress in understanding how grasses arguably form the most derived and innovative “breathing pores”. Furthermore, it laid the foundation for understanding the formation and function of SCs in succulent Crassulaceans. This leap in fundamental knowledge of how the plant kingdom forms diverse stomatal morphologies and how this affects plant-atmosphere gas exchange can contribute to breeding or engineering climate-change-resilient crops.

Publications

• Form, development and function of grass stomata. The Plant Journal, 101(4), 780-799.
  Nunes, Tiago D. G.; Zhang, Dan & Raissig, Michael T.
  
• Seed Sterilization and Seedling Growth on Plates in the Model Grass Brachypodium distachyon. BIO-PROTOCOL, 10(15).
  Haas, Aylin & Raissig, Michael
  
• Editorial: Linking Stomatal Development and Physiology: From Stomatal Models to Non-model Species and Crops. Frontiers in Plant Science, 12.
  McAdam, Scott A. M.; Chater, Caspar C. C.; Shpak, Elena D.; Raissig, Michael T. & Dow, Graham J.
  
• Morphology made for movement: formation of diverse stomatal guard cells. Current Opinion in Plant Biology, 63, 102090.
  Spiegelhalder, Roxane P. & Raissig, Michael T.
  
• Opposite polarity programs regulate asymmetric subsidiary cell divisions in grasses. eLife, 11.
  Zhang, Dan; Spiegelhalder, Roxane P.; Abrash, Emily B.; Nunes, Tiago D. G.; Hidalgo, Inés; Anleu, Gil M. Ximena; Jesenofsky, Barbara; Lindner, Heike; Bergmann, Dominique C. & Raissig, Michael T.
  
• Quantitative effects of environmental variation on stomatal anatomy and gas exchange in a grass model. Quantitative Plant Biology, 3.
  Nunes, Tiago D. G.; Slawinska, Magdalena W.; Lindner, Heike & Raissig, Michael T.
  
• The wild grass Brachypodium distachyon as a developmental model system. Current Topics in Developmental Biology, 33-71.
  Raissig, Michael T. & Woods, Daniel P.
  
• From grasses to succulents – development and function of distinct stomatal subsidiary cells. New Phytologist, 239(1), 47-53.
  Cheng, Xin & Raissig, Michael T.
  
• Regulation of hair cell and stomatal size by a hair cell-specific peroxidase in the grass Brachypodium distachyon. Current Biology, 33(9), 1844-1854.e6.
  Nunes, Tiago D.G.; Berg, Lea S.; Slawinska, Magdalena W.; Zhang, Dan; Redt, Leonie; Sibout, Richard; Vogel, John P.; Laudencia-Chingcuanco, Debbie; Jesenofsky, Barbara; Lindner, Heike & Raissig, Michael T.