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Title: Calpain-Mediated positional information directs cell wall orientation to sustain plant stem cell activity, growth and development

Author
item LIANG, ZHE - Norwegian University Of Life Sciences
item BROWN, ROY - University Of Louisiana
item Fletcher, Jennifer
item OPSAHL-SORTEBERG, HILDE-GUNN - Norwegian University Of Life Sciences

Submitted to: Plant and Cell Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/17/2015
Publication Date: 8/27/2015
Citation: Liang, Z., Brown, R.C., Fletcher, J.C., Opsahl-Sorteberg, H. 2015. Calpain-Mediated positional information directs cell wall orientation to sustain plant stem cell activity, growth and development. Plant And Cell Physiology. 56(9):1855-1866.

Interpretive Summary: In this work we studied the role of the DEFECTIVE KERNEL1 (DEK1) calpain gene in the early development of Arabidopsis plants. Calpains are found in both plants and animals and function in communicating information between neighboring cells. We determined that during the plant life cycle most actively dividing tissues express the DEK1 gene. We found that plants that do not make any DEK1 protein die as embryos with severe defects in the cellular machinery that enables the cells to divide in regular patterns. By reducing the amount of active DEK1 protein in plant cells, we could show that DEK1 is also important to sustain the activity of the shoot apical meristem, the very tip of the plant that maintains the growth of the seedling. Our results show that the DEK1 gene plays a fundamental role in setting up the orientation of new cell walls during cell division in plants, which is necessary for proper embryo formation as well as for the continuous growth habit of the seedling.

Technical Abstract: Eukaryotic development and stem cell control depend on the integration of cell positional sensing with cell cycle control and cell wall positioning, yet few factors that directly link these events are known. The DEFECTIVE KERNEL1 (DEK1) gene encoding the unique plant calpain protein is fundamental for development and growth, being essential to confer and maintain epidermal cell identity that allows development beyond the globular embryo stage. We show that DEK1 expression is highest in the actively dividing cells of seeds, meristems and vasculature. We further show that eliminating Arabidopsis DEK1 function leads to changes in developmental cues from the first zygotic division onward, altered microtubule patterns and misshaped cells resulting in early embryo abortion. Expression of the embryonic marker genes WOX2, ATML1, PIN4, WUS, and STM, related to axis organization, cell identity and meristem functions, are also altered in dek1 embryos. By monitoring cell layer-specific DEK1 down-regulation, we show that L1- and 35S-induced down-regulation mainly affects stem cell functions, causing severe shoot apical meristem phenotypes. These results are consistent with a requirement for DEK1 to direct layer-specific cellular activities and set downstream developmental cues. Our data suggest that DEK1 may anchor cell wall positions and control cell division and differentiation, thereby balancing the plant's requirement to maintain totipotent stem cell reservoirs while simultaneously directing growth and organ formation. A role for DEK1 in regulating microtubule-orchestrated cell wall orientation during cell division can explain its effects on embryonic development, and suggests a more general function for calpains in microtubule organization in eukaryotic cells.