A polarized nuclear position specifies the correct division plane during maize stomatal development

Abstract

Asymmetric cell division generates different cell types and is a feature of development in multicellular organisms. Prior to asymmetric cell division, cell polarity is established. Maize (Zea mays) stomatal development serves as an excellent plant model system for asymmetric cell division, especially the asymmetric division of the subsidiary mother cell (SMC). In SMCs, the nucleus migrates to a polar location after the accumulation of polarly localized proteins but before the appearance of the preprophase band. We examined a mutant of an outer nuclear membrane protein that is part of the LINC (linker of nucleoskeleton and cytoskeleton) complex that localizes to the nuclear envelope in interphase cells. Previously, maize linc kash sine-like2 (mlks2) was observed to have abnormal stomata. We confirmed and identified the precise defects that lead to abnormal asymmetric divisions. Proteins that are polarly localized in SMCs prior to division polarized normally in mlks2. However, polar localization of the nucleus was sometimes impaired, even in cells that have otherwise normal polarity. This led to a misplaced preprophase band and atypical division planes. MLKS2 localized to mitotic structures; however, the structure of the preprophase band, spindle and phragmoplast appeared normal in mlks2. Timelapse imaging revealed that mlks2 has defects in pre-mitotic nuclear migration towards the polarized site and unstable position at the division site after formation of the preprophase band. Overall, our results show that nuclear envelope proteins promote pre-mitotic nuclear migration and stable nuclear position and that the position of the nucleus influences division plane establishment in asymmetrically dividing cells.

Is the nucleus the unwitting architect of asymmetric cell division in plants?

“…To test this idea, the authors examined nuclear positioning in the SMCs and found that a significantly higher number of nuclei failed to migrate toward the GMC in mlks2. Therefore, Ashraf et al (2023) provide evidence that MLKS2 is required for proper nuclear positioning independent of cell polarity.…”

“…C) Schematic representation of nuclear positioning and cell division structures in wild-type and mlks2 SMCs. Ashraf et al (2023) found that the mispositioned nucleus in mlks2 SMCs correlates with misplaced PPB (dotted line) and incorrect division plane during cytokinesis (dashed line), indicating a role of nuclear positioning in cell division site specification. DZ, division zone; EZ, elongation zone; MZ, maturation zone.…”

“…However, it is not yet known whether the nucleus itself plays a role. In this issue of Plant Physiology , Ashraf et al (2023) address that question. Using maize mutants defective in the outer nuclear membrane protein MAIZE LINC KASH SINE-LIKE2 (MLKS2) ( Gumber et al 2019 ), the authors provide genetic and cellular evidence that nuclear positioning plays a role in the specification of the division plane during stomatal development.…”

“… Ashraf et al (2023) used time-lapse imaging to show that PPB and nuclear positions determine spindle and phragmoplast positions in dividing SMCs. In wild-type cells, the nuclei correctly positioned next to the GMC, the PPBs formed normally, and the spindle and phragmoplast formed perpendicular to each other at the expected division site.…”

De NovoTANGLED1 Recruitment to Aberrant Cell Plate Fusion Sites in Maize

“…An invariantly localized asymmetric division generates the small, crescent shaped subsidiary cell and a larger pavement cell (Facette et al ., 2015; Gray, Liu and Facette, 2020; Durney et al ., 2023). Subsidiary cell division positioning is an excellent system due to the consistently positioned divisions and its well-characterized signaling pathways (Frank, Cartwright and Smith, 2003; Cartwright, Humphries and Smith, 2009; Humphries et al ., 2011; Zhang et al ., 2012, 2022; Sutimantanapi, Pater and Smith, 2014; Raissig et al ., 2017; H. Wang et al ., 2019; Wu et al ., 2019; Li et al ., 2021; Ashraf, Liu and Facette, 2023; Durney et al ., 2023; Nan, Char, et al ., 2023; Nan, Liang, et al ., 2023).…”