Spatio-temporal diversification of the cell wall matrix materials in the developing stomatal complexes of Zea mays

Abstract

The matrix cell wall materials, in developing Zea mays stomatal complexes are asymmetrically distributed, a phenomenon appearing related to the local cell wall expansion and deformation, the establishment of cell polarity, and determination of the cell division plane. In cells of developing Zea mays stomatal complexes, definite cell wall regions expand determinately and become locally deformed. This differential cell wall behavior is obvious in the guard cell mother cells (GMCs) and the subsidiary cell mother cells (SMCs) that locally protrude towards the adjacent GMCs. The latter, emitting a morphogenetic stimulus, induce polarization/asymmetrical division in SMCs. Examination of immunolabeled specimens revealed that homogalacturonans (HGAs) with a high degree of de-esterification (2F4- and JIM5-HGA epitopes) and arabinogalactan proteins are selectively distributed in the extending and deformed cell wall regions, while their margins are enriched with rhamnogalacturonans (RGAs) containing highly branched arabinans (LM6-RGA epitope). In SMCs, the local cell wall matrix differentiation constitutes the first structural event, indicating the establishment of cell polarity. Moreover, in the premitotic GMCs and SMCs, non-esterified HGAs (2F4-HGA epitope) are preferentially localized in the cell wall areas outlining the cytoplasm where the preprophase band is formed. In these areas, the forthcoming cell plate fuses with the parent cell walls. These data suggest that the described heterogeneity in matrix cell wall materials is probably involved in: (a) local cell wall expansion and deformation, (b) the transduction of the inductive GMC stimulus, and

Mechanical stress initiates and sustains the morphogenesis of wavy leaf epidermal cells

“…Two main structural components of the primary cell wall are pectins and cellulose microfibrils (Bidhendi and Geitmann, 2016;Cosgrove, 2015Cosgrove, , 2018. Cellulose microfibrils are generally recognized as the main load-bearing component of the cell wall that confer anisotropy (Anderson et al, 2010;Baskin, 2005;Burgert and Fratzl, 2009;Crowell et al, 2011), whereas pectin chemistry is mostly recognized in the context of the local stiffness of the wall matrix (Bidhendi and Geitmann, 2016;Braybrook and Peaucelle, 2013;Carter et al, 2017;Giannoutsou et al, 2016;Torode et al, 2017). Both cellulose microfibrils and pectins are thought to direct the local shaping of cells, but hitherto these concepts have mostly been investigated in cells with simple shapes such as pollen tubes (Fayant et al, 2010), root hairs (Shaw et al, 2000), trichome branches (Yanagisawa et al, 2015), or cells of root and shoot epidermis (Baskin, 2005;Bou Daher et al, 2018;Peaucelle et al, 2015).…”

Stomatal Complex Development and F-Actin Organization in Maize Leaf Epidermis Depend on Cellulose Synthesis

“…It is therefore tempting to assume that lack of cellulose, due to DCB or isoxaben, affects the overall cell wall properties, inhibiting thus the induction of SMC division. In addition, the SMC wall area facing the inducing GMC exhibits normally higher expansibility, in comparison to the flanking SMC wall areas [ 34 ], resulting in local SMC bulging towards the inducing GMC, which triggers the F-actin patch formation. Consequently, cellulose deficiency due to the inhibitors may affect this expansibility pattern, resulting in inhibition of SMC local bulging.…”

Form, development and function of grass stomata

“…There is mechanical strain at the GMC/SMC interface due to differential elongation rates between GMCs and flanking SMCs. Furthermore, the cell walls at this interface are differentially modified; the homogalacturan antibody 2F4‐HGA, for example, covered the interface and extended apically and basally (Giannoutsou et al , ). Strikingly, the 2F4‐HGA zone, which often can be associated with growing cells (Bidhendi and Geitmann, ), ended exactly where the pre‐mitotic SMC preprophase band (PPB) was positioned that guides phragmoblast extension of the future SC during asymmetric cell division (Figure d; Panteris et al , ; Giannoutsou et al , ).…”

“…Furthermore, the cell walls at this interface are differentially modified; the homogalacturan antibody 2F4‐HGA, for example, covered the interface and extended apically and basally (Giannoutsou et al , ). Strikingly, the 2F4‐HGA zone, which often can be associated with growing cells (Bidhendi and Geitmann, ), ended exactly where the pre‐mitotic SMC preprophase band (PPB) was positioned that guides phragmoblast extension of the future SC during asymmetric cell division (Figure d; Panteris et al , ; Giannoutsou et al , ). This suggests that also microtubular PPB positioning might follow mechanical stress patterns during SC development, which has been shown in other developmental contexts (Landrein and Hamant, ; Sampathkumar et al , ).…”

“…the coleoptile) produces kidney-shaped GCs (Galatis and Apostolakos, 2004). Clearly, differential modification of cell wall properties at distinct positions both contribute and enable the dramatic morphogenesis of grass stomatal complexes (Giannoutsou et al, 2016). Apart from FAMA and SCRM2, ZmPAN2 seems to have a role in SC morphogenesis in maize as zmpan2 mutants failed to develop Panicoid-like triangular SCs but rather produced Pooid-like dome-shaped SCs (Sutimantanapi et al, 2014).…”