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

Abstract

Main conclusion

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 (c) the determination of the division plane in GMCs and SMCs.

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Abbreviations

AGPs:

Arabinogalactan proteins

GMC:

Guard cell mother cell

HGAs:

Homogalacturonans

MLGs:

Mixed-linkage glucans

PPB:

Preprophase band

ROS:

Reactive oxygen species

SC:

Subsidiary cell

SMC:

Subsidiary cell mother cell

RGAs:

Rhamnogalacturonans

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Acknowledgments

This work was supported by a grant from the National and Kapodistrian University of Athens, Greece. The authors would like to thank Plant Probes for the kind offer of certain antibodies used in this study.

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Suppl. Figure 1 Median paradermal section of a stomatal row area observed with TEM. A “young” GMC (GMC 1) and two “advanced” GMCs (GMC 2 and GMC 3) are shown. Note the changes at the shape and the dimensions between GMC 1 and GMC 2 and 3. The arrows show the transverse cell wall of the GMCs that bulge towards the intervening cell of the stomatal row (IS). In the SMC marked by the square, the nucleus (N) has occupied its polar position and the cell protrudes towards the inducing GMC. Note the shape of the young SCs (circles). Scale bars: 5 μm (TIFF 3235 kb)

Suppl. Figure 2 A newly formed stomatal complex at a median paradermal section, observed with TEM. The arrows point to the ventral cell wall. GC: guard cell, SC: subsidiary cell. Scale bars: 2 μm (TIFF 9617 kb)

Suppl. Figure 3 a-d Hand-made sections of fresh material depicting stomatal rows displaying young (a, b) and mature (c, d) GMCs, as seen in DIC optics (a, c) and in epifluorescence microscope (b, d) under the filter used in this study. The cell walls do not exhibit any autofluorescence (b, d). e–h Protodermal areas of material that has been subjected to the immunolabeling protocol procedure, omitting the addition of the first antibody (control), as seen in DIC optics (e, g) and in epifluorescence microscope (f, h). In (f, h) no fluorescent signal is observed. In (e, f) young GMCs, while in (g, h) a mature GMC and a young stomatal complex are shown. The asterisks mark the GMCs, the squares the SMCs, the rhombi the guard cells and the circles the SCs. N: nucleus. Scale bars: 5 μm (TIFF 10692 kb)

Suppl. Figure 4 GMC in transverse longitudinal section, observed with TEM. The arrow points to the median region of the external periclinal cell wall, presented thinner than the rest of the cell wall. N: nucleus. Scale bars: 1 μm (TIFF 9164 kb)

Suppl. Figure 5 Young (a, b) and advanced (c-f) GMCs of Triticum turgidum as seen after immunolabeling of 2F4-HGA epitope (a, c, e) and in DIC optics (b, d, f). 2F4 fluorescent signal is emitted by the lateral GMC cell walls only (arrowheads). The asterisks mark the GMCs, the squares the SMCs, the rhombi the guard cells and the circles the SCs. N: nucleus. Scale bars: 10 μm (TIFF 11575 kb)

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Giannoutsou, E., Apostolakos, P. & Galatis, B. Spatio-temporal diversification of the cell wall matrix materials in the developing stomatal complexes of Zea mays . Planta 244, 1125–1143 (2016). https://doi.org/10.1007/s00425-016-2574-7

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Keywords

  • Arabinogalactan proteins
  • Cell wall deformation
  • Cell wall expansion
  • Cell polarity
  • Determination of cell division plane
  • Mixed-linkage glucans
  • Pectins
  • Stomatal complexes
  • Zea mays