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Actin filament-organized local cortical endoplasmic reticulum aggregations in developing stomatal complexes of grasses

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Abstract

Endoplasmic reticulum (ER) immunolabeling in developing stomatal complexes and in the intervening cells of the stomatal rows (ICSRs) of Zea mays revealed that the cortical-ER forms distinct aggregations lining locally expanding wall regions. The polarized subsidiary cell mother cells (SMCs), displayed a cortical-ER-patch lining the wall region shared with the inducing guard cell mother cell (GMC), which disorganized during mitosis. In dividing SMCs, ER persisted in the preprophase band region and was unequally distributed in the mitotic spindle poles. The subsidiary cells (SCs) formed initially an ER-patch lining the common wall with the GMC or the young guard cells and afterwards an ER-ring in the junction of the SC wall with the neighboring ones. Distinct ER aggregations lined the ICSR wall regions shared with the SCs. The cortical-ER aggregations in stomatal cells of Z. mays were co-localized with actin filament (AF) arrays but both were absent from the respective cells of Triticum turgidum, which follow a different morphogenetic pattern. Experimental evidence showed that the interphase ER aggregations are organized by the respective AF arrays, while the mitotic ER aggregations by microtubules. These results revealed that AF and ER demarcated “cortical cytoplasmic domains” are activated below the locally expanding stomatal cell wall regions, probably via a mechanosensing mechanism triggered by the locally stressed plasmalemma/cell wall continuum. The probable role(s) of the local ER aggregations are discussed.

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Abbreviations

AF:

Actin filament

but-1:

Butanol-1

but-2:

Butanol-2

ER:

Endoplasmic reticulum

GC:

Guard cell

GMC:

Guard cell mother cell

ICSR:

Intervening cell of the stomatal row

lat-B:

Latrunculin-B

MT:

Microtubule

PLC:

Phospholipase-C

PLD:

Phospholipase –D

PPB:

Preprophase band

SC:

Subsidiary cell

SMC:

Subsidiary cell mother cell

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Acknowledgments

The authors wish to express their thanks to Dr. H. Quader (Biocentre Klein Flotbek, University of Hamburg) and Prof. R. Boston (Department of Botany, North Karolina State University) for their kind offer of the antibodies used in this study. They also thank Dr. E. Rigana (Biological Imaging Unit, Foundation of Biomedical Research, Athens, Greece) for the use of the CLSM.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Botany, Faculty of Biology, University of Athens, Athens, 15784, Greece

    Eleni P. Giannoutsou, Panagiotis Apostolakos & Basil Galatis

Authors
  1. Eleni P. Giannoutsou
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  2. Panagiotis Apostolakos
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  3. Basil Galatis
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Corresponding author

Correspondence to Basil Galatis.

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Handling Editor: Jaideep Mathur

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Suppl. Fig. 1

a–h AF organization in developing stomatal complexes of Zea mays. The asterisks mark the inducing GMCs, while the squares the SCs. Scale bars 10 μm. a–c Preprophase/prophase (a), mitotic (b; projection of all CLSM images) and cytokinetic (c) SMC. The arrows indicate the AF-patch. The arrowhead in (b) marks the AFs in the mitotic spindle. Inset in (c) The daughter nuclei after DNA staining with Hoechst 33258. d Young stomatal complex, the SCs of which display a lens-like shape. The arrows indicate the AF-patch in SCs, while the arrowheads the local AF aggregation in the cortical cytoplasm of ICSRs. e, f CLSM sections through an external (e) and a median (f) plane of a stomatal complex displaying kidney-like GCs. The arrows show the AF-ring in SCs. g, h CLSM sections through an external (g) and a median (h) plane of a stomatal complex at the stage of GC elongation. The arrows point to the AF bundles in the cytoplasm occupying the sites of junction of the SCs with the adjacent GCs (GIF 266 kb)

High resolution image (TIFF 3155 kb)

Suppl. Fig. 2

a, b AF organization in ICSRs of Zea mays. AF aggregations (arrows) line the wall regions of ICSRs that bulge towards the neighboring SCs. Scale bars 10 μm (GIF 70 kb)

High resolution image (TIFF 883 kb)

Suppl. Fig. 3

a, b ER immunolabeling by 2E7 antibody in dilution 1:40, in SMCs of Zea mays treated by DMSO (a) and acetone (b). The arrows indicate ER-patches, while the asterisk the inducing GMCs. Treatments: (a) paradermal leaf sections floating on 0.2% (v/v) DMSO for 5 h, (b) seedlings from which the roots have been dissected were placed in 0.5% (v/v) acetone for 24 h. Scale bars 10 μm (GIF 76 kb)

High resolution image (TIFF 987 kb)

Suppl. Fig. 4

a–c ER immunolabeling by 2E7 antibody in dilution 1:1,500 (a) and anti-CRT antibody in dilution 1:1,500 (b) or 1:40 (c) in Zea mays SMCs. These specimens were fixed in a fixative containing 0.1% (v/v) Triton X-100. The SMCs lack ER-patches (cf. Fig. 7 c, d). Asterisks mark the inducing GMCs. n: nucleus. Scale bars 10 μm. d ER immunolabeling by 2E7 antibody in dilution 1:1,500, in a SMC of Zea mays. The material was fixed in the absence of Triton X-100. The arrow shows a relatively well-organized ER-patch (cf. Fig. 7c) and the asterisk the inducing GMC. n: nucleus. Scale bar 10 μm (GIF 140 kb)

High resolution image (TIFF 1623 kb)

Suppl. Fig. 5

Mature stomatal complex of Zea mays as seen in epifluorescent microscope. Filters used were the same as those during ER immunolocalization experiments observation. Note the autofluorescence of the cell walls. Scale bar 10 μm (GIF 44 kb)

High resolution image (TIFF 768 kb)

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Giannoutsou, E.P., Apostolakos, P. & Galatis, B. Actin filament-organized local cortical endoplasmic reticulum aggregations in developing stomatal complexes of grasses. Protoplasma 248, 373–390 (2011). https://doi.org/10.1007/s00709-010-0180-2

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