Photosynthesis-dependent formation of convoluted plasma membrane domains in Chara internodal cells is independent of chloroplast position.

Ilse Foissner,Aniela Sommer,Margit Hoeftberger

doi:10.1007/s00709-014-0742-9

Abstract

The characean green alga Chara australis forms complex plasma membrane convolutions called charasomes when exposed to light. Charasomes are involved in local acidification of the surrounding medium which facilitates carbon uptake required for photosynthesis. They have hitherto been only described in the internodal cells and in close contact with the stationary chloroplasts. Here, we show that charasomes are not only present in the internodal cells of the main axis, side branches, and branchlets but that the plasma membranes of chloroplast-containing nodal cells, protonemata, and rhizoids are also able to invaginate into complex domains. Removal of chloroplasts by local irradiation with intense light revealed that charasomes can develop at chloroplast-free “windows” and that the resulting pH banding pattern is independent of chloroplast or window position. Charasomes were not detected along cell walls containing functional plasmodesmata. However, charasomes formed next to a smooth wound wall which was deposited onto the plasmodesmata-containing wall when the neighboring cell was damaged. In contrast, charasomes were rarely found at uneven, bulged wound walls which protrude into the streaming endoplasm and which were induced by ligation or puncturing. The results of this study show that charasome formation, although dependent on photosynthesis, does not require intimate contact with chloroplasts. Our data suggest further that the presence of plasmodesmata inhibits charasome formation and/or that exposure to the outer medium is a prerequisite for charasome formation. Finally, we hypothesize that the absence of charasomes at bulged wound walls is due to the disturbance of uniform laminar mass streaming.Electronic supplementary materialThe online version of this article (doi:10.1007/s00709-014-0742-9) contains supplementary material, which is available to authorized users.

Highlights

The plasma membrane of plant and other cells is laterally compartmented into a wide range of different types of domains
In the upward-growing green protonema, the internodal cell charasomes were detected by confocal laser scanning microscope (CLSM) of FM1-43 stained cells (Fig. 1g) and by the electron microscopy
Charasomes were found in chloroplast-containing nodal cells, irrespective whether chloroplasts were anchored in Charasome formation is not dependent on close contact with chloroplasts or mitochondria In the internodal cells, charasomes usually develop in close proximity to the stationary chloroplasts, and they are absent from the chloroplast-free neutral line and the chloroplast-free cross walls as confirmed in this study

Summary

Introduction

The plasma membrane of plant and other cells is laterally compartmented into a wide range of different types of domains. Among these domains, lipid rafts are considered to be small (10–200 nm in diameter) and highly dynamic (Lingwood and Simons 2009; Mongrand et al 2011), whereas micro- and macrodomains are larger (up to several micrometers) and more stable (Boutte and Moreau 2014; Jarsch et al 2014; Malinsky et al 2013). Membrane domains have been shown to be involved in signal transduction, cell to cell interactions, transport, stress, and polarized growth. They are enriched or depleted in membrane components but structurally similar to the “normal” plasma membrane. Plasma membrane domains with a similar structure and a similar function are present in the highly evolved characean alga, Chara australis, as described below

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