Rhizoids and protonemata of characean algae: model cells for research on polarized growth and plant gravity sensing

Abstract

Gravitropically tip-growing rhizoids and protonemata of characean algae are well-established unicellular plant model systems for research on gravitropism. In recent years, considerable progress has been made in the understanding of the cellular and molecular mechanisms underlying gravity sensing and gravity-oriented growth. While in higher-plant statocytes the role of cytoskeletal elements, especially the actin cytoskeleton, in the mechanisms of gravity sensing is still enigmatic, there is clear evidence that in the characean cells actin is intimately involved in polarized growth, gravity sensing, and the gravitropic response mechanisms. The multiple functions of actin are orchestrated by a variety of actin-binding proteins which control actin polymerisation, regulate the dynamic remodelling of the actin filament architecture, and mediate the transport of vesicles and organelles. Actin and a steep gradient of cytoplasmic free calcium are crucial components of a feedback mechanism that controls polarized growth. Experiments performed in microgravity provided evidence that actomyosin is a key player for gravity sensing: it coordinates the position of statoliths and, upon a change in the cell's orientation, directs sedimenting statoliths to specific areas of the plasma membrane, where contact with membrane-bound gravisensor molecules elicits short gravitropic pathways. In rhizoids, gravitropic signalling leads to a local reduction of cytoplasmic free calcium and results in differential growth of the opposite subapical cell flanks. The negative gravitropic response of protonemata involves actin-dependent relocation of the calcium gradient and displacement of the centre of maximal growth towards the upper flank. On the basis of the results obtained from the gravitropic model cells, a similar fine-tuning function of the actomyosin system is discussed for the early steps of gravity sensing in higher-plant statocytes.

Green Algae and the Origins of Multicellularity in the Plant Kingdom

“…These similarities include a long, branched body axis and indeterminate apical meristem cell. Charophyceans do not have multicellular tissues, but their giant multinucleated cells show differentiation into specialized types including long intermodal cells, nodal cells that undergo asymmetric cell divisions to form branches, and rhizoid cells that act as holdfasts and show tip-polarized growth (Cook et al 1998;Braun and Limbach 2006). Charophyceae also have male (antheridia) and female (oogonia) sexual reproductive structures (see below) that are formed by complex division patterns to generate simple three-dimensional multicellular tissues (Fritsch 1948;PickettHeaps 1968;Kwiatkowska 2003;Graham et al 2009).…”

“…Polarized gravitropic growth of the apical meristem and rhizoid cells in Chara and Nitella has been investigated, particularly with respect to actin cytoskeletal dynamics (Braun and Limbach 2006). However, little is known about other developmental patterning cues in charophytes such as light signaling (Rethy 1968;Dring 1988).…”

Ground-Based Facilities for Simulation of Microgravity: Organism-Specific Recommendations for Their Use, and Recommended Terminology

“…Experiments have been performed on board space shuttles (IML-2, SMM-05; Braun et al, 1996Braun et al, , 1999aBraun et al, , 1999b, during several sounding rocket flights (MAXUS and TEXUS; Buchen et al, 1991Buchen et al, , 1993 and parabolic plane flights (Limbach et al, 2005), in several types of clinostats (classical, fast-rotating 2-D, 3-D clinostats), and in a RPM and a magnetic levitator of the HFML. The transparency and the relatively large size make this gravitropically tip-growing cell a suitable model system for research on plant gravity sensing and gravity-regulated growth responses (Limbach et al, 2005;Braun and Limbach, 2006;Braun, 2007;Hemmersbach and Braun, 2007). The apical actin cytoskeleton keeps the statoliths, membrane-bound vacuoles filled with BaSO 4 crystals, in a dynamically stable position close to tip by precisely counteracting the apically directed force of gravity (Braun and Wasteneys, 2000;.…”

Análisis gravitrópico de la raíz primordial de plantas mesoamericanas, en condiciones de microgravedad simulada

“…Rhizoids and protonemata of characean algae model cells for research on polarized growth and plant gravity sensing [Artículo Cientifico] Esta señal inicia una cascada de eventos que envuelve un cambio local de la actividad de los canales de calcio. Un incremento de la concentración de Ca+2 citoplasmá-tico libre en la célula inferior conduce a la diferencia de crecimiento de células sub-apicales (Células encargadas de formar el tejido diferenciado en los vegetales) opuestas en forma de una suave inclinación hacia abajo como se muestra en la figura 1 (Braun & Limbach, 2006).…”