Plasmodesmata: A history of conceptual surprises

Abstract

Since the initial postulate of plasmodesmata (PDs) and their function (Tangl 1879), three books have captured the progress in plasmodesmal (PD) research. The first (Gunning and Robards 1976) surveyed PD research extending over approximately 100 years. At the time of its publication, electron microscopy had confirmed the existence of previously putative intercellular cytoplasmic channels without a clear notion of the ultrastructure. PDs were no longer regarded as redundant evolutionary appendices, but solid evidence of their function was lacking. Over the years the hypothesis that higher plants were subdivided into symplasmic domains having some physiological role had been strengthened, but the significance of these domains remained uncertain. Exchange of low molecular weight solutes through PDs was a likely (but unproven) option, whereas passage of macromolecules was beyond the horizon of possibility at the time (Carr 1976). Over two decades later, two other books (van Bel and van Kesteren 1999; Oparka 2005) illustrated the booming interest and progress in the preceding years. Doubts on issues put forward in the first book had been eliminated. Symplasmic domains were demonstrated to be of paramount importance for transport physiology (root transport, phloem transport) and developmental biology. The PD substructure had been assessed better and a number of components associated with PDs were identified. PDs turned out to be subject to strictly regulated constriction and dilation. The functional PD molecular exclusion limits were found to vary between the initially measured 1 kDa up to about 60 kDa. The latter values gave rise to the concept of macromolecular trafficking through PDs. As a result, new concepts on PD significance for short-distance and long-distance signaling emerged, including the key role of PDs in intercellular and long-distance transport of plant viruses. This chapter is subdivided in line with the emergence of techniques that enabled new waves of experimental approaches in PD research. The discoveries that collectively led to the current concepts on PD structure and function are presented in chronological order. The emphasis is on the development of PD research rather than on the present state of the art. Therefore, recent research is discussed in less detail than work from the period before 2000.