ReviewXylogenesis: the birth of a corpse
Introduction
Plants, animals and fungi undergo processes of cell specialisation such that specific groups of cells are adapted to carry out particular functions. One of the more remarkable examples of cellular development in higher plants is the formation of long files of water-conducting cells that are capable of supporting a column of water that reaches from the roots to hundreds of feet in the air for some trees. The development of files of these cells is a critical feature of land plants that allows the delivery of water to every living cell. Each cell in a file must divide and elongate, before hoops of cell-wall material are deposited at right angles to the direction of cell elongation. This deposition reinforces the cells against the compressive forces of the surrounding tissues that are created by the suction forces of transpiration. The cell-wall material is stiffened and waterproofed by the deposition of phenolic compounds. Finally, the end walls of the cells are broken down and the cell contents are destroyed. The resulting hollow water-conducting tubes are called xylem vessels or tracheids, and the individual cells that form them are called vessel or tracheary elements (TEs) (Fig. 1). The formation of TEs involves several processes that are fundamental to plant development, including cell division, local cell signalling, cell elongation, cell specification, cell-wall synthesis and deposition, lignification and programmed cell death (PCD). Together, these processes involve many hundreds of genes [1]. Many of these genes have been identified in two large-scale screens involving cDNA sequencing of material derived from young xylem tissue from loblolly pine [2] and from poplar trees [3]. The large number of genes identified in this way is impressive, but it remains to be seen how many of them are really involved in xylogenesis itself, as these databases include cDNAs from a mixture of cell types at different developmental stages. Two alternative generic strategies are being used to try to identify genes involved in the various stages of xylem formation and to investigate their function: the use of Arabidopsis mutants and the use of a remarkable in vitro cell system, the Zinnia mesophyll cell system.
The Zinnia system consists of cells isolated from the leaves of Zinnia elegans cv. Envy, an ornamental garden plant, that are put into liquid culture and supplied with two plant growth regulators, auxin and cytokinin. By 96 hours, 80% of the cells, which were already specialised as photosynthetic cells in the leaf, are induced to form TEs [4]. The Zinnia system is unique among plant systems for two reasons. First, the entry into a new developmental pathway is induced by adding plant growth regulators, which act like a molecular switch to turn on the process of trans-differentiation. Second, about 80% of the cells synchronously undergo trans-differentiation, making it possible to precisely stage the events involved in building a TE. Thus, one cell type can be reproducibly and synchronously switched by known external signals into a totally different cell type. The Zinnia system is simple and amenable to biochemical and molec-ular analyses, and offers a real hope of understanding the nature of the molecular machinery whereby plant cells become specialised to carry out particular functions.
Section snippets
The role of auxin in establishing patterns of vascular tissue in plant organs
Polar auxin transport has long been known to be involved in the patterning of vascular strands within the plant, during both normal plant development and the creation of new strands in response to wounding [5]. In early embryonic development, this process is intimately tied up with establishing cell polarity and, subsequently, the apical–basal axis of the embryo. The polar movement of auxin depends on the progressive allocation and separation of the appropriate auxin influx and efflux carriers
Elucidating the signal transduction cascade that is involved in the specification of xylem cell fate
The specification of a xylem vessel or a TE is a long and complex process that requires a succession of signalling events and a progressive restriction of developmental fate to that of a TE. In the Zinnia cell system, the various signalling inputs that are known to influence different steps in the process include the initial wound signal, together with light, auxin, cytokinin, ethylene, brassinosteroids, and phytosulfokine (Fig. 2). Even if the intervening signal-transduction steps remain
Genes involved in secondary-wall formation and lignification
A range of xylem mutants in Arabidopsis has emerged from screens designed to look directly for vessel elements with an altered physical appearance [23]. The IRREGULAR XYLEM 3 locus encodes a cellulose synthase that is required to deposit the secondary-cell-wall cellulose, which thickens and reinforces the wall of the developing xylem-vessel elements [24]. Other genes involved in the manufacture of the secondary wall, and its subsequent lignification, are likely to emerge as other mutants from
Death, a necessary end…
In the past few years, the surge of interest in apoptotic death in animal cells has prompted consideration of the mechanism of cell death involved in xylogenesis, senescence and the hypersensitive response (HR) in plant cells. PCD is distinguished from necrotic death by involving cell-autonomous, active and ordered suicide in which specific proteases are recruited to destroy a limited number of key cellular proteins [30]. The detection of fragmented nuclear DNA (nDNA) in the vessel elements of
Conclusions
The use of mutants and transgenic plants, coupled with large EST and genome-sequencing projects, has begun to make a significant impact on xylem biology. This impact has been felt most in two intimately connected areas: the mechanisms that orchestrate the ordered patterning of vascular tissues and the signalling pathways that specify xylem cell fate. The Zinnia mesophyll system is proving to be both an engine for gene discovery for understanding xylogenesis in planta and a useful cell-culture
Acknowledgements
Maureen McCann thanks the Royal Society of London for a University Research Fellowship, and Keith Roberts’ work is funded by the Biotechnology and Biological Sciences Research Council (BBSRC).
References and recommended reading
Papers of particular interest, published within the annual period of review, have been highlighted as:
• of special interest
•• of outstanding interest
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