Review
Plant morphogenesis: long-distance coordination and local patterning

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Abstract

The overall morphology of a plant is largely determined by developmental decisions taken within or near the terminally positioned apical meristems of shoots and roots. The spatial separation of these developmental centers emphasizes the need for long-distance signaling. The same signaling events may simultaneously coordinate differentiation within meristems and in the connecting vascular tissues. Recent genetic and molecular analyses not only confirm the proposed role of auxin as a coordinating signal across the plant, but also implicate auxin as a patterning signal in embryo and meristem organization.

Introduction

Auxin has been implicated in a bewildering array of developmental processes. A partial list includes responses to the environmental cues of light and gravity, the control of dominance relations among shoot apices, the initiation of new root meristems, the organization of embryos, the patterned differentiation of vascular tissues and the differentiation of single cells to become tracheary elements [1], [2], [3], [4], [5], [6], [7]. These phenomena are not only varied, they also occur at different levels of organization from the whole plant to the single cell [8radical dot].

Recent molecular genetic work appears to add to the confusion by implicating auxin directly in the patterning processes in embryos and meristems. In this review, we make suggestions for the integration of long-distance coordinating auxin functions with local-patterning functions in embryos and meristems. Further, we attempt to show that these suggestions offer some insights concerning both the most recent contributions to auxin research and future possibilities.

Section snippets

Coordination of morphogenesis throughout the plant

Auxin serves as a major integrator of developmental processes at many levels and throughout the plant [3], [6], [9]. More specifically, it is a signal that coordinates the development of various plant tissues with the state and size of the shoot tissues that are morphologically above them (Fig. 1). Auxin coordinates the growth of new leaves with the initiation of new roots. At the same time, it determines both the differentiation of and the relations among cells of the vascular contacts between

Embryo axis formation

Recently identified mutations in two genes, AUXIN RESISTANT 6 (AXR6) [22radical dot] and BODENLOS (BDL) [23radical dot], result in phenotypically similar rootless seedlings with reduced vascular systems and occasionally fused cotyledons. In the embryos of mutants affected in these genes, early cell divisions are abnormally oriented and do not establish cell files along the apical–basal axis. By all these criteria, both mutants resemble the previously identified monopteros (mp) mutants, and the MP gene has been

Root meristem formation and maintenance

The promoting influence of auxin on root meristem formation is experimentally well established, and the rootless embryos of axr6, bdl and mp mutants suggest that auxin signals are also required for the initiation of the primary root early in embryogenesis. A recent study seems to provide not only a molecular explanation for the auxin-dependence of root meristem initiation, but also evidence for a role of auxin as a positional signal in the cell-patterning process within the root meristem [27radical dotradical dot].

Lateral organ formation in the shoot apex

Although the distribution of auxin sources in the shoot apex is still unclear, there is general agreement that young leaf and flower primordia are important sources of auxin [2], [3]. Interestingly, these lateral outgrowths within shoot apical meristems are not formed when auxin transport is impaired, suggesting that auxin transport either towards or away from a primordium is required for its patterned growth. In a recent study, Reinhard et al. [29radical dot] demonstrated that lateral organ formation in

Auxin as a coordinating and patterning signal

The work reviewed above shows that the analysis of auxin's developmental roles continues at an increasing pace. The phenotypes of a number of auxin response mutants suggest that they are caused by mutations that influence ‘master processes’ of cellular change. An example of such a master process is the specification of cell orientation (i.e. polarity), which appears to be a basic process that precedes a variety of more specific differentiation events [6], [15]. The recent results summarized

Conclusions

Auxin has long been known to regulate a wide variety of plant responses, but recent molecular genetic findings directly implicate auxin in the organization of cell patterns and in genetically programmed morphogenesis. Closer inspection of these developmental patterning processes shows that they do not seem to be rigidly specified. Rather, they appear to be flexible and to emerge from complex intercellular cross-talk. It is plausible that auxins act as intercellular messengers in patterning

Acknowledgements

We would like to thank Jim Mattsson for discussions and critical reading, and Cris Kuhlemeier and Ben Scheres for helpful comments.

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • radical dotof special interest

  • radical dotradical dotof outstanding interest

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