Essay 19.2

Apical Basal Polarity is Maintained in Mature Plants

Jiří Friml, Center for Plant Molecular Biology, University of Tübingen, Tübingen, Germany; Angus Murphy, Department of Horticulture, Purdue University, West Lafayette, Indiana, USA

August, 2006

Nomenclature for Apical/Basal Polarity in Plants

Polarity Nomenclature in "Classical" Plant Anatomy

Throughout this and most other plant biology textbooks, the tips of post-embryonic plant shoots and roots are referred to as apices. The attachment/transition point between stem and root is referred to as a base. This nomenclature has its origins in classical descriptive plant anatomy (Esau 1977). The word "apex" comes from the Latin word for the summit of a hill, mountain, or building, and the word "base" from the word for the bottom of the same structures. The adjectives "apical" and "basal" then mean relating to, located or situated at, or constituting, an apex or base, respectively. Directions are defined as acropetal (toward the apex) and basipetal (towards the base, or away from the apex). Consequently, and sometimes confusingly, the "downward" direction from the shoot apex towards the root tip is termed basipetal in the shoot, but acropetal in the root. However, for lateral organs, the base always refers to the point of attachment to the main plant body and the apex corresponds to the organ tip.

To complicate matters, another, noncompatible nomenclature is equally well-established for the description of early embryos (Esau 1977). In general, this has not posed much of a problem, as it is usually clear when embryo or post-embryonic structure is being described. All adult plants originate from a single-celled zygote, whose pole of attachment to the maternal tissue is defined as basal and its opposite pole as apical. This early polarity serves as a reference for the developmental concept of the apical-basal body axis, with the root embryo pole designated as the base and the opposite end as the apex (Figure 1). However, it is not clearly defined when and where the anatomical base of the embryo arises and at which embryo stage the zygotic nomenclature should be replaced by the nomenclature used with mature plants. In general, zygotic nomenclature is consistent with that used in mature plants when discussing shoots but leads to considerable confusion when discussing roots. For the balance of this essay, whenever we refer to classical anatomical terminology, the term will be in italics, and when we refer zygotic terminology, the term will be underlined.

Figure 1 Apical/basal terminology in the plant embryo and seedling. Anatomical nomenclature describes tips of organs, including roots and shoots, as apices. Zygotic nomenclature defines the embryo root pole as basal and the shoot pole as apical. For a description of individual cells by anatomical terms—apical is the side always facing the apex and basal is the opposite side; whereas, the zygote point of view apical is always the upper side of the cell (facing shoot apex) and basal is the lower side (facing root apex). For cells or early organ primordia, such as lateral root primordia (LRP), without clearly defined cellular polarity, the terms proximal/distal are often substituted for basal/apical terminology. Position of polarity marker PIN1 is depicted. (Click image to enlarge.)

The problems are most apparent when the term apical and basal are used in cell biology for a description of the apical and basal sides of cells. In root cells, the lower side of a cell is basal in the zygotic nomenclature but becomes apical in the context of the mature plant in the anatomical nomenclature. The terminology employed can become particularly confusing when describing, at the same time, directions of polar auxin transport and the polar subcellular localization of transport proteins in roots.

Developmental Studies Favor the Use of Zygotic Terminology

Recent developmental studies indicate that the polar localization of many components of plant cells is established in the embryo and that this polar localization is conserved in the roots and shoots of mature plants. For example, the PIN1 auxin transport protein becomes asymmetrically positioned at the lower (basal) ends of provascular cells early during embryogenesis and stays at the same position in the descended vascular cells of the post-embryonic shoot (basal, basal) or root (basal, apical) (Friml 2003). The underlying mechanisms involved in the establishment and maintenance of cell polarity appear to be independent of tissue or cell type, as manipulations of these mechanisms have similar effects, regardless of the cell type or developmental stage of the plant (Friml 2004).

This polar organization of cells in the main plant axis is recapitulated in the development of post-embryonically initiated organs (aerial organs or lateral roots) where new cell polarities mimic those along the main body axis, as demonstrated by the identical position of morphological and PIN polarity markers in developed organs (Benková 2003). Even when plants respond plastically to external stimuli such as light and gravity, the cellular polarity of the main plant axis is essentially maintained in the reoriented tissues.

Use of nomenclature based on zygotic development also corresponds better to the nomenclature used in animal developmental biology and doesn't require continuous specification of the developmental stage and the position of the cell in order to know which cell side is actually intended. However, a drawback of the use of zygotic nomenclature in describing plant roots is that one must know the origin of a particular cell to define its polarity rather than characterizing its polarity in terms of its current position relative to the root apex.

Avoiding Confusion

For descriptions of cell polarity, the zygote-derived convention appears to be more appropriate from a mechanistic point of view. It certainly would make it easier for plant physiology students studying auxin transport if they could equate "apical" with "up" and "basal" with "down," in all cases. On the other hand the classical anatomical nomenclature is very elegant for describing the post-embryonic plant body and is entrenched as a result of its use in anatomical and physiological studies for centuries. The current consensus is that the anatomical terms apex, base, acropetal, basipetal are used to describe physiological experiments in post-embryonic plants, but the zygote-derived, apical-basal body axis is used as a reference for the description of the polarity of individual cells in cell biology. To simplify things, many researchers use the intuitive and neutral terms upper and lower to describe surfaces and boundaries of root cells. In all cases, the system of nomenclature employed should be unambiguously stated when results are reported.

References

Benková, E., Michniewicz, M., Sauer, M., Teichman, T., Seifertova, D., Jurgens, G., and Friml, J. (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115: 591–602.

Esau, K. (1977) Plant Anatomy, 2nd ed., John Wiley & Sons, Inc., New York.

Friml, J. (2003) Auxin transport: Shaping the plant. Curr. Opin. Plant Biol. 6: 7–12.

Friml, J., Yang, X., Michniewicz, M., Weijers, D., Quint, A., Tietz, O., Benjamins, R., Ouwerkerk, P. B., Ljung, K., Sandberg, G., Hooykaas, P. J., Palme, K., and Offringa, R. (2004) A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science 306: 862–865.