Plant development: Cell movement relative to each other is both common and very important

Abstract

The common view that “plant cells cannot move relative to each other” is incorrect. Relative movement of plant cells relative to each other is expressed during fiber elongation, growth of arms of branched sclereids, intrusive growth of the tips of fusiform initials in the cambium, the increase in diameter of vessel members, growth in length of vessel-member elements in the secondary xylem of the few monocotyledons that express secondary growth, growth of laticifers, formation of tylosis, dilatation in the bark via parenchyma cell expansion, and growth of pollen tubes in the style. In all these cases, part of the plant cell remains in its original position, while other parts of the cell grow to the new locations, moving significantly relative to other cells. Not considering these movements will cause a delay in studying and understanding many aspects of differentiation of plant cells and tissues.

Keywords:

• cell movement
• differentiation
• fibers
• intrusive growth
• lateral roots

Traas and Sassi¹ in a stimulating commentary about the initiation and early development of lateral roots, posited that “plant cells cannot move relative to each other” and that the extracellular, polysaccharidic matrix, the cell wall, which links plant cells together, prevents any form of cell migration or sliding. This widely held belief is not in accord with a fundamental process in vascular plant structural development known as intrusive growth.² In addition, this common view preempts the study of the delicate and very poorly understood molecular and cell biology events involved in the many cases where extensions of various plant cell types do move relative to each other.

The issue of movement of plant cells relative to each other was reviewed more than a decade ago³ and there are 9 well-known plant cell types in which cell parts grow a lot in length or width and move relative to other cells, invade in between other groups of cells or tissues, or even grow into the lumen of other cells. These nine cases are: (1) fiber elongation; (2) growth of arms of branched sclereids; (3) intrusive growth of the tips of fusiform initials in the cambium; (4) the increase in diameter of vessel members; (5) growth of laticifers; (6) growth of vessel-member elements in the secondary xylem of the few monocotyledons that express secondary growth; (7) formation of tylosis; (8) dilatation in the bark via parenchyma cell expansion; and (9) growth of pollen tubes in the style. In all these cases, part of the plant cell remains in its original position, while other parts of the cell grow to the new locations, moving significantly relative to other cells. Some cells (e.g., multinuclear laticifers) may grow to be several meters long, passing in the middle lamella between the primary cell walls of hundreds of thousands if not millions of other cells. Others (e.g.,, fusiform initials in the cambium) grow not more than a few millimeters and usually less than a millimeter³ but still move relative to other cells. Fibers, for instance, a cell type probably found in almost all if not all vascular land plants, commonly start as initials typically 10–50 μm long, and grow in length among many other non-moving cells to several millimeters if they are short, to several centimeters in plants such as flax and even to more than half a meter in extreme cases.² Even in a small and short-lived model plant, such as Arabidopsis thaliana, the fibers in the inflorescence stems attain a length of several milimeters⁴ and can be used to study the molecular and cellular aspects of intrusive growth.⁵

Intrusive growth must disrupt huge numbers of plasmodesmata and probably damage the middle lamella that connects adjacent cells, but only very infrequently it induces wound responses.³ The exact mechanisms by which plants distinguish between the penetration into a tissue of a pathogen that should be blocked and penetration of self-cells during intrusive growth that should be allowed to move are practically unknown. Similarly, the regulation or coordination of this complicated process is also unknown. The recent and expected progress in molecular and cell biology techniques is an excellent opportunity of advancing the understanding of the practically non-understood cell biology issues of the precise and orchestrated movements of parts of so many plant cells relative to others. Exploiting this opportunity is a great and certainly rewarding challenge for modern students of cell biology and plant development, such as the authors of,¹ to pursue this common, important and overlooked fundamental phenomenon of various plant cells that regularly move their growing extensions relative to other cells.