PerspectivePlant Science

A Window on the Sophistication of Plants

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Science  26 Aug 2011:
Vol. 333, Issue 6046, pp. 1103-1104
DOI: 10.1126/science.1211194

Flowering plants possess the remarkable capacity to selectively move large, functional proteins and RNA molecules between cells through regulated channels called plasmodesmata (1). For example, within a meristem (a group of stem cells) plants can steer macromolecular traffic in particular directions along these “highways” to orchestrate stem cell division and the development of specialized tissues. How they control this cell-to-cell traffic, however, has been a question of major importance. On page 1141 of this issue, Xu et al. (2) reach a major milestone in the quest for an answer. They show that selective trafficking of a functional protein, the maize transcription factor KNOTTED1 (KN1), requires KN1 to unfold and then be refolded in the destination cell by a group of proteins known as the chaperonin complex.

Plasmodesmata create highways along which proteins move from synthesis sites on the endoplasmic reticulum (ER) within one cell, through a plasmodesmal channel, and into a neighboring cell. When a protein arrives at a plasmodesma, there are two main possibilities for how it might get through the narrow channel. One is that the channel dilates to permit passage; the other is that the protein is unfolded to allow passage and then refolded when it reaches its destination.

Xu et al. used a clever research design, involving genes that control the growth of leaf hairs (trichomes) in Arabidopsis plants engineered to express maize KN1, to investigate which of these two mechanisms was involved in KN1 trafficking between leaf cells. It enabled the researchers to show that KN1 trafficking in the shoot apical meristem (the growing tip of a stem) requires CCT8, a subunit of the type II chaperonin complex. In their experimental system, they found that trafficking required the presence of the chaperonin complex in destination cells, which were located on leaf surfaces, but not in the cells where KN1 was produced, which were located in the inner leaf mesophyll, the site of photosynthesis. This suggests that KN1 is unfolded, moves through the plasmodesmal channel, and then is refolded at its destination to restore function (see the figure).

Xu et al.'s findings have broad implications for understanding other plant processes, such as the induction of flowering. Nearly 50 years ago, the late plant physiologist Jan Zeevaart remarked that the most urgent problem in flowering physiology was identifying the signaling molecule known as “florigen” (3). Today, we know that florigen is the protein FLOWERING LOCUS T (FT). It initiates flowering by moving from leaves, where it is produced in vascular tissues in response to environmental stimulus, into the phloem stream and up the stem to the vegetative apex, where it reprograms the shoot apical meristem, causing the plant to produce flowers rather than leaves (4). Now, however, plant biologists can shift from just identifying “what” is moving between plant cells to understanding how the plant controls the movements of these molecules and how it “chooses” to move a specific protein to orchestrate complex transformations, such as from stem cells into organs, from epidermal cells into hair cells, and from vegetative development into reproductive development.

This is not the only window that Xu et al. have helped open into the “how” of selective trafficking. Plants not only move functional proteins; they also traffic full-length, functional mRNA molecules, both between cells and via the phloem long-distance transport stream (1). It will be fascinating to learn how plants accomplish this, whether by means of RNA chaperones or other means. In addition, plants traffic short interfering RNA (siRNA) molecules that mediate RNA interference in the cytoplasm and epigenetic alteration of chromatin states; this movement occurs both between cells and throughout the plant via the phloem stream (5). Clearly, the “how” questions are likely to be extensive, because the “what” targets are so diverse. In addition, plant biologists must continue to uncover the full repertoire of plant processes that depend on selective trafficking.

This brings us to the most difficult, but most important, question: Why? What evolutionary advantage have plants derived from this remarkable ability? And in what ways might this capability make them unique and different from animals and fungi? For example, plants may look placid and unintelligent, but perhaps we need to reconsider the sophistication of their information processing systems, especially given the diverse types of plant informational proteins and RNA molecules that can move about in a regulated fashion, respond to the environment, and enter the nuclei of distant cells to orchestrate intricate symphonies of responses (as in the case of florigen). The computational capabilities of such a system can only be imagined, but they are potentially enormous.

Unfolding story.

Plants move regulatory proteins from cell to cell, often over long distances, to control a wide range of activities, including growth and flowering. The mechanisms, however, have been unclear. Now, Xu et al. (2) show that the movement of the maize transcriptional factor KN1 through channels known as plasmodema requires the presence of a CCT in the destination cell. This suggests that KN1 unfolds to gain passage, and is then refolded in the destination cell by CCT.

Researchers have already shown that flowering plants can “remember” newly induced states for long periods by altering the form of chromatin states at particular genetic loci, through self-reinforcing protein modifications, or through stable metabolic or developmental states—and conceivably there might be thousands of such states. This suggests that we should at least consider the possibility that flowering plants possess sophisticated abilities to integrate, process, store, and retrieve information—and that they possess an advanced mode of intelligence based on novel mechanisms that we are only beginning to understand, and that this intelligence is quite different from animal or artificial intelligence. Thus, the real importance of understanding selective trafficking mechanisms is highlighted by the question: What is the unique nature of intelligence in plants?

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