PerspectivePLANT SCIENCES

Yoda Would Be Proud: Valves for Land Plants

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Science  04 Jun 2004:
Vol. 304, Issue 5676, pp. 1461-1462
DOI: 10.1126/science.1099445

Stomata are structures in the plant epidermis that regulate the exchange of gases between a plant and its environment. Stomata comprise two guard cells on either side of a pore through which carbon dioxide required for photosynthesis passes. The stomata also reduce loss of water vapor to the environment. These structures are critical for plant productivity and were crucial to the evolution of land plants some half a billion years ago. Each leaf contains thousands of stomata, a number influenced by environmental factors during shoot development (1). The stomata are evenly spaced, one cell apart, to optimize gas exchange between the cell and its environment. The, as yet unidentified, genes that specify a stomatal fate are likely to be key targets of signaling pathways that control where and how often stomata form. On page 1494 of this issue, Bergmann et al. (2) identify a mitogen- activated protein kinase kinase (MAPKK) kinase called YODA as an important regulator of stomatal cell fate in the model plant Arabidopsis.

The unequal division of a protodermal cell results in the formation of a smaller cell, a precursor to the stomatal guard cell, and a larger cell that becomes a pavement cell and does not generate a stomatal cell unless it too divides unequally (see the first figure) (3). Such “piggyback” divisions place the smaller precursor cell at a distance from the original parent cell, implicating signaling between cells in the control of asymmetric cell division. Previous work has shown that two Arabidopsis genes—TOO MANY MOUTHS (TMM) and STOMATAL DENSITY AND DISTRIBUTION1 (SDD1)—regulate early events in asymmetric cell division (3, 4). Mutations in either gene induce production of too many stomata, which are often misplaced, suggesting that proteins encoded by normal versions of these genes are important for limiting unequal divisions and for ensuring that stomata are spaced one-cell apart. TMM is expressed in both daughter cells of the unequal division (5); SDD1 is expressed in just the smaller one (6). SDD1 is a predicted subtilisin-like protease that is probably secreted. Similar proteases mediate developmental processes such as receptor activation and pattern generation. TMM is a probable extracellular receptor associated with the cell membrane. Both genes appear to act in an intercellular communication pathway that controls cell behavior in response to extracellular positional cues (7). Among the many notable players missing from this pathway are genes likely to participate in the signaling pathways within target cells.

Making stomata.

MAPKK kinase signaling regulates the formation of stomata in shoot epidermis. (Top) Stomata are valves comprising two guard cells surrounding a pore that is open to the atmosphere and modulates gas exchange between the plant and its environment. (Bottom) In Arabidopsis, both guard cells are derived from the smaller daughter cell (green) produced when a protodermal cell (yellow) divides unequally. The larger daughter cell of the asymmetric division either divides again or becomes a generic pavement epidermal cell.

CREDIT: (PHOTO) F. SACK/OHIO STATE UNIVERSITY

Enter the plant MAPKK kinase YODA. Plants containing mutations in YODA produce an excessive number of stomata, many of which are misplaced, occurring side by side without any space between them. Like TMM and SDD1, YODA restricts the formation of stomata but, in addition, seems to play a more pivotal part in stomatal formation. For example, when two copies of a permanently active version of YODA are introduced into normal plants, stomata are eliminated and only generic epidermal cells are formed. Stomatal formation evidently requires that YODA activity be turned off or reduced at least some of the time. YODA seems to be a central molecular switch that controls the pathway that regulates the number of cells destined for a stomatal fate.

Given that the functions of all three genes overlap, they might act in the same developmental and molecular pathway. Indeed, the introduction of a single copy of the permanently active version of YODA into TMM- or SDD1-defective plants restores the correct distribution of stomata. This striking finding led Bergmann et al. to propose that YODA acts downstream of SDD1 and TMM (see the second figure). TMM, which lacks an intracellular domain, possibly may associate with another cell surface receptor that has a cytoplasmic kinase domain (5). The authors propose a scenario whereby information from extracellular signals is transduced across the cell membrane. Extracellular ligands modified by SDD1 bind to the TMM receptor and associated proteins, resulting in phosphorylation of YODA. The extent of the resulting MAPKK kinase cascade then regulates whether a stomatal cell fate is restricted or promoted. Although it is likely that YODA helps to switch this fate on or off, how it does so during plant development is still unclear. If the divisions in YODA mutants are normal (apart from their overabundance), then YODA might control stomatal number primarily by restricting division frequency. Further analysis may identify additional functions of YODA in cell fate specification. An intriguing possibility is that YODA prevents cells, other than small daughter cells, from directly becoming stomata.

YODA's many talents.

Model for control of the number of stomata by the signaling kinase YODA. A putative ligand (orange) is modified by SDD1 and then binds to a cell surface receptor such as TMM, resulting in phosphorylation and activation of the MAPKK kinase YODA. YODA's activity triggers an intracellular signaling cascade that limits the frequency of unequal divisions, thus controlling the number of stomatal cells.

CREDIT: KATHARINE SUTLIFF/SCIENCE

It has been established that YODA participates in cell fate specification early during plant embryonic development (8). Some plants with a defective YODA protein survive but remain small and fuzzy, like their namesake of Star Wars movie fame. However, most YODA mutant plants die at the embryo stage because of a disruption in the unequal divisions of the zygote. YODA is active in the non-embryo-forming cell, and mutations in this protein may lead to abnormalities that in turn alter the fate of the embryo-forming cell. It is therefore likely that this MAPKK kinase, which is expressed throughout the plant, plays a central role in cell fate determination and asymmetric divisions in multiple developmental pathways.

Until now, stomatal development genes (of which few are known) have been identified largely by screening for morphological defects. In a twist on this approach, Bergmann et al. used microarray-based gene discovery to assay stomatal absence or abundance phenotypes. They identified a set of genes whose pattern of differential expression correlated with genes already known to affect stomatal development. This set included many predicted signaling proteins and transcription factors. The authors then found that plants defective in one of those transcription factors, FAMA, exhibited caterpillar-like clusters of developmentally arrested stomata. Comparable clusters also are found in four lips mutants (9), suggesting that both genes act together to control events late in the stomatal formation pathway. The clever strategy of Bergmann et al.—using YODA to pull out FAMA—shows that the era of ignorance about plant genes controlling stomatal formation may soon be over.

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