September 13, 2006 | David F. Coppedge

Plant Protection: A Modern Medieval Castle Story

Vigilant guards stand at the gates.  In times of peace, they let down the drawbridge, and the townspeople carry on their trade.  Farmers bring in their crops for the marketplace, and local craftsmen and pedlars keep the local economy bustling.  Yet the sentries maintain a watchful eye, aware that numerous interlopers are about.  Aliens constantly seek entry into these most vulnerable points in the castle walls.  The guards, however, are well trained.  They know the behavior patterns of most would-be intruders.  Any attempted invasion is usually rebuffed by a rapid “drawbridge up!” response till the danger has passed.  Day and night, through all seasons and all kinds of weather, these diligent sentries stand ready at their posts, maintaining security for the townspeople inside.
    One day, after the gates had been closed after a day of feasting and celebration, a clever interloper showed up.  He looked a little strange, but dressed as a local merchant, he insisted he had important business in town that couldn’t wait till morning.  The guards, a bit wary at first but in high spirits from the long party, checked his I.D.  He had the necessary documents, and knew the password.  Yet this interloper, armed and dangerous, carried a secret weapon: a chemical spray able to intoxicate the guards and make them susceptible to the power of suggestion.  “Let me in,” the interloper whispered softly after surprising the guards with his potent perfume.  “It’s all right.  Everything will be just fine.  No one will ever know.”  He imitated the motions of turning the cranks that would relax the heavy chains.  Overcome by the hypnotic vapors, the guards followed his motions, and soon the drawbridge came winding down.
    Once inside, the interloper went quickly to work.  A local constable was quickly put out of commission by turning his gun against him.  The intruder entered a house, subdued the occupants, and set up a base of operations.  He signaled his cohorts, and before long, before the townspeople even knew what happened, the defenses in which they had trusted had been compromised: an enemy force was inside the gates.
    A medieval tale?  No; look at your house plant.  It could be happening right there.  Yellow or sickly leaves could have suffered a similar fate.  Scientists have just discovered that bacteria can trick a leaf’s guard cells into letting down their defenses.
    Botanists have known about guard cells for a long time.  Leaf surfaces are pockmarked by openings (sing. stoma, plural stomata), each surrounded by a pair of guard cells that regulate the opening and closing of the stomata.  The openings are important for exchange of gases and for transpiration, the release of water vapor from cellular respiration to the atmosphere.  Like water balloons under pressure, the sausage-shaped cells become rigid as water is pumped in, creating turgor pressure.  Unable to increase their girth, the guard cells curve outward, opening a pore between them.  Relaxation of the turgor closes the stoma.  There can be a thousand stomata per square millimeter on a leaf surface (see CSBSJU lecture notes), each with their own pair of guard cells.
    The opening and closing of stomata is not merely a function of water availability.  A host of specialized proteins and molecules regulate the guard cells’ actions.  The complexity of these regulators was described this month by a trio of researchers at Penn State.  Reporting in PLoS Biology,1 they identified more than 40 components of the guard cell regulatory network, and that the network is robust against a wide variety of perturbations.  From conifers to cacti, from African violets to garden weeds, stomata with their guard cells keep trillions of leaves operating as effective harvesters of sunlight, with benefits for all life.  “To our knowledge,” the researchers said without mentioning evolution, “this is one of the most complex biological networks ever modeled in a dynamical fashion.”
    But back to our castle story.  Other scientists just made a surprising discovery.  Stomata are not only avenues for gas and water exchange: they really have “guard” cells with a security role.  Melotto et al. at Michigan State, writing in Cell,2 found that guard cells respond to the presence of bacteria.  They can sense the flagellin molecules in Pseudomonas syringae, a common leaf pathogen, and close the stomata to defend against invasion.  This clever bacterium, though, like our castle intruder, carries a molecule that mimics the “open sesame” command of regulators inside, and can trick the guard cells into letting down the leaf defenses.  Once inside, the bacteria have a much easier time going about their work of using leaf resources for their own needs.  Some infected cells will try to stop the invasion by committing suicide, but the inner defense system is not nearly as effective as the stomata.  We can no longer think of stomata as simple, passive ports of entry for bacteria.  “Surprisingly,” they wrote, “we found that stomatal closure is part of a plant innate immune response to restrict bacterial invasion.”  In the same issue of Cell,3 Schultz-Lefert and Robatzek commented on this discovery, adding that “pathogenic bacteria have evolved strategies to suppress the closure of stomata.”

1Li, Assman and Albert, “Predicting Essential Components of Signal Transduction Networks: A Dynamic Model of Guard Cell Abscisic Acid Signaling,” Public Library of Science: Biology, Volume 4, Issue 10, September 2006.
2Melotto et al., “Plant Stomata Function in Innate Immunity against Bacterial Invasion,” Cell, Volume 126, Issue 5, 8 September 2006, Pages 969-980.
3Schultz-Lefert and Robatzek, “Plant Pathogens Trick Guard Cells into Opening the Gates,” Cell, Volume 126, Issue 5, 8 September 2006, Pages 831-834.

We tricked you by posing this as a contest between good and evil, between peace-loving leaf cells and dastardly bacteria up to no good.  Metaphors bewitch you, remember? (see 07/04/2003).  Plants and bacteria are not sentient beings.  We should liberate our minds from the tendency to view these ecological interactions in anthropomorphic terms.  The converse is not true; human beings are sentient moral agents; no one should take this commentary as support for viewing terrorism as a natural regulatory response to civilization, for instance.  But it is possible that bacteria act as a counterbalance in the overall ecology.  Nature is filled with counterbalances, with accelerator pedals and brakes, with promoters and terminators.  Bacteria invading a leaf may look to us like selfish invaders, but what if they have a role to play, preventing a plant community from growing beyond its resources?  Many bacterial invasions occur after periods of high humidity or drenching rainstorms.  It’s possible to look at the ecological community as a well-regulated system of checks and balances, responding to perturbations in a way that ensures the long-term survival of the whole.  Most of the time, it works.  Plant communities endure despite major geological and climatic changes.  Clearly, things get out of balance sometimes, but maybe that was not the original intent of these well-regulated systems in the original creation.  We don’t need to resort to the evolutionary selfishness metaphors.  We should not personify bacteria, speculating that they “have evolved strategies” to get their own way.  Maybe they’re just doing the best job they can in a messed-up world.
    The important point of these articles is not in some moral anthropomorphism, but in the realization that here is another example of an interrelated, regulated system that could never have evolved by some unguided processes.  Stomata may have looked like simple pores to earlier scientists; now we know that there is a whole network of regulators and detectors, composed of at least 40 parts, that work together to ensure the proper functioning and security of the photosynthetic factories on which all multicellular life depends.  This has been the pattern of scientific discovery ever since the discovery of DNA.  No matter where you look, life is much more sophisticated than one could have imagined.
    An evolutionary astrobiologist was heard today commenting on the arrangement of cells in leaves.  He pointed out that not only are individual leaf cells optimized to filter in the solar wavelengths most useful for photosynthesis, but that they are stacked in formations that act as waveguides, funneling in the vital green wavelengths while reflecting and passing through the infrared wavelengths that would otherwise overheat the power generators.  In other words, here are two separate and independent designs that contribute to the optimization of photosynthesis.  In a declaration of folly astonishing in its dimensions, he exclaimed, without even batting an eye, isn’t it amazing that plants figured this out by themselves!.

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