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"Enough absorbing science to concede that plants continue to inspire and amaze us." The Wall Street Journal How does a Venus flytrap know when to snap shut? Can it feel an insect's tiny, spindly legs? And how do cherry blossoms know when to bloom? Can they remember the weather? For centuries we have marveled at plant diversity and formfrom Charles Darwin's early fascination with stems to Seymour Krelborn's distorted doting in Little Shop of Horrors. But now, in What a Plant Knows, the renowned biologist Daniel Chamovitz presents an intriguing and scrupulous look at how plants themselves experience the worldfrom the colors they see to the schedules they keep. Highlighting the latest research in genetics and more, he takes us into the inner lives of plants and draws parallels with the human senses to reveal that we have much more in common with sunflowers and oak trees than we may realize. Chamovitz shows how plants know up from down, how they know when a neighbor has been infested by a group of hungry beetles, and whether they appreciate the Led Zeppelin you've been playing for them or if they're more partial to the melodic riffs of Bach. Covering touch, sound, smell, sight, and even memory, Chamovitz encourages us to consider whether plants might even be aware. A rare inside look at what life is really like for the grass we walk on, the flowers we sniff, and the trees we climb, What a Plant Knowsoffers us a greater understanding of science and our place in nature.

Daniel Chamovitz, Ph.D., is the director of the Manna Center for Plant Biosciences at Tel Aviv University. He has served as a visiting scientist at Yale University and at the Fred Hutchinson Cancer Research Center, and has lectured at universities around the world. His research has appeared in leading scientific journals. Chamovitz lives with his wife and three children in Hod HaSharon, Israel.

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What a Plant Knows
ONEWhat a Plant SeesShe turns, always, towards the sun, though her roots hold her fast, and, altered, loves unaltered.--Ovid, Metamorphoses

Think about this: plants see you.In fact, plants monitor their visible environment all the time. Plants see if you come near them; they know when you stand over them. They even know if you're wearing a blue or a red shirt. They know if you've painted your house or if you've moved their pots from one side of the living room to the other.Of course plants don't "see" in pictures as you or I do. Plants can't discern between a slightly balding middle-aged man with glasses and a smiling little girl with brown curls. But they do see light in many ways and colors that we can only imagine. Plants see the same ultraviolet light that gives us sunburns and infrared light that heats us up. Plants can tell when there's very little light, like from a candle, or when it's the middle of the day, or when the sun is about to set into the horizon. Plants know if the light is coming from the left, the right, or from above. They know if anotherplant has grown over them, blocking their light. And they know how long the lights have been on.So, can this be considered "plant vision"? Let's first examine what vision is for us. Imagine a person born blind, living in total darkness. Now imagine this person being given the ability to discriminate between light and shadow. This person could differentiate between night and day, inside and outside. These new senses would definitely be considered rudimentary sight and would enable new levels of function. Now imagine this person being able to discern color. She can see blue above and green below. Of course this would be a welcome improvement over darkness or being able to discern only white or gray. I think we can all agree that this fundamental change--from total blindness to seeing color--is definitely "vision" for this person.Merriam-Webster's defines "sight" as "the physical sense by which light stimuli received by the eye are interpreted by the brain and constructed into a representation of the position, shape, brightness, and usually color of objects in space." We see light in what we define as the "visual spectra." Light is a common, understandable synonym for the electromagnetic waves in the visible spectrum. This means that light has properties shared with all other types of electrical signals, such as micro- and radio waves. Radio waves for AM radio are very long, almost half a mile in length. That's why radio antennas are many stories tall. In contrast, X-ray waves are very, very short, one trillion times shorter than radio waves, which is why they pass so easily through our bodies.Light waves are somewhere in the middle, between 0.0000004 and 0.0000007 meter long. Blue light is the shortest, while red light is the longest, with green, yellow, and orange in the middle. (That's why the color pattern of rainbows is alwaysoriented in the same direction--from the colors with short waves, like blue, to the colors with long waves, like red.) These are the electromagnetic waves we "see" because our eyes have special proteins called photoreceptors that know how to receive this energy, to absorb it, the same way that an antenna absorbs radio waves.The retina, the layer at the back of our eyeballs, is covered with rows and rows of these receptors, sort of like the rows and rows of LEDs in flat-screen televisions or sensors in digital cameras. Each point on the retina has photoreceptors called rods, which are sensitive to all light, and photoreceptors called cones, which respond to different colors of light. Each cone or rod responds to the light focused on it. The human retina contains about 125 million rods and 6 million cones, all in an area about the size of a passport photo. That's equivalent to a digital camera with a resolution of 130 megapixels. This huge number of receptors in such a small area gives us our high visual resolution. For comparison, the highest-resolution outdoor LED displays contain only about 10,000 LEDs per square meter, and common digital cameras have a resolution of only about 8 megapixels.Rods are more sensitive to light and enable us to see at night and under low-light conditions but not in color. Cones allow us to see different colors in bright light since cones come in three flavors--red, green, and blue. The major difference between these different photoreceptors is the specific chemical they contain. These chemicals, called rhodopsin in rods and photopsins in cones, have a specific structure that enables them to absorb light of different wavelengths. Blue light is absorbed by rhodopsin and the blue photopsin; red light by rhodopsin and the red photopsin. Purple light is absorbed by rhodopsin, blue photopsin, and red photopsin, but not green photopsin, and so on. Once the rod or cone absorbs the light, it sends a signal to the brain thatprocesses all of the signals from the millions of photoreceptors into a single coherent picture.Blindness results from defects at many stages: from light perception by the retina due to a physical problem in its structure; from the inability to sense the light (because of problems in the rhodopsin and photopsins, for example); or in the ability to transfer the information to the brain. People who are color-blind for red, for example, don't have any red cones. Thus the red signals are not absorbed and passed on to the brain. Human sight involves cells that absorb the light, and the brain then processes this information, which we in turn respond to. So what happens in plants?Darwin the BotanistIt's not widely known that for the twenty years following his publication of the landmark On the Origin of Species, Charles Darwin conducted a series of experiments that still influence research in plants to this day.Darwin was fascinated by the effects of light on plant growth, as was his son Francis. In his final book, The Power of Movement in Plants, Darwin wrote: "There are extremely few [plants], of which some part ... does not bend toward lateral light." Or in less verbose modern English: almost all plants bend toward light. We see that happen all the time in houseplants that bow and bend toward rays of sunshine coming in from the window. This behavior is called phototropism. In 1864 a contemporary of Darwin's, Julius von Sachs, discovered that blue light is the primary color that induces phototropism in plants, while plants are generally blind to other colors that have little effect on theirbending toward light. But no one knew at that time how or which part of a plant sees the light coming from a particular direction.In a very simple experiment, Darwin and his son showed that this bending was due not to photosynthesis, the process whereby plants turn light into energy, but rather to some inherent sensitivity to move toward light. For their experiment, the two Darwins grew a pot of canary grass in a totally dark room for several days. Then they lit a very small gas lamp twelve feet from the pot and kept it so dim that they "could not see the seedlings themselves, nor see a pencil line on paper." But after only three hours, the plants had obviously curved toward the dim light. The curving always occurred at the same part of the young plant, an inch or so below the tip.This led them to question which part of the plant saw the light. The Darwins carried out what has become a classic experimentin botany. They hypothesized that the "eyes" of the plant were found at the seedling tip and not at the part of the seedling that bends. They checked phototropism in five different seedlings, illustrated by the following diagram:a. The first seedling was untreated and shows that the conditions of the experiment are conducive to phototropism.b. The second had its tip pruned off.c. The third had its tip covered with a lightproof cap.d. The fourth had its tip covered with a clear glass cap.e. The fifth had its middle section covered by a lightproof tube.They carried out the experiment on these seedlings in the same conditions as their initial experiment, and of course the untreated seedling bent toward the light. Similarly, the seedling with the lightproof tube around its middle (see e above) bent toward the light. If they removed the tip of a seedling, however, or covered it with a lightproof cap, it went blind and couldn't bend toward the light. Then they witnessed the behavior of theplant in scenario four (d): this seedling continued to bend toward the light even though it had a cap on its tip. The difference here was that the cap was clear. The Darwins realized that the glass still allowed the light to shine onto the tip of the plant. In one simple experiment, published in 1880, the two Darwins proved that phototropism is the result of light hitting the tip of a plant's shoot, which sees the light and transfers this information to the plant's midsection to tell it to bend in that direction. The Darwins had successfully demonstrated rudimentary sight in plants.Maryland Mammoth: The Tobacco That Just Kept GrowingSeveral decades later, a new tobacco strain cropped up in the valleys of southern Maryland and reignited interest in the ways that plants see the world. These valleys have been home to some of America's greatest tobacco farms since the first settlers arrived at the end of the seventeenth century. Tobacco farmers, learning from the Native tribes such as the Susquehannock, who had grown tobacco for centuries, would plant their crop in the spring and harvest it in late summer. Some of the plants weren't harvested for their leaves and made flowers that provided the seed for the next year's crop. In 1906, farmers began to notice a new strain of tobacco that never seemed to stop growing. It could reach fifteen feet in height, produce almost a hundred leaves, and would only stop growing when the frosts set in. On the surface, such a robust, ever-growing plant would seem a boon to tobacco farmers. But as is so often the case, this new strain, aptly named Maryland Mammoth, was like the two-faced Roman god Janus. On the one hand, it never stopped growing; on the other,it rarely flowered, meaning farmers couldn't harvest seed for the next year's crop.In 1918, Wightman W. Garner and Harry A. Allard, two scientists at the U.S. Department of Agriculture, set out to determine why Maryland Mammoth didn't know when to stop making leaves and start making flowers and seeds instead. They planted the Maryland Mammoth in pots and left one group outside in the fields. The other group was put in the field during the day but moved to a dark shed every afternoon. Simply limiting the amount of light the plants saw was enough to cause Maryland Mammoth to stop growing and start flowering. In other words, if Maryland Mammoth was exposed to the long days of summer, itwould keep growing leaves. But if it experienced artificially shorter days, then it would flower.This phenomenon, called photoperiodism, gave us the first strong evidence that plants measure how much light they take in. Other experiments over the years have revealed that many plants, just like the Mammoth, flower only if the day is short; they are referred to as "short-day" plants. Such short-day plants include chrysanthemums and soybeans. Some plants need a long day to flower; irises and barley are considered "long-day" plants. This discovery meant that farmers could now manipulate flowering to fit their schedules by controlling the light that a plant sees. It's not surprising that farmers in Florida soon figured out that they could grow Maryland Mammoth for many months (without the effects of frost encountered in Maryland) and that the plants would eventually flower in the fields in midwinter when the days were shortest.What a Difference a (Short) Day MakesThe concept of photoperiodism sparked a rush of activity among scientists who were brimming with follow-up questions: Do plants measure the length of the day or the night? And what color of light are plants seeing?Around the time of World War II, scientists discovered that they could manipulate when plants flowered simply by quickly turning the lights on and off in the middle of the night. They could take a short-day plant like the soybean and keep it from making flowers in short days if they turned on the lights for only a few minutes in the middle of the night. On the other hand, the scientists could cause a long-day plant like the iris to makeflowers even in the middle of the winter (during short days, when it shouldn't normally flower), if in the middle of the night they turned on the lights for just a few moments. These experiments proved that what a plant measures is not the length of the day but the length of the continuous period of darkness.Using this technique, flower farmers can keep chrysanthemums from flowering until just before Mother's Day, which is the optimal time to have them burst onto the spring flower scene. Chrysanthemum farmers have a problem since Mother's Day comes in the spring but the flowers normally blossom in the fall as the days get shorter. Fortunately, chrysanthemums grown in greenhouses can be kept from flowering by turning on the lights for a few minutes at night throughout the fall and winter. Then ... boom ... two weeks before Mother's Day, the farmers stop turning on the lights at night, and all the plants start to flower at once, ready for harvest and shipping.These scientists were curious about the color of light that the plants saw. What they discovered was surprising: the plants, and it didn't matter which ones were tested, only responded to a flash of red during the night. Blue or green flashes during the night wouldn't influence when the plant flowered, but only a few seconds of red would. Plants were differentiating between colors: they were using blue light to know which direction to bend in and red light to measure the length of the night.Then, in the early 1950s, Harry Borthwick and his colleagues in the USDA lab where Maryland Mammoth was first studied made the amazing discovery that far-red light--light that has wavelengths that are a bit longer than bright red and is most often seen, just barely, at dusk--could cancel the effect of the red light on plants. Let me spell this out more clearly: if you takeirises, which normally don't flower in long nights, and give them a shot of red light in the middle of the night, they'll make flowers as bright and as beautiful as any iris in a nature preserve. But if you shine far-red light on them right after the pulse of red, it's as if they never saw the red light to begin with. They won't flower. If you then shine red light on them after the far-red, they will. Hit them again with far-red light, and they won't. And so on. We're also not talking about lots of light; a few seconds of either color is enough. It's like a light-activated switch: The red light turns on flowering; the far-red light turns it off. If you flip the switch back and forth fast enough, nothing happens. On a more philosophical level, we can say that the plant remembers the last color it saw.By the time John F. Kennedy was elected president, Warren L. Butler and colleagues had demonstrated that a single photoreceptor in plants was responsible for both the red and the far-red effects. They called this receptor "phytochrome," meaning "plant color." In its simplest model, phytochrome is the light-activated switch. Red light activates phytochrome, turning it into a form primed to receive far-red light. Far-red light inactivates phytochrome, turning it into a form primed to receive red light. Ecologically, this makes a lot of sense. In nature, the last light any plant sees at the end of the day is far-red, and this signifies to the plant that it should "turn off." In the morning, it sees red light and it wakes up. In this way a plant measures how long ago it last saw red light and adjusts its growth accordingly. Exactly which part of the plant sees the red and far-red light to regulate flowering?We know from Darwin's studies of phototropism that the "eye" of a plant is in its tip while the response to the light occursin the stem. So we might conclude, then, that the "eye" for photoperiodism is also in the tip of the plant. Surprisingly, this isn't the case. If in the middle of the night you shine a beam of light on different parts of the plant, you discover that it's sufficient to illuminate any single leaf in order to regulate flowering in the entire plant. On the other hand, if all the leaves are pruned, leaving only the stem and the apex, the plant is blind to any flashes of light, even if the entire plant is illuminated. If the phytochrome in a single leaf sees red light in the middle of the night, it's as if the entire plant were illuminated. Phytochrome in the leaves receives the light cues and initiates a mobile signal that propagates throughout the plant and induces flowering.Blind Plants in the Age of GeneticsWe have four different types of photoreceptors in our eyes: rhodopsin for light and shadows, and three photopsins for red, blue, and green. We also have a fifth light receptor called cryptochrome that regulates our internal clocks. So far we've seen that plants also have multiple photoreceptors: they see directional blue light, which means they must have at last one blue-light photoreceptor, now known as phototropin, and they see red and far-red light for flowering, which points to at least one phytochrome photoreceptor. But in order to determine just how many photoreceptors plants possess, scientists had to wait for the era of molecular genetics, which began several decades after the discovery of phytochrome.The approach spearheaded in the early 1980s by Maarten Koornneef at Wageningen University in Holland, and repeated and refined in numerous labs, used genetics to understand plantsight. Koornneef asked a simple question: What would a "blind" plant look like? Plants grown in darkness or dim light are taller than those grown in bright light. If you ever took care of bean sprouts for a sixth-grade science experiment, you'd know that the plants in the hall closet grew up tall, spindly, and yellow, but the ones out on the playground were short, vigorous, and green. This makes sense because plants normally elongate in darkness, when they're trying to get out of the soil into the light or when they're in the shade and need to make their way to the unobstructed light. If Koornneef could find a blind mutant plant, perhaps it would be tall in bright light as well. If he could identify and grow blind mutant plants, he would be able to use genetics to figure out what was wrong with them.He carried out his experiments on Arabidopsis thaliana, a small laboratory plant similar to wild mustard. He treated a batch of arabidopsis seeds with chemicals known to induce mutations in DNA (and also cause cancer in laboratory rats) and then grew the seedlings under various colors of light and looked for mutant seedlings that were taller than the others. He found many of them. Some of the mutant plants grew taller under blue light, but were of normal height when grown under red light. Some were taller under red light but normal under blue. Some were taller under UV light but normal under all other kinds, and some were taller under red and blue lights. A few were taller only under dim light, while others were taller only under bright-light conditions.Many of these mutants that were blind to specific colors of light were defective in the particular photoreceptors that absorb the light. A plant that had no phytochrome grew in red light as if it were in the dark. Surprisingly, a few of the photoreceptors came in pairs, with one being specific for dim light and the otherspecific for bright light. To make a long and complex story short, we now know that arabidopsis has at least eleven different photoreceptors: some tell a plant when to germinate, some tell it when to bend to the light, some tell it when to flower, and some let it know when it's nighttime. Some let the plant know that there's a lot of light hitting it, some let it know that the light is dim, and some help it keep time.1So plant vision is much more complex than human sight at the level of perception. Indeed, light for a plant is much more than a signal; light is food. Plants use light to turn water and car-bondioxide into sugars that in turn provide food for all animals. But plants are sessile, unmoving organisms as well. They are literally rooted in one place, unable to migrate in search of food. To compensate for this sessile life, plants must have the ability to find their food--to seek out and capture light. That means they need to know where the light is, and rather than moving toward the food, as an animal would, a plant grows toward its food.A plant needs to know if another plant has grown above it, filtering out the light for photosynthesis. If a plant senses that it is in the shade, it will start growing faster to get out. And plants need to survive, which means they need to know when to "hatch" out of their seeds and when to reproduce. Many types of plants start growing in the spring, just as many mammals give birth then. How do plants know when the spring has started? Phytochrome tells them that the days are getting progressively longer. Plants also flower and set seed in the fall before the snow comes. How do they know it's autumn? Phytochrome tells them that the nights are getting longer.What Plants and Humans SeePlants must be aware of the dynamic visual environment around them in order to survive. They need to know the direction, amount, duration, and color of light to do so. Plants undoubtedly detect visible (and invisible) electromagnetic waves. While we can detect electromagnetic waves in a relatively tight spectrum, plants detect ones that are both shorter and longer than those we can detect. Although plants see a much larger spectrum than we do, they don't see in pictures. Plants don't have a nervous system that translates light signals into pictures. Instead, they translatelight signals into different cues for growth. Plants don't have eyes, just as we don't have leaves.2But we can both detect light.Sight is the ability not only to detect electromagnetic waves but also the ability to respond to these waves. The rods and cones in our retinas detect the light signal and transfer this information to the brain, and we respond to the information. Plants are also able to translate the visual signal into a physiologically recognizable instruction. It wasn't enough that Darwin's plants saw the light in their tips; they had to absorb this light and then somehow translate it into an instruction that told the plant to bend. They needed to respond to the light. The complex signals arising from multiple photoreceptors allow a plant to optimally modulate its growth in changing environments, just as our four photoreceptors allow our brains to make pictures that enable us to interpret and respond to our changing environments.To put things in a broader perspective: plant phytochrome and human red photopsin are not the same photoreceptor; while they both absorb red light, they are different proteins with different chemistries. What we see is mediated through photoreceptors found only in other animals. What a daffodil sees is mediated through photoreceptors found only in plants. But the plant and human photoreceptors are similar in that they all consist of a protein connected to a chemical dye that absorbs the light; these are the physical limitations required for a photoreceptor to work.But there are exceptions to every rule, and despite billions of years of independent evolution plant and animal visual systems do have some things in common. Both animals and plants con-tainblue-light receptors called cryptochromes.3 Cryptochrome has no effect on phototropism in plants, but it plays several other roles in regulating plant growth, one of which is its control over a plant's internal clock. Plants, like animals, have an internal clock called the "circadian clock" that is in tune with normal day-night cycles. In our case, this internal clock regulates all parts of our life, from when we're hungry, when we have to go to the bathroom, when we're tired, and when we feel energetic. These daily changes in our body's behavior are called circadian rhythms, because they continue on a roughly twenty-four-hour cycle even if we keep ourselves in a closed room that never gets sunlight. Flying halfway around the world puts our circadian clock out of sync with the day-night signals, a phenomenon we call jet lag. The circadian clock can be reset by light, but this takes a few days. This is also why spending time outside in the light helps us recover from jet lag faster than spending time in a dark hotel room.Cryptochrome is the blue-light receptor primarily responsible for the resetting of our circadian clocks by light. Cryptochrome absorbs blue light and then signals the cell that it's daytime. Plants also have internal circadian clocks that regulate many plant processes, including leaf movements and photosyn-thesis.If we artificially change a plant's day-night cycle, it also goes through jet lag (but doesn't get grumpy), and it takes a few days for it to readjust. For example, if a plant's leaves normally close in the late afternoon and open in the morning, reversing its light-dark cycle will initially lead to its leaves opening in the dark (at the time that used to be day) and closing in the light (at the time that used to be night). This opening and closing of leaves will readjust to the new light-dark patterns within a few days.The plant cryptochrome, just like the cryptochrome in fruit flies and mice, has a major role in coordinating external light signals with the internal clock. At this basic level of blue-light control of circadian rhythms, plants and humans "see" in essentially the same way. From an evolutionary perspective, this amazing form of conservation of cryptochrome function is actually not so surprising. Circadian clocks developed early in evolution in single-celled organisms, before the animal and the plant kingdoms split off. These original clocks probably functioned to protect the cells from damage induced by high UV radiation. In this early clock, an ancestral cryptochrome monitored the light environment and relegated cell division to the night. Relatively simple clocks are even found today in most single-celled organisms, including bacteria and fungi. The evolution of light perception continued from this one common photoreceptor in all organisms and diverged into the two distinct visual systems that distinguish plants from animals. What may be more surprising, though, is that plants also smell ...Copyright © 2012 by Daniel Chamovitz

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What a Plant Knows A Field Guide to the Senses

What a Plant Knows A Field Guide to the Senses

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