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  For Shira, Eytan, Noam, and Shani

  Prologue

  In the five years since the publication of the first edition of What a Plant Knows, we’ve seen a blossoming of interest in plant senses. The rate of scientific discovery in plant biology is so fast that this new edition contains groundbreaking information that completely contradicts conclusions made in the first. Both the scientific community and the popular press have moved well beyond the pseudoscience that characterized so much of the early interest in plant senses that established plant scientists railed against. And in an age of growing national isolationism, the global interest in how plants respond to their environment is reassuring. The popularity of What a Plant Knows in Beijing and in Munich, in San Francisco and in Seoul, attests to a universal desire to comprehend our green neighbors.

  And why shouldn’t the interest be universal? After all, we are utterly dependent on plants. We wake up in our house made of wood from the forests of Maine, pour a cup of coffee brewed from coffee beans grown in Brazil, throw on a T-shirt made of Egyptian cotton, print out a report on paper made from eucalyptus trees grown in Tasmania, and drive our kid to school in our car fueled by gasoline derived from cycads that died millions of years ago and with tires made of rubber that was grown in Africa. Chemicals extracted from plants reduce fever (think of aspirin) and treat cancer (Taxol). Wheat sparked the end of one age and the dawn of another, and the humble potato led to mass migrations. And plants continue to inspire and amaze us: the mighty sequoias are the largest singular independent organism on Earth; algae are some of the smallest; and roses definitely make anyone smile.

  My interest in the parallels between plant and human senses got its start when I was a young postdoctoral fellow at Yale University in the 1990s. I was interested in studying a biological process specific to plants and not connected to human biology (probably as a response to the six other doctors in my family, all of whom are physicians). Hence I was drawn to the question of how plants use light to regulate their development. In my research, I discovered a unique group of genes necessary for a plant to determine if it’s in the light or in the dark. Much to my surprise and against all of my plans, I later discovered that this same group of genes is also part of the human DNA. This led to the obvious question as to what these seemingly “plant-specific” genes do in people. Many years later and after much research, we now know that these genes not only are conserved between plants and animals but also regulate (among other developmental processes) responses to light in both!

  This led me to realize that the genetic difference between plants and animals is not as significant as I had once believed. I began to question the parallels between plant and human biology even as my own research evolved from studying plant responses to light to leukemia in fruit flies. What I discovered was that while there’s no plant that knows how to say “Feed me, Seymour!” there are many plants that “know” quite a bit.

  Indeed, we tend not to pay much attention to the immensely sophisticated sensory machinery in the flowers and trees that can be found right in our own backyards. While most animals can choose their environments, seek shelter in a storm, search for food and a mate, or migrate with the changing seasons, plants must be able to withstand and adapt to constantly changing weather, encroaching neighbors, and invading pests, without being able to move to a better environment. Because of this, plants have evolved complex sensory and regulatory systems that allow them to modulate their growth in response to ever-changing conditions. An elm tree has to know if its neighbor is shading it from the sun so that it can find its own way to grow toward the light that’s available. A head of lettuce has to know if there are ravenous aphids about to eat it up so that it can protect itself by making poisonous chemicals to kill the pests. A Douglas fir tree has to know if whipping winds are shaking its branches so that it can grow a stronger trunk. Cherry trees have to know when to flower.

  On a genetic level, plants are more complex than many animals, and some of the most important discoveries in all of biology came from research carried out on plants. Robert Hooke first discovered cells in 1665 while studying cork in the early microscope he built. In the nineteenth century, Gregor Mendel worked out the principles of modern genetics using pea plants, and in the mid-twentieth century Barbara McClintock used Indian corn to show that genes can transpose, or jump. We now know that these “jumping genes” are a characteristic of all DNA and are intimately connected to cancer in humans. And while we recognize that Darwin was a founding father of modern evolutionary theory, some of his most important findings were in plant biology specifically, and we’ll see quite a few of these in the pages of this book.

  Clearly, my use of the word “know” is unorthodox. Plants don’t have a central nervous system; a plant doesn’t have a brain that coordinates information for its entire body. Yet different parts of a plant are intimately connected, and information regarding light, chemicals in the air, and temperature is constantly exchanged between roots and leaves, flowers and stems, to yield a plant that is optimized for its environment. We can’t equate human behavior to the ways in which plants function in their worlds, but I ask that you humor me while I use terminology throughout the book that is usually reserved for human experience. When I explore what a plant sees or what it smells, I am not claiming that plants have eyes or noses (or a brain that colors all sensory input with emotion). But I believe this terminology will help challenge us to think in new ways about sight, smell, what a plant is, and ultimately what we are.

  My book is not The Secret Life of Plants; if you’re looking for an argument that plants are just like us, you won’t find it here. As the renowned plant physiologist Arthur Galston pointed out back in 1974 during the height of interest in this extremely popular but scientifically anemic book, we must be wary of “bizarre claims presented without adequate supporting evidence.” Worse than leading the unwary reader astray, The Secret Life of Plants led to scientific fallout that stymied important research on plant behavior as scientists became wary of any studies that hinted at parallels between animal senses and plant senses.

  In the more than four decades since The Secret Life of Plants caused a great media stir, the depth at which scientists understand plant biology has increased immensely. In What a Plant Knows, I will explore the latest research in plant biology and argue that plants do indeed have senses. By no means is this book an exhaustive and complete review of what modern science has to say about plant senses; that would necessitate a textbook inaccessible to all but the most dedicated readers. Instead, in each chapter I highlight a human sense and compare what the sense is for people and what it is for plants. I describe how the sensory information is perceived, how it is processed, what the ecological implications of the sense are for a plant. And in each chapter I’ll present both a historical perspective and a modern look at the topic.

  Knowing what plants do for us, why not take a mo
ment to find out more about what scientists have found out about them? Let’s embark on our journey to explore the science behind the inner lives of plants. We’ll start by uncovering what plants really see while they’re hanging out in the backyard.

  ONE

  What a Plant Sees

  She 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, from the right, or from above. They know if another plant 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 always oriented 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 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 that processes 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 Botanist

  It’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 their bending 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.

  Canary grass (Phalaris canariensis)

  This led them to question which part of the plant saw the light. The Darwins carried out what has become a classic experiment in 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:

  Summary of Darwin’s experiments on phototropism

  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 se
edlings 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 the plant 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 Growing

  Several 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, could 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.