Why Leaves Turn Red Pigments called anthocyanins probably protect leaves from light damage by direct shielding and by scavenging free radicals David W. Lee and Kevin S. Gould any forests, like those spread the forest’s 70 percent of tree species gave them their name, deriving antho- Mthroughout New England, have that contain anthocyanin pigments cyanin from the Greek anthos, meaning just changed color in a spectacular (which produce colors ranging from flower, and kyanos, meaning blue. way, as they do each fall. The phenom- brown to red, depending on how Many long-standing misconceptions enon is familiar as well as dramatic, yet much chlorophyll the leaves retain), about anthocyanin function date from why it should happen has been a long- the story is quite different. For exam- these early observations, notably that standing enigma. When we were in ple, the brilliant fall foliage of the red these pigments arise from the break- school, the standard textbooks said oak (Quercus rubra) results from the ac- down of chlorophyll during autumn. that foliage changes color because the cumulation of anthocyanin in the vac- Given how striking and attractive breakdown of green chlorophyll mole- uoles (large, fluid-filled cavities) of red foliage is, it may seem baffling that cules unmasks other pigments, like the cells lying just under the leaves’ upper botanists remained ignorant about the yellow-to-orange xanthophylls and the epidermis layer. phenomenon for so long. There are red-or-blue anthocyanins, which, we Anthocyanins are elaborate pigment various reasons for this. First, because were told, serve no particular function molecules, widespread among land anthocyanins are responsible for the during the autumn senescence of plants. They account not only for the colors of fruits and flowers as well as of leaves. Now botanists know better. autumn hues of temperate woodlands, leaves, it was natural to concentrate on Indeed, a completely new apprecia- but also for the flushes of developing pigmentation in the former economi- tion for these colorful pigments has de- red foliage seen in tropical forests, on cally important organs, for which the veloped over the past decade or so, in the undersurface of shaded leaves and function of anthocyanin seems obvi- part from our studies of trees in the in crop plants suffering drought or nu- ous—to attract animals for pollination Harvard Forest, a nature sanctuary in trient deficiency. But plants can also and seed dispersal. Second, because central Massachusetts maintained for have other red pigments. Carotenoids, the discoveries of Richard Willstätter scientific research. There, during Sep- often rhodoxanthin, produce red color and his colleagues about the molecu- tember and October, one sees the in the senescing leaves of some conifers lar structure of anthocyanins from 1912 leaves on dozens of woody species as well as in the common box (Buxus to 1916 were made shortly after the re- changing color. In some plants, such as sempervirens), which decorates many discovery of Mendel’s laws of inheri- the witch hazel (Hamamelis virginiana), suburban lawns. Betalain pigments tance, the anthocyanins became an ear- it is indeed the loss of chlorophyll that color leaves red in a single order of ly subject of research in molecular reveals yellow carotenoid pigments, flowering plants, and a few other mis- genetics, rather than physiology. just as the textbooks say. However, for cellaneous pigments produce bur- (Mendel’s peas had distinctively col- gundy hues in very rare cases. But of ored flowers because of anthocyanins.) David Lee is a professor in the Department of Bio- all the red pigments, the anthocyanins Third, the discovery that light can in- logical Sciences at Florida International Universi- are the most widespread. duce anthocyanin production inspired ty and Research Collaborator at Fairchild Tropical We have collaborated in studying an- molecular biologists to study how light Garden in Miami. He has studied leaf color and thocyanin pigments since 1993 and are exposure activates genes involved in function since 1973. He received his Ph.D. in beginning to develop some working anthocyanin synthesis, again at the ex- botany from Rutgers University in 1970. Kevin hypotheses about their function. It’s cu- pense of research into anthocyanin Gould is an associate professor in the School of Bi- rious that an understanding has been function. ological Sciences at the University of Auckland in so long in coming, given the fact these Botanists of the late 19th-century, most New Zealand. He received his Ph.D. in botany red pigments have been subjected to notably the Germans who studied plant from the University of Manchester in 1985. He has applied his background in plant cell and devel- scientific scrutiny for nearly 200 years. anatomy and physiology, noticed that opmental biology to the mysteries of the functional anthocyanin production rises when a ecology of New Zealand’s diverse plants. Address The Discovery of Anthocyanins plant is subjected to low temperatures for Lee: Department of Biological Sciences, Florida Anthocyanins had been observed for and high light conditions. This observa- International University, Miami, FL 33199. Inter- centuries as “colored cell sap.” In 1835 tion led to the popular explanations that net: [email protected] the German botanist Ludwig Marquart anthocyanins protect the photosynthetic ©Sigma Xi, The Scientific Research Society. Reproduction with 524 American Scientist, Volume 90 permission only. Contact [email protected]. Figure 1. Anthocyanins are common in the autumn leaves of mid-latitude trees, but these pigments also add flashes of red color to the foliage of tropical forests and to crop plants exposed to drought or nutrient deficiency. Occasionally, anthocyanins are present in leaves year-round, as in the variegated leaves of Horopito (Pseudowintera colorata), a common tree in New Zealand forests (above). The patterns of coloration in this species make the leaves ideal for studying the antioxidant properties of these intriguing molecules. (Except where noted, all photographs by the authors.) structures against intense sunlight and Red Sunscreen variety of factors can contribute to help to warm leaves by increasing their When surroundings are bright and photoinhibition: intense sunlight; low rates of metabolism. These scientists cold, photosynthetic efficiency often temperature; acclimation of leaves to lacked the instrumentation and detailed declines. The phenomenon, known as extreme shade with a subsequent ex- knowledge of photosynthesis to test their photoinhibition, has been attributed in posure to high light; and inadequate ideas. In the mid-20th century, investiga- part to impairment in one of the func- phosphorus, which is important in the tors became aware that ultraviolet (UV) tional elements of photosynthesis. Nor- production of two energy-rich com- radiation could induce anthocyanin syn- mally, two units consisting of pig- pounds crucial for photosynthesis— thesis, leading to the hypothesis that an- ments, proteins and electron-transfer adenosine triphosphate (ATP) and the thocyanins protect plant tissues against molecules—known as photosystems I reduced form of nicotinamide adenine UV damage. But, as it turns out, antho- and II—absorb light energy. Photoinhi- dinucleotide phosphate (NADPH). cyanins absorb rather weakly in the UV- bition apparently involves a block in When chloroplasts are overwhelmed B region of the spectrum (wavelengths photosystem II. Unchecked, this im- with energy, the excess causes chemical of 285–320 nanometers), which is most pairment can permanently damage and, ultimately, physical damage. responsible for damage to biological tis- chloroplasts, cells and tissues. Plants have evolved several strate- sues; other colorless flavonoid pigments Investigators can observe photoinhi- gies to prevent photoinhibitory damage that are equally, or more, abundant in the bition because when photosynthetic tis- from intense light, in particular the in- leaves absorb UV-B much more strongly. sues receive a pulse of intense light, terconversion of certain xanthophyll Furthermore, anthocyanins are most they immediately emit a pulse of visi- pigments as a way of quenching the commonly produced in the interiors of ble light—that is, they fluoresce. De- overload of energy. Anthocyanins also leaves and hence are poorly placed to tailed analysis of this flash reveals efficiently protect against photoinhibi- protect leaves from the widespread ef- much about photosynthetic function. tion because they soak up radiant ener- fects of UV-B. These weaknesses were re- New techniques to measure this fluo- gy at wavelengths poorly absorbed by futed by one of us (Lee) in 1987. So what rescence have helped investigators test other accessory pigments, such as in good are anthocyanins to a leaf? Two re- the efficiency of the light reaction of the green waveband at around 530 cent discoveries have shed light on the photosynthesis under different condi- nanometers. In intact tissues, the range mystery. tions and to detect photoinhibition. A of absorbance also extends into shorter ©Sigma Xi, The Scientific Research Society. Reproduction with permission only. Contact [email protected]. 2002 November–December 525 Figure 2. Some senescing autumn leaves, such as the witch hazel (Hamamelis virginiana, left) are yellow. A transverse section of a leaf (right) shows that the yellow pigments are clustered exclusively in the chloroplasts, which are degrading. The loss of chlorophyll reveals