A Volatile Environment – Plant communication that makes scents
Gardens are considered quiet spaces where we can retire to for relaxation and rejuvenation. As a gardener, I don't often actually take the time to sit and meditate in the garden, but I try to enjoy the serenity plants project. One aspect of plants I particularly delight in are plants scents, or fragrances (Russian sage excepted), whether I'm just among them or working around the plants.
However, recent studies have called into question whether nature operates under sylvan harmony or whether plants are on guard, at alert to attack by pathogens and herbivores, summoning sympathetic armies when needed. Scientists are discovering the complex world of plant communication, mostly centered around plant scents, volatile organic compounds (VOC's sometimes called BVOC's, biogenic volatile organic compounds).
VOC's are organic molecules that are often in a liquid state within the plant's cells, and evaporate easily when exposed to the air; that is, they are volatile. Fragrances, scents and odors are called volatile organic compounds because of the multitude combinations of carbon atom compounds. VOC's becomes noticeable and often recognizable to us as a fragrance when exposed to air, when breaking or crushing mint leaves or pine needles. The weekly routine of cutting the grass releases volatile organic compounds (green leaf volatiles) into the air, a scent we are all pleasantly familiar. (Pichersky, Plant Scents.)
The first plant volatile, ethylene, was discovered over 70 years ago. Plants emit organic volatile molecules all the time from all parts of the plant, even the roots, although our noses may not be able to detect these small quantities. Most of the compounds are emitted in minute quantities and disperse quickly when exposed to air. Others aren't released until the plant surface is nicked, damaged or penetrated. Research into plant volatiles was difficult due to the low quantity of molecules released and their volatile nature. VOC's can now be gathered and analyzed with the aid of the scientific instruments, namely, gas chromatographs and mass spectrometers. (Pichersky, Plant Scents.)
Volatiles – fragrances – are pleasant to us, but many of them are toxic when eaten (in large enough quantities). Volatiles were and continued to be used for their anti-microbial qualities to prevent or retard spoilage and as antiseptics. Phytoncides, volatiles that are harmful to dangerous microbes, are another name for volatiles with potent bactericidal activities. (Plant Biotechnology and Agriculture: Prospects for the 21st Century.) The volatile oils in Oriental spices were heavily relied upon hundreds of years ago by Europeans. When Ottoman Turks cut off the land spice routes in the sixteenth century, European nations roamed the high seas in search of a short maritime spice route, in the process, discovering the New World and eventually, America. (Pichersky, Plant Scents.)
Herbal volatiles are thought to refresh and relieve humans. An activity known as “forest bathing”, called shinrin-yoku in Japan, is said to increase human brain activity and help fight off cancer cells. Promoted by the Forestry Agency in Japan, it is not known if staying and walking for several hours a day causes decreased stress levels due to exercise, because of increased uptake of plant volatiles or whether this is clever marketing by the Forest Agency. However, whenever I take a walk in the forest, I experience increased feelings of well-being, usually while on vacation.
With hands in the soil and nose in the plants, can this be why gardeners are healthier and happier people?
Volatiles – The Language Plants use to Communicate
Volatile organic compounds play a much more important role in the life of the plant than providing pleasing fragrances for humans. Plants produce VOC's for both specific and general functions (or rather, specific functions we haven't yet identified). They beckon pollinators, fend off herbivores and pathogens, summon helpful insect predators and alert other parts of the plants, as well as other plants to the presence of danger. A few plants, notably rosemary and conifers use VOC's to lower air temperature in their immediate vicinity. This sounds like something right out of The Secret Life of Plants! (By Thompkins and Bird.)
There are tens of thousands of VOC's synthesized by plants, over 40,000 and counting. Plant volatiles are the 'words' by which plants communicate with itself and with other plants. Different compounds make up their 'vocabulary'. “The quantities and relative proportions of VOC's in the bouquet emitted by plants allow the plant to send complex signals, which using the linguistic analogy could be described as 'sentences'.” (Holopainen and Blande, Molecular Plant Volatile Communication.) We've discovered their language and are working on the interpretation.
Volatiles are emitted from stored pools throughout plant tissues diurnally or are controlled by circadian clock rhythms. The composition of volatiles changes as the plant matures as well as during all the stages of flowering and seed production. “Environmental factors such as light, temperature and moisture status can greatly influence the emission of volatiles and the yield and composition of essential oils.” (Dudareva, Pickersky and Gershenzon, Biochemistry of Plant Volatiles.) Environmental factors such as air pollution, and global climate changes in temperature, precipitation, land use, concentrations of ozone and atmospheric CO2, and UV radiation most likely impact the synthesizing of VOC's, affecting the plant-pollinator relationships, however, little is yet known on exactly the effect they will have as global warming continues. (Farre-Armengol, Filella, Llusia and Penuelas, Floral Volatile Organic Compounds.)
The role of volatile organic compounds in pollination more closely corresponds to our image of blissful harmony within one's summer garden. Odors, or as we call the pleasant ones, fragrances, are powerful attractants to humans. But they are even more powerful for pollinators for it is their signal for food, much like a flashing neon sign – “Open for Dinner”. Flower color was long thought as the main attractant of pollinators. However, more and more research is focused on the understanding of floral scent and its use by plants in attracting pollinators. Tests with bees have shown that odors, more so than flower color, is the device that brings pollen and pollinator together. It is also the odor, or scent, that is carried back to the hive and communicated to others, rather than directions pertaining to flower color. Learning scents comes much easier and quicker than learning colors or shapes. (Barth, Insects and Flowers.)
“Flowers produce the most diverse and highest amount of volatile compounds, which peak when the flowers are ready for pollination.” (Dudareva, Pickersky and Gershenzon, Biochemistry of Plant Volatiles.) Benzenoids are the VOC's most present in floral scents. Over 85% of the flowering plant species depend on insects for pollination. (Farre-Armengol, Filella, Llusia and Penuelas, Floral Volatile Organic Compounds.) Some scents (VOC's) are used to attract pollinators to the flowers, and once at the flower, directs pollinators to the pollen. The flowers of plants contains olfactory, along with visual guide marks, that help the pollinator to quickly find the pollen. They may be called scent spots, odor gradients, and even odor mosaics. A predominance of flowers employ odor guides to direct their pollinators to the pollen. Different colors or UV patterns have different scents; flowers without these color visual guides have odor guides. (Barth, Insects and Flowers.)
The more strongly scented flowers attract insect pollinators. Birds that pollinate flowers do not have a well developed sense of smell, and the flowers they visit are much less scented. To humans, bird pollinated flowers have no scent. In actuality, they do have scents, just much less, and their pollen is less scented than pollen visited by insects. The complexity of scent in flowers is evident in both the plants and the receptors or scent detectors of the various insects. (Barth, Insects and Flowers.)
Flowers with scents less pleasing and attractive to humans usually are attractive to fly pollinators. Flower scents that attract flies fall into two categories, those that are rich in essential oils, such as the umbelliferous flowers, and those we term having meat aromas (many flies search for meat in which to lay their eggs so that the hatching larvae will have food). A small group of plants with sapromyophilous flowers - flowers that mimic the odor (and sometimes color and texture) of carrion – attract fly pollinators that are deceived into laying eggs on them and accidentally pollinate the flowers as they do so. Clever plants, such as the Stapelia and Amorphophallus titanum play this trick on pollinators.
It has been thought that the release of floral volatiles coincides with the foraging habit of pollinators. Different plants release scents at different times, some predominantly at night, some in the morning, some during the day. It's been shown that bees remember the timing of scent release and come back as often as a plant releases the scent. This is just another circumstance that begs the question, 'which came first'. (Barth, Insects and Flowers.)
Because conservation of energy is always of primary concern to members of both the plant and animal kingdom, the strength and composition of VOC's used to attract pollinators varies from flower to flower, depending on whether the flower and or flowers are completely pollinated. Additionally, the scent of pollen will differ from general flower scent in some flowers. These differing pollen scents may be connected to only attracting insects that will be effective in its pollination, rather than just consuming pollen without pollinating in return. The strength and composition of VOC's also varies depending on the specific pollinator the plants wants to attract. Other volatile compound mixtures act as filters that selects beneficials and deter detrimental insects. If one combination of volatiles fails to attract a pollinator, many plants can try other combinations until pollination is achieved.(Farre-Armengol, Filella, Llusia and Penuelas, Floral Volatile Organic Compounds.)
Once flowers are pollinated, often both the scent will diminish or disappear, and the flower color will change – clear signals to pollinators to move on (perhaps further studies will show relationships between colors and scents?). It is thought this is done to avoid damage of the pollinated flower by too many or too persistent pollinators. The plant's ultimate goal is always to reproduce, not to provide scent or food, or a pretty flower.
Volatiles are an important component of nectar, containing both primary metabolites (sugars and amino acids) and secondary metabolites (alkaloids, phenolics, and nonprotein amino acids that offer both attractant and deterrent effects). (Farre-Armengol, Filella, Llusia and Penuelas, Floral Volatile Organic Compounds).
The world of insects and flowers is a very complex world we are just now gaining a glimpse. Of interest are the relationships between orchid bees and orchid flowers and scents. About ten percent of orchid flowers produce a volatile that is a narcotic to bees and causes intoxication. Apparently, it is a pleasurable experience, as the orchid bees return again and again to sample it. It is thought that bees under the influence take paths they wouldn't normally take, such as sliding down a narrow tube, and in scrambling out, perform the pollination service. (Barth, Insects and Flowers.)
Fending off Herbivores
It is hard to say which is the most important role of VOC's for plants: aiding pollination or defending itself from attack. Plants are firmly rooted in the ground and cannot flee their enemies. To escape some degree of attack by herbivores – insects and larger animals that feed on plants – plants produce a plethora of airborne volatile chemicals used as a defense against an attack, to thwart herbivores once attacked, to signal help when under attack, to self-alert parts of itself that lack a direct chemical pathway to an attack or impending attack, and to signal both plant-clones and non-clone plants of imminent danger. That's a lot of communication!
Herbivore-induced plant volatiles, HIPV's, are emitted by plants when suffering from mechanical injury, injury by herbivory or from pathogens. The volatiles are emitted by all plant vegetative parts: flowers, leaves and roots, and not just from the site of injury. (Dudareva, Pickersky and Gershenzon, Biochemistry of Plant Volatiles.) Lab tests using gas chromatographs and mass spectrometers (GC-MS) reveal the VOC's emitted by mechanical injury differ from the volatiles synthesized when under attack from insects or pathogens.
Terpenes are the largest family of volatiles synthesized and released by plants upon attack. They attract arthropods that prey upon or parasitize herbivores. Some terpenes repel or intoxicate herbivores, and also act in airborne plant-to-plant communication. An example of a well known terpene is the fossilized resin, amber. Amber forms when the trunk of a pine tree is injured, possibly by a beetle. The tree exudes a odoriferous resin composed of mostly terpenes -- hydrocarbons with 10, 15 or 20 carbon atoms and oxygen. The heavier C20 terpenes (diterpenes) are glue like and cover the wound in the process trapping and preserving the intruder, the lighter C10 (monoterpenes) and C15 (sesquiterpenes) are toxic and evaporate into the air. These resin terpenes are stored in resin ducts and are released when the ducts are broken by the beetle; production of terpenes is increased after attack. The purpose of the release of the volatiles in the air is still unknown. (Pichersky, Plant Scents.)
Other volatile compounds released when leaves are damaged are called green leaf volatiles. Green leaf volatiles are released after plant tissue suffers mechanical damage. Volatiles are synthesized by plants at the site from which they are released. Others are produced in the epidermal cells of plant tissues or in the secretory structures. Only a fraction of available compounds are released into the air. (Dudareva, Pickersky and Gershenzon, Biochemistry of Plant Volatiles, and Farre-Armengol, Filella, Llusia and Penuelas, Floral Volatile Organic Compounds.)
Studies have concluded that plants can detect compounds in the oral regurgitant of insect herbivores --plants recognize insects by the compounds they exude. This signals the plant to release its stored volatiles and begins to synthesize more and different compounds to attract predators of the herbivores, different from volatiles produced due to mechanical damage. Some of the volatile blends can contain up to 200 compounds. The synthesis of the signal VOC's may take from a few hours to a few days depending on the plant and VOC needed.
Other plants, such as our bedding geranium, Pelargonium zonale, contain VOC's that are toxic to their predators, in this case, the Japanese beetle, Popillia japonica. After consuming some of the leaf, within 30 minutes, the beetle rolls on its back, paralyzed. The effects of the toxin last for about 24 hours. Beetles rarely resume their eating, as they themselves become prey to their predators while in this defenseless position. (Flores, Geraniums.)
Alerting Plants to Danger
Airborne plant volatiles are emitted to alert other parts of the same plants, plant clones and nearby non-clone plants. Roots also exude volatiles that travel in the rhizosphere. The releasing of volatiles has been equated to a 'cry for help', but its complex nature suggests a more 'eloquent monologue'. (Holopainen and Blande, Molecular Plant Volatile Communication.)
Plants that are damaged by herbavores emit different chemicals or chemical compounds (terpenes) than do plants damaged by mechanical means (green leaf volatiles), and different from undamaged plants. In additional to warding off direct attack by herbivores, plants emit airborne signals about the probability of an attack, referred to as a priming systemic defense, similar to a country raising the terrorist alert level. This “priming prepares the plant or its undamaged parts for accelerated defense but delays the response until the actual attack.” (Dudareva and Pickersky, Metabolic Engineering of Plant Volatiles and Holopainen and Blande, Molecular Plant Volatile Communication.) Neighboring plants receive this signal and begins to produce more defensive volatile compounds, holding at the ready.
The volatile chemicals that serve as messengers between neighboring plants and members of the same species are called “semiochemicals”. Pheromones, kairomones and allomones are all semiochemicals – chemicals that signal. Pheromones are volatiles that are produced and detected by members of the same species, while kairomones are volatiles emitted by a host and detected by a beneficial species. Allomones are emitted by one species to the detriment of the attacking species. Certain types of allelopathy can act as semiochemicals. (Pare and Tumlinson, Plant Volatiles as a Defense Against Insect Herbivores). It is unclear whether these different volatile responses are intended to alert non-clone nearby plants or if other species are 'eavesdropping' on signals sent out for both within-plant and plant-clones.
As is typical on Planet Earth, all this communication and defense is for a few bad actors. Roughly speaking, 98% of all insect species are not insect pests. Most are food for other insects or animals further up the food chain, and some are beneficial to the plants as pollinators or predators and parasites that help ward off the 1 or 2 percent that are pests.
Present and Future Research
Scientists have discovered how humans sense fragrances and how insects detect odors. Much is known recently of the many plant volatiles and some of the roles they play, but almost nothing is known of the mechanism by which plants detect plant volatiles. We know their communication is elaborate, we know some of what they're saying, we don't know how they hear the messages.
Scientists are investigating the feasibility of using the priming response of plants to increase their resistance to herbivores and pathogens by companion planting with a few transgenic plants that have been genetically engineered to continually emit airborne warning signals. (Dudareva and Pickersky, Metabolic Engineering of Plant Volatiles). However, this may prove tricky as plant enemies have evolved to take advantage of plants early warning systems to locate plants for food and reproduction. Because of the complexity of plants, insects and volatile compounds, this research and subsequent use is considered to be in the very early stages of development for these new biological controls.
In addition to the 'beacon' plant research, research continues in hopes of new biological (rather than chemical) plant insecticides or deterrents based on the plant's own defensive volatiles. Additionally, research is underway to re-introduce fragrances into roses and other ornamentals where the scent was bred out in lieu of other more important qualities – larger and longer bloom periods, disease and pest resistance.
Another area of research is the enhancing and augmenting of volatiles that aid in pollination. Scientists are aware that the pollinator population has decreased and find it necessary to boost pollination-friendly volatiles. Perhaps some additional research is needed on the effect of herbicides and pesticides on the plants production of volatiles and their interaction with the remaining pollinators. Their effect of 'cides' on pollinators has already been aptly documented by numerous studies.
Change of habitat by weather, climate, or introduction of other volatiles disrupts the natural harmony. It is easy to see how the normal plant-insect exchange is challenged by large-scale monoculture modules and current chemical horticultural practices. The natural world of plants may not be the idealized, serene environment we've long envisioned, but it does function with a certain and natural harmony, good will and cooperation among themselves not before imagined, surviving for thousands of years in this delicate balance with insects.
And maybe Russian Sage is signaling me it doesn't want to be bothered.
Barth, Friedrich G., Insects and Flowers, the Biology of a Partnership, Princeton University Press, 1991.
Dudareva, Natalia and Eran Pickersky, “Metabolic Engineering of Plant Volatiles”, Current Opinion in Biotechnology, 2008, 19:1-9.
Dudareva, Natalia, Eran Pickersky and Jonathan Gershenzon, “Biochemistry of Plant Volatiles”, Plant Physiology, August 2004.
Farre-Armengol, Gerard; Ioland Filella; Joan Llusia; and Joseph Penuelas, “Floral Volatile Organic Compounds: Between Attraction and Deterrence of Visitors Under Global Change” Perspectives in Plant Ecology, Evolution and Systematics, 2013.
Flores, Alfredo, Geraniums Could Help Control Devastating Japanese Beetle, USDA, Agriculture Research Services, March 8, 2010.
Holopainen, Jarmo K and James D. Blande, “Molecular Plant Volatile Communication”, Sensing in Nature, edited by Carlos Lopez-Larrea, 2012.
Pare, Paul W. and James H. Tumlinson, “Plant Volatiles as a Defense Against Insect Herbivores,” Plant Physiology, October, 1999.
Pichersky, Eran, American Scientist, “Plant Scents”, Volume 92, November-December, 2004.
Angie Hanna, September 2, 2014