Updated: May 20, 2021
(The tomato is one of the most amazing foods we eat and the complex flavors and healthy attributes are not an accident of nature. Yet, we grow tomatoes as if the color and appearance are all that matter. The tomato’s full potential is only realized when the environment that created that potential is allowed to act on the individual and to elicit inherent abilities. Humans are no different: the stresses of our environment shape us and our environment should be as natural and healthy as possible.)
“The individual, as he is now, is nothing else than the exaggerated expression of environment, environment being the past and the present, the inherited and the acquired.” -Jiddu Krishnamurti
The modern store-bought version of a tomato is a tasteless, uninspiring, watery, artificial imitation of a garden tomato. In stark contrast, a garden-grown tomato is the epitome of fresh food. Of all the fresh foods we eat, it’s hard to come up with another example that elicits the same response from the first, the second, and the third bite. The eater’s response is almost rhapsodic; no one can take a bite of a garden-fresh tomato and not comment on the flavors. Such a tomato makes so many common foods better, even special. Almost as rewarding as eating a good tomato is watching others eat one and noting their rapturous facial expressions.
So, what just happened here? Do we have a special relationship with the garden tomato? Why does the garden tomato get that response, but not the store-bought tomato? Let’s explore in a different way what a tomato is and what it represents, from an ecological and evolutionary point of view, and what that means to our human senses. And then I’ll use the tomato to explain how and why you and I, humans, are tomatoes, yet more than tomatoes, and yet in the same problematic situation as the tomato.
To begin with, a tomato plant is really a small ecosystem nested within a much larger ecosystem. The tomato plant reaches its roots into the soil and its leaves into the air. Like all plants, it interacts with both living and non-living aspects of the external environment, and the internal biochemistry of the tomato plant is the synthesis of those interactions. The internal ecosystem of the plant works with the external ecosystem surrounding it to collaboratively produce the ultimate physical structure: the juicy, red, seed-filled tomato fruit. The fruit is the result of the plant ecosystem interacting with the ecosystem around it. The fruit is the interaction of those two ecosystems, the product of their meeting, one nested within the other. The importance of this “nestedness” should not be underestimated and it is a key concept that seems to have been forgotten in the race toward technological improvements in agriculture over the past few decades.
What does it mean to be a tomato? The tomato plant begins life as a seed in the soil, responding to different environmental cues, mostly water and temperature, that stimulate the dormant embryo to begin rapid cell division and expansion. As the seedling grows, the roots extend into the soil and begin to interact with vast numbers of bacteria, fungi, minute nematodes, and a large number of other microbes and invertebrates. Many of these interactions are negative, but many are beneficial. Importantly, the positive interactions are necessary for growth, but the negative interactions can also have an important influence on the normal growth and health of the plant. Some fungal interactions, such as with fungi that interact with roots (mycorrhizal fungi), provide necessary nutrients that the plant otherwise would have trouble obtaining.
Aboveground, the plant matures and produces flowers that are pollinated by bees, flies, and butterflies, and the number of pollinations determines the number of seeds each fruit produces. Many small organisms roam the surfaces of the plant, some attempting to eat the leaves and fruit, others in search of those organisms to prey on them. The tomato plant not only represents a very large number of interactions with the environment, but acts as the context for a great many other interactions. Some interactions are an invariable part of the life of the plant and others are serendipitous or chance encounters. All in all, the plant is both favored by and endures these interactions.
The ultimate biological goal of the tomato plant is reproduction, that is, making as many seeds as possible to carry on the lineage. The success of the tomato plant in achieving its reproductive potential depends on the quality and quantity of the interactions between the plant and the external ecosystem. Some tomato plants will be more susceptible to the herbivores who are attempting to maximize their own reproductive potential. Others will be better able to resist and defend themselves from enemies. Some plants will respond better to the belowground microbial interactions and by doing so will gain access to larger quantities of necessary nutrients. The faster growing plants will be more likely to receive the most sunlight and energy. Overall, the negative and beneficial outcomes of these interactions will depend considerably on the genetic makeup of each plant.
In biology, the genetic makeup of the individual organism is its genotype, that is, the specific DNA that codes for each trait of each individual. Every gene in an individual is contained in the DNA found in every cell, but not all genes are expressed. For example, every cell in your finger contains your entire genome, every single chromosome with every single gene, yet the finger cells only use an extremely small portion of all that genetic information. The task of being a finger cell is perhaps not as complex as some other cells in the body, but all of the genes are present even if they will never be used. Some genes are initially turned off, but are turned on after receiving a biochemical signal (e.g., the growth of body hair after puberty); some genes are turned on initially and then turned off after a period of time (e.g., fetal hemoglobin after a human baby is born); and some genes are recessive (e.g., alleles that cause genetic diseases) and are best left unused and unseen. In other words, every cell in the body possesses all of the potential of the entire individual, but very little of that potential is expressed at any one time.
That expression of the genotype- what we actually see in an individual- is called the phenotype, which can be thought of as the expression of the genotype in a particular environment. That is to say, the environment stimulates the genotype to be expressed in different ways under different conditions. For example, in summer, an arctic fox is entirely brown, but in winter is completely snow white, and that pattern switches back and forth between the seasons. The fox has the genetic capacity for being either white or brown, but the cues from the environment trigger the change in coloration.
However, if the environment doesn’t provide the right cues, the genotype will not express a particular phenotype. For example, the Hydrangea is a popular garden plant that produces large heads of flowers, which can range in color from white to pink to blue to purple. The particular color depends largely on the acidity (pH) of the soil which restricts the availability of certain soil nutrients and more acidic soils cause plants to produce flowers at the blue end of the spectrum. The potential for a range of flower colors is always present, but the environment determines what flower color will be expressed on a particular plant.
The garden tomato is just such an expression of the genotype interacting with the environment. A fully ripened, freshly picked tomato grown in an outdoor garden is an amazing taste sensation; it’s a literal explosion of flavors. In contrast, a tomato grown in a greenhouse environment is an insipid pretender; it can have a granular texture, poor color, and very little taste or smell. It lacks biochemical complexity.
The two fruits can have the same appearance, but the taste and texture of each can be wildly different. They can share essentially the same genotype, but clearly not the same phenotype. How is this possible? To understand this, let’s consider the purpose of the tomato fruit and its role in the evolutionary history of the tomato plant.
A “plant” is a very long record of evolutionary interactions between an organism and its environment. For almost as long as there have been flowering plants, there have been any number of insects that have attempted to eat the roots, stems, leaves, flowers, fruits, and seeds or to drink the fluids of those plants. Plants have very little recourse in their defense against a hungry world; they can’t run away and so must defend themselves where they grow. To do this they can defend themselves with physical protections in the form of spines, bristles, hairs, and other forms of external weaponry. Or they can defend themselves with chemicals that are toxic in one way or another.
Not every plant has physical protections, but every wild plant possesses chemical defenses and they typically are adaptations to insects. As these defenses have evolved to ward off a very hungry insect world, the insects were forced to adapt to overcome the plant’s defense chemicals. In turn, as insects became less susceptible to the defenses and renewed their attack, the plant was forced to adapt to produce better or different chemicals in response.
This back and forth process has been going on for millions of years and is the gist of my book Chasing the Red Queen.[i] The evolutionary arms race is the battle between organisms in which one is typically attempting to prey on the other, the other is defending itself, and under natural conditions neither organism ever holds the upper hand for very long. Every living species of plant, for its entire history, has survived the threat of herbivory in its external environment, and most of the time this was accomplished with chemical defenses.
As a result of this very long evolutionary saga of survival, the tomato is biochemically very complex. All plants produce an array of chemical compounds that are necessary for the day-to-day functions of the plant. These primary compounds perform all of the normal processes required for the growth and health of the plant and include, for example, DNA, proteins, sugar, and chlorophyll.
In contrast, the defense chemicals are secondary compounds (metabolites) that have been derived from the primary compounds. They originated from mutations to the genes for the primary compounds that resulted in somewhat modified chemicals with new functions. If the modified chemicals assisted the plant in defending itself in any way from herbivores, and that led to the successful production of more seeds, then that mutation would have been positive and would have become an important part of the genotype. As an example, if a mutation to a protein molecule resulted in an unpleasant flavor, some insects might be less likely to eat the plant.
Within a single plant, we may find dozens to hundreds of secondary compounds and we assume their presence in the plant is evidence of a long and successful history of defense against plant-eating animals. These compounds can be found in every part of the plant from the root tips to the shoot tips, and especially in the fruits and seeds. Importantly, the defense molecules in different parts of the plant will break down as the plant ages or as it passes through different life stages. The breakdown of secondary metabolites often results in smaller volatile organic molecules that are directly involved in flavor. Over 7000 flavor-related molecules have been identified in plants.
In the tomato, there are up to 400 different volatile organic compounds, mostly from secondary metabolites, of which about 30 are also important contributors to flavor.[ii] The flavor of the tomato fruit is a delicate balance of the volatile components in addition to the basic tastes, such as sweet, sour, and bitter, that may be contributed by the non-volatile components. Why are these so-called defense compounds involved in flavor and especially what we consider good flavor? Why does there have to be a balance between toxicity and flavor? And how can a fruit be toxic now, but non-toxic later? This is all part of the strategy for being a successful tomato.
Herbivores attack the tomato at every stage in life. If we consider just insects, the plant must defend itself from attacks on every part of the plant and at every growth stage. To complete its life cycle, the plant must protect each of its different parts. Leaves are needed to produce sugars that are used in every aspect of growth, so leaves are vital and must be protected. Roots are needed to absorb water and nutrients from the soil to facilitate photosynthesis in the leaves, so the roots must be protected. Eventually, the plant must produce flowers, fruits, and seeds to ensure the genetic continuation to the next generation and these structures must be defended vigorously. The defense of the leaves, roots and stems helps the plant produce enough energy to complete the reproductive cycle, and so the defense of every part of the plant is critical.
However, the plant is faced with attracting friends while repelling enemies, and so different parts of the plant are defended to different degrees. Flowers are chemically defended in different ways than are seeds. Flowers are the window dressing, the advertisement, that attracts pollinators, and pollinators ensure that seeds are produced. But flowers are only necessary to attract the pollinators; once pollination has been achieved, the colorful flower parts typically fade or fall away and cease to be a visual attraction.
In contrast, seeds are the offspring of the plant, the next generation, and have a very different value. After pollination and during seed development, the seeds are not colorful or obvious, they are hidden or obscured. At that point, the young fruit (usually the ovary containing the developing seeds) is a shifting biochemical combination of flowers and seeds because it is both defended and not defended depending on the developmental stage. The attractive aspects of the flower are disappearing and the plant shifts into a defense mode as the fruits are growing.
Eventually, the plant shifts again and uses the fruit to attract fruit-eating animals (frugivores), but this is only true when the fruit is brightly colored, not when it is green. Until the fruit is “ripe”, it is physically or chemically defended, potentially toxic to many would-be herbivores, because the seeds contained inside are still developing and highly vulnerable. During this stage the fruit is not colorful or obvious.
As the seeds reach maturity, the fruit “ripens” and begins to change color. The change to a bright color that contrasts with the green of the leaves and the change in aroma are both indicators to fruit lovers that the fruit is ready for eating and is not only undefended but, like a flower, is being actively advertised as food. At that point, animals consume the sweet, tasty, nutritious, and non-toxic fruits that contain the mature seeds. The fruit passes through the animals very quickly and before the seeds can be digested. They are thus dispersed throughout the surrounding habitat. (The high fiber content of fruits and the consequent rapid rate of passage through the frugivore digestive system should not be considered accidental.)
Therefore, the stages of development in the tomato plant require a wide range of different chemical compounds for ensuring completion of many different processes that lead to the ultimate goal of dispersing tomato seeds. The abundance of these compounds inside the plant goes up and down, and the numbers of different compounds are surprisingly high.
The taste of the ripe tomato that we find so attractive is a combination of many chemicals and many of them are the very last to develop in the fruit. It is not until the fruit is fully ripened that the full complement of flavors is present. The quantities and intensities of these flavors have been fine-tuned by evolutionary selection (although also modified by plant breeders). The vitamins, proteins, amino acids, and sugars are all substances that are nutritious to animals. The wide array of volatile secondary compounds contributes to flavor, but these can be residual defensive compounds from the earlier stages of the plant or degraded primary and secondary metabolic compounds. All of these chemicals come together to give the tomato its characteristic qualities, but many of them are initially produced in the plant for very different purposes.
Today, we grow the vast majority of the tomatoes that we eat in greenhouses, hothouses, hydroponically, and in other controlled environments. Literally all tomatoes sold in conventional grocery stores, including most “organic” and heirloom tomatoes, are grown indoors rather than outdoors in a natural setting. They are grown in very small amounts of relatively sterile soil, or often with no soil at all, and with a steady supply of nutrients from artificial fertilizers. We have bred tomato varieties to produce enormous quantities of fruit in a way that is analogous to breeding “modern” chickens to lay 4-5 eggs a week (up to 250 a year) when one egg every other day for about a month (10-15 eggs in a season) is more typical for wild birds. This high level of production, either in tomatoes or eggs, results in foods with diluted nutritional content and quality, but it’s important to appreciate the different factors affecting quality.
The sterile environment of greenhouse production is a far cry from the growing of tomatoes in a garden. When we taste a greenhouse tomato, we should not wonder at its lack of ‘tomato’ flavor.[iii] Instead, we should ask the much more relevant question: if the phenotype of the plant is the interaction between the environment and the genotype, then how can it be possible to achieve the natural phenotype if the environment is prevented from interacting with the genotype? In simpler terms, how can a tomato grow up properly if it never goes outdoors?
To grow the best tomato fruit, the tomato plant must go outdoors. It must interact with the environment to which it is adapted so that its genotype can be fully expressed. The tomato plant, like many plants, doesn’t have to produce defensive compounds at all times. Many plants don’t use energy for that purpose unless that effort is needed. Therefore, plants often defend themselves only after detecting physical damage from an herbivore.
When we grow food plants that never experience the stress of being attacked, they may not be induced to produce the compounds that create the best tasting fruit or those that have the most health benefits. By analogy, a human individual can have the genetic potential for being a very fast runner, but unless she forces her bones and muscles to become stronger by the stress of exercise, she will never achieve that physical potential. It is the stress of the environment that generates the optimal outcome. Greenhouse tomatoes will never be as delicious as garden tomatoes because their true character can only be expressed under somewhat stressful conditions, conditions similar to those that caused the plant to evolve and maintain that genotype in the first place.
So, the tomato we eat should be thought of as the physical expression of the tomato genotype when exposed to the natural environment. The natural environment is a multi-species, multi-stress period of time in which the plant adjusts to and accommodates stress while fulfilling the evolutionary goal of successfully producing a new generation. When we eat a wonderfully tasty garden tomato, we are experiencing the full expression of the plant’s genetic potential with all of its vitamin, protein, and antioxidant benefits. When we eat a greenhouse tomato, we are being cheated.
These principles apply to all organisms. Unless the genetic, biochemical, and multispecies internal ecosystem of any organism is exposed to the multi-factor, multi-stress, multi-species external ecosystem in which it resides, the “tomato” of that organism cannot be produced. This is to say, the full genetic expression of each individual organism is a function of many required interactions with many other organisms. For tomatoes, this means being exposed to predators and experiencing stress so that the genome of the tomato is stimulated to fight back against the negative forces of the environment.
As humans, we are in the same evolutionary situation: each of us possesses an incredibly diverse world of minute organisms inside our bodies, an internal ecosystem that interacts with our genome, stimulating it to respond to stress. These interactions must take place for humans to fully express their potential. An active and strong immune system is evidence of a healthy rapport with the external environment. It is essential that our internal environment receives appropriate contributions from the external environment if we are to remain physiologically healthy.
In a sense, to produce a good human “tomato”, the internal environment of the human must receive good “tomatoes” from the external environment. The interactions between the internal environment and the external environment result in the proper expression of the human genome. For us to be good tomatoes, we must eat good tomatoes (in whatever form they happen to take).
In the coming posts, I will attempt to convince you that not only are all individual plants actually ecosystems, but that humans are ecosystems and the human ecosystem must interact with the surrounding ecosystem. We are small ecosystems nested within local ecosystems nested within the regional ecosystem. The ecosystem of the individual is adapted to the larger external ecosystem in innumerable ways (mostly unknown) and the full potential of the individual is expressed when its healthy internal ecosystem is interacting with the surrounding external ecosystem, which must also be healthy. The recent research on the microbiome is clearly indicating that this is a non-negotiable criterion for a healthy life.
A second point is this: organisms that are adapted to a certain environment will best express their abilities in that environment. Their internal ecosystems are healthiest when they are embedded in the external ecosystems to which they are adapted. When they grow in a different environment, whether more stressful or less stressful, the genetic potential of the organism might not be fully realized.
In addition, if the natural environment is lacking important factors or has been simplified and lacks natural complexity, this will change the relationship between internal and external ecosystems. This concept applies to all organisms, but I’ll focus on humans; our ability to thrive can be either enhanced or compromised by the quality of the external environment because it interacts with and determines the quality of our internal environment.
This last part is very important to us and to our world. How do we perceive our place within our ecosystems? The concept of the individual as being separate from the external world originated with Aristotle, (but amplified and extended by 18th Century philosophers and coincident with the Industrial Revolution.) He created a worldview of the individual as an observer of nature and separate from it. This view, of course, was applied only to humans and not to the other animals. However, whether human or not, nothing could possibly be further from the truth.
At no point in our lives are we separate from our environment and, in fact, nothing could be more dangerous for our well-being. Even before our birth, whatever our mothers ate, drank, and consumed affected our nutrition and biochemical balance. Were this not true, pregnant mothers would not be discouraged from limiting their caffeine and alcohol intake, nor would prenatal health checkups be necessary. But they are. Infant health issues and mortality rates dramatically decline when pregnant women are more aware of how the outside world affects their inside world.
Humans are products of our ecosystems. We not only can’t exist without our surrounding ecosystem, we wouldn’t be here without it. Even more than that, we are absolutely and wholly dependent on the health of our personal ecosystem (the one we’re just learning about) as well as our surrounding ecosystem (the one everyone talks about). Our internal balance is dependent on the quality of the food and water we consume because of the direct importance to our health, but that quality determines the health of our digestive systems, each of which is home to trillions of very useful and mutualistic bacteria of a great many different species. When that ecosystem is not happy, we are not happy. This is the underlying reason for the maladies suffered by many tourists visiting new countries and eating unusual (for them) food. Our internal ecosystems are adjusted to our normal diets and are temporarily unbalanced by the introduction of unfamiliar foods, particularly cuisines with different nutritional compositions. More importantly, it now appears that imbalances in our internal ecosystems may be responsible for the slew of “modern diseases”[iv] that are reaching epidemic, even pandemic, proportions.
Life is the product of interactions with the environment. The interaction between our internal ecosystem and the external ecosystem is more than just the exchange of food before and after it is eaten. Yes, the bacteria in the gut are colonized and recolonized from outside, but the human body has far more interaction with the world than that. We have at least five senses that take information from the outside and interpret it on the inside. We breathe in the air. We drink in the water. We react to allergens. We provide a haven for bacteria, pathogens, parasites. We are home to more bacterial cells than human cells. When the environment surrounding us doesn’t help us maintain a healthy internal ecosystem, our personal health suffers. And we are simplifying and damaging our ecosystems in many different ways. The long-term effects of a simplified external ecosystem surrounding a simplified internal ecosystem health are just beginning to be recognized and the implications are not happy ones. In fact, the mounting evidence suggests an impending crisis.
There are a growing number of books focused on the importance of the internal ecosystem of humans, now called the microbiome, and the consequences for human health of disturbing that ecosystem. The microbiome is the most fascinating realm of scientific and medical research ever and every human should make an attempt to educate themselves about the microbiome and its relationship with personal health. I will not go to great lengths to discuss the latest breakthroughs concerning our understanding of the microbiome and its importance to our health.[v] Instead, this blog is an attempt to take a different approach, first, by discussing how we got where we are today in terms of public health and our relationship with bacteria; second, by reviewing what the microbiome is, why we have one, and why we should care about it; and, third, how we use that information to behave in a way that strengthens our role as a walking, talking, and healthy ecosystem.
We’ll first consider how the world has changed in the past few generations, especially our relationship with the technologies we use to modify the world we live in. For example, our single-minded focus on producing calories at a very low cost has resulted in a heavy reliance on technology to produce vast quantities of food in a very industrial context. This reliance on technology to solve our food quantity problems to feed ever-increasing human and livestock populations has come at the cost of food quality, which I believe has created a new set of problems.
Essentially, this is a cautionary tale: high productivity to maintain low cost equals low quality. We embarked on this quest in earnest about 70 years ago with the deployment of synthetic pesticides and fertilizers and the wave of technology being applied to food production has only grown and grown – to the point that the agro-technology sector, not the wishes of the public, determines the directions we take in food production. We are now experiencing en masse the health consequences of decisions concerning the quality of our food that began immediately after the end of WWII.
As we attempt to understand the rapidly escalating health problems now terrorizing our societies, I will suggest that we may be asking the wrong questions. In particular, our absolute conviction that technology will solve our problems is, in my opinion, completely misplaced. Television and cable channels are inundating us with the latest and greatest drugs to alleviate modern medical problems. These are also technological solutions and they are being proffered to a public that does not understand that it is the technological solutions to food production and disease that underlie their growing medical problems. One should not take strychnine to cure cyanide poisoning.
We have to understand the role of our internal ecosystem in maintaining our health before we can manage our health. We’ve been aware of the microbiota of our digestive system for quite some time, but we’ve never considered the presence of that microbiome as something essential, as something that integrates a number of important physiological and biochemical functions in our bodies not the least of which is our immune system. This critical emerging information must be incorporated into a more ecosystem-oriented context for us to appreciate how we should interpret and understand the complex inter-relationships between our internal and external worlds. As we become more and more urban and sedentary and completely dependent nutritionally on what we find at the grocery stores, we must become more informed and responsible for the management of our internal ecosystems if we expect to stay healthy personally and to regain our health as a society. In essence, we may have to relearn what is food and what isn’t food.
As a preface, I’ve used a plant, the tomato, as an example of the importance of the external environment to the physical and biochemical expression of the potential of the internal environment. We need to appreciate that all species, especially humans, are fully dependent on their internal ecosystems and the internal ecosystems are fully dependent on the external ecosystem. More specifically, the health of our internal ecosystem is dependent on the health of the external ecosystem, and the health of our internal ecosystem is responsible for our health as individuals. We not only are what we eat, we also are not what we don’t eat, and in some ways that might lead to more important complications in terms of our health.
[i] Andy Dyer. 2014. Chasing the Red Queen: The Evolutionary Race Between Agricultural Pest and Poisons. Island Press. [ii] Stephen A. Goff and Harry J. Klee. 2006. Plant volatile compounds: sensory cues for health and nutritional value? Science 311:815-819. Elizabeth A. Baldwin, et al. 2000. Flavor trivia and tomato aroma. HortScience 35:1013-1022. [iii] Having said that, the tomato industry has intentionally bred tomatoes (and essentially all crops) not for taste, but for productivity, uniformity of appearance, shelf life, and durability in shipping. Some reports suggest the food industry cares little for flavor if the other marketing criteria are met. For an excellent review of changes in food quality and flavor, see Mark Schatzker’s book The Dorito Effect (2015, Simon & Schuster). [iv] Which may include autism, obesity, diabetes, asthma, allergies, ADHD, and depression; auto-immune diseases such as lupus, rheumatoid arthritis, psoriasis; digestive diseases such as colitis, coeliac disease/gluten sensitivity, irritable bowel syndrome; and late onset diseases such as multiple sclerosis, Alzheimer’s, Parkinson’s, ALS. [v] There are already several excellent books focused on the microbiome. For starters, consider those by Alanna Collen (10% Human), Martin Blaser (Missing Microbes), Giulia Enders (GUT), and Ed Yong (I Contain Multitudes).