Benzoxazinoids are produced in very different plants, such as the zebra plant Aphelandra squarrosa (left), the golden dead-nettle Lamium galeobdolon (right) and maize. Comparative studies of the plant metabolites and the genes expressed have now demonstrated how flexible plant metabolism is. The formation of benzoxazinoids in the three species is based on different enzyme classes and has thus evolved independently of one another.
© Karin Groten, Max Planck Institute for Chemical Ecology
Imagine for a moment that you're a supremely intelligent designer and you just designed a metabolic pathway for producing a substance in plants that is intended to deter other creatures you designed earlier to eat the plants, from eating them.
No! I know that's not an intelligent thing to do but work with me on this one!
Then, the same problem you've created which the animals you've designed doing what you've designed them to do, and eating other plants you've designed, so how do you solve that problem?
Being intelligent, you give those plants the same metabolic pathway to produce the same deterrent substances you've just designed, don't you?
Well, yes, if you were truly intelligent you would, but not if you're creationism's putative intelligent [sic] designer. If you're creationism’s putative intelligent [sic] designer, you set about creating entirely new metabolic pathways for each plant to produce the same deterrent chemicals! In metaphorical design terms, it’s the equivalent of inventing the wheel anew every time you need to put wheels on a cart.
Would you employ such a designer?
Creationists regard this as supreme intelligence - which probably tells us a great deal about creationists and probably explains why they're creationists in the first place.
You might think this example is made up to make creationists look even more gullible, but it's actually based on real science as revealed recently by researchers from the Max Planck Institute for Chemical Ecology, Jena, Germany. These researchers have found that distantly related plants use different enzymes and different biochemical pathways to produce the defence compounds, benzoxazinoids, and with different enzymes come different sets of genes.
The researchers found that these biochemical pathways have evolved in plants at least three time and don't have their origins in a common ancestor.
What are benzoxazinoids and how do plants use them defensively? Benzoxazinoids are a group of chemical compounds found in various plant species, primarily in the grass family (Poaceae). They serve as defensive compounds that plants produce to protect themselves from herbivores and pathogens. Benzoxazinoids are most commonly associated with cereal crops like maize (corn), wheat, and rye, but they can also be found in other plants. The defensive functions of benzoxazinoids in plants include:The team's work is published in Proceeding of the National Academy of Science (PNAS), sadly behind a paywall, but the work is described in a news release by the Max Planck Institute for Chemical Ecology:
- Anti-Herbivore Properties: Benzoxazinoids deter herbivores by acting as feeding deterrents, toxins, or by interfering with herbivore digestion. When herbivores, such as insects, consume plant tissues containing benzoxazinoids, they often experience reduced feeding rates and growth. In some cases, these compounds can be toxic to herbivores, leading to their death or reduced fitness.
- Antimicrobial Activity: Some benzoxazinoids possess antimicrobial properties, which help protect plants from various pathogens, including fungi and bacteria. These compounds can inhibit the growth and proliferation of microorganisms that can cause diseases in plants.
- Allelopathic Effects: Benzoxazinoids can also act as allelopathic chemicals, which means they can inhibit the growth of neighboring plants. This allelopathic effect can help reduce competition from other plant species and provide the producing plant with a competitive advantage in its ecosystem.
The biosynthesis of benzoxazinoids involves several enzymatic steps, starting with the conversion of indole-3-glycerol phosphate to indole, which is then transformed into the key precursor compound, 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA). DIMBOA is the central benzoxazinoid compound, and it can be further converted into various derivatives with specific defensive properties.
Plants that produce benzoxazinoids usually accumulate these compounds in different plant tissues, such as leaves, stems, and roots, to provide comprehensive protection throughout the plant. The production and release of benzoxazinoids can be induced when plants sense herbivore damage or other stressors, making them part of the plant's inducible defense mechanisms.
It's important to note that the specific types and quantities of benzoxazinoids can vary among plant species, and some plants have evolved different chemical defense strategies in addition to or instead of benzoxazinoids. Overall, benzoxazinoids are an example of the diverse array of chemical compounds that plants have developed to defend themselves against a wide range of threats in their environments.
The production of special plant defense compounds has evolved independently in distantly related plant familiesAlthough the body of the paper is behind a paywall, the statement of significance and the abstracts are freely available:
Individual species of very different plant families produce special indole-derived defense compounds called benzoxazinoids. However, the biosynthetic pathway of these compounds was so far only known for grasses such as maize. A team from the Max Planck Institute for Chemical Ecology has now been able to show, by studying two distantly related plant species, the golden dead-nettle and zebra plant, that completely different enzymes are responsible for the formation of these special defense compounds. Hence, plants evolved the biosynthetic pathway for the same compounds several times independently (PNAS, October 2023, doi: 10.1073/pnas.2307981120).
Maize plants form special compounds derived from indole, the so-called benzoxazinoids. They are considered ecologically important because they act against a wide range of herbivores and reduce their feeding. Benzoxazinoids also exhibit antimicrobial properties and are thought to be involved in mediating plant-plant interactions. Their biosynthesis in maize has been known since the 1990s. Meanwhile, their biosynthetic pathway has been described in several grasses, but benzoxazinoids have also been found in other plant species. Their distribution is peculiar: While specialized metabolites often occur in specific evolutionary related plant species, benzoxazinoids show the opposite behavior and occur sporadically in many distantly related plant families. Several attempts to elucidate this metabolic pathway not only in maize but also in distantly related species were unsuccessful. Accordingly, the research goal of Tobias Köllner's group in the Department of Natural Product Biosynthesis at the Max Planck Institute for Chemical Ecology was clear:The team used two distantly related eudicot plant species that produce benzoxazinoids for the studies: the golden dead-nettle Lamium galeobdolon, which is found in sparse forests and forest edges on nutrient-rich soils in Europe, and the zebra plant Aphelandra squarrosa, a popular houseplant. For both species, the researchers created data sets of the compounds and genes expressed in different tissues and compared them to closely related species that do not produce benzoxazinoids.We wanted to find out whether the ability to form benzoxazinoids evolved independently in different species.
Tobias G. Köllner, co-corresponding author
Department of Natural Product Biosynthesis
Max Planck Institute for Chemical Ecology, Jena, GermanyThe researchers were able to show that the benzoxazinoid metabolic pathway evolved independently in maize and the two species under investigation.This approach allowed us to identify candidate genes that may be involved in the formation of these compounds. We further characterized the candidate genes by expressing them in tobacco to find out if they are really involved in the production of benzoxazinoids.
Matilde Florean, first author
Department of Natural Product Biosynthesis
Max Planck Institute for Chemical Ecology, Jena, Germany
In particular the discovery that the golden dead-nettle and the zebra plant use a dual-function flavin-containing monooxygenase, rather than two different cytochrome P450 enzymes as in grasses, was completely unexpected. Overall, the research team was surprised to find such a diversity of enzymes performing the same reactions.We found that, in contrast to maize where a number of closely related cytochrome P450 enzymes carry out specific steps of the metabolic pathway, different enzyme classes as well as unrelated enzyme families of cytochrome P450 were recruited.
Tobias G, Köllner
In the future, the team hopes to elucidate the biosynthesis of these compounds in even more plant families.With this work, we have shown how flexible plant metabolism can be. We have shown that plants can independently invent very different strategies to make the same chemical compounds, and this has happened at least three times in the evolutionary history of benzoxazinoids.
Sarah E. O’Connor, co-corresponding author
Department of Natural Product Biosynthesis
Max Planck Institute for Chemical Ecology, Jena, Germany.
SignificanceWhat we have here then is an example of convergent evolution, where the same environmental selectors can result in the same solutions, albeit by different routes. This is perfectly understandable to anyone with a basic understanding of how evolution works. What is not understandable is how any normal person can regard it as evidence of an intelligence behind the process or of the work of a single creator.
Enzymes that catalyze the same chemical reaction can evolve independently many times. However, examples of independent evolution of an entire pathway that consists of many enzymatic steps are rare. In this manuscript, we report the discovery of two biosynthetic pathways that both synthesize a class of plant defensive molecule called benzoxazinoid. Our discoveries demonstrate that the benzoxazinoid pathway has evolved independently in flowering plants at least three times. These findings provide a deeper understanding of the mechanisms underlying the evolution of metabolic pathways. In addition, the discovery of these benzoxazinoid biosynthetic pathways that have independently evolved in distantly related plants will allow us to probe the biological functions of these molecules.
Abstract
Benzoxazinoids (BXDs) form a class of indole-derived specialized plant metabolites with broad antimicrobial and antifeedant properties. Unlike most specialized metabolites, which are typically lineage-specific, BXDs occur sporadically in a number of distantly related plant orders. This observation suggests that BXD biosynthesis arose independently numerous times in the plant kingdom. However, although decades of research in the grasses have led to the elucidation of the BXD pathway in the monocots, the biosynthesis of BXDs in eudicots is unknown. Here, we used a metabolomic and transcriptomic-guided approach, in combination with pathway reconstitution in Nicotiana benthamiana, to identify and characterize the BXD biosynthetic pathways from both Aphelandra squarrosa and Lamium galeobdolon, two phylogenetically distant eudicot species. We show that BXD biosynthesis in A. squarrosa and L. galeobdolon utilize a dual-function flavin-containing monooxygenase in place of two distinct cytochrome P450s, as is the case in the grasses. In addition, we identified evolutionarily unrelated cytochrome P450s, a 2-oxoglutarate-dependent dioxygenase, a UDP-glucosyltransferase, and a methyltransferase that were also recruited into these BXD biosynthetic pathways. Our findings constitute the discovery of BXD pathways in eudicots. Moreover, the biosynthetic enzymes of these pathways clearly demonstrate that BXDs independently arose in the plant kingdom at least three times. The heterogeneous pool of identified BXD enzymes represents a remarkable example of metabolic plasticity, in which BXDs are synthesized according to a similar chemical logic, but with an entirely different set of metabolic enzymes.
Florean, Matilde; Luck, Katrin; Hong, Benke; Nakamura, Yoko; O’Connor, Sarah E.; Köllner, Tobias G.
Reinventing metabolic pathways: Independent evolution of benzoxazinoids in flowering plants
Proceedings of the National Academy of Sciences, 120 (42) e2307981120. DOI: 10.1073/pnas.2307981120
© 2023 PNAS.
Reprinted under the terms of s60 of the Copyright, Designs and Patents Act 1988.
No competent watchmaker would reinvent the movement for every watch he made. This is how we can tell that species are not designed by an intelligent designer, as William Palley thought when he devises his 'Watchmaker' analogy without the benefit of microscopy and biochemistry, but by a mindless natural process without a plan and no ability to remember solutions to problems in other species and insert them into unrelated ones. So, we end up with nested hierarchies and lots of examples of nature solving the same problem lots of different ways, or metaphorically reinventing the wheel, and a superficial resemblance of design which disappears the moment we look at the detail below the surface.
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