QNAS
QnAs with Ian T. Baldwin Beth Azar Science Writer
Chemical ecologist Ian T. Baldwin has devoted his career to understanding the traits that allow plants to survive in the wild. The founding director of the Max Planck Institute for Chemical Ecology in Jena, Germany, and current head of its department of molecular ecology, Baldwin has developed a molecular toolbox for North America’s native coyote tobacco. He uses the tools to study gene function in the plant’s natural habitat in the Lytle Ranch Preserve in Utah, asserting that the best way to measure a gene’s effect on an organism’s fitness is in the environment in which it evolved. Elected to the National Academy of Sciences in 2013, Baldwin talks to PNAS about his latest findings. PNAS: Your work focuses on coyote tobacco (Nicotiana attenuate). What makes this plant particularly interesting? Baldwin: Its natural habitat is the postfire environment, where there’s lots of nitrogen and phosphorus and no competitors, exactly like the slash and burn agricultural niche we use to grow crop plants. If we can figure out how this plant lives in the habitat that we force our agricultural plants to grow in, maybe we can learn some tricks to make agricultural plants ecologically a little more sophisticated and not require all that pampering. One of the cool things we’ve worked out over the past 10 years is that when the tobacco hornworm attacks, a spit factor in saliva activates a signaling component in the plant that immediately starts the plant pumping out this very complex perfume that functions as an alarm call. The predators that normally attack the caterpillar get lured in and kill the caterpillar. PNAS: Why do you move between the laboratory and the field? Baldwin: You can’t always understand gene function simply by understanding [the] biochemical function of the proteins that genes produce. You frequently have to alter [gene] expression in the organism and then
1226 | PNAS | January 28, 2014 | vol. 111 | no. 4
put the organism back in its native environment and see what’s different. That’s what we do. We alter expression of genes based on their differential regulation in response to ecological traits like getting attacked by herbivores. The [plants] usually don’t have any phenotype at all in the greenhouse. However, when we put them in the field we can watch how insects, fungi, bacteria, and pollinators react, and allow them to phenotype the plant for us. PNAS: Your Inaugural Article focuses on tobacco hornworm (Manduca sexta) caterpillars—the herbivore that holds the record for how much nicotine it can ingest without dying—and whether it uses nicotine as a defense against its own predators. Where did this idea come from? Baldwin: We start with the notion that nicotine is a gorgeous mechanism for poisoning predators because it poisons anyone with a nervous system, but it can’t hurt the plant because [plants] don’t have a nervous system. We also knew that when you invent a really good defense, you put strong selection on [predators] to evolve a resistance mechanism. The tobacco hornworm detoxifies nicotine by excreting it. It regularly ingests four- to five-times the lethal dose for a human per day, but [excretes] most of it right out. Because many insects hijack plant defenses for their own purposes, we wondered whether the hornworm did that with nicotine. We knew that, in the early signaling cascade, when the plant detects the hornworm and begins to call its enemies, one of the first things the plant does is shut down its nicotine production. PNAS: In the study you created a tobacco plant that, when eaten by tobacco hornworm caterpillars, silences a gene in the caterpillars that is typically turned on when they ingest nicotine. Then you had some caterpillars eating regular tobacco and some eating the
Ian T. Baldwin. Image credit: Celia Diezel.
modified tobacco, and you watched what their natural predators did. What did you find? Baldwin: When we ran our experiments through the night, we saw big differences in caterpillar [survival] that we did not see during the day. Caterpillars eating the modified tobacco were dying in large numbers. That told us there was a predator that could tell the difference between the caterpillars. It was the wolf spider. Once we discovered that these spiders care whether the caterpillar expresses this gene, we were able to tease out the gene’s function. The spider’s feeding behavior told us that the caterpillar was doing something on the surface of [its] body with the nicotine. That got us to look at the caterpillar’s headspace and, sure enough, there’s nicotine coming out of the caterpillar’s spiracles. That allowed us understand that the gene was functioning to repurpose a little bit of the nicotine into the blood and from the blood to the spiracles where they puff it out, giving the caterpillar toxic halitosis. The big message here isn’t as much about this particular gene, but rather that we were able to use other organisms, out in nature, for phenotyping and understanding gene function. This is a QnAs with a recently elected member of the National Academy of Sciences to accompany the member’s Inaugural Article on page 1245.
www.pnas.org/cgi/doi/10.1073/pnas.1320016110
QnAs with Ian T. Baldwin Beth Azar Science Writer
Chemical ecologist Ian T. Baldwin has devoted his career to understanding the traits that allow plants to survive in the wild. The founding director of the Max Planck Institute for Chemical Ecology in Jena, Germany, and current head of its department of molecular ecology, Baldwin has developed a molecular toolbox for North America’s native coyote tobacco. He uses the tools to study gene function in the plant’s natural habitat in the Lytle Ranch Preserve in Utah, asserting that the best way to measure a gene’s effect on an organism’s fitness is in the environment in which it evolved. Elected to the National Academy of Sciences in 2013, Baldwin talks to PNAS about his latest findings. PNAS: Your work focuses on coyote tobacco (Nicotiana attenuate). What makes this plant particularly interesting? Baldwin: Its natural habitat is the postfire environment, where there’s lots of nitrogen and phosphorus and no competitors, exactly like the slash and burn agricultural niche we use to grow crop plants. If we can figure out how this plant lives in the habitat that we force our agricultural plants to grow in, maybe we can learn some tricks to make agricultural plants ecologically a little more sophisticated and not require all that pampering. One of the cool things we’ve worked out over the past 10 years is that when the tobacco hornworm attacks, a spit factor in saliva activates a signaling component in the plant that immediately starts the plant pumping out this very complex perfume that functions as an alarm call. The predators that normally attack the caterpillar get lured in and kill the caterpillar. PNAS: Why do you move between the laboratory and the field? Baldwin: You can’t always understand gene function simply by understanding [the] biochemical function of the proteins that genes produce. You frequently have to alter [gene] expression in the organism and then
1226 | PNAS | January 28, 2014 | vol. 111 | no. 4
put the organism back in its native environment and see what’s different. That’s what we do. We alter expression of genes based on their differential regulation in response to ecological traits like getting attacked by herbivores. The [plants] usually don’t have any phenotype at all in the greenhouse. However, when we put them in the field we can watch how insects, fungi, bacteria, and pollinators react, and allow them to phenotype the plant for us. PNAS: Your Inaugural Article focuses on tobacco hornworm (Manduca sexta) caterpillars—the herbivore that holds the record for how much nicotine it can ingest without dying—and whether it uses nicotine as a defense against its own predators. Where did this idea come from? Baldwin: We start with the notion that nicotine is a gorgeous mechanism for poisoning predators because it poisons anyone with a nervous system, but it can’t hurt the plant because [plants] don’t have a nervous system. We also knew that when you invent a really good defense, you put strong selection on [predators] to evolve a resistance mechanism. The tobacco hornworm detoxifies nicotine by excreting it. It regularly ingests four- to five-times the lethal dose for a human per day, but [excretes] most of it right out. Because many insects hijack plant defenses for their own purposes, we wondered whether the hornworm did that with nicotine. We knew that, in the early signaling cascade, when the plant detects the hornworm and begins to call its enemies, one of the first things the plant does is shut down its nicotine production. PNAS: In the study you created a tobacco plant that, when eaten by tobacco hornworm caterpillars, silences a gene in the caterpillars that is typically turned on when they ingest nicotine. Then you had some caterpillars eating regular tobacco and some eating the
Ian T. Baldwin. Image credit: Celia Diezel.
modified tobacco, and you watched what their natural predators did. What did you find? Baldwin: When we ran our experiments through the night, we saw big differences in caterpillar [survival] that we did not see during the day. Caterpillars eating the modified tobacco were dying in large numbers. That told us there was a predator that could tell the difference between the caterpillars. It was the wolf spider. Once we discovered that these spiders care whether the caterpillar expresses this gene, we were able to tease out the gene’s function. The spider’s feeding behavior told us that the caterpillar was doing something on the surface of [its] body with the nicotine. That got us to look at the caterpillar’s headspace and, sure enough, there’s nicotine coming out of the caterpillar’s spiracles. That allowed us understand that the gene was functioning to repurpose a little bit of the nicotine into the blood and from the blood to the spiracles where they puff it out, giving the caterpillar toxic halitosis. The big message here isn’t as much about this particular gene, but rather that we were able to use other organisms, out in nature, for phenotyping and understanding gene function. This is a QnAs with a recently elected member of the National Academy of Sciences to accompany the member’s Inaugural Article on page 1245.
www.pnas.org/cgi/doi/10.1073/pnas.1320016110
