Evolutionary Genomics

Courtesy of Photographic Services, Indiana University Jeffrey Palmer Mention gene sequencing and most people probably think of disease cures and supercrops. But genes mean a whole lot more, including deep insight into how present-day species got here. Indiana University biology professor Jeffrey Palmer practically invented the field of plant molecular systematics and phylogeny--using genes to inform taxonomic relationships and evolutionary history. According to Palmer's colleague at India

Aug 21, 2000
Barry Palevitz

Courtesy of Photographic Services, Indiana University

Jeffrey Palmer
Mention gene sequencing and most people probably think of disease cures and supercrops. But genes mean a whole lot more, including deep insight into how present-day species got here.

Indiana University biology professor Jeffrey Palmer practically invented the field of plant molecular systematics and phylogeny--using genes to inform taxonomic relationships and evolutionary history. According to Palmer's colleague at Indiana, Loren Rieseberg, "Palmer is considered by many to be the world leader in evolutionary genomics .... I can think of no one who has contributed more to our understanding of how eukaryotic genomes evolve and interact." Robert Jansen, Palmer's first postdoctoral fellow and now a biology professor at the University of Texas in Austin, agrees: "He's largely responsible for the field exploding into what it is now."

Palmer started his scientific career as a Stanford University graduate student in the late 1970s exploring the chloroplast genome, and he quickly recognized its value for deciphering plant evolution. In those days, people used Cot curves, or the kinetics of renaturation, to assess the similarity of DNA samples. Palmer's strategy was so logical and successful--especially with the advent of restriction site mapping and then DNA sequencing--that a bevy of young scientists would later flock to his laboratory, eager to jump on the train before it left the station.

Palmer is quick to point out that some of his early postdoctoral fellows--he's trained about 30--came with little or no experience in molecular biology, having gotten their degrees in more traditional disciplines. They left Palmer's laboratory as a retooled, enthusiastic cadre, passing their knowledge on to the next generation. Jansen affirms Palmer's early insight and influence: "Jeff is kind of a rare individual. He recognized the power of these types of data for resolving phylogenetic relationships. He was more than willing to push the limit. I had only classical training in plant taxonomy. Jeff was willing to take me on."

Palmer has also made important discoveries about mitochondrial genomes, transfer of mitochondrial genes to the nucleus during evolution, and the origin of introns and plasmids.1-4 Recently, his laboratory combined nuclear, mitochondrial, and chloroplast gene sequences to help decipher early branches in the plant family tree.5-7

Palmer recently reflected on his career in biology, and the edited conversation follows in question-and-answer format.

 

Q: How did you end up working on what's now known as molecular systematics?

A: I've always loved plants, and that's how I got into science. I got interested in biology and gardening in high school. A Benedictine monk with a master's degree in botany, Father Peter, influenced me at St. Anselm's School in Washington, D.C. But it wasn't until the end of college that I found out what a gene was. As a graduate student at Stanford, I decided to work on chloroplast genes. I got into molecular evolution and phylogeny, and I've been doing it ever since.

 

Q: In hindsight, when did you realize that chloroplast genes would be so important in systematics?

A: Hindsight, of course, being problematic, it was actually pretty clear in work that I did at the very end of my Ph.D. in 1981 on chloroplast DNA phylogeny of tomato and related species8 that the chloroplast genome was going to be very useful in plant systematics. I started working on several different plant groups with this approach in '81-'82, and it was clear that the approach would work on all of them. I believe the first conference talk I gave on the use of chloroplast DNA in plant systematics was in 1982. It became clear at the same time that molecular systematics as a whole would be very important, with seminal work from Allan Wilson [of the University of California, Berkeley] and John Avise [of the University of Georgia].

 

Q: You also branched out beyond chloroplasts. How did that happen?

A: I got interested in larger questions--general questions about genome evolution, like the significance of intron evolution. When did the vast number of nuclear introns arise and how? Walter Gilbert proposed that introns arose very early, in primordial times, and current organisms that don't have them, like many bacteria, lost them.9 Now the data don't support an ancient origin of introns. Instead, they arose early in the evolution of eukaryotes. I got into the mitochondrial genome because it was there. I asked myself, why not take the fraction I was throwing down the sink and look at it?

 

Q: Why are chloroplast and mitochondrial genomes so useful in molecular phylogeny, for probing deep time?

A: Organelle genomes are better because it's easier to isolate the genes, and because of the high copy number per cell. On average, they also have fewer or no introns. There's also less gene duplication, which is a problem in the nuclear genome. Also, the neutral mutation rate is substantially higher in the nucleus than in chloroplast and mitochondrial genomes. [The reverse is true in animals, where the mutation rate for mitochondrial genes is higher.]

Genome evolution is interesting in its own right. It gets at the heart and soul of the problem of organelle gene transfer to the nucleus and the genetic coevolution of the eukaryotic cell. How did three genomes interact during evolution?

I like to say that plants do it and animals don't--functional gene transfer to the nucleus, that is. We first worked on this with the cytochrome oxidase [cox] genes in legumes, but we're now doing surveys of gene transfer. The genes for mitochondrial ribosomal proteins have a very high rate of transfer.

I like to think of plants as model systems to study transfer of functional genes to the nucleus. They're the only place that it's still occurring to any degree, but the process was so important in making eukaryotic cells. In animals, there's nothing left to study about it.

I also wonder why organelle genomes persist at all. They've already lost most of their genes. In the case of mitochondria, it's up to 90-99 percent.

And why don't genes move in the opposite direction, from the nucleus to mitochondria and chloroplasts? It could be that selection doesn't care, but there are other mechanistic biases that drive it in one direction.

 

Q: How does gene transfer occur at all, given the compartmentation of eukaryotic cells, with all the membranes to cross?

A: Remember, these events occur on evolutionary time scales; they're still rare on a cellular time scale. It's interesting because transfer is a very complex process, but with these ribosomal genes it occurs more frequently than silent base substitutions. When they enter the nucleus, the genes must cannibalize nuclear genes for things like promoters [which allow mRNA synthesis] and transit peptide sequences [which enable the encoded proteins to get into the organelles]. Apparently, almost anything goes.

 

Q: Some people fear that, with so many genomes being sequenced, science is moving too fast. They're concerned that we're getting beyond ourselves. Perhaps that's behind recent skepticism about genetically modified foods and gene patenting. What do you think?

"Genomes have bizarre properties. Evolution has played with genes so much, what we're doing is tiny."

A: There's so much diversity that we never suspected. Genomes have bizarre properties. Evolution has played with genes so much, what we're doing is tiny. I think genetic modification of plants can have detrimental effects, but that's already happening when we move species around. ... I don't think we're going to upset plants in any fundamental way by putting genes into chloroplasts. I think it's a great idea. Based on our work with cox genes, plants don't seem to care where genes are expressed.

 

Q: Looking back, what goes through your mind about how the field exploded over the years? Are you surprised?

A: I was certainly pleased, if not a bit surprised, by how well the DNA approaches and their results were received by most traditional plant systematists. A number of us Young Turks were afraid that the molecular approach would be met with hostility from this quarter, but that really didn't happen, despite the fact that the early attempts in the '70s to use plant protein sequences in systematics were largely poo-pooed by the old guard.

Overall, I'm not really surprised at how the field has exploded, taking into account technical developments--especially PCR and rapid DNA sequencing--that came along after our initial efforts ... and which, of course, I wouldn't have predicted. In one important and truly wonderful sense the field has developed unusually rapidly. The way in which plant molecular systematists have cooperated, exchanged reagents, pooled sequences, etc., has been really gratifying and has helped push the field a bit faster than it otherwise would have [gone].

 

Q: Do you have any idea what you'll be doing five or 10 years from now? Where will the field be?

A: I can't go there [laughing]. I could not predict what I'd be doing in two years! It hasn't worked in the past. There are too many surprises.

 

Q: What was your reaction to being elected to the National Academy of Sciences recently?

A: I was absolutely thrilled and honored. I was fortunate to have a large number of exceptional people in the lab, especially early on. I want to pay tribute to them, and to the current people in my lab.

I guess I was in the right place at the right time. Molecular evolution was a relatively uncrowded field. I didn't have to worry as much about competition. It's now surprisingly competitive.S

 

Barry A. Palevitz is a contributing editor for The Scientist.

 

References

1. J.D. Palmer, J.M. Logsdon Jr., "The recent origins of introns," Current Opinion in Genetic Development, 1:470-7, 1991.

2. C.F. Delwiche, J.D. Palmer, "The origin of plastids and their spread via secondary symbiosis," Plant Systematics and Evolution, Supp. 11:53-86, 1997.

3. K.L. Adams et al., "Intracellular gene transfer in action: dual transcription and multiple silencings of nuclear and mitochondrial cox2 genes in legumes," Proceedings of the National Academy of Sciences (PNAS), 96:13863-8, Nov. 23, 1999.

4. J.D. Palmer et al., "Dynamic evolution of plant mitochondrial genomes: mobile genes and introns, and highly variable mutation rates," PNAS, 97:6960-6, June 20, 2000.

5. Y.-L. Qiu et al., "The gain of three mitochondrial introns identifies liverworts as the earliest land plants," Nature, 394:671-4, 1998.

6. C.L. Parkinson et al., "Multigene analyses identify the three earliest lineages of extant flowering plants," Current Biology, 9:1485-8, Dec. 6, 1999.

7. S.-M. Chaw et al., "Seed plant phylogeny inferred from all three plant genomes: monophyly of extant gymnosperms and origin of Gnetales from conifers," PNAS, 97: 4086-91, April 11, 2000.

8. J.D. Palmer, D. Zamir, "Chloroplast DNA evolution and phylogenetic relationships in lycopersicon," PNAS, 79:5006-10, 1982.

9. W. Gilbert et al., "On the antiquity of introns," Cell, 46:151-4, 1986.