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Baroque Botany: Elaborate but Functional

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In the documentary Biology of the Baroque, Michael Denton considers the challenge to Darwinian explanations of "biological features that may be adaptive, but they appear to be far beyond what is needed for mere survival." The film explores numerous examples that are "completely outside the domain of natural selection" because they emerge without ancestors, are gratuitously complex, and would have had no adaptive value even if ancestors were known. A good example is flowering plants.

The origin of angiosperms is frequently called "Darwin's abominable mystery" because the rise and diversification of flowering plants in the fossil record is so sudden. Denton quotes a biologist in Evolution: Still a Theory in Crisis who admits to other "mini-abominations" found in the various families of angiosperms.

The mystery goes much deeper than the lack of ancestors, however. On pages 151-156, Denton pulls back the curtain on one of the most elaborate reproductive cycles in nature: the pollination of flowers. In particular, the "arduous" journey of the pollen tube to its target synergids in the ovule, leading to double fertilization -- unique to angiosperms -- is part of a pathway so complex it "simply beggars belief." There's no way, Denton contends, this "baroque" arrangement could have arisen by natural selection.

The curtain pulled open a little more with the publication of two papers in Nature about pollen tube guidance. Pollen grains are as fine as dust, from 6 to 100 micrometers across depending on the species. Yet when they land on the pistil of a flower, an amazing transformation begins. The pollen grain grows a tube down the long style on the pistil toward the ovary, where ovules await fertilization. The tip of the tube contains two sperm cells needed to fertilize the egg and build the endosperm, a food source that the future seedling will consume upon sprouting. (The endosperm is triploid -- another novelty that Denton describes on page 155.) An animation by Michael Fletcher illustrates the basics of the "baroque" process of double fertilization.

How does the pollen tube find its target in the dark? That's what the Nature papers discuss. The process requires detailed signaling between pollen and ovule. "In flowering plants, the female gametophyte secretes chemoattractant peptides to guide pollen tube growth so that it delivers the immobile sperm to the ovule-enclosed female gametophyte," the Editor's summary states (emphasis added). Cheung and Wu introduce the plant's challenge and solution: the ovule "LUREs" the pollen tube.

For flowering plants to achieve fertilization, pollen must transport sperm across long distances. Sperm-containing pollen grains land on the stigma of the female reproductive organ (the pistil), but the female gametophyte structures that bear eggs are located in distant ovules, so each grain produces a pollen tube that grows towards them (Fig. 1a). How pollen tubes find their target has long puzzled biologists. The female gametophyte is known to produce chemoattractant molecules, such as cysteine-rich peptides called LUREs, but the identity of their receptors on pollen tubes has been unclear. Two papers in this issue identify several molecules on the cell membrane that are involved in sensing one such attractant -- AtLURE1 -- in the model plant Arabidopsis thaliana. These discoveries underscore the molecular complexity of this male-female communication process, and provide a foundation for understanding the mechanism by which pollen tubes sense attractants.

The female cell needs to produce the AtLURE1 peptide, coded in DNA and translated by its ribosome, and get it up the pistil to the pollen grain. The pollen tube, in turn, needs to produce a receptor that recognizes this attractant and can follow it back. The complexity of these interactions has begun to become evident in the two papers summarized by Cheung and Wu.

It is well established that pollen-specific receptor-like kinase (RLK) proteins can regulate the growth of pollen tubes. These proteins typically have three domains: an ectodomain that interacts with extracellular signal molecules; a membrane-spanning domain; and a cytoplasmic domain that attaches phosphate groups to target molecules, inducing cellular responses to incoming signals (Fig. 1b). Using different genetic strategies and starting from an overlapping list of almost 30 pollen-expressed RLKs, the two groups searched for proteins that support ovule targeting by pollen tubes.

The receptors, in other words, are complex three times over. They need to have docking ports for the incoming signal molecules (called "male discoverer" 1 and 2, as well as a pair of RLKs that regulate the tube growth). They need to span the membrane of the pollen tube. And they need to respond by switching on genes in the nucleus. Another team found a second pair of pollen-specific receptor kinases that also are involved.

Taken together, the groups' results indicate that the perception system for AtLURE1 involves multiple RLKs that are functionally redundant, acting together to support ovule targeting by pollen tubes and ensure reproductive success.

The number of players in just this one aspect of angiosperm fertilization has grown, and the scientists are still not sure they have found them all. This underscores Denton's point: these are all novelties that defy Darwinian selection. If all that is needed is getting sperm and egg together, there are simpler ways to do it than building a long pistil that requires an arduous journey by a pollen tube, multiple signaling molecules and receptors, and the elaborate dance of double fertilization. All the novel processes and parts seem superfluous if survival were the only criterion.

The arsenal of signalling molecules in plants -- in particular peptide signal molecules and RLKs -- is immense. It will not be surprising if more attractant-receptor pairs are discovered. The current studies, together with our knowledge of other growth regulatory molecules that interact with pollen tubes before they encounter ovule attractants, bring us closer to fully understanding a process that is vital for plant reproduction.

What's clear is that angiosperms are very, very successful. We've talked before about the "angiosperm explosion" as a challenge to Darwinism. How much more do these recent discoveries present a challenge! We may not understand why so many players are involved, but what we do know is that flowering plants inhabit almost every habitat on the earth, from the hottest deserts to the Arctic Circle. Complex as it is, the process works.

They are not just successful. They are beautiful. Look again at the mathematical perfection of some of the flowers shown in Biology of the Baroque. Why should any organism follow mathematical forms like the Fibonacci series? Why the non-adaptive artistry in color and form? All angiosperms share the general theme, but the variations make a Bach fugue look trite by comparison.

Maybe scientists need to look beyond the mechanics to higher levels of purpose and design. Focusing on pipes, pedals and air pumps won't help an investigator understand the Bach fugue that opens the video. Denton acknowledges near the end of the video that a designer might have made things because he liked a particular pattern -- because it's beautiful or symmetrical.

"In other words, on a designer hypothesis, you don't need to show that all the order of biology in the world is specifically adaptive in a specific organism," he says.

"Natural selection has no reason to produce beauty," Ann Gauger says in Metamorphosis about a principle that applies to flowers as well as butterflies. "Beauty is a sign of the transcendent. It's purely gratuitous. We all recognize it. We just have to acknowledge what it points to."

Paul Nelson reaches deeper with his speculation that "There may well be in butterflies"(and in flowers) "aspects of beauty that are there not for the sake of reproduction or survival, but for us to appreciate."