Life's big homeobox of tricks

The Pinciples of Development - Molecular Embryology of Flowering Plants
June 12, 1998

You probably take for granted your multicellularity, but not everyone does. Biologists, especially developmental biologists, have a penchant for multicellular organisms. Yeast, bacteria and a few other single-celled organisms attract attention, but the real action is in "multicellulars". The reasons are not immediately obvious to the non-biologist: multicellulars are not necessarily big (witness mites and fleas) and the biggest ones are not necessarily very complicated. The giant sequoia tree, made up of billions upon billions of cells, is a fairly simple structure. What is so special about multicellularity then?

In animals multicellularity means that the germ line is sequestered from the rest of the cells that make up the body. This technical phrase simply means that some of the cells in animals - the sperm and eggs - are specially anointed for reproduction. Reproduction is all they do, and none of the other cells ever gets to be one of them. Virtually all developmental biology follows from this. Even so, the separation of germ cells from what is known as soma was discovered only about 100 years ago by a German biologist called August Weismann. His germ-soma discovery would prove to be the final nail in the coffin of a doctrine known as Lamarckism, and would herald the modern era of developmental biology.

The Chevalier de Lamarck was a French aristocrat-cum-biologist who proposed the theory of the "inheritance of acquired characters" to explain how species obtain their features. Based on the principle of "use and disuse", Lamarck asserted, inter alia, that giraffes develop longer necks in their lifetimes from stretching to feed from the tops of trees. Successive generations of giraffes then inherit elongated necks. Blacksmiths' sons tend to have the sinewy arms of their fathers. Cave-dwelling animals lose their eyesight. Weismann showed that the trouble with Lamarck's view was that the cells that will eventually contribute to the next generation - the progenitors of sperm and eggs - are separated from the somatic cells in some of the earliest stages of embryonic development. They never get stretched or strengthened or have any contact with cells that do. If you do not believe Weismann just consider that successive generations of Jewish boys doggedly emerge from the womb with foreskins intact despite the stoic sacrifices their fathers make.

Sequestered germ lines lay the foundation stones for development by enslaving all of the somatic cells to the common purpose of promoting germ cells into the next generation. A somatic cell's only stake in the next generation is its genetic relatedness to the germ cells. Successful somatic cells, then, are ones that make bodies that grow up and reproduce. Competition among bodies leads to ever-greater complexity and specialisation. Somatic cells must learn to produce hands and feet, ears, eyes, noses and teeth all deployed to promote germ lines into the next generation. Organisms lacking sequestered germ lines never get this complex.

Lewis Wolpert is one of the best known of developmental biologists. With the help of five colleagues he has produced a textbook, The Principles of Development, of remarkable clarity to explain how somatic cells go about making bodies. To get a sense of how daunting this task is, consider that a lowly and very simple bacterium has over three million letters in its genetic handbook. Humans have over three billion. And that is just the start. There are, for example, vastly more neural connections in the brain alone than could ever be specified by the genes. This means that developmental biologists must not only be expert geneticists, they must also be expert ecologists. Why ecologists? Because so much of the information needed to build a body arises spontaneously out of how the various cells of the body interact with each other and on the local (ecological) conditions that prevail when they do.

Consider the most fundamental problem of development, that of how the emerging collection of cells in the early embryo specifies the "north-south" axis of all the major body parts from head to tail. Developmental biologists have discovered that this task is controlled by a cluster of genes called the "homeobox". Tantalisingly the homeobox genes line up along the chromosome in the same order as the body parts whose position they identify. Head genes first, followed by thorax genes and so on. Within a domain of such genes there is further positional ordering. In vertebrates,for example, forebrain, mid-brain and hindbrain genes also line up.

If the homeobox genes can be coaxed to work in succession, the rudiments of a body with pieces in the right order will emerge. But how to get them to do this? Wolpert thinks that the genes have evolved to pay attention to local concentrations of various signalling molecules. So long as the head genes start first, the necessary concentration gradient emerges and the body parts will follow in order. Wolpert has called this the "French Flag problem" to illustrate how a group of unordered cells might spontaneously produce a tricolour.

Homeobox genes were discovered in Drosophila, the fruit fly, which contain a single homeobox cluster. Since then developmental biologists have discovered that many of the homeobox genes found in higher animals such as frogs and mice may be descendants of drosophila homeobox genes. To a first approximation all animals share an ancient system of specifying their body plans. This is why researchers studying fruit flies, salamanders and mice can say such important things about human foetal development, genetic diseases and limb and organ regeneration, to name a few. Wolpert et al's description and presentation of these and many other ideas of development are first rate. The book is accessible to undergraduates and will prove valuable even to researchers.

Compared with the fun of being an animal developmental biologist, plant embryology can seem something of a poor relation. Plants lack a sequestered germ line. They consequently have comparatively few structures - they are not segmented like insects nor do they have heads, bodies, arms, legs, and tails like most animals - and therefore lack most of the requirements of homeobox patterning. If you are a plant seed, gravity and sunlight provide most of the positional information you need. This is one reason why Nasa scientists are so eager to see how well plants grow in space.

The real action with plants revolves around sex. Plants cannot get up and move around to find mates. They must either drop their germ cells into the air in hopes they will land in an appropriate spot or entice insects or other "pollinators" to carry their gametes around for them. This means attracting the pollinator with some sort of dazzling display or powerful perfume - few people realise that the Chelsea Flower Show owes its success to the fact that plants cannot walk.

Given all this it is perhaps not surprising that V. Raghavan's hefty Molecular Embryology of Flowering Plants devotes about 60 per cent of its pages to issues of gamete development, pollination and fertilisation. Immobility means that plants have to contend with the possibility that no individual of the opposite sex will be available. Many plant species solve this problem by carrying both kinds of sex organs on their bodies. If no females are available to rain down your pollen gametes on, you can let the local males rain on you. The trouble is you might also rain on yourself - a phenomenon known as self-fertilisation. Usually this is undesirable - anyone who has frequented small villages knows of the trenchant effects of inbreeding - so plants have developed mechanisms for avoiding it. Raghavan describes a complex system of genetic self-incompatibility loci operating in several plant systems. His treatment of this delicate issue is the most thorough I have seen, ranging from the pure molecular biology of self-incompatibility through to its developmental features.

The volume of work Raghavan reports on self-incompatibility, gene expression, pistil and anther development and embryogenesis makes his book an up-to-date reference suitable for research botanists. Raghavan's style is technical and precise; he is not writing for the beginner. The book represents more than a personal obsession with plants. Understanding self-incompatibility, for example, helps to predict just how far agricultural scientists can go in producing genetically homogeneous strains for crops. In the limit, too much similarity in a crop may result in plants that do not wish to fertilise each other. For technical genetic reasons, plants are prone to suffering from male sterility. Viagra will not help these poor fellows, but painstaking investigation of the genetic systems responsible might, and has agro-economic implications.

So there is far more to multicellularity than meets the eye (itself a highly complex multicellular structure). Next time you find yourself at a loss for words in a social situation try asking someone if they have ever been to the Chelsea Flower Show. Then take it from there.

Mark Pagel is a senior research fellow in the department of zoology, University of Oxford.

The Pinciples of Development

Author - Lewis Wolpert, Rosa Beddington, Jeremy Brockes, Thomas Jessell, Peter Lawrence, Elliot Meyerowitz
ISBN - 0 19 850263 X
Publisher - Oxford University Press
Price - £25.95
Pages - 484

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