Flowers and metamorphoses. A photo.

The Metamorphosis of Flowers
Enrico S. Coen’ and Rosemary Carpenter
John lnnes Institute, Colney Lane, Norwich NR4 7UH, United Kingdom

One of the unifying theories of plant biology is that the variety
of plant forms are simply different modifications of a common
growth plan. Different permutations of a few key features of
plant growth can generate a bewildering array of seemingly
distinct forms. There is perhaps no better illustration of this
than the comparison of a flower and a shoot. The idea that
these two apparently different structures might be fundamentally
equivalent goes back to Goethe’s treatise on metamorphosis,
published in 1790. He concluded, “Flowers which
develop from lateral buds are to be regarded as entire plants,
which are set in the mother plant, as the mother plant is set
in the earth” (Goethe, 1790). In equating flowers and shoots,
four key assertions need to be made.
First, the different parts of the flower (sepals, petals, stamens,
and carpels) are equivalent to the leaves of a shoot.
Second, the organs of both shoot and flower are separated
by internodes, but in the case of the flower these are so short
as to be barely visible. Third, the organs of shoot and flower
usually have a distinct phyllotaxy, or arrangement around the
central axis. Finally, the indeterminate growth that so characterizes
a shoot is suppressed in the case of a flower, both
apically, because it eventually stops producing organs around
the central axis, and laterally, because branches do not normally
alise in the axils of floral organs.
The comparison of flower and shoot therefore highlights four
key variables: organ identity, internode length, phyllotaxy, and
determinacy. The numerous forms and habits of plants simply
reflect different variations and permutations of these four
fundamental aspects of growth. What is their developmental
basis?
The development of shoots and flowers depends on the behavior
of meristems. On the periphery of meristems, groups
of cells are partitioned off to form either secondary meristems
or organ primordia. Phyllotaxy depends on the precise pattern
in which partitioning occurs. Determinacy also reflects
partitioning, most importantly whether it favors meristems or
primordia. Organ identity depends on the developmental characteristics
of primordia. Finally, the growth of regions between
primordia determines internode length. In the last few years,
the systematic analysis of flower development has allowed
genetic control of these key aspects of plant development to
be dissected and studied in detail. Some of the findings have
been reviewed elsewhere (Schwarz-Sommer et al., 1990; Coen
and Meyerowitz, 1991). The aim of this review is to give a
general overview of the field, highlighting some of the more
recent problems and results obtained from studies of Antirrhinum
and Arabidopsis.
Genetic studies have defined two main types of gene as
being involved in flower development, meristem and organ
identity genes. Meristem identity genes generally affect all four
of the key aspects of plant growth and, therefore, the properties
of meristems as a whole. Organ identity genes more
specifically affect the fate of primordia and, hence, the types
of organ that are made. However, there is considerable overlap
between these categories. Meristem identity genes may
sometimes have more restrictive effects. Conversely, organ
identity genes can have more extensive effects and influence
aspects of growth other than just the fate of primordia.