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Abstract

Two genes, LEAFY (LFY) and APETALA1 (AP1), are required to specify floral
identity in Arabidopsis. Expression of LFY in otherwise non-reproductive
meristems can cause their conversion into floral meristems in a variety of
species, demonstrating that it is a master regulator of floral development.
AP1 is a direct target of LFY, and both act in a partially redundant manner to
specify floral meristem identity. At least some of this function is due to activation
and regulation of various homeotic genes, which control the identity of
different floral organs. Biochemically, LFY is a sequence specific DNA-binding
protein with no similarity to any other plant or animal protein.
Homologs of LFY have been cloned from many seed plants (angiosperms and
gymnosperms), as well as from the more distant non-flowering Pteridophytes
and Bryophytes (ferns and mosses). All share two highly conserved domains.
Despite their similarity to their seed plant counterparts, the function of the
LFY homologs in species that arose prior to evolution of floral structure is
unclear. We have decided to take advantage of the molecular diversity generated
during evolution to obtain insights into the structure-function relationships of
LFY. We sampled a set of homologs derived from all major clades of extant
plants and tested the functionality in several ways. By combining classical
phenotypic analysis with genome-wide molecular profiling, we assayed the
potency of the different homologs to rescue a strong null allele of LFY. We
also assayed in yeast models their transcriptional activity and DNA binding
activity. Several conclusions arose from this study. First, flowers and activity
of LFY homologs in Arabidopsis date to the same evolutionary time point.
Almost all angiosperms homologs are functionally interchangeable. However,
homologs from the non-flowering clades can only partially complement a
lfy null allele, their potency being inversely proportional to their evolutionary
distance. Second, among the molecular targets of LFY, AP1 is the main
output. AP1 is the only target upregulated by the homologs from non-flowering
plants. Third, the different homologs vary in their DNA binding affinity.
By building chimera between reference homologs, we have established that
the conserved domains contribute more than the non-conserved domains
to diversification of LFY activity. Finally the role of criticals amino-acids for
evolution of LFY function is examined.