INTRODUCTION
The carriers of protein translation in eukaryotic cells, the
ribosomes, have a complex structure consisting of two subunits
– the 60S (Large) and 40S (Small) subunit – that are each built
from a considerable number of ribosomal proteins (RPs) and
ribosomal RNAs (Moore, 1998). From one of the most well-
studied models for ribosome structure and constitution, the rat,
we now know that eukaryotic ribosomes consist of 82 different,
highly conserved proteins (Wool et al., 1995).
The importance of the protein translation machinery in a
given process can be studied by analysing the effect of a single
rp mutation, as the absence of a single RP prevents assembly
of the corresponding ribosomal subunit (Volarevic ´ et al., 2000).
Notably, apart from expected defects such as growth arrest or
delay, mutations in RP genes often result in specific defects in
the development of an organism (Wool, 1996). In some cases,
RP gene mutations affect DNA replication, RNA processing
and DNA repair (Wool, 1996), suggesting roles for RPs that
are additional to protein translation.
One of the most prominent examples of specific
developmental defects due to RP gene mutations is the Minute
syndrome in Drosophila. The Minute class of mutants was
described, as early as in 1919 (Lambertsson, 1998), and today
over 50 different Minute loci have been mapped. The Minute
syndrome is characterised by semi-dominant phenotypes, such
as delay in larval development, smaller body size and several
pleiotropic morphological aberrations (e.g. short thoracic
bristles), and recessive embryo lethality. Kongsuwan and co-
workers (Kongsuwan et al., 1985) first showed that a Minute
phenotype was caused by a deletion of a RP gene, and now,
at least 11 Minute loci have been assigned to RP genes
(Lambertsson, 1998), demonstrating that ribosome function is
essential during specific stages of fly development and that
individual RPs can easily become rate-limiting for various
processes.
Only few mutations in RP genes have been described in the
plant Arabidopsis thaliana. Two such mutations were
identified during screens for either aberrant seedling
phenotypes (van Lijsebettens et al., 1994) or altered sensitivity
to genotoxic stress (Revenkova et al., 1999). A third rp mutant,
identified through sequence analyses of Ds transposon
insertion sites, also appeared to show specific defects in
seedling development (Ito et al., 2000). Strikingly, all three of
the above rp phenotypes were found to be recessive. Semi-
dominant phenotypes, as described for the Drosophila Minute
mutants, have not been reported in plants. This might be a
consequence of the fact that RP genes are single copy
in Drosophila (Kay and Jacobs-Lorena, 1987), while in
Arabidopsis each RP is represented by a small gene family
4289 Development 128, 4289-4299 (2001)
Printed in Great Britain © The Company of Biologists Limited 2001
DEV0353
Mutations in ribosomal protein (RP) genes in Drosophila
lead to strong developmental phenotypes, expressed in the
semi-dominant Minute syndrome. In plants, however,
mutations in RP genes have so far only been reported to
result in recessive developmental phenotypes. We present
the analysis of an Arabidopsis promoter-trap line, in which
a T-DNA insertion in an RPS5 gene (AtRPS5A) causes semi-
dominant developmental phenotypes. Most cell-division
processes are delayed or disturbed in the heterozygous
mutant, and development is completely arrested at an early
embryonic stage in the homozygous mutant. By analogy
with Drosophila rp mutants, we have named this mutant
Arabidopsis Minute-like 1 (aml1). As with other Arabidopsis
RPs, RPS5 is represented by a small gene family, but
in contrast to other described plant RPs, this family
comprises only two members. The AtRPS5A gene (mutated
in aml1) is strongly expressed in dividing cells, whereas
expression of the second RPS5 gene, AtRPS5B, is lower
than that of AtRPS5A, and is correlated with cell
differentiation rather than cell division. From expression
analyses we conclude that AtRPS5A is the most abundantly
expressed RPS5 gene in Arabidopsis. The Minute-like
defects in the aml1 mutant provide the first evidence that
ribosome insufficiency leads to similar consequences in
both plants and insects, and emphasize the general
importance of efficient protein translation for cell
proliferation in higher eukaryotes.
Key words: Arabidopsis, Semi-dominant mutation, Cell division,
Ribosomal protein, Minute syndrome, Haplo-insufficiency
SUMMARY
An Arabidopsis Minute-like phenotype caused by a semi-dominant mutation
in a RIBOSOMAL PROTEIN S5 gene
Dolf Weijers, Marry Franke-van Dijk, Robert-Jan Vencken, Ab Quint, Paul Hooykaas and Remko Offringa*
Institute of Molecular Plant Sciences, Leiden University, Clusius Laboratory, Wassenaarseweg 64, 2333 AL, Leiden, The
Netherlands
*Author for correspondence (e-mail: offringa@rulbim.leidenuniv.nl)
Accepted 8 August 2001