INTRODUCTION
In the Lecanoid chromosome system of Coccids, or mealybugs,
two important genetic phenomena are widely expressed:
facultative heterochromatization and chromosome imprinting.
The classical cytogenetic descriptions of Coccids (Hughes-
Schrader, 1948; Brown and Nur, 1964) showed that both of
these chromosomal processes are developmentally regulated.
In the Lecanoid system, chromosomes are holocentric and
there are no sex chromosomes. All embryos start development
from fertilized eggs and both males and females begin with
diploid euchromatic chromosome complements. The paternal
and maternal chromosome sets remain euchromatic throughout
ontogeny of females in the soma and the germline (Brown and
Nur, 1964). By contrast, in embryos that are to become male,
the entire paternally derived haploid chromosome set becomes
heterochromatic at mid-cleavage. In subsequent cell divisions,
the derivatives of the paternal chromosome set appear as
chromocenters in interphase nuclei in most tissues. The
heterochromatic set retains the cytological properties of
condensed metaphase chromosomes throughout the cell cycle.
It is distinguishable from the euchromatic one until metaphase,
when both sets reach the same degree of condensation. During
spermatogenesis, the heterochromatic set is eliminated and
only the maternally derived euchromatic chromosomes are
included in the sperm. The inactivation of the haploid paternal
set of chromosomes represents a dramatic example of
facultative heterochromatization that renders male individuals
functionally haploid (parahaploidy). Moreover it is evident that
there is a mechanism for distinguishing between chromosome
sets of maternal and paternal origins (genomic imprinting) in
the developing male embryo (Nur, 1990; Bongiorni et al.,
1999).
Our previous work on imprinting in Coccids (Bongiorni et
al., 1999) suggested that the paternal and maternal
chromosome sets are characterized by different levels of CpG
methylation in embryos. Specifically, we provided cytological
evidence for hypomethylation of the paternal set of
chromosomes relative to the maternal set. Interestingly, both
male and female embryos showed this difference, suggesting
that methylation state at a whole chromosomal level might
serve as a distinguishing mark of parental origin but it does not
reflect overall transcriptional activity of the chromosome sets.
We now further investigate the underlying molecular basis for
imprinting by asking whether a chromosomal protein, HP-1,
which is implicated in heterochromatization in other systems,
is involved in imprinting and faculative heterochromatization
in Coccids.
In 1928, Heitz defined the heterochromatin as regions of
chromosomes that do not undergo cyclical changes in
condensation during cell cycle as the other chromosome
regions (euchromatin) do (Heitz, 1928). The condensed
appearance of heterochromatin in higher eukaryotes is thought
to be due to a specialized nucleoprotein structure. Thus far,
3809 Development 128, 3809-3817 (2001)
Printed in Great Britain © The Company of Biologists Limited 2001
DEV5453
The behavior of chromosomes during development of the
mealybug Planococcus citri provides one of the most
dramatic examples of facultative heterochromatization.
In male embryos, the entire haploid paternal chromosome
set becomes heterochromatic at mid-cleavage. Male
mealybugs are thus functionally haploid, owing to
heterochromatization (parahaploidy). To understand the
mechanisms underlying facultative heterochromatization
in male mealybugs, we have investigated the possible
involvement of an HP-1-like protein in this process. HP-1
is a conserved, nonhistone chromosomal protein with a
proposed role in heterochromatinization in other species.
It was first identified in Drosophila melanogaster as a
protein enriched in the constitutive heterochromatin of
polytene chromosome. Using a monoclonal antibody
raised against the Drosophila HP-1 in immunoblot and
immunocytological experiments, we provide evidence for
the presence of an HP-1-like in Planococcus citri
males and females. In males, the HP-1-like protein
is preferentially associated with the male-specific
heterochromatin. In the developing male embryos, its
appearance precedes the onset of heterochromatization.
In females, the HP-1-like protein displays a scattered but
reproducible localization pattern along chromosomes.
The results indicate a role for an HP-1-like protein in the
facultative heterochromatization process.
Key words: Facultative heterochromatization, HP-1, Mealybug
SUMMARY
Facultative heterochromatization in parahaploid male mealybugs:
involvement of a heterochromatin-associated protein
Silvia Bongiorni, Milena Mazzuoli, Stefania Masci and Giorgio Prantera*
Dipartimento di Agrobiologia e Agrochimica, Università della Tuscia, 01100 Viterbo, Italy
*Author for correspondence (e-mail: prantera@unitus.it)
Accepted 12 July 2001