Infection, Genetics and Evolution 1 (2002) 297–301
Short communication
Phylogenetic analysis of the genus Plasmodium based
on the gene encoding adenylosuccinate lyase
Lukasz Kedzierski
a
, Ananias A. Escalante
b,c
, Raul Isea
d
,
Casilda G. Black
a
, John W. Barnwell
c
, Ross L. Coppel
a,*
a
Department of Microbiology, P.O. Box 53, Monash University, 3800 Vic., Australia
b
Instituto Venezolano de Investigaciones Cientificas, Apartado 21827, Caracas 1020-A, Venezuela
c
Centers for Disease Control and Prevention, Mailstop F13, 4770 Buford Hwy NE, Atlanta, GA 30341, USA
d
Centro de Calculo Cient´ ıfico de la Universidad de Los Andes, Mérida, Venezuela
Received 10 September 2001; received in revised form 17 December 2001; accepted 24 December 2001
Abstract
Phylogenetic studies of the genus Plasmodium have been performed using sequences of the nuclear, mitochondrial and plastid genes.
Here we have analyzed the adenylosuccinate lyase (ASL) gene, which encodes an enzyme involved in the salvage of host purines needed
by malaria parasites for DNA synthesis. The ASL gene is present in several eukaryotic as well as prokaryotic organisms and does not
have repeat regions, which facilitates the accuracy of the alignment. Furthermore, it has been shown that ASL is not subject to positive
natural selection. We have sequenced the ASL gene of several different Plasmodium species infecting humans, rodents, monkeys and
birds and used the obtained sequences along with the previously known P. falciparum ASL sequence, for structural and phylogenetic
analysis of the genus Plasmodium. The genetic divergence of ASL is comparable with that observed in other nuclear genes such as cysteine
proteinase, although ASL cannot be considered conserved when compared to aldolase or superoxide dismutase, which exhibit a slower
rate of evolution. Nevertheless, a protein like ASL has a rate of evolution that provides enough information for elucidating evolutionary
relationships. We modeled 3D structures of the ASL protein based on sequences used in the phylogenetic analysis and obtained a consistent
structure for four different species despite the divergence observed. Such models would facilitate alignment in further studies with a greater
number of plasmodial species or other Apicomplexa. © 2002 Elsevier Science B.V. All rights reserved.
Keywords: Malaria; Adenylosuccinate lyase; Phylogenetic analysis; Plasmodium
Malaria is an infectious disease caused by parasites of
the genus Plasmodium and remains one of the major health
problems in tropical regions. Considerable interest has
focussed on investigating the phylogenetic relationship
between malaria species. Such relationship should be deri-
ved from as large a number of genes as possible to max-
imize certainty in the observed trees. The genes already
used in analyses include the 18S small subunit (SSU) rRNA
genes (Escalante and Ayala, 1994; Escalante et al., 1997;
Qari et al., 1996; Waters et al., 1991), the circumsporozoite
protein (CSP) gene (Escalante et al., 1995), the cytochrome
b gene from the mitochondria (Escalante et al., 1998) and
the gene encoding the caseinolytic protease CLpC from the
plastid (Rathore et al., 2001). Early studies suggested that
Plasmodium falciparum shares a common ancestor with
Abbreviations: ASL, adenylosuccinate lyase; PCR, polymerase chain
reaction; SSU rRNA, small subunit ribosomal RNA; NJ, neighbor-joining
*
Corresponding author. Tel.: +61-3-9905-4822; fax: +91-3-9905-4811.
E-mail address: ross.copple@med.monash.edu.au (R.L. Coppel).
avian parasites (Waters et al., 1991; Waters et al., 1993), but
subsequent inclusion of P. reichenowi (chimpanzee malaria
species) sequences into phylogenetic analyses, showed that
P. falciparum shares a more recent ancestor with this species
(Escalante and Ayala, 1994; Escalante et al., 1995; Escalante
et al., 1998; Qari et al., 1996). Those studies were based on
18S SSU rRNA and CSP sequences. However, the pattern
of expression of ribosomal genes in Plasmodium is complex
(Corredor and Enea, 1993; McCutchan et al., 1995) and
thorough analysis of SSU rRNA sequences incorporating
secondary structure needs to be performed in order to obtain
a reliable tree (Escalante et al., 1997). Similar problems are
encountered when analysis is based on CSP data. The CSP
is a surface protein and as such is under selection by the
host immune system. Consequently, the CSP is polymor-
phic (Hughes, 1991), accumulates mutations rapidly, which
may lead to the distortion of the phylogenetic inferences.
Genes that are relatively conserved across different species
and not subject to immune selection are preferable for
determining evolutionary relationship. One such gene is
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