Organization of the Mitochondrial Genomes of Whiteflies, Aphids, and Psyllids (Hemiptera, Sternorrhyncha)
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UC Davis UC Davis Previously Published Works Title Organization of the mitochondrial genomes of whiteflies, aphids, and psyllids (Hemiptera, Sternorrhyncha) Permalink https://escholarship.org/uc/item/5p0413fv Journal BMC Evolutionary Biology, 4 ISSN 1471-2148 Authors Thao, M L Baumann, Linda Baumann, P Publication Date 2004-08-01 Peer reviewed eScholarship.org Powered by the California Digital Library University of California BMC Evolutionary Biology BioMed Central Research article Open Access Organization of the mitochondrial genomes of whiteflies, aphids, and psyllids (Hemiptera, Sternorrhyncha) MyLo L Thao, Linda Baumann and Paul Baumann* Address: Microbiology Section, University of California, One Shields Ave., Davis, California, USA, 95616-8665 Email: MyLo L Thao - [email protected]; Linda Baumann - [email protected]; Paul Baumann* - [email protected] * Corresponding author Published: 03 August 2004 Received: 10 June 2004 Accepted: 03 August 2004 BMC Evolutionary Biology 2004, 4:25 doi:10.1186/1471-2148-4-25 This article is available from: http://www.biomedcentral.com/1471-2148/4/25 © 2004 Thao et al; licensee BioMed Central Ltd. This is an open-access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Abstract Background: With some exceptions, mitochondria within the class Insecta have the same gene content, and generally, a similar gene order allowing the proposal of an ancestral gene order. The principal exceptions are several orders within the Hemipteroid assemblage including the order Thysanoptera, a sister group of the order Hemiptera. Within the Hemiptera, there are available a number of completely sequenced mitochondrial genomes that have a gene order similar to that of the proposed ancestor. None, however, are available from the suborder Sternorryncha that includes whiteflies, psyllids and aphids. Results: We have determined the complete nucleotide sequence of the mitochondrial genomes of six species of whiteflies, one psyllid and one aphid. Two species of whiteflies, one psyllid and one aphid have mitochondrial genomes with a gene order very similar to that of the proposed insect ancestor. The remaining four species of whiteflies had variations in the gene order. In all cases, there was the excision of a DNA fragment encoding for cytochrome oxidase subunit III(COIII)- tRNAgly-NADH dehydrogenase subunit 3(ND3)-tRNAala-tRNAarg-tRNAasn from the ancestral position between genes for ATP synthase subunit 6 and NADH dehydrogenase subunit 5. Based on the position in which all or part of this fragment was inserted, the mitochondria could be subdivided into four different gene arrangement types. PCR amplification spanning from COIII to genes outside the inserted region and sequence determination of the resulting fragments, indicated that different whitefly species could be placed into one of these arrangement types. A phylogenetic analysis of 19 whitefly species based on genes for mitochondrial cytochrome b, NADH dehydrogenase subunit 1, and 16S ribosomal DNA as well as cospeciating endosymbiont 16S and 23S ribosomal DNA indicated a clustering of species that corresponded to the gene arrangement types. Conclusions: In whiteflies, the region of the mitochondrial genome consisting of genes encoding for COIII-tRNAgly-ND3-tRNAala-tRNAarg-tRNAasn can be transposed from its ancestral position to four different locations on the mitochondrial genome. Related species within clusters established by phylogenetic analysis of host and endosymbiont genes have the same mitochondrial gene arrangement indicating a transposition in the ancestor of these clusters. Page 1 of 13 (page number not for citation purposes) BMC Evolutionary Biology 2004, 4:25 http://www.biomedcentral.com/1471-2148/4/25 Background addition, there are 22 tRNAs, two for leucine and two for Whiteflies, psyllids, and aphids correspond to super- serine, and one tRNA each for the remaining eighteen families within the suborder Sternorrhyncha (Hemiptera) amino acids. In general, there is conservation of the gene [1]. These insects share a number of common properties order within phyla but variation between phyla [10,13- that are a consequence of their utilization of plant phloem 17]; the tRNA genes are subject to more change in their as their diet. This mode of feeding is accomplished by position than the genes for proteins and rRNAs. The order means of needle-like stylets that probe plant tissues of mitochondrial genes has been suggested to be a good between plant cells until they enter the phloem-sieve ele- phylogenetic marker for studies of relationships [14]. The ments. Due to this mode of feeding, some species are of animal mitochondrial genome is generally very compact major agricultural importance in that they vector plant with few if any intergenic spaces. Usually there is one (or pathogens and in high numbers may cause plant debilita- rarely more) noncoding region, frequently following 12S tion due to excessive nutrient consumption [1]. White- rDNA. Such a region most often has a reduced G+C con- flies, psyllids, and aphids have an obligatory association tent and all or some of the following properties: a) direct with prokaryotic endosymbionts localized in specialized repeats, b) inverted repeats, c) stretches of "T"s, "A"s, or cells called bacteriocytes that constitute a larger structure "TA"s. By analogy with other well-studied mitochondria, called the bacteriome [2-4]. In the past, numerous studies such a region is considered to be a putative origin of DNA have been performed on the phylogeny of some of these replication and a region from which transcription is initi- endosymbionts and their hosts [2-5]. The results have ated [10,12]. Variation in mitochondrial size is generally indicated congruence between the endosymbiont and the a consequence of variation in the length of the repeats in host derived phylogeny. This observation has been inter- the noncoding region and not in the number of structural preted as being the consequence of an infection of an genes. Early studies within the class Insecta suggested con- insect ancestor by a prokaryote and the vertical transmis- servation of the gene order over a wide range of different sion of the endosymbiont resulting in cospeciation or organisms indicating an ancestral gene order for this cocladogenesis. In a recent study of whiteflies, we com- group [10,18]. However, more recent studies have shown pared the phylogeny based on endosymbiont 16S*-23S* that within the Hemipteroid assemblage, there is consid- rDNA to the phylogeny of the host based on several mito- erable variation in the order of genes in the orders chondrial genes [6]. During this study, we found that in Phthiraptera, Psocoptera, and Thysanoptera, but no varia- the whitefly, Bemisia tabaci, the order of some of the mito- tion in the order Hemiptera (that includes the suborder chondrial genes was quite different from the frequently Sternorrhyncha) [18-21]. The complete sequence of the found order of genes in the mitochondria of the class mitochondria of a representative of the Phthiraptera (wal- Insecta. This observation led us to obtain the full sequence laby louse) and the Thysanoptera (plague thrips) has been of the mitochondrial genome of representatives of the obtained [18,20]. The latter shows major differences from suborder Sternorrhyncha. Due to the observed differences the ancestral gene order. The Hemiptera and the Thysano- in the order of genes in the mitochondrial genome of ptera are sister groups and it was consequently of interest whiteflies, we obtained additional mitochondrial to obtain sequences of the mitochondrial genomes of the sequences from species representative of the major phylo- former. Since the sequence of mitochondrial genomes is genetic clusters previously established on the basis of poorly conserved, sequence determination of a portion of whitefly mitochondrial and endosymbiont genes [6]. Pre- the genome is useful for the study of closely related spe- vious studies of the phylogenetic relationships of member cies or the population structure within a species [22,23]. of the Sternorrhyncha, using host 18S rDNA, indicated The availability of completely sequenced mitochondrial that it is a monophyletic group [7-9]. These studies also genomes is also an aid to the design of primers for the showed that aphids and whiteflies were more closely PCR amplification of the regions selected for population related to each other than to psyllids. studies. In animals, the mitochondrial genome is generally circu- Results lar (14–17 kb), is maternally transmitted and has a rela- Evolutionary relationships within the Sternorrhyncha tively simple genetic structure, and a rapid rate of Table 1 gives the properties and the accession numbers of sequence change [10-12]. Of the thirty seven genes found the mitochondrial DNA sequences determined in this in animal mitochondria, thirteen encode for proteins, study. An unrooted phylogenetic tree showing the rela- consisting of three subunits of cytochrome oxidase (COI, tionships of whiteflies, psyllids and aphids, based on COII, COIII), two subunits of ATP synthase (atp6, atp8), mitochondrial cytB (partial), ND1, and 16S rDNA is pre- seven subunits of NADH dehydrogenase (ND1, ND2, sented in Fig. 1. A similar tree is obtained when the amino ND3, ND4, ND4L, ND5, ND6), and cytochrome b (cytB).