Unique structural characteristics and evolution of a cluster of venom phospholipase A2 isozyme genes of Protobothrops flavoviridis snake

Naoki Ikeda, Takahito Chijiwa, Kazumi Matsubara, Naoko Oda-Ueda, Shosaku Hattori, Yoichi Matsuda, Motonori Ohno

Research output: Contribution to journalArticle

28 Citations (Scopus)

Abstract

Protobothrops flavoviridis (Crotalinae) venom gland phospholipase A2 (PLA2) isozyme genes have evolved in an accelerated manner to acquire diverse physiological activities in their products. For elucidation of the multiplication mechanism of PLA2 genes, a 25,026 bp genome segment harboring five PLA2 isozyme genes was obtained from Amami-Oshima P. flavoviridis liver and sequenced. The gene PfPLA 2 encoded [Lys49] LA2 called BPII, the gene PfPLA 4 neurotoxic [Asp49]PLA2 called PLA-N, the gene PfPLA 5 basic [Asp49]PLA2 called PLA-B, and PfPLA 1(Ï¿) and PfPLA 3(Ï¿) were the inactivated genes. The 5' truncated reverse transcriptase (RT) elements, whose intact forms constitute long interspersed nuclear elements (LINEs), were found in close proximity to the 3' end of PLA2 genes and named PLA2 gene-coupled RT fragments (PcRTFs). The facts that PcRTFs have the stemâ¿¿loop and repetitive sequence in the 3' untranslated region (UTR) which is characteristic of CR1 LINEs suggest that PcRTFs are the debris of P. flavoviridis ancestral CR1 LINEs, denoted as PfCR1s. Since the associated pairs of PLA2 genes and PcRTFs are arranged in tandem in the 25,026 bp segment, it is thought that an ancestral PLA2 gene-PfCR1 unit (PfPLA-PfCR1) which was produced by retrotransposition of PfCR1 by itself to the 3' end of PLA2 gene duplicated several times to form a multimer of PfPLA-PfCR1, a cluster of PLA2 genes, in the period after Crotalinae and Viperinae snakes branched off. Recombinational hot spot of a 37 bp segment, named Scomb, was found in the region 548 bp upstream from the TATA box of PLA2 genes. Thus, it could be assumed that multiplication of PfPLA-PfCR1 occurred by unequal crossing over of the segment, -Scomb-PfPLA-PfCR1-Scomb-. The PfCR1 moieties were afterward disrupted in the 5' portion to PcRTFs. The detection of two types of PcRTFs different in length which were produced by elimination of two definitive sequences in PfCR1 moiety possibly by gene conversion clearly supports such process but not multiplication of the PLA2 gene-PcRTF unit.
Original languageEnglish
Pages (from-to)15-25
Number of pages11
JournalGene
Volume461
DOIs
Publication statusPublished - 2010
Externally publishedYes

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Snakes
Phospholipases A2
Venoms
Isoenzymes
Genes
RNA-Directed DNA Polymerase
Gene Conversion
TATA Box

Cite this

Ikeda, Naoki ; Chijiwa, Takahito ; Matsubara, Kazumi ; Oda-Ueda, Naoko ; Hattori, Shosaku ; Matsuda, Yoichi ; Ohno, Motonori. / Unique structural characteristics and evolution of a cluster of venom phospholipase A2 isozyme genes of Protobothrops flavoviridis snake. In: Gene. 2010 ; Vol. 461. pp. 15-25.
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title = "Unique structural characteristics and evolution of a cluster of venom phospholipase A2 isozyme genes of Protobothrops flavoviridis snake",
abstract = "Protobothrops flavoviridis (Crotalinae) venom gland phospholipase A2 (PLA2) isozyme genes have evolved in an accelerated manner to acquire diverse physiological activities in their products. For elucidation of the multiplication mechanism of PLA2 genes, a 25,026 bp genome segment harboring five PLA2 isozyme genes was obtained from Amami-Oshima P. flavoviridis liver and sequenced. The gene PfPLA 2 encoded [Lys49] LA2 called BPII, the gene PfPLA 4 neurotoxic [Asp49]PLA2 called PLA-N, the gene PfPLA 5 basic [Asp49]PLA2 called PLA-B, and PfPLA 1({\"I}¿) and PfPLA 3({\"I}¿) were the inactivated genes. The 5' truncated reverse transcriptase (RT) elements, whose intact forms constitute long interspersed nuclear elements (LINEs), were found in close proximity to the 3' end of PLA2 genes and named PLA2 gene-coupled RT fragments (PcRTFs). The facts that PcRTFs have the stem{\^a}¿¿loop and repetitive sequence in the 3' untranslated region (UTR) which is characteristic of CR1 LINEs suggest that PcRTFs are the debris of P. flavoviridis ancestral CR1 LINEs, denoted as PfCR1s. Since the associated pairs of PLA2 genes and PcRTFs are arranged in tandem in the 25,026 bp segment, it is thought that an ancestral PLA2 gene-PfCR1 unit (PfPLA-PfCR1) which was produced by retrotransposition of PfCR1 by itself to the 3' end of PLA2 gene duplicated several times to form a multimer of PfPLA-PfCR1, a cluster of PLA2 genes, in the period after Crotalinae and Viperinae snakes branched off. Recombinational hot spot of a 37 bp segment, named Scomb, was found in the region 548 bp upstream from the TATA box of PLA2 genes. Thus, it could be assumed that multiplication of PfPLA-PfCR1 occurred by unequal crossing over of the segment, -Scomb-PfPLA-PfCR1-Scomb-. The PfCR1 moieties were afterward disrupted in the 5' portion to PcRTFs. The detection of two types of PcRTFs different in length which were produced by elimination of two definitive sequences in PfCR1 moiety possibly by gene conversion clearly supports such process but not multiplication of the PLA2 gene-PcRTF unit.",
keywords = "Protobothrops flavoviridis, Phospholipase A2 gene, CR1 LINE, Multiplication, Unequal crossing over, Retrotransposition.",
author = "Naoki Ikeda and Takahito Chijiwa and Kazumi Matsubara and Naoko Oda-Ueda and Shosaku Hattori and Yoichi Matsuda and Motonori Ohno",
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journal = "Gene",
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Unique structural characteristics and evolution of a cluster of venom phospholipase A2 isozyme genes of Protobothrops flavoviridis snake. / Ikeda, Naoki; Chijiwa, Takahito; Matsubara, Kazumi; Oda-Ueda, Naoko; Hattori, Shosaku; Matsuda, Yoichi; Ohno, Motonori.

In: Gene, Vol. 461, 2010, p. 15-25.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Unique structural characteristics and evolution of a cluster of venom phospholipase A2 isozyme genes of Protobothrops flavoviridis snake

AU - Ikeda, Naoki

AU - Chijiwa, Takahito

AU - Matsubara, Kazumi

AU - Oda-Ueda, Naoko

AU - Hattori, Shosaku

AU - Matsuda, Yoichi

AU - Ohno, Motonori

PY - 2010

Y1 - 2010

N2 - Protobothrops flavoviridis (Crotalinae) venom gland phospholipase A2 (PLA2) isozyme genes have evolved in an accelerated manner to acquire diverse physiological activities in their products. For elucidation of the multiplication mechanism of PLA2 genes, a 25,026 bp genome segment harboring five PLA2 isozyme genes was obtained from Amami-Oshima P. flavoviridis liver and sequenced. The gene PfPLA 2 encoded [Lys49] LA2 called BPII, the gene PfPLA 4 neurotoxic [Asp49]PLA2 called PLA-N, the gene PfPLA 5 basic [Asp49]PLA2 called PLA-B, and PfPLA 1(Ï¿) and PfPLA 3(Ï¿) were the inactivated genes. The 5' truncated reverse transcriptase (RT) elements, whose intact forms constitute long interspersed nuclear elements (LINEs), were found in close proximity to the 3' end of PLA2 genes and named PLA2 gene-coupled RT fragments (PcRTFs). The facts that PcRTFs have the stemâ¿¿loop and repetitive sequence in the 3' untranslated region (UTR) which is characteristic of CR1 LINEs suggest that PcRTFs are the debris of P. flavoviridis ancestral CR1 LINEs, denoted as PfCR1s. Since the associated pairs of PLA2 genes and PcRTFs are arranged in tandem in the 25,026 bp segment, it is thought that an ancestral PLA2 gene-PfCR1 unit (PfPLA-PfCR1) which was produced by retrotransposition of PfCR1 by itself to the 3' end of PLA2 gene duplicated several times to form a multimer of PfPLA-PfCR1, a cluster of PLA2 genes, in the period after Crotalinae and Viperinae snakes branched off. Recombinational hot spot of a 37 bp segment, named Scomb, was found in the region 548 bp upstream from the TATA box of PLA2 genes. Thus, it could be assumed that multiplication of PfPLA-PfCR1 occurred by unequal crossing over of the segment, -Scomb-PfPLA-PfCR1-Scomb-. The PfCR1 moieties were afterward disrupted in the 5' portion to PcRTFs. The detection of two types of PcRTFs different in length which were produced by elimination of two definitive sequences in PfCR1 moiety possibly by gene conversion clearly supports such process but not multiplication of the PLA2 gene-PcRTF unit.

AB - Protobothrops flavoviridis (Crotalinae) venom gland phospholipase A2 (PLA2) isozyme genes have evolved in an accelerated manner to acquire diverse physiological activities in their products. For elucidation of the multiplication mechanism of PLA2 genes, a 25,026 bp genome segment harboring five PLA2 isozyme genes was obtained from Amami-Oshima P. flavoviridis liver and sequenced. The gene PfPLA 2 encoded [Lys49] LA2 called BPII, the gene PfPLA 4 neurotoxic [Asp49]PLA2 called PLA-N, the gene PfPLA 5 basic [Asp49]PLA2 called PLA-B, and PfPLA 1(Ï¿) and PfPLA 3(Ï¿) were the inactivated genes. The 5' truncated reverse transcriptase (RT) elements, whose intact forms constitute long interspersed nuclear elements (LINEs), were found in close proximity to the 3' end of PLA2 genes and named PLA2 gene-coupled RT fragments (PcRTFs). The facts that PcRTFs have the stemâ¿¿loop and repetitive sequence in the 3' untranslated region (UTR) which is characteristic of CR1 LINEs suggest that PcRTFs are the debris of P. flavoviridis ancestral CR1 LINEs, denoted as PfCR1s. Since the associated pairs of PLA2 genes and PcRTFs are arranged in tandem in the 25,026 bp segment, it is thought that an ancestral PLA2 gene-PfCR1 unit (PfPLA-PfCR1) which was produced by retrotransposition of PfCR1 by itself to the 3' end of PLA2 gene duplicated several times to form a multimer of PfPLA-PfCR1, a cluster of PLA2 genes, in the period after Crotalinae and Viperinae snakes branched off. Recombinational hot spot of a 37 bp segment, named Scomb, was found in the region 548 bp upstream from the TATA box of PLA2 genes. Thus, it could be assumed that multiplication of PfPLA-PfCR1 occurred by unequal crossing over of the segment, -Scomb-PfPLA-PfCR1-Scomb-. The PfCR1 moieties were afterward disrupted in the 5' portion to PcRTFs. The detection of two types of PcRTFs different in length which were produced by elimination of two definitive sequences in PfCR1 moiety possibly by gene conversion clearly supports such process but not multiplication of the PLA2 gene-PcRTF unit.

KW - Protobothrops flavoviridis

KW - Phospholipase A2 gene

KW - CR1 LINE

KW - Multiplication

KW - Unequal crossing over

KW - Retrotransposition.

U2 - 10.1016/j.gene.2010.04.001

DO - 10.1016/j.gene.2010.04.001

M3 - Article

VL - 461

SP - 15

EP - 25

JO - Gene

JF - Gene

SN - 0378-1119

ER -