Supplementary Information:
-485775-25590500The International Asian Longhorned Beetle Genome ConsortiumIII.4 Myrosinase and cyanogenic β-glycosidase-like sequencesContributorsLeslie A. Kuhn (Michigan State University, Departments of Biochemistry and Molecular Biology, Computer Science and Engineering, and Fisheries and Wildlife)Ann M. Ray (Xavier University, Department of Biology)Erin Scully (USDA-ARS, Grain, Forage, and Bioenergy Research, and University of Nebraska-Lincoln, Department of Agronomy and Horticulture, and The Pennsylvania State University, Department of Entomology and Center for Chemical Ecology)IntroductionHere we analyze whether sequences putatively identified as members of the beta-glycosyl hydrolase GH1 family (referred to as beta-glycosidases for brevity) are likely to encode for myrosinase (thioglucoside hydrolase) or cyanogenic beta-glycosidase (CBG) enzymes, two subfamilies of GH1. These enzymes are involved in detoxification of host compounds and chemical communication in plants and insects. We became interested in insect myrosinases, their roles in chemical signaling, and the possibility of controlling their activity with inhibitors when we discovered a UniProt Anoplophora glabripennis sequence annotated by sequence homology as myrosinase-1 according to PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5TY3VsbHk8L0F1dGhvcj48WWVhcj4yMDEzPC9ZZWFyPjxS
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ADDIN EN.CITE.DATA (57). A myrosinase system very similar to that in plants exists in insects such as cabbage aphids (Brevicoryne brassicae (L.)) and turnip aphids (Lipaphis (Hyadaphis) erysimi (Kaltenbach), Hemiptera: Aphididae), which use the isothiocyanate products of myrosinase (ITCs) as components of an alarm pheromone in combination with E-β-farnesene PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5EYXdzb248L0F1dGhvcj48WWVhcj4xOTg3PC9ZZWFyPjxS
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ADDIN EN.CITE.DATA (50, 96-98). Experiments are in progress to test the hypothesis that A. glabripennis adults and larvae produce myrosinase, and that field and laboratory-reared beetles differ in their expression of myrosinase. Additional studies are in progress to address the interesting question of whether myrosinase products act as chemical attractants for adults of A. glabripennis, possibly in combination with known male-produced compounds PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5Dcm9vazwvQXV0aG9yPjxZZWFyPjIwMTQ8L1llYXI+PFJl
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ADDIN EN.CITE PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5Dcm9vazwvQXV0aG9yPjxZZWFyPjIwMTQ8L1llYXI+PFJl
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ADDIN EN.CITE.DATA (99, 100).Cyanogenic beta-glycosidases (CBGs) are another GH1 subfamily involved in food detoxification by insects. CBGs are known to detoxify the “cyanide bomb” that plants use to deter herbivory, with cyanide-containing compounds such as amygdalin (also known as laetrile) being synthesized in trees of the genus Prunus ADDIN EN.CITE <EndNote><Cite><Author>Gleadow</Author><Year>2014</Year><RecNum>333</RecNum><DisplayText>(101)</DisplayText><record><rec-number>333</rec-number><foreign-keys><key app="EN" db-id="atawvvssk9f2soeepwy55091ppssa509t9aa" timestamp="1444254105">333</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Gleadow, R. M.</author><author>Moller, B. L.</author></authors></contributors><auth-address>School of Biological Sciences, Monash University, 3800 Victoria, Australia; email: ros.gleadow@monash.edu.</auth-address><titles><title>Cyanogenic glycosides: synthesis, physiology, and phenotypic plasticity</title><secondary-title>Annu Rev Plant Biol</secondary-title><alt-title>Annual review of plant biology</alt-title></titles><periodical><full-title>Annu Rev Plant Biol</full-title><abbr-1>Annual review of plant biology</abbr-1></periodical><alt-periodical><full-title>Annu Rev Plant Biol</full-title><abbr-1>Annual review of plant biology</abbr-1></alt-periodical><pages>155-85</pages><volume>65</volume><keywords><keyword>Glycosides/biosynthesis/*physiology</keyword><keyword>Plant Physiological Phenomena</keyword><keyword>Plants/*metabolism</keyword></keywords><dates><year>2014</year></dates><isbn>1545-2123 (Electronic)
1543-5008 (Linking)</isbn><accession-num>24579992</accession-num><urls><related-urls><url>;(101). Insect herbivores may metabolize cyanogenic glucosides or sequester them, also for use in defense against predators ADDIN EN.CITE <EndNote><Cite><Author>Zagrobelny</Author><Year>2004</Year><RecNum>310</RecNum><DisplayText>(102)</DisplayText><record><rec-number>310</rec-number><foreign-keys><key app="EN" db-id="atawvvssk9f2soeepwy55091ppssa509t9aa" timestamp="1437763577">310</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Zagrobelny, M.</author><author>Bak, S.</author><author>Rasmussen, A. V.</author><author>Jorgensen, B.</author><author>Naumann, C. M.</author><author>Lindberg Moller, B.</author></authors></contributors><auth-address>Department of Plant Biology and Center of Molecular Plant Physiology (PlaCe), Royal Veterinary and Agricultural University, 40 Thorvaldsensvej, DK-1871 Frederiksberg C, Copenhagen, Denmark.</auth-address><titles><title>Cyanogenic glucosides and plant-insect interactions</title><secondary-title>Phytochemistry</secondary-title><alt-title>Phytochemistry</alt-title></titles><periodical><full-title>Phytochemistry</full-title></periodical><alt-periodical><full-title>Phytochemistry</full-title></alt-periodical><pages>293-306</pages><volume>65</volume><number>3</number><keywords><keyword>Animals</keyword><keyword>Arthropods/physiology</keyword><keyword>Butterflies/physiology</keyword><keyword>Cyanides/chemistry/metabolism</keyword><keyword>Glycosides/*chemistry/*metabolism</keyword><keyword>Host-Parasite Interactions</keyword><keyword>Insects/*physiology</keyword><keyword>Lepidoptera/physiology</keyword><keyword>Nitriles/*chemistry/*metabolism</keyword><keyword>Pest Control, Biological</keyword><keyword>Plants, Edible/chemistry/*physiology</keyword></keywords><dates><year>2004</year><pub-dates><date>Feb</date></pub-dates></dates><isbn>0031-9422 (Print)
0031-9422 (Linking)</isbn><accession-num>14751300</accession-num><urls><related-urls><url>;(102). A few species of Arthropoda (within the classes Diplopoda, Chilopoda, and Insecta) synthesize cyanogenic glucosides de novo, and some of these same species are able to sequester cyanogenic glucosides from their host plants, e.g., Insecta: Lepidoptera: Zygaenidae (forester and burnet moths) ADDIN EN.CITE <EndNote><Cite><Author>Zagrobelny</Author><Year>2004</Year><RecNum>310</RecNum><DisplayText>(102)</DisplayText><record><rec-number>310</rec-number><foreign-keys><key app="EN" db-id="atawvvssk9f2soeepwy55091ppssa509t9aa" timestamp="1437763577">310</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Zagrobelny, M.</author><author>Bak, S.</author><author>Rasmussen, A. V.</author><author>Jorgensen, B.</author><author>Naumann, C. M.</author><author>Lindberg Moller, B.</author></authors></contributors><auth-address>Department of Plant Biology and Center of Molecular Plant Physiology (PlaCe), Royal Veterinary and Agricultural University, 40 Thorvaldsensvej, DK-1871 Frederiksberg C, Copenhagen, Denmark.</auth-address><titles><title>Cyanogenic glucosides and plant-insect interactions</title><secondary-title>Phytochemistry</secondary-title><alt-title>Phytochemistry</alt-title></titles><periodical><full-title>Phytochemistry</full-title></periodical><alt-periodical><full-title>Phytochemistry</full-title></alt-periodical><pages>293-306</pages><volume>65</volume><number>3</number><keywords><keyword>Animals</keyword><keyword>Arthropods/physiology</keyword><keyword>Butterflies/physiology</keyword><keyword>Cyanides/chemistry/metabolism</keyword><keyword>Glycosides/*chemistry/*metabolism</keyword><keyword>Host-Parasite Interactions</keyword><keyword>Insects/*physiology</keyword><keyword>Lepidoptera/physiology</keyword><keyword>Nitriles/*chemistry/*metabolism</keyword><keyword>Pest Control, Biological</keyword><keyword>Plants, Edible/chemistry/*physiology</keyword></keywords><dates><year>2004</year><pub-dates><date>Feb</date></pub-dates></dates><isbn>0031-9422 (Print)
0031-9422 (Linking)</isbn><accession-num>14751300</accession-num><urls><related-urls><url>;(102). Given that Prunus is one of the host genera for A. glabripennis PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5IYWFjazwvQXV0aG9yPjxZZWFyPjIwMTA8L1llYXI+PFJl
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ADDIN EN.CITE.DATA (95). In fact, some CBG sequences are more distantly related to each other than they are to myrosinase sequences or other GH1s ADDIN EN.CITE <EndNote><Cite><Author>Rask</Author><Year>2000</Year><RecNum>303</RecNum><DisplayText>(104)</DisplayText><record><rec-number>303</rec-number><foreign-keys><key app="EN" db-id="atawvvssk9f2soeepwy55091ppssa509t9aa" timestamp="1437763094">303</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Rask, L.</author><author>Andreasson, E.</author><author>Ekbom, B.</author><author>Eriksson, S.</author><author>Pontoppidan, B.</author><author>Meijer, J.</author></authors></contributors><auth-address>Dept. of Medical Biochemistry and Microbiology, Uppsala University, Sweden.</auth-address><titles><title>Myrosinase: gene family evolution and herbivore defense in Brassicaceae</title><secondary-title>Plant Mol Biol</secondary-title><alt-title>Plant molecular biology</alt-title></titles><periodical><full-title>Plant Mol Biol</full-title><abbr-1>Plant molecular biology</abbr-1></periodical><alt-periodical><full-title>Plant Mol Biol</full-title><abbr-1>Plant molecular biology</abbr-1></alt-periodical><pages>93-113</pages><volume>42</volume><number>1</number><keywords><keyword>Amino Acid Sequence</keyword><keyword>Animals</keyword><keyword>Brassicaceae/enzymology/genetics</keyword><keyword>Evolution, Molecular</keyword><keyword>Glucosinolates/metabolism</keyword><keyword>Glycoside Hydrolases/*genetics/metabolism</keyword><keyword>Insects/growth & development</keyword><keyword>Molecular Sequence Data</keyword><keyword>Multigene Family</keyword><keyword>Phylogeny</keyword><keyword>Plant Diseases/genetics</keyword><keyword>Sequence Homology, Amino Acid</keyword></keywords><dates><year>2000</year><pub-dates><date>Jan</date></pub-dates></dates><isbn>0167-4412 (Print)
0167-4412 (Linking)</isbn><accession-num>10688132</accession-num><urls><related-urls><url>;(104). Yet another member of the GH1 family, lactase-phlorizin hydrolase (also known as lactase or LPH; see ), is found in the midguts of Lepidoptera such as the fall armyworm (Spodoptera frugiperda (Smith), Noctuidae) and hydrolyzes galactolipids and hemicelluloses by cleaving them at two different active sites ADDIN EN.CITE <EndNote><Cite><Author>Marana</Author><Year>2000</Year><RecNum>302</RecNum><DisplayText>(105)</DisplayText><record><rec-number>302</rec-number><foreign-keys><key app="EN" db-id="atawvvssk9f2soeepwy55091ppssa509t9aa" timestamp="1437763061">302</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Marana, S. R.</author><author>Terra, W. R.</author><author>Ferreira, C.</author></authors></contributors><auth-address>Departamento de Bioquimica, Instituto de Quimica, Universidade de Sao Paulo, C.P. 26077, 05513-970, Sao Paulo, Brazil.</auth-address><titles><title>Purification and properties of a beta-glycosidase purified from midgut cells of Spodoptera frugiperda (Lepidoptera) larvae</title><secondary-title>Insect Biochem Mol Biol</secondary-title><alt-title>Insect biochemistry and molecular biology</alt-title></titles><periodical><full-title>Insect Biochem Mol Biol</full-title><abbr-1>Insect biochemistry and molecular biology</abbr-1></periodical><alt-periodical><full-title>Insect Biochem Mol Biol</full-title><abbr-1>Insect biochemistry and molecular biology</abbr-1></alt-periodical><pages>1139-46</pages><volume>30</volume><number>12</number><keywords><keyword>Animals</keyword><keyword>Digestive System/enzymology</keyword><keyword>Glycoside Hydrolases/isolation & purification/*metabolism</keyword><keyword>Larva</keyword><keyword>Spodoptera/*enzymology</keyword><keyword>Substrate Specificity</keyword></keywords><dates><year>2000</year><pub-dates><date>Dec</date></pub-dates></dates><isbn>0965-1748 (Print)
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ADDIN EN.CITE.DATA (108) suggested that myrosinase and cyanogenic beta-glucosidase act identically on substrates.Methods and ResultsTwenty-three potential A. glabripennis myrosinase amino acid sequences were identified by BLAST search ADDIN EN.CITE <EndNote><Cite><Author>Altschul</Author><Year>1990</Year><RecNum>51</RecNum><DisplayText>(37)</DisplayText><record><rec-number>51</rec-number><foreign-keys><key app="EN" db-id="atawvvssk9f2soeepwy55091ppssa509t9aa" timestamp="1432674533">51</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Altschul, S. F.</author><author>Gish, W.</author><author>Miller, W.</author><author>Myers, E. W.</author><author>Lipman, D. J.</author></authors></contributors><auth-address>Altschul, Sf
Nih,Natl Lib Med,Natl Ctr Biotechnol Informat,Bethesda,Md 20892, USA
Nih,Natl Lib Med,Natl Ctr Biotechnol Informat,Bethesda,Md 20892, USA
Penn State Univ,Dept Comp Sci,University Pk,Pa 16802
Univ Arizona,Dept Comp Sci,Tucson,Az 85721</auth-address><titles><title>Basic Local Alignment Search Tool</title><secondary-title>Journal of Molecular Biology</secondary-title><alt-title>J Mol Biol</alt-title></titles><periodical><full-title>Journal of Molecular Biology</full-title><abbr-1>J Mol Biol</abbr-1></periodical><alt-periodical><full-title>Journal of Molecular Biology</full-title><abbr-1>J Mol Biol</abbr-1></alt-periodical><pages>403-410</pages><volume>215</volume><number>3</number><dates><year>1990</year><pub-dates><date>Oct 5</date></pub-dates></dates><isbn>0022-2836</isbn><accession-num>WOS:A1990ED16700008</accession-num><urls><related-urls><url><Go to ISI>://WOS:A1990ED16700008</url></related-urls></urls><electronic-resource-num>Doi 10.1006/Jmbi.1990.9999</electronic-resource-num><language>English</language></record></Cite></EndNote>(37) for the highest-scoring alignments (typical identity of ~44%) between A. glabripennis GH1s and Tribolium castaneum sequences annotated as myrosinases in the SwissProt/UniProt database ADDIN EN.CITE <EndNote><Cite><Author>Magrane</Author><Year>2011</Year><RecNum>338</RecNum><DisplayText>(109)</DisplayText><record><rec-number>338</rec-number><foreign-keys><key app="EN" db-id="atawvvssk9f2soeepwy55091ppssa509t9aa" timestamp="1444254170">338</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Magrane, M.</author><author>Consortium, U.</author></authors></contributors><auth-address>European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SD, UK. magrane@ebi.ac.uk</auth-address><titles><title>UniProt Knowledgebase: a hub of integrated protein data</title><secondary-title>Database (Oxford)</secondary-title><alt-title>Database : the journal of biological databases and curation</alt-title></titles><periodical><full-title>Database (Oxford)</full-title><abbr-1>Database : the journal of biological databases and curation</abbr-1></periodical><alt-periodical><full-title>Database (Oxford)</full-title><abbr-1>Database : the journal of biological databases and curation</abbr-1></alt-periodical><pages>bar009</pages><volume>2011</volume><keywords><keyword>Amino Acid Sequence</keyword><keyword>*Databases, Protein</keyword><keyword>*Knowledge Bases</keyword><keyword>Molecular Sequence Annotation</keyword><keyword>Protein Binding</keyword><keyword>Proteins/*chemistry</keyword><keyword>Sequence Analysis, Protein</keyword></keywords><dates><year>2011</year></dates><isbn>1758-0463 (Electronic)
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ADDIN EN.CITE.DATA (110-114), including a set of five aligned sequence blocks available in the PRINTS database (). The ProSite database contains a simpler set of two sequence motifs, the first also defined by Henrissat and colleagues () as the consensus pattern:F-x-[FYWM]-[GSTA]-x-[GSTA]-x-[GSTA](2)-[FYNH]-[NQ]-x-E-x- [GSTA]All known GH1 sequences in SwissProt at the time the ProSite motif was defined in 1995 satisfied the above pattern, and there were no false positives. The second ProSite motif for GH1s, labeled PS00572, is:[LIVMFSTC]-[LIVFYS]-[LIV]-[LIVMST]-E-N-G-[LIVMFAR]-[CSAGN]According to ProSite, SwissProt sequence matches to this motif included 105 true positives, 95 false negatives, and 59 false positives. This motif is thus less discriminatory for GH1s. A third, nonredundant GH1 motif has been defined (Fig. 3 in ADDIN EN.CITE <EndNote><Cite><Author>Cicek</Author><Year>1999</Year><RecNum>317</RecNum><DisplayText>(115)</DisplayText><record><rec-number>317</rec-number><foreign-keys><key app="EN" db-id="atawvvssk9f2soeepwy55091ppssa509t9aa" timestamp="1437765838">317</key></foreign-keys><ref-type name="Thesis">32</ref-type><contributors><authors><author>Cicek, M. </author></authors></contributors><titles><title>Mechanism of Substrate Specificity and Catalysis in Retaining B-Glucosidases From Maize and Sorghum</title></titles><volume>Ph D.</volume><dates><year>1999</year></dates><publisher>Department of Biology, Virginia Tech (URN etd-093099-112234) </publisher><urls></urls></record></Cite></EndNote>(115)), corresponding to the VKYWLTINQLYSVPTR region in S. alba myrosinase in which the central glutamine (Q) residue corresponds to the conserved glutamate acid/base residue found in other GH1s.To analyze relationships between the 23 A. glabripennis myrosinase-like GH1 sequences and known myrosinases and CBGs, multiple sequence analysis was performed with MUSCLE ADDIN EN.CITE <EndNote><Cite><Author>Edgar</Author><Year>2004</Year><RecNum>296</RecNum><DisplayText>(31)</DisplayText><record><rec-number>296</rec-number><foreign-keys><key app="EN" db-id="atawvvssk9f2soeepwy55091ppssa509t9aa" timestamp="1437762773">296</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Edgar, R. C.</author></authors></contributors><auth-address>Edgar, RC
195 Roque Moraes Dr, Mill Valley, CA 94941 USA
195 Roque Moraes Dr, Mill Valley, CA 94941 USA</auth-address><titles><title>MUSCLE: multiple sequence alignment with high accuracy and high throughput</title><secondary-title>Nucleic Acids Research</secondary-title><alt-title>Nucleic Acids Res</alt-title></titles><periodical><full-title>Nucleic Acids Res</full-title><abbr-1>Nucleic acids research</abbr-1></periodical><alt-periodical><full-title>Nucleic Acids Res</full-title><abbr-1>Nucleic acids research</abbr-1></alt-periodical><pages>1792-1797</pages><volume>32</volume><number>5</number><keywords><keyword>protein-structure</keyword><keyword>phylogenetic trees</keyword><keyword>psi-blast</keyword><keyword>database</keyword><keyword>programs</keyword><keyword>domains</keyword><keyword>smart</keyword><keyword>tool</keyword><keyword>identification</keyword><keyword>algorithms</keyword></keywords><dates><year>2004</year><pub-dates><date>Mar</date></pub-dates></dates><isbn>0305-1048</isbn><accession-num>WOS:000220487200025</accession-num><urls><related-urls><url><Go to ISI>://WOS:000220487200025</url></related-urls></urls><electronic-resource-num>Doi 10.1093/Nar/Gkh340</electronic-resource-num><language>English</language></record></Cite></EndNote>(31), as implemented in the software suite Mega6 (Molecular Evolutionary Genetics Analysis; ). The set of 23 myrosinase-like GH1 sequences was seeded with an additional set of seven GH1 sequences of known function (Fig. S14): B. brassicae myrosinase 1 (sp|Q95X01), P. striolata myrosinase (tr|A0A059UAD7), S. alba myrosinase (Protein Data Bank entry 2wxd, chain M), P. striolata GH1 (gi|634006832), Lepisosteus oculatus (Winchell) lactase-like protein (lactase-phlorizin hydrolase, a CBG homolog; gi|573881201), Trifolium repens CBG (Protein Data Bank entry 1cbg, chain A), and a beta-glycosidase from S. sulfataricus (Protein Data Bank entry 1uwt, chain A). From this multiple sequence alignment, which correctly aligned the conserved GH1 motifs for the subset of 17 A. glabripennis sequences with complete coverage of the catalytic domain (AGLA004459, 4460, 4461, 9627, 9636, 9638, 9643, 9644, 14364, 14878, 16146, 16153, 16544, 16545, 17752, 18044, and 18242) and the 7 additional previously characterized GH1 sequences, a pairwise distance matrix between sequences was calculated in Mega6 by using the ADDIN EN.CITE <EndNote><Cite><Author>Jones</Author><Year>1992</Year><RecNum>301</RecNum><DisplayText>(116)</DisplayText><record><rec-number>301</rec-number><foreign-keys><key app="EN" db-id="atawvvssk9f2soeepwy55091ppssa509t9aa" timestamp="1437763010">301</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Jones, D. T.</author><author>Taylor, W. R.</author><author>Thornton, J. M.</author></authors></contributors><auth-address>Department of Biochemistry and Molecular Biology, University College, London, UK.</auth-address><titles><title>The rapid generation of mutation data matrices from protein sequences</title><secondary-title>Comput Appl Biosci</secondary-title><alt-title>Computer applications in the biosciences : CABIOS</alt-title></titles><periodical><full-title>Comput Appl Biosci</full-title><abbr-1>Computer applications in the biosciences : CABIOS</abbr-1></periodical><alt-periodical><full-title>Comput Appl Biosci</full-title><abbr-1>Computer applications in the biosciences : CABIOS</abbr-1></alt-periodical><pages>275-82</pages><volume>8</volume><number>3</number><keywords><keyword>*Algorithms</keyword><keyword>Amino Acid Sequence</keyword><keyword>*Mutation</keyword><keyword>Phylogeny</keyword><keyword>Proteins/*genetics</keyword><keyword>Sequence Alignment/*methods/statistics & numerical data</keyword><keyword>Software</keyword></keywords><dates><year>1992</year><pub-dates><date>Jun</date></pub-dates></dates><isbn>0266-7061 (Print)
0266-7061 (Linking)</isbn><accession-num>1633570</accession-num><urls><related-urls><url>;(116) model of amino acid substitution likelihood, with uniform rates across sites and pairwise deletion for handling any sequence gaps. Based on the pairwise distance matrix, agglomerative cluster analysis of these 24 sequences was performed in SciPy ADDIN EN.CITE <EndNote><Cite><Author>Jones</Author><Year>2001</Year><RecNum>315</RecNum><DisplayText>(117)</DisplayText><record><rec-number>315</rec-number><foreign-keys><key app="EN" db-id="atawvvssk9f2soeepwy55091ppssa509t9aa" timestamp="1437765448">315</key></foreign-keys><ref-type name="Web Page">12</ref-type><contributors><authors><author>Jones, E</author><author>Oliphant, E</author><author>Peterson, P</author><author>et al. </author></authors></contributors><titles><title>SciPy: Open Source Scientific Tools for Python</title></titles><volume>2015</volume><number>06-22</number><dates><year>2001</year></dates><urls><related-urls><url>. scipy. org </url></related-urls></urls></record></Cite></EndNote>(117) by using the complete linkage clustering function (scipy.cluster.plete). Complete linkage clustering has several practical and intuitive advantages. At any given sequence similarity cutoff (using the similarity values defined in the pairwise distance matrix described above), all sequences grouped in a cluster are guaranteed to have at least that pairwise degree of similarity. Furthermore, the defined clusters are guaranteed to be the densest such grouping of sequences for a given degree of similarity. The results are deterministic and do not depend on the order in which sequences are input. Upon clustering of the 17 complete A. glabripennis GH1-like sequences and seven GH1 sequences of known function (results not shown), the known myrosinases split across different sequence clusters; in particular, the S. alba myrosinase that uses an ascorbate cofactor appears in a separate cluster from the others (as was also found by the ADDIN EN.CITE <EndNote><Cite><Author>Rask</Author><Year>2000</Year><RecNum>303</RecNum><DisplayText>(104)</DisplayText><record><rec-number>303</rec-number><foreign-keys><key app="EN" db-id="atawvvssk9f2soeepwy55091ppssa509t9aa" timestamp="1437763094">303</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Rask, L.</author><author>Andreasson, E.</author><author>Ekbom, B.</author><author>Eriksson, S.</author><author>Pontoppidan, B.</author><author>Meijer, J.</author></authors></contributors><auth-address>Dept. of Medical Biochemistry and Microbiology, Uppsala University, Sweden.</auth-address><titles><title>Myrosinase: gene family evolution and herbivore defense in Brassicaceae</title><secondary-title>Plant Mol Biol</secondary-title><alt-title>Plant molecular biology</alt-title></titles><periodical><full-title>Plant Mol Biol</full-title><abbr-1>Plant molecular biology</abbr-1></periodical><alt-periodical><full-title>Plant Mol Biol</full-title><abbr-1>Plant molecular biology</abbr-1></alt-periodical><pages>93-113</pages><volume>42</volume><number>1</number><keywords><keyword>Amino Acid Sequence</keyword><keyword>Animals</keyword><keyword>Brassicaceae/enzymology/genetics</keyword><keyword>Evolution, Molecular</keyword><keyword>Glucosinolates/metabolism</keyword><keyword>Glycoside Hydrolases/*genetics/metabolism</keyword><keyword>Insects/growth & development</keyword><keyword>Molecular Sequence Data</keyword><keyword>Multigene Family</keyword><keyword>Phylogeny</keyword><keyword>Plant Diseases/genetics</keyword><keyword>Sequence Homology, Amino Acid</keyword></keywords><dates><year>2000</year><pub-dates><date>Jan</date></pub-dates></dates><isbn>0167-4412 (Print)
0167-4412 (Linking)</isbn><accession-num>10688132</accession-num><urls><related-urls><url>;(104) analysis of complete myrosinase sequences).Because analyses like the above treat all parts of the amino acid sequence as equally important, clustering aimed at functional annotation may be led astray by the low degree of conservation of solvent-exposed surface residues outside the active site, due to few steric, folding, or functional constraints on their evolution. Instead, focusing on active site and functional motif sequence conservation within the context of overall protein fold conservation is a better indicator of the conservation of substrate binding and reaction mechanism. Thus, to analyze the likelihood of myrosinase function in one or more of the A. glabripennis GH1-like sequences, we developed a sequence fingerprint consisting of only the residues contributing to the characteristic GH1 and myrosinase motifs described above, plus additional residues that contribute to the active site based on the available S. alba myrosinase crystal structure (Protein Data Bank entry 2wxd). These residues are not necessarily contiguous in sequence, since active sites typically involve discontiguous residues forming a substrate interaction surface. The motifs and active site residues only are presented in N-terminal to C-terminal order in the fingerprint (Fig. S14), as extracted from the MUSCLE alignment of the complete protein sequences. This fingerprint shows several interesting features:AGLA009631, 9633, and 9636 have an unusual residue (Asp) in place of the highly conserved Glu at the acid/base catalyst position in the ADDIN EN.CITE <EndNote><Cite><Author>Cicek</Author><Year>1999</Year><RecNum>317</RecNum><DisplayText>(115)</DisplayText><record><rec-number>317</rec-number><foreign-keys><key app="EN" db-id="atawvvssk9f2soeepwy55091ppssa509t9aa" timestamp="1437765838">317</key></foreign-keys><ref-type name="Thesis">32</ref-type><contributors><authors><author>Cicek, M. </author></authors></contributors><titles><title>Mechanism of Substrate Specificity and Catalysis in Retaining B-Glucosidases From Maize and Sorghum</title></titles><volume>Ph D.</volume><dates><year>1999</year></dates><publisher>Department of Biology, Virginia Tech (URN etd-093099-112234) </publisher><urls></urls></record></Cite></EndNote>(115) motif centered on the catalytic acid/base. Unconserved but chemically similar residues are known to occur in this position in some active GH1s: Gln in the S. alba myrosinase that uses ascorbate as a cofactor and Asn in the L. oculatus CBG-like lactase. Furthermore, Asp may provide a catalytic acid/base appropriate for interacting with a larger substrate than is found in active sites with Glu, as these side chains differ by just one methylene group in length.AGLA009636 and 9643 are unlikely to be active GH1s based on having an Ala or Gln substitution, respectively, for the conserved Glu in ProSite motif 2 (catalytic nucleophile position).The pairwise distance matrix for the above aligned active site sequence motifs was calculated in Mega6 (using parameters described above), followed by complete linkage cluster analysis in order to group subfamilies of these sequences according to active site and GH1 motif similarity (Fig. S15). This analysis of motifs, unlike the full sequence analysis, groups the known myrosinases (lower blue lines in Fig. S15) and suggests that one of the A. glabripennis sequences in particular, AGLA018242-PA, is closely similar to a known insect myrosinase (UniProt Q95X01 from B. brassicae).A known CBG and CBG-related GH1, lactase-phlorizin hydrolase, also fall in a single cluster when GH1 motifs and active site residues are used to assess similarity (green lines in Fig. S15). Further analysis is needed to evaluate the red cluster of A. glabripennis sequences, because they are intriguingly intermediate in similarity to known myrosinases and the known cyanogenic beta-glycosidase. Husebye et al., PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5IdXNlYnllPC9BdXRob3I+PFllYXI+MjAwNTwvWWVhcj48
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ADDIN EN.CITE.DATA (95) noted that B. brassicae myrosinase shows close sequence and structural similarity to both T. repens CBG (41% sequence identity) and S. alba myrosinase (34% identity).The 3-dimensional compatibility of A. glabripennis sequences to the myrosinase atomic structure can be assessed by homology modeling. For instance, a 3-dimensional structural model (Fig. S16) was built for one of the GH1 myrosinase candidates (AGLA009643-PA, annotated by PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5TY3VsbHk8L0F1dGhvcj48WWVhcj4yMDEzPC9ZZWFyPjxS
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ADDIN EN.CITE.DATA (57) as V5GKP2 in the SwissProt/UniProt database) based on its alignment with B. brassicae myrosinase, by using SwissModel homology modeling software ADDIN EN.CITE <EndNote><Cite><Author>Schwede</Author><Year>2003</Year><RecNum>348</RecNum><DisplayText>(118)</DisplayText><record><rec-number>348</rec-number><foreign-keys><key app="EN" db-id="atawvvssk9f2soeepwy55091ppssa509t9aa" timestamp="1444254192">348</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Schwede, T.</author><author>Kopp, J.</author><author>Guex, N.</author><author>Peitsch, M. C.</author></authors></contributors><auth-address>Biozentrum der Universitat Basel, Klingelbergstr. 50-70, CH 4056 Basel, Switzerland. torsten.schwede@unibas.ch</auth-address><titles><title>SWISS-MODEL: An automated protein homology-modeling server</title><secondary-title>Nucleic Acids Res</secondary-title><alt-title>Nucleic acids research</alt-title></titles><periodical><full-title>Nucleic Acids Res</full-title><abbr-1>Nucleic acids research</abbr-1></periodical><alt-periodical><full-title>Nucleic Acids Res</full-title><abbr-1>Nucleic acids research</abbr-1></alt-periodical><pages>3381-5</pages><volume>31</volume><number>13</number><keywords><keyword>Computer Graphics</keyword><keyword>Internet</keyword><keyword>*Models, Molecular</keyword><keyword>Proteins/chemistry</keyword><keyword>Sequence Alignment</keyword><keyword>Sequence Analysis, Protein</keyword><keyword>*Software</keyword><keyword>*Structural Homology, Protein</keyword><keyword>User-Computer Interface</keyword></keywords><dates><year>2003</year><pub-dates><date>Jul 1</date></pub-dates></dates><isbn>1362-4962 (Electronic)
0305-1048 (Linking)</isbn><accession-num>12824332</accession-num><urls><related-urls><url>;(118) (). The resulting model was judged to be of reasonable accuracy, based on the SwissModel structural evaluation of bond stereochemistry and intramolecular contacts indicating similar quality to well-resolved crystal structures. This model for the A. glabripennis protein structure (Fig. S16) also provides an unambiguous definition of the active site residues and their relative orientation, which is valuable for assessing the positioning of catalytic groups and the likelihood of interacting with glycosidic versus other substrates. An alternative model for this V5GKP2 sequence based on using the T. repens CBG structure (Protein Data Bank entry 1CBG) was of much lower stereochemical quality, consistent with the active-site and motif cluster analysis (above) indicating that the AGLA009643 GH1 motifs and active site are more closely related to myrosinases.DiscussionGiven that A. glabripennis is highly polyphagous (not limited to one food source) and not known to feed on glucosinolate-myrosinase system containing plants, it is unclear why the beetles would express one or more myrosinase-like enzymes. Myrosinase is necessary to defuse the so-called defensive “mustard oil bomb” produced by plants in the order Brassicales in order to deter herbivory ADDIN EN.CITE <EndNote><Cite><Author>Hopkins</Author><Year>2009</Year><RecNum>298</RecNum><DisplayText>(119)</DisplayText><record><rec-number>298</rec-number><foreign-keys><key app="EN" db-id="atawvvssk9f2soeepwy55091ppssa509t9aa" timestamp="1437762874">298</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Hopkins, R. J.</author><author>van Dam, N. M.</author><author>van Loon, J. J.</author></authors></contributors><auth-address>Department of Ecology, Swedish University of Agricultural Sciences, Uppsala S-750 07, Sweden. Richard.hopkins@ekol.slu.se</auth-address><titles><title>Role of glucosinolates in insect-plant relationships and multitrophic interactions</title><secondary-title>Annu Rev Entomol</secondary-title><alt-title>Annual review of entomology</alt-title></titles><periodical><full-title>Annual Review of Entomology</full-title><abbr-1>Annu Rev Entomol</abbr-1></periodical><alt-periodical><full-title>Annual Review of Entomology</full-title><abbr-1>Annu Rev Entomol</abbr-1></alt-periodical><pages>57-83</pages><volume>54</volume><keywords><keyword>Animals</keyword><keyword>*Appetitive Behavior</keyword><keyword>Brassicaceae/genetics/*metabolism</keyword><keyword>Breeding</keyword><keyword>Crops, Agricultural/genetics</keyword><keyword>Feeding Behavior</keyword><keyword>*Food Chain</keyword><keyword>Glucosinolates/chemistry/*metabolism</keyword><keyword>Insects/*metabolism</keyword><keyword>Oviposition</keyword></keywords><dates><year>2009</year></dates><isbn>0066-4170 (Print)
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Tm90ZT5=
ADDIN EN.CITE.DATA (103). These genera are not known to contain the myrosinase system. However, glucosinolates could be taken up from another food source by A. glabripennis.Myrosinase could also play a role in chemical signaling in A. glabripennis adults, as is the case for P. striolata. A. glabripennis may sequester glucosinolates or respond to the products of myrosinase hydrolysis (ITCs), and these compounds may synergize the attraction of adult beetles to the male-produced compounds, 4-(n-heptyloxy)butan-1-ol, 4-(n-heptyloxy)butanal, and (3E,6E)-α-farnesene PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5Dcm9vazwvQXV0aG9yPjxZZWFyPjIwMTQ8L1llYXI+PFJl
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ADDIN EN.CITE.DATA (99, 100). This finding would be analogous to a system already known to exist in cabbage and turnip aphids, which combine ITCs with (E)-β-farnesene as an alarm pheromone PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5EYXdzb248L0F1dGhvcj48WWVhcj4xOTg3PC9ZZWFyPjxS
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ADDIN EN.CITE PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5EYXdzb248L0F1dGhvcj48WWVhcj4xOTg3PC9ZZWFyPjxS
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ADDIN EN.CITE.DATA (94, 95). Experiments are in progress to evaluate the response of A. glabripennis adults to ITCs alone, and in combination with male-produced attractants (A.M.R., unpub. data). Another intriguing possibility is that one or more A. glabripennis sequences is active as a CBG, as suggested by the presence of a cluster of A. glabripennis sequences intermediate between known CBGs and myrosinases. Toxic cyanogenic glycosides are used by plants as a defense system analogous to the myrosinase system. Cyanogenic glycoside substrates are packaged in an adjacent compartment to CBGs in plants. Herbivory breaches the compartments, initiating the breakdown of cyanogenic glycosides and release of hydrogen cyanide gas ADDIN EN.CITE <EndNote><Cite><Author>Zagrobelny</Author><Year>2004</Year><RecNum>310</RecNum><DisplayText>(102)</DisplayText><record><rec-number>310</rec-number><foreign-keys><key app="EN" db-id="atawvvssk9f2soeepwy55091ppssa509t9aa" timestamp="1437763577">310</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Zagrobelny, M.</author><author>Bak, S.</author><author>Rasmussen, A. V.</author><author>Jorgensen, B.</author><author>Naumann, C. M.</author><author>Lindberg Moller, B.</author></authors></contributors><auth-address>Department of Plant Biology and Center of Molecular Plant Physiology (PlaCe), Royal Veterinary and Agricultural University, 40 Thorvaldsensvej, DK-1871 Frederiksberg C, Copenhagen, Denmark.</auth-address><titles><title>Cyanogenic glucosides and plant-insect interactions</title><secondary-title>Phytochemistry</secondary-title><alt-title>Phytochemistry</alt-title></titles><periodical><full-title>Phytochemistry</full-title></periodical><alt-periodical><full-title>Phytochemistry</full-title></alt-periodical><pages>293-306</pages><volume>65</volume><number>3</number><keywords><keyword>Animals</keyword><keyword>Arthropods/physiology</keyword><keyword>Butterflies/physiology</keyword><keyword>Cyanides/chemistry/metabolism</keyword><keyword>Glycosides/*chemistry/*metabolism</keyword><keyword>Host-Parasite Interactions</keyword><keyword>Insects/*physiology</keyword><keyword>Lepidoptera/physiology</keyword><keyword>Nitriles/*chemistry/*metabolism</keyword><keyword>Pest Control, Biological</keyword><keyword>Plants, Edible/chemistry/*physiology</keyword></keywords><dates><year>2004</year><pub-dates><date>Feb</date></pub-dates></dates><isbn>0031-9422 (Print)
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ADDIN EN.CITE.DATA (103). The cyanogenic glycosides prunasin and amygalin are found in tissues of Prunus ADDIN EN.CITE <EndNote><Cite><Author>Hegnauer</Author><Year>1964</Year><RecNum>316</RecNum><DisplayText>(120)</DisplayText><record><rec-number>316</rec-number><foreign-keys><key app="EN" db-id="atawvvssk9f2soeepwy55091ppssa509t9aa" timestamp="1437765701">316</key></foreign-keys><ref-type name="Book">6</ref-type><contributors><authors><author>Hegnauer, R. </author></authors></contributors><titles><title>Chemotaxonomie der Pflanzen</title></titles><volume>3-6</volume><dates><year>1964</year></dates><pub-location>Birkhaeuser Verlag, Basel and Stuttgart</pub-location><urls></urls></record></Cite></EndNote>(120), often in levels that are toxic to herbivores, including humans and domestic animals ADDIN EN.CITE <EndNote><Cite><Author>USDA Forest Products Laboratory</Author><Year>1979</Year><RecNum>349</RecNum><DisplayText>(121)</DisplayText><record><rec-number>349</rec-number><foreign-keys><key app="EN" db-id="atawvvssk9f2soeepwy55091ppssa509t9aa" timestamp="1444254349">349</key></foreign-keys><ref-type name="Book">6</ref-type><contributors><authors><author>USDA Forest Products Laboratory, Forest Service</author></authors></contributors><titles><title>Extractives in Eastern Hardwoods - A review</title><secondary-title>General Technical Report Fpl 18</secondary-title></titles><dates><year>1979</year></dates><pub-location>Madison, Wisconsin </pub-location><urls></urls></record></Cite></EndNote>(121). Aside from amygdalin and prunasin, linamarin and lotaustralin are cyanogenic glycosides that are widespread in plants and often occur together, particularly in Fabaceae ADDIN EN.CITE <EndNote><Cite><Author>Bernays</Author><Year>1994</Year><RecNum>318</RecNum><DisplayText>(122)</DisplayText><record><rec-number>318</rec-number><foreign-keys><key app="EN" db-id="atawvvssk9f2soeepwy55091ppssa509t9aa" timestamp="1437765911">318</key></foreign-keys><ref-type name="Book">6</ref-type><contributors><authors><author>Bernays, E.A. </author><author>Chapman, R.F. </author></authors></contributors><titles><title>Host-Plant Selection by Phytophagous Insects, </title></titles><dates><year>1994</year></dates><pub-location>Chapman & Hall, New York, NY. </pub-location><urls></urls></record></Cite></EndNote>(122). Both cyanogenic glycosides and their release of hydrogen cyanide gas can affect the behavior of herbivorous insects and other animals. Specialist insect herbivores have developed CBG systems mirroring those in plants to metabolize cyanogenic glucosides or sequester them for use in predator defense, just as insects developed myrosinase systems to combat predation and aid in signaling to conspecifics ADDIN EN.CITE <EndNote><Cite><Author>Zagrobelny</Author><Year>2004</Year><RecNum>310</RecNum><DisplayText>(102)</DisplayText><record><rec-number>310</rec-number><foreign-keys><key app="EN" db-id="atawvvssk9f2soeepwy55091ppssa509t9aa" timestamp="1437763577">310</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Zagrobelny, M.</author><author>Bak, S.</author><author>Rasmussen, A. V.</author><author>Jorgensen, B.</author><author>Naumann, C. M.</author><author>Lindberg Moller, B.</author></authors></contributors><auth-address>Department of Plant Biology and Center of Molecular Plant Physiology (PlaCe), Royal Veterinary and Agricultural University, 40 Thorvaldsensvej, DK-1871 Frederiksberg C, Copenhagen, Denmark.</auth-address><titles><title>Cyanogenic glucosides and plant-insect interactions</title><secondary-title>Phytochemistry</secondary-title><alt-title>Phytochemistry</alt-title></titles><periodical><full-title>Phytochemistry</full-title></periodical><alt-periodical><full-title>Phytochemistry</full-title></alt-periodical><pages>293-306</pages><volume>65</volume><number>3</number><keywords><keyword>Animals</keyword><keyword>Arthropods/physiology</keyword><keyword>Butterflies/physiology</keyword><keyword>Cyanides/chemistry/metabolism</keyword><keyword>Glycosides/*chemistry/*metabolism</keyword><keyword>Host-Parasite Interactions</keyword><keyword>Insects/*physiology</keyword><keyword>Lepidoptera/physiology</keyword><keyword>Nitriles/*chemistry/*metabolism</keyword><keyword>Pest Control, Biological</keyword><keyword>Plants, Edible/chemistry/*physiology</keyword></keywords><dates><year>2004</year><pub-dates><date>Feb</date></pub-dates></dates><isbn>0031-9422 (Print)
0031-9422 (Linking)</isbn><accession-num>14751300</accession-num><urls><related-urls><url>;(102).AcknowledgmentsWe sincerely thank Sebastian Raschka (Michigan State University) for his contributions to the Mega6 and SciPy cluster analysis of sequences, and also Kathryn Morris, Vanessa Lopez, Scott Gula, and Brenna Walters (Xavier University) for their help with the preliminary laboratory bioassays.Author contributionsL.A.K. developed the chemical signaling hypothesis for myrosinases and cyanogenic beta-glycosidases in A. glabripennis, performed the sequence and structural bioinformatics analysis, and drafted this section on myrosinase and cyanogenic β-glycosidase-like sequences; A.M.R. designed and performed experiments and contributed to writing and editing the manuscript; E.S. provided myrosinase-like genomic sequence data for analysis, suggested roles for these enzymes in digestive physiology, and edited the manuscript.-107952290445ProSite GH1 motif 1 region AS Cicek motif for GH1 including AS (discontig- ProSite GH1 motif 2; AS conserved E, the acid/base uous residues) E is a catalytic catalyst (Wang, 1990); preceding nucleophile Asn H-bonds to 2-OH in GH1s (Withers,1990)00ProSite GH1 motif 1 region AS Cicek motif for GH1 including AS (discontig- ProSite GH1 motif 2; AS conserved E, the acid/base uous residues) E is a catalytic catalyst (Wang, 1990); preceding nucleophile Asn H-bonds to 2-OH in GH1s (Withers,1990)Fig. S14. GH1 and myrosinase motifs for 23 A. glabripennis proteins and seven known GH1s from other organisms, as described in the Methods, colored by Mega6 according to amino acid chemistry: yellow, hydrophobic; light green, Tyr; dark green, polar; blue-green, His; pink, Gly; brown, Cys; red, Asp or Glu; dark blue, Lys or Arg. A. glabripennis sequences with substantial gaps (indicated by dashes on white background in the fingerprint) were omitted from the subsequent distance matrix calculation and clustering due to being incomplete sequences (unable to form the GH1 fold), though the corresponding full-length sequence, if expressed, could be a GH1. In the annotations beneath the fingerprint, “AS” indicates active site glucose or aglycone binding residues in myrosinase or CBG, as defined in Fig. 3 of (95). Additional active-site residues were identified by using PyMOL software (v. 1.5.0.5, Schr?dinger, LLC, NY, NY) based on occurring within contact distance (5 ?ngstroms) of the E18 inhibitor in Protein Data Bank crystal structure 2wxd (S. alba myrosinase). Fig. S15. Complete linkage clustering showing similarity in active site motif regions in AGLAB myrosinase- and cyanogenic β-glycosidase-like sequences and characterized GH1s from other organisms, based on pairwise Jones-Taylor-Thornton amino acid substitution distance followed by complete linkage clustering. Known myrosinases (MYR) appear in a cluster with candidate MYRs from AGLAB (blue) and known cyanogenic β-glycosidases (CBG) and close relatives also form a cluster (green). 45577645756275000000110490077047Jones-Taylor-Thornton Amino Acid Substitution DistanceJones-Taylor-Thornton Amino Acid Substitution Distance1215390196215Fig. S16. Evaluation of a potential A. glabripennis myrosinase by 3-dimensional modeling (carbon atoms and main-chain ribbons shown in yellow), using the X-ray structure of B. brassicae myrosinase (Protein Data Bank entry 1WCG; carbon atoms and main-chain ribbons in green) as a template for the A. glabripennis sequence AGLA009643-PA. The glucosinolate substrate-like E18 inhibitor from S. alba myrosinase is shown with carbon atoms in pink, for reference. Immediately beneath the alpha carbon of the phenyl group in E18, the GH1 conserved catalytic Glu acid/base appears in overlapping positions in the B. brassicae myrosinase and the A. glabripennis myrosinase-like protein. However, the Glu catalytic nucleophile conserved in GH1s including myrosinase is not conserved in this A. glabripennis sequence, suggesting it is not active as a myrosinase. 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