The use of an acetoacetyl‐CoA synthase in place of a β‐ketothiolase enhances poly‐3‐hydroxybutyrate production in sugarcane mesophyll cells
Summary Engineering the production of polyhydroxyalkanoates (PHAs) into high biomass bioenergy crops has the potential to provide a sustainable supply of bioplastics and energy from a single plant feedstock. One of the major challenges in engineering C4 plants for the production of poly[(R)‐3‐hydrox...
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| Veröffentlicht in: | Plant biotechnology journal 2015-06, Vol.13 (5), p.700-707 |
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| creator | McQualter, Richard B. Petrasovits, Lars A. Gebbie, Leigh K. Schweitzer, Dirk Blackman, Deborah M. Chrysanthopoulos, Panagiotis Hodson, Mark P. Plan, Manuel R. Riches, James D. Snell, Kristi D. Brumbley, Stevens M. Nielsen, Lars K. |
| description | Summary
Engineering the production of polyhydroxyalkanoates (PHAs) into high biomass bioenergy crops has the potential to provide a sustainable supply of bioplastics and energy from a single plant feedstock. One of the major challenges in engineering C4 plants for the production of poly[(R)‐3‐hydroxybutyrate] (PHB) is the significantly lower level of polymer produced in the chloroplasts of mesophyll (M) cells compared to bundle sheath (BS) cells, thereby limiting the full PHB yield‐potential of the plant. In this study, we provide evidence that the access to substrate for PHB synthesis may limit polymer production in M chloroplasts. Production of PHB in M cells of sugarcane is significantly increased by replacing β‐ketothiolase, the first enzyme in the bacterial PHA pathway, with acetoacetyl‐CoA synthase. This novel pathway enabled the production of PHB reaching an average of 6.3% of the dry weight of total leaf biomass, with levels ranging from 3.6 to 11.8% of the dry weight (DW) of individual leaves. These yields are more than twice the level reported in PHB‐producing sugarcane containing the β‐ketothiolase and illustrate the importance of producing polymer in mesophyll plastids to maximize yield. The molecular weight of the polymer produced was greater than 2 × 106 Da. These results are a major step forward in engineering a high biomass C4 grass for the commercial production of PHB. |
| doi_str_mv | 10.1111/pbi.12298 |
| format | Article |
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Engineering the production of polyhydroxyalkanoates (PHAs) into high biomass bioenergy crops has the potential to provide a sustainable supply of bioplastics and energy from a single plant feedstock. One of the major challenges in engineering C4 plants for the production of poly[(R)‐3‐hydroxybutyrate] (PHB) is the significantly lower level of polymer produced in the chloroplasts of mesophyll (M) cells compared to bundle sheath (BS) cells, thereby limiting the full PHB yield‐potential of the plant. In this study, we provide evidence that the access to substrate for PHB synthesis may limit polymer production in M chloroplasts. Production of PHB in M cells of sugarcane is significantly increased by replacing β‐ketothiolase, the first enzyme in the bacterial PHA pathway, with acetoacetyl‐CoA synthase. This novel pathway enabled the production of PHB reaching an average of 6.3% of the dry weight of total leaf biomass, with levels ranging from 3.6 to 11.8% of the dry weight (DW) of individual leaves. These yields are more than twice the level reported in PHB‐producing sugarcane containing the β‐ketothiolase and illustrate the importance of producing polymer in mesophyll plastids to maximize yield. The molecular weight of the polymer produced was greater than 2 × 106 Da. These results are a major step forward in engineering a high biomass C4 grass for the commercial production of PHB.</description><identifier>ISSN: 1467-7644</identifier><identifier>EISSN: 1467-7652</identifier><identifier>DOI: 10.1111/pbi.12298</identifier><identifier>PMID: 25532451</identifier><language>eng</language><publisher>England: John Wiley & Sons, Inc</publisher><subject>acetoacetyl‐CoA synthase ; Acetyl-CoA C-Acyltransferase - genetics ; Acetyl-CoA C-Acyltransferase - metabolism ; Acyl Coenzyme A - metabolism ; Bacteria ; Biodiesel fuels ; Biofuels ; Biomass ; Bioplastics ; biopolymer ; Biosynthesis ; Biosynthetic Pathways ; Bundling ; Chemical synthesis ; Chloroplasts ; Chloroplasts - genetics ; Crops, Agricultural ; Dry weight ; Drying ; Energy crops ; Enzymes ; Hydroxybutyrates - metabolism ; Leaves ; Lignocellulose ; M cells ; Mesophyll ; Mesophyll Cells - metabolism ; Molecular weight ; NphT7 ; Pathways ; PHB ; Plant Leaves - enzymology ; Plant Leaves - genetics ; Plant Leaves - growth & development ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Plants (botany) ; Plants (organisms) ; Plants, Genetically Modified ; Plastids - metabolism ; Poly-3-hydroxybutyrate ; Polyesters ; Polyesters - metabolism ; Polyhydroxyalkanoates ; Polyhydroxyalkanoates - metabolism ; Polyhydroxybutyrate ; Polyhydroxybutyric acid ; Polymers ; Renewable energy ; Saccharum - enzymology ; Saccharum - genetics ; Saccharum - growth & development ; Sheaths ; Substrates ; Sugarcane ; Transgenic plants ; β‐ketothiolase</subject><ispartof>Plant biotechnology journal, 2015-06, Vol.13 (5), p.700-707</ispartof><rights>2014 Society for Experimental Biology, Association of Applied Biologists and John Wiley & Sons Ltd</rights><rights>2014 Society for Experimental Biology, Association of Applied Biologists and John Wiley & Sons Ltd.</rights><rights>2015. This work is published under https://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><orcidid>0000-0002-1341-7871</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fpbi.12298$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fpbi.12298$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,11541,27901,27902,45550,45551,46027,46451</link.rule.ids><linktorsrc>$$Uhttps://onlinelibrary.wiley.com/doi/abs/10.1111%2Fpbi.12298$$EView_record_in_Wiley-Blackwell$$FView_record_in_$$GWiley-Blackwell</linktorsrc><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25532451$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>McQualter, Richard B.</creatorcontrib><creatorcontrib>Petrasovits, Lars A.</creatorcontrib><creatorcontrib>Gebbie, Leigh K.</creatorcontrib><creatorcontrib>Schweitzer, Dirk</creatorcontrib><creatorcontrib>Blackman, Deborah M.</creatorcontrib><creatorcontrib>Chrysanthopoulos, Panagiotis</creatorcontrib><creatorcontrib>Hodson, Mark P.</creatorcontrib><creatorcontrib>Plan, Manuel R.</creatorcontrib><creatorcontrib>Riches, James D.</creatorcontrib><creatorcontrib>Snell, Kristi D.</creatorcontrib><creatorcontrib>Brumbley, Stevens M.</creatorcontrib><creatorcontrib>Nielsen, Lars K.</creatorcontrib><title>The use of an acetoacetyl‐CoA synthase in place of a β‐ketothiolase enhances poly‐3‐hydroxybutyrate production in sugarcane mesophyll cells</title><title>Plant biotechnology journal</title><addtitle>Plant Biotechnol J</addtitle><description>Summary
Engineering the production of polyhydroxyalkanoates (PHAs) into high biomass bioenergy crops has the potential to provide a sustainable supply of bioplastics and energy from a single plant feedstock. One of the major challenges in engineering C4 plants for the production of poly[(R)‐3‐hydroxybutyrate] (PHB) is the significantly lower level of polymer produced in the chloroplasts of mesophyll (M) cells compared to bundle sheath (BS) cells, thereby limiting the full PHB yield‐potential of the plant. In this study, we provide evidence that the access to substrate for PHB synthesis may limit polymer production in M chloroplasts. Production of PHB in M cells of sugarcane is significantly increased by replacing β‐ketothiolase, the first enzyme in the bacterial PHA pathway, with acetoacetyl‐CoA synthase. This novel pathway enabled the production of PHB reaching an average of 6.3% of the dry weight of total leaf biomass, with levels ranging from 3.6 to 11.8% of the dry weight (DW) of individual leaves. These yields are more than twice the level reported in PHB‐producing sugarcane containing the β‐ketothiolase and illustrate the importance of producing polymer in mesophyll plastids to maximize yield. The molecular weight of the polymer produced was greater than 2 × 106 Da. These results are a major step forward in engineering a high biomass C4 grass for the commercial production of PHB.</description><subject>acetoacetyl‐CoA synthase</subject><subject>Acetyl-CoA C-Acyltransferase - genetics</subject><subject>Acetyl-CoA C-Acyltransferase - metabolism</subject><subject>Acyl Coenzyme A - metabolism</subject><subject>Bacteria</subject><subject>Biodiesel fuels</subject><subject>Biofuels</subject><subject>Biomass</subject><subject>Bioplastics</subject><subject>biopolymer</subject><subject>Biosynthesis</subject><subject>Biosynthetic Pathways</subject><subject>Bundling</subject><subject>Chemical synthesis</subject><subject>Chloroplasts</subject><subject>Chloroplasts - genetics</subject><subject>Crops, Agricultural</subject><subject>Dry weight</subject><subject>Drying</subject><subject>Energy crops</subject><subject>Enzymes</subject><subject>Hydroxybutyrates - metabolism</subject><subject>Leaves</subject><subject>Lignocellulose</subject><subject>M cells</subject><subject>Mesophyll</subject><subject>Mesophyll Cells - metabolism</subject><subject>Molecular weight</subject><subject>NphT7</subject><subject>Pathways</subject><subject>PHB</subject><subject>Plant Leaves - enzymology</subject><subject>Plant Leaves - genetics</subject><subject>Plant Leaves - growth & development</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Plants (botany)</subject><subject>Plants (organisms)</subject><subject>Plants, Genetically Modified</subject><subject>Plastids - metabolism</subject><subject>Poly-3-hydroxybutyrate</subject><subject>Polyesters</subject><subject>Polyesters - metabolism</subject><subject>Polyhydroxyalkanoates</subject><subject>Polyhydroxyalkanoates - metabolism</subject><subject>Polyhydroxybutyrate</subject><subject>Polyhydroxybutyric acid</subject><subject>Polymers</subject><subject>Renewable energy</subject><subject>Saccharum - enzymology</subject><subject>Saccharum - genetics</subject><subject>Saccharum - growth & development</subject><subject>Sheaths</subject><subject>Substrates</subject><subject>Sugarcane</subject><subject>Transgenic plants</subject><subject>β‐ketothiolase</subject><issn>1467-7644</issn><issn>1467-7652</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkk1u1TAUhS0EoqUwYAPIEhMmr_V_kmF5olCpEgzK2LKTG5LiF4c4UfGMJXTASlgIi2Al3LyWDhjVku0rn09Xx7qHkJecHXNcJ6Pvj7kQVfmIHHJlik1htHh8Xyt1QJ6ldMWY4Eabp-RAaC2F0vyQ_LzsgC4JaGypG6irYY7rkcOfHzfbeEpTHubOIdAPdAwo7Un6-xfqXxGeuz6GVYehc0MNiY4xZBQl7i43U_ye_TLnyc1Axyk2Sz33cVjbpeWLm2o3AN1BimOXQ6A1hJCekyetCwle3N1H5PPZu8vth83Fx_fn29OLzSiNLjet8so7ZZpCqbIohK5rKJnkujK-dMC9ccYrfOfAK6y5cRVAxVXb-LqQrTwib277oq9vC6TZ7vq0OkBPcUmWm0pIVSldPQAtpdSiZOYhKBdGaSYRff0fehWXacA_W8lMYQocJEPq1R21-B00dpz6nZuy_TdFBE5uges-QL7XObNrPCzGw-7jYT-9Pd8X8i94hrHe</recordid><startdate>201506</startdate><enddate>201506</enddate><creator>McQualter, Richard B.</creator><creator>Petrasovits, Lars A.</creator><creator>Gebbie, Leigh K.</creator><creator>Schweitzer, Dirk</creator><creator>Blackman, Deborah M.</creator><creator>Chrysanthopoulos, Panagiotis</creator><creator>Hodson, Mark P.</creator><creator>Plan, Manuel R.</creator><creator>Riches, James D.</creator><creator>Snell, Kristi D.</creator><creator>Brumbley, Stevens M.</creator><creator>Nielsen, Lars K.</creator><general>John Wiley & Sons, Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>7QO</scope><scope>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>7X8</scope><scope>7U5</scope><scope>F28</scope><scope>L7M</scope><orcidid>https://orcid.org/0000-0002-1341-7871</orcidid></search><sort><creationdate>201506</creationdate><title>The use of an acetoacetyl‐CoA synthase in place of a β‐ketothiolase enhances poly‐3‐hydroxybutyrate production in sugarcane mesophyll cells</title><author>McQualter, Richard B. ; Petrasovits, Lars A. ; Gebbie, Leigh K. ; Schweitzer, Dirk ; Blackman, Deborah M. ; Chrysanthopoulos, Panagiotis ; Hodson, Mark P. ; Plan, Manuel R. ; Riches, James D. ; Snell, Kristi D. ; Brumbley, Stevens M. ; Nielsen, Lars K.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-p3658-f4b4ba46d74487725cce8031596b8ae1b6a6b47251e196a616a9ee914fdbc73f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>acetoacetyl‐CoA synthase</topic><topic>Acetyl-CoA C-Acyltransferase - genetics</topic><topic>Acetyl-CoA C-Acyltransferase - metabolism</topic><topic>Acyl Coenzyme A - metabolism</topic><topic>Bacteria</topic><topic>Biodiesel fuels</topic><topic>Biofuels</topic><topic>Biomass</topic><topic>Bioplastics</topic><topic>biopolymer</topic><topic>Biosynthesis</topic><topic>Biosynthetic Pathways</topic><topic>Bundling</topic><topic>Chemical synthesis</topic><topic>Chloroplasts</topic><topic>Chloroplasts - genetics</topic><topic>Crops, Agricultural</topic><topic>Dry weight</topic><topic>Drying</topic><topic>Energy crops</topic><topic>Enzymes</topic><topic>Hydroxybutyrates - metabolism</topic><topic>Leaves</topic><topic>Lignocellulose</topic><topic>M cells</topic><topic>Mesophyll</topic><topic>Mesophyll Cells - metabolism</topic><topic>Molecular weight</topic><topic>NphT7</topic><topic>Pathways</topic><topic>PHB</topic><topic>Plant Leaves - enzymology</topic><topic>Plant Leaves - genetics</topic><topic>Plant Leaves - growth & development</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Plants (botany)</topic><topic>Plants (organisms)</topic><topic>Plants, Genetically Modified</topic><topic>Plastids - metabolism</topic><topic>Poly-3-hydroxybutyrate</topic><topic>Polyesters</topic><topic>Polyesters - metabolism</topic><topic>Polyhydroxyalkanoates</topic><topic>Polyhydroxyalkanoates - metabolism</topic><topic>Polyhydroxybutyrate</topic><topic>Polyhydroxybutyric acid</topic><topic>Polymers</topic><topic>Renewable energy</topic><topic>Saccharum - enzymology</topic><topic>Saccharum - genetics</topic><topic>Saccharum - growth & development</topic><topic>Sheaths</topic><topic>Substrates</topic><topic>Sugarcane</topic><topic>Transgenic plants</topic><topic>β‐ketothiolase</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>McQualter, Richard B.</creatorcontrib><creatorcontrib>Petrasovits, Lars A.</creatorcontrib><creatorcontrib>Gebbie, Leigh K.</creatorcontrib><creatorcontrib>Schweitzer, Dirk</creatorcontrib><creatorcontrib>Blackman, Deborah M.</creatorcontrib><creatorcontrib>Chrysanthopoulos, Panagiotis</creatorcontrib><creatorcontrib>Hodson, Mark P.</creatorcontrib><creatorcontrib>Plan, Manuel R.</creatorcontrib><creatorcontrib>Riches, James D.</creatorcontrib><creatorcontrib>Snell, Kristi D.</creatorcontrib><creatorcontrib>Brumbley, Stevens M.</creatorcontrib><creatorcontrib>Nielsen, Lars K.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>Biotechnology Research Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Solid State and Superconductivity Abstracts</collection><collection>ANTE: Abstracts in New Technology & Engineering</collection><collection>Advanced Technologies Database with Aerospace</collection><jtitle>Plant biotechnology journal</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext_linktorsrc</fulltext></delivery><addata><au>McQualter, Richard B.</au><au>Petrasovits, Lars A.</au><au>Gebbie, Leigh K.</au><au>Schweitzer, Dirk</au><au>Blackman, Deborah M.</au><au>Chrysanthopoulos, Panagiotis</au><au>Hodson, Mark P.</au><au>Plan, Manuel R.</au><au>Riches, James D.</au><au>Snell, Kristi D.</au><au>Brumbley, Stevens M.</au><au>Nielsen, Lars K.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The use of an acetoacetyl‐CoA synthase in place of a β‐ketothiolase enhances poly‐3‐hydroxybutyrate production in sugarcane mesophyll cells</atitle><jtitle>Plant biotechnology journal</jtitle><addtitle>Plant Biotechnol J</addtitle><date>2015-06</date><risdate>2015</risdate><volume>13</volume><issue>5</issue><spage>700</spage><epage>707</epage><pages>700-707</pages><issn>1467-7644</issn><eissn>1467-7652</eissn><abstract>Summary
Engineering the production of polyhydroxyalkanoates (PHAs) into high biomass bioenergy crops has the potential to provide a sustainable supply of bioplastics and energy from a single plant feedstock. One of the major challenges in engineering C4 plants for the production of poly[(R)‐3‐hydroxybutyrate] (PHB) is the significantly lower level of polymer produced in the chloroplasts of mesophyll (M) cells compared to bundle sheath (BS) cells, thereby limiting the full PHB yield‐potential of the plant. In this study, we provide evidence that the access to substrate for PHB synthesis may limit polymer production in M chloroplasts. Production of PHB in M cells of sugarcane is significantly increased by replacing β‐ketothiolase, the first enzyme in the bacterial PHA pathway, with acetoacetyl‐CoA synthase. This novel pathway enabled the production of PHB reaching an average of 6.3% of the dry weight of total leaf biomass, with levels ranging from 3.6 to 11.8% of the dry weight (DW) of individual leaves. These yields are more than twice the level reported in PHB‐producing sugarcane containing the β‐ketothiolase and illustrate the importance of producing polymer in mesophyll plastids to maximize yield. The molecular weight of the polymer produced was greater than 2 × 106 Da. These results are a major step forward in engineering a high biomass C4 grass for the commercial production of PHB.</abstract><cop>England</cop><pub>John Wiley & Sons, Inc</pub><pmid>25532451</pmid><doi>10.1111/pbi.12298</doi><tpages>8</tpages><orcidid>https://orcid.org/0000-0002-1341-7871</orcidid><oa>free_for_read</oa></addata></record> |
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| ispartof | Plant biotechnology journal, 2015-06, Vol.13 (5), p.700-707 |
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| subjects | acetoacetyl‐CoA synthase Acetyl-CoA C-Acyltransferase - genetics Acetyl-CoA C-Acyltransferase - metabolism Acyl Coenzyme A - metabolism Bacteria Biodiesel fuels Biofuels Biomass Bioplastics biopolymer Biosynthesis Biosynthetic Pathways Bundling Chemical synthesis Chloroplasts Chloroplasts - genetics Crops, Agricultural Dry weight Drying Energy crops Enzymes Hydroxybutyrates - metabolism Leaves Lignocellulose M cells Mesophyll Mesophyll Cells - metabolism Molecular weight NphT7 Pathways PHB Plant Leaves - enzymology Plant Leaves - genetics Plant Leaves - growth & development Plant Proteins - genetics Plant Proteins - metabolism Plants (botany) Plants (organisms) Plants, Genetically Modified Plastids - metabolism Poly-3-hydroxybutyrate Polyesters Polyesters - metabolism Polyhydroxyalkanoates Polyhydroxyalkanoates - metabolism Polyhydroxybutyrate Polyhydroxybutyric acid Polymers Renewable energy Saccharum - enzymology Saccharum - genetics Saccharum - growth & development Sheaths Substrates Sugarcane Transgenic plants β‐ketothiolase |
| title | The use of an acetoacetyl‐CoA synthase in place of a β‐ketothiolase enhances poly‐3‐hydroxybutyrate production in sugarcane mesophyll cells |
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