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Analysis of the Rice ADP-Glucose Transporter (OsBT1) Indicates the Presence of Regulatory Processes in the Amyloplast Stroma That Control ADP-Glucose Flux into Starch.
Plant Physiol. 2016 Mar; 170(3):1271-83.PP

Abstract

Previous studies showed that efforts to further elevate starch synthesis in rice (Oryza sativa) seeds overproducing ADP-glucose (ADPglc) were prevented by processes downstream of ADPglc synthesis. Here, we identified the major ADPglc transporter by studying the shrunken3 locus of the EM1093 rice line, which harbors a mutation in the BRITTLE1 (BT1) adenylate transporter (OsBt1) gene. Despite containing elevated ADPglc levels (approximately 10-fold) compared with the wild-type, EM1093 grains are small and shriveled due to the reduction in the amounts and size of starch granules. Increases in ADPglc levels in EM1093 were due to their poor uptake of ADP-[(14)C]glc by amyloplasts. To assess the potential role of BT1 as a rate-determining step in starch biosynthesis, the maize ZmBt1 gene was overexpressed in the wild-type and the GlgC (CS8) transgenic line expressing a bacterial glgC-TM gene. ADPglc transport assays indicated that transgenic lines expressing ZmBT1 alone or combined with GlgC exhibited higher rates of transport (approximately 2-fold), with the GlgC (CS8) and GlgC/ZmBT1 (CS8/AT5) lines showing elevated ADPglc levels in amyloplasts. These increases, however, did not lead to further enhancement in seed weights even when these plant lines were grown under elevated CO2. Overall, our results indicate that rice lines with enhanced ADPglc synthesis and import into amyloplasts reveal additional barriers within the stroma that restrict maximum carbon flow into starch.

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Authors+Show Affiliations

Cakir B
Institute of Biological Chemistry, Washington State University, Pullman, Washington 99164 (B.C., A.T., S.-K.H., T.W.O.);Faculty of Agriculture, Kyushu University, Fukuoka 812-8581, Japan (S.Sh., H.M., R.S., H.S.);Department of Agricultural Biotechnology, Assam Agricultural University, Jorhat-785013, Assam, India (S.Si.); andDepartment of Biological Production, Akita Prefectural University, Akita City, Akita 010-01195, Japan (N.C., Y.H., N.F.).
Shiraishi S
Institute of Biological Chemistry, Washington State University, Pullman, Washington 99164 (B.C., A.T., S.-K.H., T.W.O.);Faculty of Agriculture, Kyushu University, Fukuoka 812-8581, Japan (S.Sh., H.M., R.S., H.S.);Department of Agricultural Biotechnology, Assam Agricultural University, Jorhat-785013, Assam, India (S.Si.); andDepartment of Biological Production, Akita Prefectural University, Akita City, Akita 010-01195, Japan (N.C., Y.H., N.F.).
Tuncel A
Institute of Biological Chemistry, Washington State University, Pullman, Washington 99164 (B.C., A.T., S.-K.H., T.W.O.);Faculty of Agriculture, Kyushu University, Fukuoka 812-8581, Japan (S.Sh., H.M., R.S., H.S.);Department of Agricultural Biotechnology, Assam Agricultural University, Jorhat-785013, Assam, India (S.Si.); andDepartment of Biological Production, Akita Prefectural University, Akita City, Akita 010-01195, Japan (N.C., Y.H., N.F.).
Matsusaka H
Institute of Biological Chemistry, Washington State University, Pullman, Washington 99164 (B.C., A.T., S.-K.H., T.W.O.);Faculty of Agriculture, Kyushu University, Fukuoka 812-8581, Japan (S.Sh., H.M., R.S., H.S.);Department of Agricultural Biotechnology, Assam Agricultural University, Jorhat-785013, Assam, India (S.Si.); andDepartment of Biological Production, Akita Prefectural University, Akita City, Akita 010-01195, Japan (N.C., Y.H., N.F.).
Satoh R
Institute of Biological Chemistry, Washington State University, Pullman, Washington 99164 (B.C., A.T., S.-K.H., T.W.O.);Faculty of Agriculture, Kyushu University, Fukuoka 812-8581, Japan (S.Sh., H.M., R.S., H.S.);Department of Agricultural Biotechnology, Assam Agricultural University, Jorhat-785013, Assam, India (S.Si.); andDepartment of Biological Production, Akita Prefectural University, Akita City, Akita 010-01195, Japan (N.C., Y.H., N.F.).
Singh S
Institute of Biological Chemistry, Washington State University, Pullman, Washington 99164 (B.C., A.T., S.-K.H., T.W.O.);Faculty of Agriculture, Kyushu University, Fukuoka 812-8581, Japan (S.Sh., H.M., R.S., H.S.);Department of Agricultural Biotechnology, Assam Agricultural University, Jorhat-785013, Assam, India (S.Si.); andDepartment of Biological Production, Akita Prefectural University, Akita City, Akita 010-01195, Japan (N.C., Y.H., N.F.).
Crofts N
Institute of Biological Chemistry, Washington State University, Pullman, Washington 99164 (B.C., A.T., S.-K.H., T.W.O.);Faculty of Agriculture, Kyushu University, Fukuoka 812-8581, Japan (S.Sh., H.M., R.S., H.S.);Department of Agricultural Biotechnology, Assam Agricultural University, Jorhat-785013, Assam, India (S.Si.); andDepartment of Biological Production, Akita Prefectural University, Akita City, Akita 010-01195, Japan (N.C., Y.H., N.F.).
Hosaka Y
Institute of Biological Chemistry, Washington State University, Pullman, Washington 99164 (B.C., A.T., S.-K.H., T.W.O.);Faculty of Agriculture, Kyushu University, Fukuoka 812-8581, Japan (S.Sh., H.M., R.S., H.S.);Department of Agricultural Biotechnology, Assam Agricultural University, Jorhat-785013, Assam, India (S.Si.); andDepartment of Biological Production, Akita Prefectural University, Akita City, Akita 010-01195, Japan (N.C., Y.H., N.F.).
Fujita N
Institute of Biological Chemistry, Washington State University, Pullman, Washington 99164 (B.C., A.T., S.-K.H., T.W.O.);Faculty of Agriculture, Kyushu University, Fukuoka 812-8581, Japan (S.Sh., H.M., R.S., H.S.);Department of Agricultural Biotechnology, Assam Agricultural University, Jorhat-785013, Assam, India (S.Si.); andDepartment of Biological Production, Akita Prefectural University, Akita City, Akita 010-01195, Japan (N.C., Y.H., N.F.).
Hwang SK
Institute of Biological Chemistry, Washington State University, Pullman, Washington 99164 (B.C., A.T., S.-K.H., T.W.O.);Faculty of Agriculture, Kyushu University, Fukuoka 812-8581, Japan (S.Sh., H.M., R.S., H.S.);Department of Agricultural Biotechnology, Assam Agricultural University, Jorhat-785013, Assam, India (S.Si.); andDepartment of Biological Production, Akita Prefectural University, Akita City, Akita 010-01195, Japan (N.C., Y.H., N.F.).
Satoh H
Institute of Biological Chemistry, Washington State University, Pullman, Washington 99164 (B.C., A.T., S.-K.H., T.W.O.);Faculty of Agriculture, Kyushu University, Fukuoka 812-8581, Japan (S.Sh., H.M., R.S., H.S.);Department of Agricultural Biotechnology, Assam Agricultural University, Jorhat-785013, Assam, India (S.Si.); andDepartment of Biological Production, Akita Prefectural University, Akita City, Akita 010-01195, Japan (N.C., Y.H., N.F.) okita@wsu.edu hikaru.satoh.682@m.kyushu-u.ac.jp.
Okita TW
Institute of Biological Chemistry, Washington State University, Pullman, Washington 99164 (B.C., A.T., S.-K.H., T.W.O.);Faculty of Agriculture, Kyushu University, Fukuoka 812-8581, Japan (S.Sh., H.M., R.S., H.S.);Department of Agricultural Biotechnology, Assam Agricultural University, Jorhat-785013, Assam, India (S.Si.); andDepartment of Biological Production, Akita Prefectural University, Akita City, Akita 010-01195, Japan (N.C., Y.H., N.F.) okita@wsu.edu hikaru.satoh.682@m.kyushu-u.ac.jp.

MeSH

Adenosine Diphosphate GlucoseGenes, PlantGlucose Transport Proteins, FacilitativeMutationOryzaPlant ProteinsPlants, Genetically ModifiedPlastidsRecombinant ProteinsSeedsStarchZea mays

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

26754668

Citation

Cakir, Bilal, et al. "Analysis of the Rice ADP-Glucose Transporter (OsBT1) Indicates the Presence of Regulatory Processes in the Amyloplast Stroma That Control ADP-Glucose Flux Into Starch." Plant Physiology, vol. 170, no. 3, 2016, pp. 1271-83.
Cakir B, Shiraishi S, Tuncel A, et al. Analysis of the Rice ADP-Glucose Transporter (OsBT1) Indicates the Presence of Regulatory Processes in the Amyloplast Stroma That Control ADP-Glucose Flux into Starch. Plant Physiol. 2016;170(3):1271-83.
Cakir, B., Shiraishi, S., Tuncel, A., Matsusaka, H., Satoh, R., Singh, S., Crofts, N., Hosaka, Y., Fujita, N., Hwang, S. K., Satoh, H., & Okita, T. W. (2016). Analysis of the Rice ADP-Glucose Transporter (OsBT1) Indicates the Presence of Regulatory Processes in the Amyloplast Stroma That Control ADP-Glucose Flux into Starch. Plant Physiology, 170(3), 1271-83. https://doi.org/10.1104/pp.15.01911
Cakir B, et al. Analysis of the Rice ADP-Glucose Transporter (OsBT1) Indicates the Presence of Regulatory Processes in the Amyloplast Stroma That Control ADP-Glucose Flux Into Starch. Plant Physiol. 2016;170(3):1271-83. PubMed PMID: 26754668.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Analysis of the Rice ADP-Glucose Transporter (OsBT1) Indicates the Presence of Regulatory Processes in the Amyloplast Stroma That Control ADP-Glucose Flux into Starch. AU - Cakir,Bilal, AU - Shiraishi,Shota, AU - Tuncel,Aytug, AU - Matsusaka,Hiroaki, AU - Satoh,Ryosuke, AU - Singh,Salvinder, AU - Crofts,Naoko, AU - Hosaka,Yuko, AU - Fujita,Naoko, AU - Hwang,Seon-Kap, AU - Satoh,Hikaru, AU - Okita,Thomas W, Y1 - 2016/01/11/ PY - 2015/12/17/received PY - 2016/01/07/accepted PY - 2016/1/13/entrez PY - 2016/1/13/pubmed PY - 2017/2/14/medline SP - 1271 EP - 83 JF - Plant physiology JO - Plant Physiol VL - 170 IS - 3 N2 - Previous studies showed that efforts to further elevate starch synthesis in rice (Oryza sativa) seeds overproducing ADP-glucose (ADPglc) were prevented by processes downstream of ADPglc synthesis. Here, we identified the major ADPglc transporter by studying the shrunken3 locus of the EM1093 rice line, which harbors a mutation in the BRITTLE1 (BT1) adenylate transporter (OsBt1) gene. Despite containing elevated ADPglc levels (approximately 10-fold) compared with the wild-type, EM1093 grains are small and shriveled due to the reduction in the amounts and size of starch granules. Increases in ADPglc levels in EM1093 were due to their poor uptake of ADP-[(14)C]glc by amyloplasts. To assess the potential role of BT1 as a rate-determining step in starch biosynthesis, the maize ZmBt1 gene was overexpressed in the wild-type and the GlgC (CS8) transgenic line expressing a bacterial glgC-TM gene. ADPglc transport assays indicated that transgenic lines expressing ZmBT1 alone or combined with GlgC exhibited higher rates of transport (approximately 2-fold), with the GlgC (CS8) and GlgC/ZmBT1 (CS8/AT5) lines showing elevated ADPglc levels in amyloplasts. These increases, however, did not lead to further enhancement in seed weights even when these plant lines were grown under elevated CO2. Overall, our results indicate that rice lines with enhanced ADPglc synthesis and import into amyloplasts reveal additional barriers within the stroma that restrict maximum carbon flow into starch. SN - 1532-2548 UR - https://www.unboundmedicine.com/medline/citation/26754668/Analysis_of_the_Rice_ADP_Glucose_Transporter__OsBT1__Indicates_the_Presence_of_Regulatory_Processes_in_the_Amyloplast_Stroma_That_Control_ADP_Glucose_Flux_into_Starch_ DB - PRIME DP - Unbound Medicine ER -