植物叶片淀粉分解与淀粉超量积累研究
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摘要
植物叶片白天进行光合作用合成过渡型淀粉,夜间过渡型淀粉分解供植物生理代谢和生长发育所需。以往研究显示叶片中过渡型淀粉的分解受着严格的生理节律调控,但是,当淀粉分解代谢及其下游代谢基因功能出现异常时,淀粉通常会在叶片中超量积累。植物学家通过筛选叶片淀粉超量积累突变体与目标基因功能解析,初步完成了对植物叶片淀粉分解代谢网络图谱的绘制。笔者通过对植物叶片过渡型淀粉分解与超量积累现象的最新研究进行梳理,以探寻提高作物叶片淀粉含量的可能途径。
Plants produce transitory starch via photosynthesis in leaves during the day and remobilize it for normal physiological metabolism and growth at night. Leaf transitory starch degradation is rigorously regulated by circadian rhythm,however,the function deficiency of key genes involving in leaf starch degradation and its downstream metabolism would lead to leaf starch excess phenomenon. To explore the molecular mechanisms of leaf starch degradation,botanists have screened a large number of leaf starch excess mutants and identified numerous responsible genes,that a model of leaf starch degradation pathway in higher plant has been established based on those excellent work. This review summarizes the recent advances in leaf starch degradation and leaf starch excess research and discusses the potential strategies for improving crop leaf starch content.
Plants produce transitory starch via photosynthesis in leaves during the day and remobilize it for normal physiological metabolism and growth at night. Leaf transitory starch degradation is rigorously regulated by circadian rhythm,however,the function deficiency of key genes involving in leaf starch degradation and its downstream metabolism would lead to leaf starch excess phenomenon. To explore the molecular mechanisms of leaf starch degradation,botanists have screened a large number of leaf starch excess mutants and identified numerous responsible genes,that a model of leaf starch degradation pathway in higher plant has been established based on those excellent work. This review summarizes the recent advances in leaf starch degradation and leaf starch excess research and discusses the potential strategies for improving crop leaf starch content.
引文
[1]ZEEMAN S C,TIESSEN A,PILLING E,et al.Starch synthesis in Arabidopsis granule synthesis,composition,and structure[J].Plant Physiologyogy,2002,129(2):516-529.
[2]FEIKE D,SEUNG D,GRAF A,et al.The starch granuleassociated protein early starvation1 is required for the control of starch degradation in Arabidopsis thaliana leaves[J].The Plant Cell,2016,28(6):1472-1489.
[3]LLOYD J R,KOSSMANN J,RITTE G.Leaf starch degradation comes out of the shadows[J].Trends in Plant Science,2005,10(3):130-137.
[4]KOTTING O,SANTELIA D,EDNER C,et al.STARCH-EXCESS4 is a laforin-like phosphoglucan phosphatase required for starch degradation in Arabidopsis thaliana[J].The Plant Cell,2009,21(1):334-346.
[5]SANTELIA D,ZEEMAN S C.Progress in Arabidopsis starch research and potential biotechnological applications[J].Current Opinion in Biotechnology,2011,22(2):271-280.
[6]WEISE S E,VAN WIJK K J,SHARKEY T D.The role of transitory starch in C3,CAM,and C4 metabolism and opportunities for engineering leaf starch accumulation[J].Journal of Experimental Botany,2011,62(9):3109-3118.
[7]HIROSE T,AOKI N,HARADA Y,et al.Disruption of a rice gene forα-glucan water dikinase,Os GWD1,leads to hyperaccumulation of starch in leaves but exhibits limited effects on growth[J].Frontiers in Plant Science,2013,4:147.
[8]邓平壤,唐向民,韦清源,等.植物叶片淀粉分解机理研究进展[J].广西农业科学,2009,40(2):147-152.
[9]张东方,崔大方,赵赣,等.植物叶片暂时淀粉分解途径研究进展[J].西北植物学报,2011,31(9):1927-1932.
[10]MIKKELSEN R,MUTENDA K E,MANT A,et al.Α-Glucan,water dikinase(GWD):A plastidic enzyme with redox-regulated and coordinated catalytic activity and binding affinity[J].Proceedings of the National Academy of Sciences of the United States of America,2005,102(5):1785-1790.
[11]EDNER C,LI J,ALBRECHT T,et al.Glucan,water dikinase activity stimulates breakdown of starch granules by plastidialβ-amylases[J].Plant Physiology,2007,145(1):17-28.
[12]RITTE G,LLOYD J R,ECKERMANN N,et al.The starch-related R1 protein is anα-glucan,water dikinase[J].Proceedings of the National Academy of Sciences of the United States of America,2002,99(10):7166-7171.
[13]YU T S,KOFLER H,HAUSLER R E,et al.The Arabidopsis sex1 mutant is defective in the R1 protein,a general regulator of starch degradation in plants,and not in the chloroplast hexose transporter[J].The Plant Cell,2001,13(8):1907-1918.
[14]RITTE G,HEYDENREICH M,MAHLOW S,et al.Phosphorylation of C6-and C3-positions of glucosyl residues in starch is catalysed by distinct dikinases[J].FEBS Letters,2006,580(20):4872-4876.
[15]KOTTING O,PUSCH K,TIESSEN A,et al.Identification of a novel enzyme required for starch metabolism in Arabidopsis leaves,the phosphoglucan,water dikinase[J].Plant Physiology,2005,137(1):242-252.
[16]SMITH A M,ZEEMAN S C,SMITH S M.Starch degradation[J].Annual Review of Plant Biology,2005,56:73-98.
[17]STREB S,EICKE S,ZEEMAN S C.The simultaneous abolition of three starch hydrolases blocks transient starch breakdown in Arabidopsis[J].The Journal of Biological Chemistry,2012,287(50):41745-41756.
[18]HAIDER M S,BARNES J D,CUSHMAN J C,et al.ACAM and starch-deficient mutant of the facultative CAMspecies mesembryanthemum crystallinum reconciles sink demands by repartitioning carbon during acclimation to salinity[J].Journal of Experimental Botany,2012,63(5):1985-1996.
[19]COMPAROT M S,KOTTING O,STETTLER M,et al.Aputative phosphatase,LSF1,is required for normal starch turnover in Arabidopsis leaves[J].Plant Physiology,2010,152(2):685-697.
[20]SCHEIDIG A,FROHLICH A,SCHULZE S,et al.Downregulation of a chloroplast-targetedβ-amylase leads to a starch-excess phenotype in leaves[J].The Plant Journal,2002,30(5):581-591.
[21]HUSSAIN H,MANT A,SEALE R,et al.Three isoforms of isoamylase contribute different catalytic properties for the debranching of potato glucans[J].The Plant Cell,2003,15(1):133-149.
[22]WATTEBLED F,DONG Y,DUMEZ S,et al.Mutants of Arabidopsis lacking a chloroplastic isoamylase accumulate phytoglycogen and an abnormal form of amylopectin[J].Plant Physiology,2005,138(1):184-195.
[23]STITT M,ZEEMAN S C.Starch turnover:Pathways,regulation and role in growth[J].Current Opinion in Plant Biology,2012(15):282-292.
[24]NIITTYLA T,MESSERLI G,TREVISAN M,et al.A previously unknown maltose transporter essential for starch degradation in leaves[J].Science,2004,303(5654):87-89.
[25]CHIA T,THORNEYCROFT D,CHAPPLE A,et al.A cytosolic glucosyltransferase is required for conversion of starch to sucrose in Arabidopsis leaves at night[J].The Plant Journal,2004,37(6):853-863.
[26]ZEEMAN S C,SMITH S M,SMITH A M.The breakdown of starch in leaves[J].New Phytologist,2004,163(2):247-261.
[27]ZEEMAN S C,THORNEYCROFT D,SCHUPP N,et al.Plastidialα-glucan phosphorylase is not required for starch degradation in Arabidopsis leaves but has a role in the tolerance of abiotic stress[J].Plant Physiology,2004,135(2):849-858.
[28]LLOYD J R,BLENNOW A,BURHENNE K,et al.Repression of a novel isoform of disproportionating enzyme(st DPE2)in potato leads to inhibition of starch degradation in leaves but not tubers stored at low temperature[J].Plant Physiology,2004,134(4):1347-1354.
[29]GRAF A,SCHLERETH A,STITT M,et al.Circadian control of carbohydrate availability for growth in Arabidopsis plants at night[J].Proceedings of the National Academy of Sciences of the United States of America,2010,107(20):9458-9463.
[30]ZEEMAN S C,KOSSMANN J,SMITH A M.Starch:Its metabolism,evolution,and biotechnological modification in plants[J].Annual Review of Plant Biology,2010,61:209-234.
[31]NASHILEVITZ S,MELAMED B C,AHARONI A,et al.The legwd mutant uncovers the role of starch phosphorylation in pollen development and germination in tomato[J].The Plant Journal,2009,57(1):1-13.
[32]VRIET C,WELHAM T,BRACHMANN A,et al.A suite of Lotus japonicus starch mutants reveals both conserved and novel features of starch metabolism[J].Plant Physiology,2010,154(2):643-655.
[33]LIANG C,HIROSE T,OKAMURA M,et al.Phenotypic analyses of rice lse2 and lse3 mutants that exhibit hyperaccumulation of starch in the leaf blades[J].Rice,2014,7(1):32.
[34]LO Y C,HUANG L F,CHENG C L,et al.Using a starchrich mutant of Arabidopsis thaliana as feedstock for fermentative hydrogen production[J].Bioresource Technology,2011,102(18):8543-8546.
[35]WEISE S E,AUNG K,JAROU Z J,et al.Engineering starch accumulation by manipulation of phosphate metabolism of starch[J].Plant Biotechnology Journal,2012(10):545-554.
[36]FULTON D C,STETTLER M,METTLER T,et al.β-AM-YLASE4,a noncatalytic protein required for starch breakdown,acts upstream of three activeβ-amylases in Arabidopsis chloroplasts[J].The Plant Cell,2008,20(4):1040-1058.
[37]DELATTE T,UMHANG M,TREVISAN M,et al.Evidence for distinct mechanisms of starch granule breakdown in plants[J].The Journal of Biological Chemistry,2006,281(17):12050-12059.
[38]BAUNSGAARD L,LUTKEN H,MIKKELSEN R,et al.Anovel isoform of glucan,water dikinase phosphorylates pre-phosphorylatedα-glucans and is involved in starch degradation in Arabidopsis[J].The Plant Journal,2005,41(4):595-605.
[39]CRITCHLEY J H,ZEEMAN S C,TAKAHA T,et al.Acritical role for disproportionating enzyme in starch breakdown is revealed by a knock-out mutation in Arabidopsis[J].The Plant Journal,2001,26(1):89-100.
[40]GOTTWALD J R,KRYSAN P J,YOUNG J C,et al.Genetic evidence for the in planta role of phloem-specific plasma membrane sucrose transporters[J].Proceedings of the National Academy of Sciences of the United States of America,2000,97(25):13979-13984.
[41]SRIVASTAVA A C,GANESAN S,ISMAIL I O,et al.Functional characterization of the Arabidopsis At SUC2 sucrose/H+symporter by tissue-specific complementation reveals an essential role in phloem loading but not in long-distance transport[J].Plant Physiology,2008,148(1):200-211.
[42]DINGES J R,COLLEONI C,JAMES M G,et al.Mutational analysis of the pullulanase-type debranching enzyme of maize indicates multiple functions in starch metabolism[J].The Plant Cell,2003,15(3):666-680.
[43]RUSSIN W A,EVERT R F,VANDERVEER P J,et al.Modification of a specific class of plasmodesmata and loss of sucrose export ability in the sucrose export defective1maize mutant[J].The Plant Cell,1996,8(4):645-658.
[44]PROVENCHER L M,MIAO L,SINHA N,et al.Sucrose export defective1 encodes a novel protein implicated in chloroplast-to-nucleus signaling[J].The Plant Cell,2001,13(5):1127-1141.
[45]SATTLER S E,CAHOON E B,COUGHLAN S J,et al.Characterization of tocopherol cyclases from higher plants and cyanobacteria evolutionary implications for tocopherol synthesis and function[J].Plant Physiology,2003,132(4):2184-2195.
[46]MA Y,BAKER R F,MAGALLANES L M,et al.Tiedyed1 and Sucrose export defective1 act independently to promote carbohydrate export from maize leaves[J].Planta,2008,227(3):527-538.
[47]BRAUN D M,MA Y,INADA N,et al.Tie-dyed1 regulates carbohydrate accumulation in maize leaves[J].Plant Physiology,2006,142(4):1511-1522.
[48]MA Y,SLEWINSKI T L,BAKER R F,et al.Tie-dyed1encodes a novel,phloem-expressed transmembrane protein that functions in carbohydrate partitioning[J].Plant Physiology,2009,149(1):181-194.
[49]BAKER R F,BRAUN D M.Tie-dyed2 functions with tiedyed1 to promote carbohydrate export from maize leaves[J].Plant Physiology,2008,146(3):1085-1097.
[50]SLEWINSKI T L,BAKER R F,STUBERT A,et al.Tiedyed2 encodes a callose synthase that functions in vein development and affects symplastic trafficking within the phloem of maize leaves[J].Plant Physiology,2012,160(3):1540-1550.
[51]SLEWINSKI T L,BRAUN D M.The psychedelic genes of maize redundantly promote carbohydrate export from leaves[J].Genetics,2010,185(1):221-232.
[52]SLEWINSKI T L,MEELEY R,BRAUN D M.Sucrose transporter1 functions in phloem loading in maize leaves[J].Journal of Experimental Botany,2009,60(3):881-892.
[53]YUN M,UMEMOTO T,KAWAGOE Y.Rice debranching enzyme isoamylase3 facilitates starch metabolism and affects plastid morphogenesis[J].Plant and Cell Physiology,2011,52(6):1068-1082.
[2]FEIKE D,SEUNG D,GRAF A,et al.The starch granuleassociated protein early starvation1 is required for the control of starch degradation in Arabidopsis thaliana leaves[J].The Plant Cell,2016,28(6):1472-1489.
[3]LLOYD J R,KOSSMANN J,RITTE G.Leaf starch degradation comes out of the shadows[J].Trends in Plant Science,2005,10(3):130-137.
[4]KOTTING O,SANTELIA D,EDNER C,et al.STARCH-EXCESS4 is a laforin-like phosphoglucan phosphatase required for starch degradation in Arabidopsis thaliana[J].The Plant Cell,2009,21(1):334-346.
[5]SANTELIA D,ZEEMAN S C.Progress in Arabidopsis starch research and potential biotechnological applications[J].Current Opinion in Biotechnology,2011,22(2):271-280.
[6]WEISE S E,VAN WIJK K J,SHARKEY T D.The role of transitory starch in C3,CAM,and C4 metabolism and opportunities for engineering leaf starch accumulation[J].Journal of Experimental Botany,2011,62(9):3109-3118.
[7]HIROSE T,AOKI N,HARADA Y,et al.Disruption of a rice gene forα-glucan water dikinase,Os GWD1,leads to hyperaccumulation of starch in leaves but exhibits limited effects on growth[J].Frontiers in Plant Science,2013,4:147.
[8]邓平壤,唐向民,韦清源,等.植物叶片淀粉分解机理研究进展[J].广西农业科学,2009,40(2):147-152.
[9]张东方,崔大方,赵赣,等.植物叶片暂时淀粉分解途径研究进展[J].西北植物学报,2011,31(9):1927-1932.
[10]MIKKELSEN R,MUTENDA K E,MANT A,et al.Α-Glucan,water dikinase(GWD):A plastidic enzyme with redox-regulated and coordinated catalytic activity and binding affinity[J].Proceedings of the National Academy of Sciences of the United States of America,2005,102(5):1785-1790.
[11]EDNER C,LI J,ALBRECHT T,et al.Glucan,water dikinase activity stimulates breakdown of starch granules by plastidialβ-amylases[J].Plant Physiology,2007,145(1):17-28.
[12]RITTE G,LLOYD J R,ECKERMANN N,et al.The starch-related R1 protein is anα-glucan,water dikinase[J].Proceedings of the National Academy of Sciences of the United States of America,2002,99(10):7166-7171.
[13]YU T S,KOFLER H,HAUSLER R E,et al.The Arabidopsis sex1 mutant is defective in the R1 protein,a general regulator of starch degradation in plants,and not in the chloroplast hexose transporter[J].The Plant Cell,2001,13(8):1907-1918.
[14]RITTE G,HEYDENREICH M,MAHLOW S,et al.Phosphorylation of C6-and C3-positions of glucosyl residues in starch is catalysed by distinct dikinases[J].FEBS Letters,2006,580(20):4872-4876.
[15]KOTTING O,PUSCH K,TIESSEN A,et al.Identification of a novel enzyme required for starch metabolism in Arabidopsis leaves,the phosphoglucan,water dikinase[J].Plant Physiology,2005,137(1):242-252.
[16]SMITH A M,ZEEMAN S C,SMITH S M.Starch degradation[J].Annual Review of Plant Biology,2005,56:73-98.
[17]STREB S,EICKE S,ZEEMAN S C.The simultaneous abolition of three starch hydrolases blocks transient starch breakdown in Arabidopsis[J].The Journal of Biological Chemistry,2012,287(50):41745-41756.
[18]HAIDER M S,BARNES J D,CUSHMAN J C,et al.ACAM and starch-deficient mutant of the facultative CAMspecies mesembryanthemum crystallinum reconciles sink demands by repartitioning carbon during acclimation to salinity[J].Journal of Experimental Botany,2012,63(5):1985-1996.
[19]COMPAROT M S,KOTTING O,STETTLER M,et al.Aputative phosphatase,LSF1,is required for normal starch turnover in Arabidopsis leaves[J].Plant Physiology,2010,152(2):685-697.
[20]SCHEIDIG A,FROHLICH A,SCHULZE S,et al.Downregulation of a chloroplast-targetedβ-amylase leads to a starch-excess phenotype in leaves[J].The Plant Journal,2002,30(5):581-591.
[21]HUSSAIN H,MANT A,SEALE R,et al.Three isoforms of isoamylase contribute different catalytic properties for the debranching of potato glucans[J].The Plant Cell,2003,15(1):133-149.
[22]WATTEBLED F,DONG Y,DUMEZ S,et al.Mutants of Arabidopsis lacking a chloroplastic isoamylase accumulate phytoglycogen and an abnormal form of amylopectin[J].Plant Physiology,2005,138(1):184-195.
[23]STITT M,ZEEMAN S C.Starch turnover:Pathways,regulation and role in growth[J].Current Opinion in Plant Biology,2012(15):282-292.
[24]NIITTYLA T,MESSERLI G,TREVISAN M,et al.A previously unknown maltose transporter essential for starch degradation in leaves[J].Science,2004,303(5654):87-89.
[25]CHIA T,THORNEYCROFT D,CHAPPLE A,et al.A cytosolic glucosyltransferase is required for conversion of starch to sucrose in Arabidopsis leaves at night[J].The Plant Journal,2004,37(6):853-863.
[26]ZEEMAN S C,SMITH S M,SMITH A M.The breakdown of starch in leaves[J].New Phytologist,2004,163(2):247-261.
[27]ZEEMAN S C,THORNEYCROFT D,SCHUPP N,et al.Plastidialα-glucan phosphorylase is not required for starch degradation in Arabidopsis leaves but has a role in the tolerance of abiotic stress[J].Plant Physiology,2004,135(2):849-858.
[28]LLOYD J R,BLENNOW A,BURHENNE K,et al.Repression of a novel isoform of disproportionating enzyme(st DPE2)in potato leads to inhibition of starch degradation in leaves but not tubers stored at low temperature[J].Plant Physiology,2004,134(4):1347-1354.
[29]GRAF A,SCHLERETH A,STITT M,et al.Circadian control of carbohydrate availability for growth in Arabidopsis plants at night[J].Proceedings of the National Academy of Sciences of the United States of America,2010,107(20):9458-9463.
[30]ZEEMAN S C,KOSSMANN J,SMITH A M.Starch:Its metabolism,evolution,and biotechnological modification in plants[J].Annual Review of Plant Biology,2010,61:209-234.
[31]NASHILEVITZ S,MELAMED B C,AHARONI A,et al.The legwd mutant uncovers the role of starch phosphorylation in pollen development and germination in tomato[J].The Plant Journal,2009,57(1):1-13.
[32]VRIET C,WELHAM T,BRACHMANN A,et al.A suite of Lotus japonicus starch mutants reveals both conserved and novel features of starch metabolism[J].Plant Physiology,2010,154(2):643-655.
[33]LIANG C,HIROSE T,OKAMURA M,et al.Phenotypic analyses of rice lse2 and lse3 mutants that exhibit hyperaccumulation of starch in the leaf blades[J].Rice,2014,7(1):32.
[34]LO Y C,HUANG L F,CHENG C L,et al.Using a starchrich mutant of Arabidopsis thaliana as feedstock for fermentative hydrogen production[J].Bioresource Technology,2011,102(18):8543-8546.
[35]WEISE S E,AUNG K,JAROU Z J,et al.Engineering starch accumulation by manipulation of phosphate metabolism of starch[J].Plant Biotechnology Journal,2012(10):545-554.
[36]FULTON D C,STETTLER M,METTLER T,et al.β-AM-YLASE4,a noncatalytic protein required for starch breakdown,acts upstream of three activeβ-amylases in Arabidopsis chloroplasts[J].The Plant Cell,2008,20(4):1040-1058.
[37]DELATTE T,UMHANG M,TREVISAN M,et al.Evidence for distinct mechanisms of starch granule breakdown in plants[J].The Journal of Biological Chemistry,2006,281(17):12050-12059.
[38]BAUNSGAARD L,LUTKEN H,MIKKELSEN R,et al.Anovel isoform of glucan,water dikinase phosphorylates pre-phosphorylatedα-glucans and is involved in starch degradation in Arabidopsis[J].The Plant Journal,2005,41(4):595-605.
[39]CRITCHLEY J H,ZEEMAN S C,TAKAHA T,et al.Acritical role for disproportionating enzyme in starch breakdown is revealed by a knock-out mutation in Arabidopsis[J].The Plant Journal,2001,26(1):89-100.
[40]GOTTWALD J R,KRYSAN P J,YOUNG J C,et al.Genetic evidence for the in planta role of phloem-specific plasma membrane sucrose transporters[J].Proceedings of the National Academy of Sciences of the United States of America,2000,97(25):13979-13984.
[41]SRIVASTAVA A C,GANESAN S,ISMAIL I O,et al.Functional characterization of the Arabidopsis At SUC2 sucrose/H+symporter by tissue-specific complementation reveals an essential role in phloem loading but not in long-distance transport[J].Plant Physiology,2008,148(1):200-211.
[42]DINGES J R,COLLEONI C,JAMES M G,et al.Mutational analysis of the pullulanase-type debranching enzyme of maize indicates multiple functions in starch metabolism[J].The Plant Cell,2003,15(3):666-680.
[43]RUSSIN W A,EVERT R F,VANDERVEER P J,et al.Modification of a specific class of plasmodesmata and loss of sucrose export ability in the sucrose export defective1maize mutant[J].The Plant Cell,1996,8(4):645-658.
[44]PROVENCHER L M,MIAO L,SINHA N,et al.Sucrose export defective1 encodes a novel protein implicated in chloroplast-to-nucleus signaling[J].The Plant Cell,2001,13(5):1127-1141.
[45]SATTLER S E,CAHOON E B,COUGHLAN S J,et al.Characterization of tocopherol cyclases from higher plants and cyanobacteria evolutionary implications for tocopherol synthesis and function[J].Plant Physiology,2003,132(4):2184-2195.
[46]MA Y,BAKER R F,MAGALLANES L M,et al.Tiedyed1 and Sucrose export defective1 act independently to promote carbohydrate export from maize leaves[J].Planta,2008,227(3):527-538.
[47]BRAUN D M,MA Y,INADA N,et al.Tie-dyed1 regulates carbohydrate accumulation in maize leaves[J].Plant Physiology,2006,142(4):1511-1522.
[48]MA Y,SLEWINSKI T L,BAKER R F,et al.Tie-dyed1encodes a novel,phloem-expressed transmembrane protein that functions in carbohydrate partitioning[J].Plant Physiology,2009,149(1):181-194.
[49]BAKER R F,BRAUN D M.Tie-dyed2 functions with tiedyed1 to promote carbohydrate export from maize leaves[J].Plant Physiology,2008,146(3):1085-1097.
[50]SLEWINSKI T L,BAKER R F,STUBERT A,et al.Tiedyed2 encodes a callose synthase that functions in vein development and affects symplastic trafficking within the phloem of maize leaves[J].Plant Physiology,2012,160(3):1540-1550.
[51]SLEWINSKI T L,BRAUN D M.The psychedelic genes of maize redundantly promote carbohydrate export from leaves[J].Genetics,2010,185(1):221-232.
[52]SLEWINSKI T L,MEELEY R,BRAUN D M.Sucrose transporter1 functions in phloem loading in maize leaves[J].Journal of Experimental Botany,2009,60(3):881-892.
[53]YUN M,UMEMOTO T,KAWAGOE Y.Rice debranching enzyme isoamylase3 facilitates starch metabolism and affects plastid morphogenesis[J].Plant and Cell Physiology,2011,52(6):1068-1082.
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