植物紫色酸性磷酸酶基因家族功能研究进展
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摘要
紫色酸性磷酸酶(PAPs)是一类广泛存在于植物体内的金属磷酸酯酶,其羧基端含有1个保守结构域,由5个保守基序和7个氨基酸残基构成。作为一种特殊的酸性磷酸酶, PAPs在酸性环境下能够有效催化磷酸酯或酸酐的水解,释放出植物可以利用的磷酸基团。此外, PAPs在调节植物碳代谢、细胞壁合成和抵御病菌侵染等方面也发挥重要生理作用。该文简要介绍了PAPs的结构、家族成员及其调控因子,并着重总结了近年来对PAPs生物学功能的研究进展,为今后系统开展PAPs功能研究提供了理论参考。
Purple acid phosphatases(PAPs) are members of the metallo-phosphoesterase family identified from a wide range of plants. They are characterized by the presence of five conserved structure motifs and seven amino acid residues in the C-terminal. PAPs have mostly been studied for their potential involvement in phosphorus acquisition and redistribution because of their ability to catalyze the hydrolysis of activated phosphate esters and anhydrides under acidic conditions. Recent studies also showed that PAPs play important roles in modulating plant carbon metabolism, cell wall synthesis and pathogen resistance, etc. This review focuses on the structure, family members and regulatory factors of PAPs, with special emphasis on the recent progress of their biological functions, which will provide theoretical reference for further study of PAPs in plants.
Purple acid phosphatases(PAPs) are members of the metallo-phosphoesterase family identified from a wide range of plants. They are characterized by the presence of five conserved structure motifs and seven amino acid residues in the C-terminal. PAPs have mostly been studied for their potential involvement in phosphorus acquisition and redistribution because of their ability to catalyze the hydrolysis of activated phosphate esters and anhydrides under acidic conditions. Recent studies also showed that PAPs play important roles in modulating plant carbon metabolism, cell wall synthesis and pathogen resistance, etc. This review focuses on the structure, family members and regulatory factors of PAPs, with special emphasis on the recent progress of their biological functions, which will provide theoretical reference for further study of PAPs in plants.
引文
刘涛,陈海英,余海英,李廷轩,高尚卿,陈光登(2016).低磷胁迫下大麦叶片磷素利用特征.植物学报51,504-514.
卢坤,张凯,柴友荣,陆俊杏,唐章林,李加纳(2010).甘蓝和白菜紫色酸性磷酸酶17基因家族的克隆和比较分析.作物学报36,517-525.
周志高,汪金舫,周健民(2005).植物磷营养高效的分子生物学研究进展.植物学报22,82-91.
Cakmak I(2002).Plant nutrition research:priorities to meet human needs for food in sustainable ways.Plant Soil 247,3-24.
Del Vecchio HA,Ying S,Park J,Knowles VL,Kanno S,Tanoi K,She YM,Plaxton WC(2014).The cell walltargeted purple acid phosphatase AtPAP25 is critical for acclimation of Arabidopsis thaliana to nutritional phosphorus deprivation.Plant J 80,569-581.
Hammond JP,Broadley MR,White PJ(2004).Genetic responses to phosphorus deficiency.Ann Bot 94,323-332.
Hur YJ,Jin BR,Nam J,Chung YS,Lee JH,Choi HK,Yun DJ,Yi G,Kim YH,Kim DH(2010).Molecular characterization of Os PAP2:transgenic expression of a purple acid phosphatase up-regulated in phosphate-deprived rice suspension cells.Biotechnol Lett 32,163-170.
James J,David WL(1992).Dependence of photosynthesis of sunflower and maize leaves on phosphate supply,ribulose-1,5-bisphosphate carboxylase/oxygenase activity,and ribulose-1,5-bisphosphate pool size.Plant Physiol 98,801-807.
Jarenmark M,Haukka M,Demeshko S,Tuczek F,Zuppiroli L,Meyer F,Nordlander E(2011).Synthesis,characterization,and reactivity studies of heterodinuclear complexes modeling active sites in purple acid phospha-tases.Inorg Chem 50,3866-3887.
Kaida R,Hayashi T,Kaneko TS(2008).Purple acid phosphatase in the walls of tobacco cells.Phytochemistry 69,2546-2551.
Kaida R,Sage-Ono K,Kamada H,Okuyama H,Syono K,Kaneko TS(2003).Isolation and characterization of four cell wall purple acid phosphatase genes from tobacco cells.Biochim Biophys Acta-Gene Regul Mech 1625,134-140.
Kaida R,Satoh Y,Bulone V,Yamada Y,Kaku T,Hayashi T,Kaneko TS(2009).Activation ofβ-glucan synthases by wall-bound purple acid phosphatase in tobacco cells.Plant Physiol 150,1822-1830.
Kaida R,Serada S,Norioka N,Norioka S,Neumetzler L,Pauly M,Sampedro J,Zarra I,Hayashi T,Kaneko TS(2010).Potential role for purple acid phosphatase in the dephosphorylation of wall proteins in tobacco cells.Plant Physiol 153,603-610.
Klabunde T,Stahl B,Suerbaum H,Hahner S,Karas M,Hillenkamp F,Krebs B,Witzel H(1994).The amino acid sequence of the red kidney bean Fe(III)-Zn(II)purple acid phosphatase.Determination of the amino acid sequence by a combination of matrix-assisted laser desorption/ionization mass spectrometry and automated Edman sequencing.Eur J Biochem 226,369-375.
Klabunde T,Str?ter N,Krebs B,Witzel H(1995).Structural relationship between the mammalian Fe(III)-Fe(II)and the Fe(III)-Zn(II)plant purple acid phosphatases.FEBS Lett367,56-60.
Kong YB,Li XH,Ma J,Li WL,Yan GJ,Zhang CY(2014).Gm PAP4,a novel purple acid phosphatase gene isolated from soybean(Glycine max),enhanced extracellular phytate utilization in Arabidopsis thaliana.Plant Cell Rep 33,655-667.
Kuang RB,Chan KH,Yeung E,Lim BL(2009).Molecular and biochemical characterization of AtPAP15,a purple acid phosphatase with phytase activity,in Arabidopsis.Plant Physiol 151,199-209.
Kusudo T,Sakaki T,Inouye K(2003).Purification and characterization of purple acid phosphatase PAP1 from dry powder of sweet potato.Biosci Biotechnol Biochem 67,1609-1611.
Law YS,Zhang RS,Guan XQ,Cheng SF,Sun F,Duncan O,Murcha MW,Whelan J,Lim BL(2015).Phosphorylation and dephosphorylation of the presequence of precursor MULTIPLE ORGANELLAR RNA EDITING FACTOR3during import into mitochondria from Arabidopsis.Plant Physiol 169,1344-1355.
Li CC,Gui SH,Yang T,Walk T,Wang XR,Liao H(2012).Identification of soybean purple acid phosphatase genes and their expression responses to phosphorus availability and symbiosis.Ann Bot 109,275-285.
Li DP,Zhu HF,Liu KF,Liu X,Leggewie G,Udvardi M,Wang DW(2002).Purple acid phosphatases of Arabidopsis thaliana.Comparative analysis and differential regulation by phosphate deprivation.J Biol Chem 277,27772-27781.
Li WYF,Shao GH,Lam HM(2008).Ectopic expression of Gm PAP3 alleviates oxidative damage caused by salinity and osmotic stresses.New Phytol 178,80-91.
Liang C,Liu X,Sun YZ,Yiu SM,Lim BL(2014).Global small RNA analysis in fast-growing Arabidopsis thaliana with elevated concentrations of ATP and sugars.BMCGenomics 15,116.
Liang C,Zhang YJ,Cheng SF,Osorio S,Sun YZ,Fernie AR,Cheung CY,Lim BL(2015).Impacts of high ATPsupply from chloroplasts and mitochondria on the leaf metabolism of Arabidopsis thaliana.Front Plant Sci 6,922.
Liang CY,Tian J,Lam HM,Lim BL,Yan XL,Liao H(2010).Biochemical and molecular characterization of PvPAP3,a novel purple acid phosphatase isolated from common bean enhancing extracellular ATP utilization.Plant Physiol152,854-865.
Liao H,Wong FL,Phang TH,Cheung MY,Li WYF,Shao GH,Yan XL,Lam HM(2003).Gm PAP3,a novel purple acid phosphatase-like gene in soybean induced by NaCl stress but not phosphorus deficiency.Gene 318,103-111.
Nakazato H,Okamoto T,Nishikoori M,Washio K,Morita N,Haraguchi K,Thompson GA,Okuyama H(1998).The glycosylphosphatidylinositol-anchored phosphatase from Spirodela oligorrhiza is a purple acid phosphatase.Plant Physiol 118,1015-1020.
Olczak M,Morawiecka B,Watorek W(2003).Plant purple acid phosphatases-genes,structures and biological function.Acta Biochim Pol 50,1245-1256.
Ravichandran S,Stone SL,Bernhard B,Prithiviraj B(2013).Purple acid phosphatase 5 is required for maintaining basal resistance against Pseudomonas syringae in Arabidopsis.BMC Plant Biol 13,107.
Robinson WD,Carson I,Ying S,Ellis K,Plaxton WC(2012a).Eliminating the purple acid phosphatase AtPAP26 in Arabidopsis thaliana delays leaf senescence and impairs phosphorus remobilization.New Phytol 196,1024-1029.
Robinson WD,Park J,Tran HT,Del Vecchio HA,Ying S,Zins JL,Patel K,Mc Knight TD,Plaxton WC(2012b).The secreted purple acid phosphatase isozymes AtPAP12and AtPAP26 play a pivotal role in extracellular phosphate-scavenging by Arabidopsis thaliana.J Exp Bot 63,6531-6542.
Rubio V,Linhares F,Solano R,Martín AC,Iglesias J,Leyva A,Paz-Ares J(2001).A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae.Genes Dev 15,2122-2133.
Schenk G,Elliott TW,Leung E,Carrington LE,Mitic N,Gahan LR,Guddat LW(2008).Crystal structures of a purple acid phosphatase,representing different steps of this enzyme’s catalytic cycle.BMC Struct Biol 8,6.
Schenk G,Guddat LW,Ge Y,Carrington LE,Hume DA,Hamilton S,de Jersey J(2000a).Identification of mammalian-like purple acid phosphatases in a wide range of plants.Gene 250,117-125.
Schenk G,Korsinczky MLJ,Hume DA,Hamilton S,DeJersey J(2000b).Purple acid phosphatases from bacteria:similarities to mammalian and plant enzymes.Gene255,419-424.
Smith VH,Schindler DW(2009).Eutrophication science:where do we go from here?Trends Ecol Evol 24,201-207.
Strater N,Klabunde T,Tucker P,Witzel H,Krebs B(1995).Crystal structure of a purple acid phosphatase containing a dinuclear Fe(III)-Zn(II)active site.Science 268,1489-1492.
Sun F,Carrie C,Law S,Murcha MW,Zhang R,Law YS,Suen PK,Whelan J,Lim BL(2012b).At PAP2 is a tail-anchored protein in the outer membrane of chloroplasts and mitochondria.Plant Signal Behav 7,927-932.
Sun F,Liang C,Whelan J,Yang J,Zhang P,Lim BL(2013).Global transcriptome analysis of At PAP2-overexpressing Arabidopsis thaliana with elevated ATP.BMCGenomics 14,752.
Sun F,Suen PK,Zhang YJ,Liang C,Carrie C,Whelan J,Ward JL,Hawkins ND,Jiang LW,Lim BL(2012a).Adual-targeted purple acid phosphatase in Arabidopsis thaliana moderates carbon metabolism and its overexpression leads to faster plant growth and higher seed yield.New Phytol 194,206-219.
Sun YZ,Law YS,Cheng SF,Lim BL(2017).RNA editing of cytochrome c maturation transcripts is responsive to the energy status of leaf cells in Arabidopsis thaliana.Mitochondrion 35,23-34.
Tian J,Liao H(2015).The role of intracellular and secreted purple acid phosphatases in plant phosphorus scavenging and recycling.In:Plaxton WC,Lambers H,eds.Annual Plant Reviews Volume 48:Phosphorus Metabolism in Plants,Vol.48.West Sussex:John Wiley&Sons,Ltd.pp.265-287.
Tran HT,Hurley BA,Plaxton WC(2010a).Feeding hungry plants:the role of purple acid phosphatases in phosphate nutrition.Plant Sci 179,14-27.
Tran HT,Qian WQ,Hurley BA,She YM,Wang DW,Plaxton WC(2010b).Biochemical and molecular characterization of AtPAP12 and AtPAP26:the predominant purple acid phosphatase isozymes secreted by phosphatestarved Arabidopsis thaliana.Plant Cell Environ 33,1789-1803.
Vance CP(2001).Symbiotic nitrogen fixation and phosphorus acquisition.plant nutrition in a world of declining renewable resources.Plant Physiol 127,390-397.
Vance CP,Uhde-Stone C,Allan DL(2003).Phosphorus acquisition and use:critical adaptations by plants for securing a nonrenewable resource.New Phytol 157,423-447.
Veneklaas EJ,Lambers H,Bragg J,Finnegan PM,Lovelock CE,Plaxton WC,Price CA,Scheible WR,Shane MW,White PJ,Raven JA(2012).Opportunities for improving phosphorus-use efficiency in crop plants.New Phytol 195,306-320.
Wang LS,Li Z,Qian WQ,Guo WL,Gao X,Huang LL,Wang H,Zhu HF,Wu JW,Wang DW,Liu D(2011).The Arabidopsis purple acid phosphatase AtPAP10 is predominantly associated with the root surface and plays an important role in plant tolerance to phosphate limitation.Plant Physiol 157,1283-1299.
Wang LS,Lu S,Zhang Y,Li Z,Du XQ,Liu D(2014).Comparative genetic analysis of Arabidopsis purple acid phosphatases AtPAP10,AtPAP12,and AtPAP26 provides new insights into their roles in plant adaptation to phosphate deprivation.J Integr Plant Biol 56,299-314.
Wasaki J,Yamamura T,Shinano T,Osaki M(2003).Secreted acid phosphatase is expressed in cluster roots of lupin in response to phosphorus deficiency.Plant Soil 248,129-136.
Zhang Q,Wang C,Tian J,Li K,Shou H(2011).Identification of rice purple acid phosphatases related to phosphate starvation signaling.Plant Biol 13,7-15.
Zhang RS,Guan XQ,Law YS,Sun F,Chen S,Wong KB,Lim BL(2016).AtPAP2 modulates the import of the small subunit of Rubisco into chloroplasts.Plant Signal Behav11,e1239687.
Zhang WY,Gruszewski HA,Chevone BI,Nessler CL(2008).An Arabidopsis purple acid phosphatase with phytase activity increases foliar ascorbate.Plant Physiol 146,431-440.
Zhang YJ,Sun F,Fettke J,Schottler MA,Ramsden L,Fernie AR,Lim BL(2014).Heterologous expression of AtPAP2 in transgenic potato influences carbon metabolism and tuber development.FEBS Lett 588,3726-3731.
Zhang YJ,Yu L,Yung KF,Leung DYC,Sun F,Lim BL(2012).Over-expression of At PAP2 in Camelina sativa leads to faster plant growth and higher seed yield.Biotechnol Biofuels 5,219.
Zhou J,Jiao FC,Wu ZC,Li YY,Wang XM,He XW,Zhong WQ,Wu P(2008).Os PHR2 is involved in phosphatestarvation signaling and excessive phosphate accumulation in shoots of plants.Plant Physiol 146,1673-1686.
Zhu HF,Qian WQ,Lu XZ,Li DP,Liu X,Liu KF,Wang DW(2005).Expression patterns of purple acid phosphatase genes in Arabidopsis organs and functional analysis of AtPAP23 predominantly transcribed in flower.Plant Mol Biol 59,581-594.
Zimmermann P,Regierer B,Kossmann J,Frossard E,Amrhein N,Bucher M(2004).Differential expression of three purple acid phosphatases from potato.Plant Biol 6,519-528.
卢坤,张凯,柴友荣,陆俊杏,唐章林,李加纳(2010).甘蓝和白菜紫色酸性磷酸酶17基因家族的克隆和比较分析.作物学报36,517-525.
周志高,汪金舫,周健民(2005).植物磷营养高效的分子生物学研究进展.植物学报22,82-91.
Cakmak I(2002).Plant nutrition research:priorities to meet human needs for food in sustainable ways.Plant Soil 247,3-24.
Del Vecchio HA,Ying S,Park J,Knowles VL,Kanno S,Tanoi K,She YM,Plaxton WC(2014).The cell walltargeted purple acid phosphatase AtPAP25 is critical for acclimation of Arabidopsis thaliana to nutritional phosphorus deprivation.Plant J 80,569-581.
Hammond JP,Broadley MR,White PJ(2004).Genetic responses to phosphorus deficiency.Ann Bot 94,323-332.
Hur YJ,Jin BR,Nam J,Chung YS,Lee JH,Choi HK,Yun DJ,Yi G,Kim YH,Kim DH(2010).Molecular characterization of Os PAP2:transgenic expression of a purple acid phosphatase up-regulated in phosphate-deprived rice suspension cells.Biotechnol Lett 32,163-170.
James J,David WL(1992).Dependence of photosynthesis of sunflower and maize leaves on phosphate supply,ribulose-1,5-bisphosphate carboxylase/oxygenase activity,and ribulose-1,5-bisphosphate pool size.Plant Physiol 98,801-807.
Jarenmark M,Haukka M,Demeshko S,Tuczek F,Zuppiroli L,Meyer F,Nordlander E(2011).Synthesis,characterization,and reactivity studies of heterodinuclear complexes modeling active sites in purple acid phospha-tases.Inorg Chem 50,3866-3887.
Kaida R,Hayashi T,Kaneko TS(2008).Purple acid phosphatase in the walls of tobacco cells.Phytochemistry 69,2546-2551.
Kaida R,Sage-Ono K,Kamada H,Okuyama H,Syono K,Kaneko TS(2003).Isolation and characterization of four cell wall purple acid phosphatase genes from tobacco cells.Biochim Biophys Acta-Gene Regul Mech 1625,134-140.
Kaida R,Satoh Y,Bulone V,Yamada Y,Kaku T,Hayashi T,Kaneko TS(2009).Activation ofβ-glucan synthases by wall-bound purple acid phosphatase in tobacco cells.Plant Physiol 150,1822-1830.
Kaida R,Serada S,Norioka N,Norioka S,Neumetzler L,Pauly M,Sampedro J,Zarra I,Hayashi T,Kaneko TS(2010).Potential role for purple acid phosphatase in the dephosphorylation of wall proteins in tobacco cells.Plant Physiol 153,603-610.
Klabunde T,Stahl B,Suerbaum H,Hahner S,Karas M,Hillenkamp F,Krebs B,Witzel H(1994).The amino acid sequence of the red kidney bean Fe(III)-Zn(II)purple acid phosphatase.Determination of the amino acid sequence by a combination of matrix-assisted laser desorption/ionization mass spectrometry and automated Edman sequencing.Eur J Biochem 226,369-375.
Klabunde T,Str?ter N,Krebs B,Witzel H(1995).Structural relationship between the mammalian Fe(III)-Fe(II)and the Fe(III)-Zn(II)plant purple acid phosphatases.FEBS Lett367,56-60.
Kong YB,Li XH,Ma J,Li WL,Yan GJ,Zhang CY(2014).Gm PAP4,a novel purple acid phosphatase gene isolated from soybean(Glycine max),enhanced extracellular phytate utilization in Arabidopsis thaliana.Plant Cell Rep 33,655-667.
Kuang RB,Chan KH,Yeung E,Lim BL(2009).Molecular and biochemical characterization of AtPAP15,a purple acid phosphatase with phytase activity,in Arabidopsis.Plant Physiol 151,199-209.
Kusudo T,Sakaki T,Inouye K(2003).Purification and characterization of purple acid phosphatase PAP1 from dry powder of sweet potato.Biosci Biotechnol Biochem 67,1609-1611.
Law YS,Zhang RS,Guan XQ,Cheng SF,Sun F,Duncan O,Murcha MW,Whelan J,Lim BL(2015).Phosphorylation and dephosphorylation of the presequence of precursor MULTIPLE ORGANELLAR RNA EDITING FACTOR3during import into mitochondria from Arabidopsis.Plant Physiol 169,1344-1355.
Li CC,Gui SH,Yang T,Walk T,Wang XR,Liao H(2012).Identification of soybean purple acid phosphatase genes and their expression responses to phosphorus availability and symbiosis.Ann Bot 109,275-285.
Li DP,Zhu HF,Liu KF,Liu X,Leggewie G,Udvardi M,Wang DW(2002).Purple acid phosphatases of Arabidopsis thaliana.Comparative analysis and differential regulation by phosphate deprivation.J Biol Chem 277,27772-27781.
Li WYF,Shao GH,Lam HM(2008).Ectopic expression of Gm PAP3 alleviates oxidative damage caused by salinity and osmotic stresses.New Phytol 178,80-91.
Liang C,Liu X,Sun YZ,Yiu SM,Lim BL(2014).Global small RNA analysis in fast-growing Arabidopsis thaliana with elevated concentrations of ATP and sugars.BMCGenomics 15,116.
Liang C,Zhang YJ,Cheng SF,Osorio S,Sun YZ,Fernie AR,Cheung CY,Lim BL(2015).Impacts of high ATPsupply from chloroplasts and mitochondria on the leaf metabolism of Arabidopsis thaliana.Front Plant Sci 6,922.
Liang CY,Tian J,Lam HM,Lim BL,Yan XL,Liao H(2010).Biochemical and molecular characterization of PvPAP3,a novel purple acid phosphatase isolated from common bean enhancing extracellular ATP utilization.Plant Physiol152,854-865.
Liao H,Wong FL,Phang TH,Cheung MY,Li WYF,Shao GH,Yan XL,Lam HM(2003).Gm PAP3,a novel purple acid phosphatase-like gene in soybean induced by NaCl stress but not phosphorus deficiency.Gene 318,103-111.
Nakazato H,Okamoto T,Nishikoori M,Washio K,Morita N,Haraguchi K,Thompson GA,Okuyama H(1998).The glycosylphosphatidylinositol-anchored phosphatase from Spirodela oligorrhiza is a purple acid phosphatase.Plant Physiol 118,1015-1020.
Olczak M,Morawiecka B,Watorek W(2003).Plant purple acid phosphatases-genes,structures and biological function.Acta Biochim Pol 50,1245-1256.
Ravichandran S,Stone SL,Bernhard B,Prithiviraj B(2013).Purple acid phosphatase 5 is required for maintaining basal resistance against Pseudomonas syringae in Arabidopsis.BMC Plant Biol 13,107.
Robinson WD,Carson I,Ying S,Ellis K,Plaxton WC(2012a).Eliminating the purple acid phosphatase AtPAP26 in Arabidopsis thaliana delays leaf senescence and impairs phosphorus remobilization.New Phytol 196,1024-1029.
Robinson WD,Park J,Tran HT,Del Vecchio HA,Ying S,Zins JL,Patel K,Mc Knight TD,Plaxton WC(2012b).The secreted purple acid phosphatase isozymes AtPAP12and AtPAP26 play a pivotal role in extracellular phosphate-scavenging by Arabidopsis thaliana.J Exp Bot 63,6531-6542.
Rubio V,Linhares F,Solano R,Martín AC,Iglesias J,Leyva A,Paz-Ares J(2001).A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae.Genes Dev 15,2122-2133.
Schenk G,Elliott TW,Leung E,Carrington LE,Mitic N,Gahan LR,Guddat LW(2008).Crystal structures of a purple acid phosphatase,representing different steps of this enzyme’s catalytic cycle.BMC Struct Biol 8,6.
Schenk G,Guddat LW,Ge Y,Carrington LE,Hume DA,Hamilton S,de Jersey J(2000a).Identification of mammalian-like purple acid phosphatases in a wide range of plants.Gene 250,117-125.
Schenk G,Korsinczky MLJ,Hume DA,Hamilton S,DeJersey J(2000b).Purple acid phosphatases from bacteria:similarities to mammalian and plant enzymes.Gene255,419-424.
Smith VH,Schindler DW(2009).Eutrophication science:where do we go from here?Trends Ecol Evol 24,201-207.
Strater N,Klabunde T,Tucker P,Witzel H,Krebs B(1995).Crystal structure of a purple acid phosphatase containing a dinuclear Fe(III)-Zn(II)active site.Science 268,1489-1492.
Sun F,Carrie C,Law S,Murcha MW,Zhang R,Law YS,Suen PK,Whelan J,Lim BL(2012b).At PAP2 is a tail-anchored protein in the outer membrane of chloroplasts and mitochondria.Plant Signal Behav 7,927-932.
Sun F,Liang C,Whelan J,Yang J,Zhang P,Lim BL(2013).Global transcriptome analysis of At PAP2-overexpressing Arabidopsis thaliana with elevated ATP.BMCGenomics 14,752.
Sun F,Suen PK,Zhang YJ,Liang C,Carrie C,Whelan J,Ward JL,Hawkins ND,Jiang LW,Lim BL(2012a).Adual-targeted purple acid phosphatase in Arabidopsis thaliana moderates carbon metabolism and its overexpression leads to faster plant growth and higher seed yield.New Phytol 194,206-219.
Sun YZ,Law YS,Cheng SF,Lim BL(2017).RNA editing of cytochrome c maturation transcripts is responsive to the energy status of leaf cells in Arabidopsis thaliana.Mitochondrion 35,23-34.
Tian J,Liao H(2015).The role of intracellular and secreted purple acid phosphatases in plant phosphorus scavenging and recycling.In:Plaxton WC,Lambers H,eds.Annual Plant Reviews Volume 48:Phosphorus Metabolism in Plants,Vol.48.West Sussex:John Wiley&Sons,Ltd.pp.265-287.
Tran HT,Hurley BA,Plaxton WC(2010a).Feeding hungry plants:the role of purple acid phosphatases in phosphate nutrition.Plant Sci 179,14-27.
Tran HT,Qian WQ,Hurley BA,She YM,Wang DW,Plaxton WC(2010b).Biochemical and molecular characterization of AtPAP12 and AtPAP26:the predominant purple acid phosphatase isozymes secreted by phosphatestarved Arabidopsis thaliana.Plant Cell Environ 33,1789-1803.
Vance CP(2001).Symbiotic nitrogen fixation and phosphorus acquisition.plant nutrition in a world of declining renewable resources.Plant Physiol 127,390-397.
Vance CP,Uhde-Stone C,Allan DL(2003).Phosphorus acquisition and use:critical adaptations by plants for securing a nonrenewable resource.New Phytol 157,423-447.
Veneklaas EJ,Lambers H,Bragg J,Finnegan PM,Lovelock CE,Plaxton WC,Price CA,Scheible WR,Shane MW,White PJ,Raven JA(2012).Opportunities for improving phosphorus-use efficiency in crop plants.New Phytol 195,306-320.
Wang LS,Li Z,Qian WQ,Guo WL,Gao X,Huang LL,Wang H,Zhu HF,Wu JW,Wang DW,Liu D(2011).The Arabidopsis purple acid phosphatase AtPAP10 is predominantly associated with the root surface and plays an important role in plant tolerance to phosphate limitation.Plant Physiol 157,1283-1299.
Wang LS,Lu S,Zhang Y,Li Z,Du XQ,Liu D(2014).Comparative genetic analysis of Arabidopsis purple acid phosphatases AtPAP10,AtPAP12,and AtPAP26 provides new insights into their roles in plant adaptation to phosphate deprivation.J Integr Plant Biol 56,299-314.
Wasaki J,Yamamura T,Shinano T,Osaki M(2003).Secreted acid phosphatase is expressed in cluster roots of lupin in response to phosphorus deficiency.Plant Soil 248,129-136.
Zhang Q,Wang C,Tian J,Li K,Shou H(2011).Identification of rice purple acid phosphatases related to phosphate starvation signaling.Plant Biol 13,7-15.
Zhang RS,Guan XQ,Law YS,Sun F,Chen S,Wong KB,Lim BL(2016).AtPAP2 modulates the import of the small subunit of Rubisco into chloroplasts.Plant Signal Behav11,e1239687.
Zhang WY,Gruszewski HA,Chevone BI,Nessler CL(2008).An Arabidopsis purple acid phosphatase with phytase activity increases foliar ascorbate.Plant Physiol 146,431-440.
Zhang YJ,Sun F,Fettke J,Schottler MA,Ramsden L,Fernie AR,Lim BL(2014).Heterologous expression of AtPAP2 in transgenic potato influences carbon metabolism and tuber development.FEBS Lett 588,3726-3731.
Zhang YJ,Yu L,Yung KF,Leung DYC,Sun F,Lim BL(2012).Over-expression of At PAP2 in Camelina sativa leads to faster plant growth and higher seed yield.Biotechnol Biofuels 5,219.
Zhou J,Jiao FC,Wu ZC,Li YY,Wang XM,He XW,Zhong WQ,Wu P(2008).Os PHR2 is involved in phosphatestarvation signaling and excessive phosphate accumulation in shoots of plants.Plant Physiol 146,1673-1686.
Zhu HF,Qian WQ,Lu XZ,Li DP,Liu X,Liu KF,Wang DW(2005).Expression patterns of purple acid phosphatase genes in Arabidopsis organs and functional analysis of AtPAP23 predominantly transcribed in flower.Plant Mol Biol 59,581-594.
Zimmermann P,Regierer B,Kossmann J,Frossard E,Amrhein N,Bucher M(2004).Differential expression of three purple acid phosphatases from potato.Plant Biol 6,519-528.