Loss-of-function mutation of rice SLAC7 decreases chloroplast stability and induces a photoprotection mechanism in rice
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摘要
Plants absorb sunlight to power the photochemical reactions of photosynthesis, which can potentially damage the photosynthetic machinery. However, the mechanism that protects chloroplasts from the damage remains unclear. In this work, we demonstrated that rice(Oryza sativa L.) SLAC7 is a generally expressed membrane protein. Lossof-function of SLAC7 caused continuous damage to the chloroplasts of mutant leaves under normal light conditions.Ion leakage indicators related to leaf damage such as H_2O_2 and abscisic acid levels were significantly higher in slac7-1 than in the wild type. Consistently, the photosynthesis ef ficiency and Fv/Fm ratio of slac7-1 were significantly decreased(similar to photoinhibition). In response to chloroplast damage, slac7-1 altered its leaf morphology(curled or fused leaf) by the synergy between plant hormones and transcriptional factors to decrease the absorption of light, suggesting that a photoprotection mechanism for chloroplast damage was activated in slac7-1. When grown in dark conditions, slac7-1 displayed a normal phenotype. SLAC7 under the control of the At SLAC1 promoter could partially complement the phenotypes of Arabidopsis slac1 mutants, indicating a partia conservation of SLAC protein functions. These results suggest that SLAC7 is essential for maintaining the chloroplast stability in rice.
Plants absorb sunlight to power the photochemical reactions of photosynthesis, which can potentially damage the photosynthetic machinery. However, the mechanism that protects chloroplasts from the damage remains unclear. In this work, we demonstrated that rice(Oryza sativa L.) SLAC7 is a generally expressed membrane protein. Lossof-function of SLAC7 caused continuous damage to the chloroplasts of mutant leaves under normal light conditions.Ion leakage indicators related to leaf damage such as H_2O_2 and abscisic acid levels were significantly higher in slac7-1 than in the wild type. Consistently, the photosynthesis ef ficiency and Fv/Fm ratio of slac7-1 were significantly decreased(similar to photoinhibition). In response to chloroplast damage, slac7-1 altered its leaf morphology(curled or fused leaf) by the synergy between plant hormones and transcriptional factors to decrease the absorption of light, suggesting that a photoprotection mechanism for chloroplast damage was activated in slac7-1. When grown in dark conditions, slac7-1 displayed a normal phenotype. SLAC7 under the control of the At SLAC1 promoter could partially complement the phenotypes of Arabidopsis slac1 mutants, indicating a partia conservation of SLAC protein functions. These results suggest that SLAC7 is essential for maintaining the chloroplast stability in rice.
Plants absorb sunlight to power the photochemical reactions of photosynthesis, which can potentially damage the photosynthetic machinery. However, the mechanism that protects chloroplasts from the damage remains unclear. In this work, we demonstrated that rice(Oryza sativa L.) SLAC7 is a generally expressed membrane protein. Lossof-function of SLAC7 caused continuous damage to the chloroplasts of mutant leaves under normal light conditions.Ion leakage indicators related to leaf damage such as H_2O_2 and abscisic acid levels were significantly higher in slac7-1 than in the wild type. Consistently, the photosynthesis ef ficiency and Fv/Fm ratio of slac7-1 were significantly decreased(similar to photoinhibition). In response to chloroplast damage, slac7-1 altered its leaf morphology(curled or fused leaf) by the synergy between plant hormones and transcriptional factors to decrease the absorption of light, suggesting that a photoprotection mechanism for chloroplast damage was activated in slac7-1. When grown in dark conditions, slac7-1 displayed a normal phenotype. SLAC7 under the control of the At SLAC1 promoter could partially complement the phenotypes of Arabidopsis slac1 mutants, indicating a partia conservation of SLAC protein functions. These results suggest that SLAC7 is essential for maintaining the chloroplast stability in rice.
引文
Asada K,Takahashi M(1987)Production and Scavenging of Active Oxygen in Photosynthesis.Photoinhibition.Elsevier,Amsterdam
Bailey-Serres J,Voesenek LA(2010)Life in the balance:A signaling network controlling survival of flooding.Curr Opin Plant Biol 13:489-494
Bearden AJ,Malkin R(1975)Primary photochemical reactions in chloroplast photosynthesis.Q Rev Biophys 7:131-177
Benjamini Y,Yekutieli D(2001)The control of the false discovery rate in multiple testing under dependency.Ann Stat 29:1165-1188
Cao WH,Liu J,He XJ,Mu RL,Zhou HL,Chen SY,Zhang JS(2007)Modulation of ethylene responses affects plant saltstress responses.Plant Physiol 143:707-719
Chang CCC,Ball L,Fryer MJ,Baker NR,Karpinski S,Mullineaux PM(2004)Induction of ASCORBATE PEROXIDASE 2 expression in wounded Arabidopsis leaves does not involve known woundsignalling pathways but is associated with changes in photosynthesis.Plant J 38:499-511
Chen T,Zhu X-G,Lin Y(2014)Major alterations in transcript profiles between C3-C4and C4photosynthesis of an amphibious species Eleocharis baldwinii.Plant Mol Biol 86:93-110
Dobrev PI,Kaminek M(2002)Fast and efficient separation of cytokinins from auxin and abscisic acid and their purification using mixed-mode solid-phase extraction.J Chromatogr A 950:21-29
Dreyer I,Gomez-Porras JL,Ria~no-Pach on DM,Hedrich R,Geiger D(2012)Molecular evolution of slow and quick anion channels(SLACs and QUACs/ALMTs).Front Plant Sci 3:263
Ehleringer JR(1988)Changes in leaf characteristics of species along elevational gradients in the Wasatch Front,Utah.Am J Bot 75:680-689
Gao JP,Chao DY,Lin HX(2007)Understanding abiotic stress tolerance mechanisms:Recent studies on stress response in rice.J Integr Plant Biol 49:742-750
Giorio P(2011)Black leaf-clips increased minimum fluorescence emission in clipped leaves exposed to high solar radiation during dark adaptation.Photosynthetica 49:371-379
Gong X,Su Q,Lin D,Jiang Q,Xu J,Zhang J,Teng S,Dong Y(2014)The rice Os V4 encoding a novel pentatricopeptide repeat protein is required for chloroplast development during the early leaf stage under cold stress.J Integr Plant Biol 56:400-410
Hong F,Breitling R,Mc Entee CW,Wittner BS,Nemhauser JL,Chory J(2006)Rank Prod:A bioconductor package for detecting differentially expressed genes in meta-analysis.Bioinformatics 22:2825-2827
Inskeep WP,Bloom PR(1985)Extinction coefficients of chlorophyll a and b in N,N-dimethylformamide and 80%acetone.Plant Physiol77:483-485
Krause G,Weis E(1991)Chlorophyll fluorescence and photosynthesis:The basics.Annu Rev Plant Biol 42:313-349
Kusumi K,Hirotsuka S,Kumamaru T,Iba K(2012)Increased leaf photosynthesis caused by elevated stomatal conductance in a rice mutant deficient in SLAC1,a guard cell anion channel protein.J Exp Bot 10:1093
Laanemets K,Wang YF,Lindgren O,Wu J,Nishimura N,Lee S,Caddell D,Merilo E,Brosche M,Kilk K(2013)Mutations in the SLAC1 anion channel slow stomatal opening and severely reduce Ktuptake channel activity via enhanced cytosolic[Ca2t]and increased Ca2tsensitivity of Ktuptake channels.New Phytol 197:88-98
Lam SK,Siu CL,Hillmer S,Jang S,An G,Robinson DG,Jiang L(2007)Rice SCAMP1 defines clathrin-coated,trans-Golgi-located tubularvesicular structures as an early endosome in tobacco BY-2 cells.Plant Cell 19:296-319
Lin Y,Zhang Q(2005)Optimising the tissue culture conditions for high efficiency transformation of indica rice.Plant Cell Rep 23:540-547
Livak KJ,Schmittgen TD(2001)Analysis of relative gene expression data using real-time quantitative PCR and the 2 DDCTmethod.Methods 25:402-408
Lu H,Rate DN,Song JT,Greenberg JT(2003)ACD6,a novel ankyrin protein,is a regulator and an effector of salicylic acid signaling in the Arabidopsis defense response.Plant Cell 15:2408-2420
Ludlow MM,Bj€orkman O(1984)Paraheliotropic leaf movement in Siratro as a protective mechanism against drought-induced damage to primary photosynthetic reactions:Damage by excessive light and heat.Planta 161:505-518
Mart?n AC,Del Pozo JC,Iglesias J,Rubio V,Solano R,De La Pe~na A,Leyva A,Paz-Ares J(2000)Influence of cytokinins on the expression of phosphate starvation responsive genes in Arabidopsis.Plant J 24:559-567
Mok DW,Mok MC(1994)Cytokinins:Chemistry,Activity,and Function.CRC Press,Boca Raton.pp.1-15
Mok DW,Mok MC(2001)Cytokinin metabolism and action.Annu Rev Plant Biol 52:89-118
Negi J,Matsuda O,Nagasawa T,Oba Y,Takahashi H,Kawai-Yamada M,Uchimiya H,Hashimoto M,Iba K(2008)CO2regulator SLAC1 and its homologues are essential for anion homeostasis in plant cells.Nature 452:483-486
Niyogi KK(1999)Photoprotection revisited:Genetic and molecular approaches.Annu Rev Plant Biol 50:333-359
Ossowski S,Schwab R,Weigel D(2008)Gene silencing in plants using artificial micro RNAs and other small RNAs.Plant J 53:674-690
Ouyang SQ,Liu YF,Liu P,Lei G,He SJ,Ma B,Zhang WK,Zhang JS,Chen SY(2010)Receptor-like kinase Os SIK1 improves drought and salt stress tolerance in rice(Oryza sativa)plants.Plant J 62:316-329
Powles SB(1984)Photoinhibition of photosynthesis induced by visible light.Annu Rev Plant Physiol 35:15-44
Price AH,Atherton NM,Hendry GA(1989)Plants under droughtstress generate activated oxygen.Free Radical Res 8:61-66
Rhodes D(1987)Metabolic responses to stress.Biochem Plant 12:201-241
Sakakibara H,Suzuki M,Takei K,Deji A,Taniguchi M,Sugiyama T(1998)A response-regulator homologue possibly involved in nitrogen signal transduction mediated by cytokinin in maize.Plant J 14:337-344
Smyth GK(2005)Limma:Linear models for microarray data.In:Gentleman R,Carey VJ,Huber W,Irizarry RA,Dudoit S,eds.Bioinformatics and computational biology solutions using R and Bioconductor.Springer,pp.397-420
Takahashi S,Badger MR(2011)Photoprotection in plants:A new light on photosystem II damage.Trends Plant Sci 16:53-60
Tsuda K,Ito Y,Sato Y,Kurata N(2011)Positive autoregulation of a KNOX gene is essential for shoot apical meristem maintenance in rice.Plant Cell 23:4368-4381
Vahisalu T,Kollist H,Wang YF,Nishimura N,Chan WY,Valerio G,Lamminm€aki A,Brosch e M,Moldau H,Desikan R(2008)SLAC1 is required for plant guard cell S-type anion channel function in stomatal signalling.Nature 452:487-491
Wang HS,Yu C,Tang XF,Wang LY,Dong XC,Meng QW(2010)Antisense-mediated depletion of tomato endoplasmic reticulum omega-3 fatty acid desaturase enhances thermal tolerance.J Integr Plant Biol 52:568-577
Wang Z,Kang S,Jensen CR,Liu F(2011)Alternate partial root-zone irrigation reduces bundle-sheath cell leakage to CO2and enhances photosynthetic capacity in maize leaves.J Exp Bot10:e1093
Warthmann N,Chen H,Ossowski S,Weigel D,Herve P(2008)Highly specific gene silencing by artificial mi RNAs in rice.PLo S ONE 3:e1829
Wu C,Li X,Yuan W,Chen G,Kilian A,Li J,Xu C,Zhou DX,Wang S,Zhang Q(2003)Development of enhancer trap lines for functional analysis of the rice genome.Plant J 35:418-427
Yang X,Wang X,Wei M(2010)Response of photosynthesis in the leaves of cucumber seedlings to light intensity and CO2concentration under nitrate stress.Turk J Bot 34:303-310
Zhang J,Li C,Wu C,Xiong L,Chen G,Zhang Q,Wang S(2006)RMD:Arice mutant database for functional analysis of the rice genome.Nucleic Acids Res 34:D745-D748
Zhang L,Guo Q,Chang Q,Zhu Z,Liu L,Chen Y(2015)Chloroplast ultrastructure,photosynthesis and accumulation of secondary metabolites in Glechoma longituba in response to irradiance.Photosynthetica 53:144-153
Zhao KF,Song J,Fan H,Zhou S,Zhao M(2010)Growth response to ionic and osmotic stress of Na Cl in salt-tolerant and saltsensitive maize.J Integr Plant Biol 52:468-475
Zheng Q,Wang XJ(2008)GOEAST:A web-based software toolkit for Gene Ontology enrichment analysis.Nucleic Acids Res 36:W358-W363
Bailey-Serres J,Voesenek LA(2010)Life in the balance:A signaling network controlling survival of flooding.Curr Opin Plant Biol 13:489-494
Bearden AJ,Malkin R(1975)Primary photochemical reactions in chloroplast photosynthesis.Q Rev Biophys 7:131-177
Benjamini Y,Yekutieli D(2001)The control of the false discovery rate in multiple testing under dependency.Ann Stat 29:1165-1188
Cao WH,Liu J,He XJ,Mu RL,Zhou HL,Chen SY,Zhang JS(2007)Modulation of ethylene responses affects plant saltstress responses.Plant Physiol 143:707-719
Chang CCC,Ball L,Fryer MJ,Baker NR,Karpinski S,Mullineaux PM(2004)Induction of ASCORBATE PEROXIDASE 2 expression in wounded Arabidopsis leaves does not involve known woundsignalling pathways but is associated with changes in photosynthesis.Plant J 38:499-511
Chen T,Zhu X-G,Lin Y(2014)Major alterations in transcript profiles between C3-C4and C4photosynthesis of an amphibious species Eleocharis baldwinii.Plant Mol Biol 86:93-110
Dobrev PI,Kaminek M(2002)Fast and efficient separation of cytokinins from auxin and abscisic acid and their purification using mixed-mode solid-phase extraction.J Chromatogr A 950:21-29
Dreyer I,Gomez-Porras JL,Ria~no-Pach on DM,Hedrich R,Geiger D(2012)Molecular evolution of slow and quick anion channels(SLACs and QUACs/ALMTs).Front Plant Sci 3:263
Ehleringer JR(1988)Changes in leaf characteristics of species along elevational gradients in the Wasatch Front,Utah.Am J Bot 75:680-689
Gao JP,Chao DY,Lin HX(2007)Understanding abiotic stress tolerance mechanisms:Recent studies on stress response in rice.J Integr Plant Biol 49:742-750
Giorio P(2011)Black leaf-clips increased minimum fluorescence emission in clipped leaves exposed to high solar radiation during dark adaptation.Photosynthetica 49:371-379
Gong X,Su Q,Lin D,Jiang Q,Xu J,Zhang J,Teng S,Dong Y(2014)The rice Os V4 encoding a novel pentatricopeptide repeat protein is required for chloroplast development during the early leaf stage under cold stress.J Integr Plant Biol 56:400-410
Hong F,Breitling R,Mc Entee CW,Wittner BS,Nemhauser JL,Chory J(2006)Rank Prod:A bioconductor package for detecting differentially expressed genes in meta-analysis.Bioinformatics 22:2825-2827
Inskeep WP,Bloom PR(1985)Extinction coefficients of chlorophyll a and b in N,N-dimethylformamide and 80%acetone.Plant Physiol77:483-485
Krause G,Weis E(1991)Chlorophyll fluorescence and photosynthesis:The basics.Annu Rev Plant Biol 42:313-349
Kusumi K,Hirotsuka S,Kumamaru T,Iba K(2012)Increased leaf photosynthesis caused by elevated stomatal conductance in a rice mutant deficient in SLAC1,a guard cell anion channel protein.J Exp Bot 10:1093
Laanemets K,Wang YF,Lindgren O,Wu J,Nishimura N,Lee S,Caddell D,Merilo E,Brosche M,Kilk K(2013)Mutations in the SLAC1 anion channel slow stomatal opening and severely reduce Ktuptake channel activity via enhanced cytosolic[Ca2t]and increased Ca2tsensitivity of Ktuptake channels.New Phytol 197:88-98
Lam SK,Siu CL,Hillmer S,Jang S,An G,Robinson DG,Jiang L(2007)Rice SCAMP1 defines clathrin-coated,trans-Golgi-located tubularvesicular structures as an early endosome in tobacco BY-2 cells.Plant Cell 19:296-319
Lin Y,Zhang Q(2005)Optimising the tissue culture conditions for high efficiency transformation of indica rice.Plant Cell Rep 23:540-547
Livak KJ,Schmittgen TD(2001)Analysis of relative gene expression data using real-time quantitative PCR and the 2 DDCTmethod.Methods 25:402-408
Lu H,Rate DN,Song JT,Greenberg JT(2003)ACD6,a novel ankyrin protein,is a regulator and an effector of salicylic acid signaling in the Arabidopsis defense response.Plant Cell 15:2408-2420
Ludlow MM,Bj€orkman O(1984)Paraheliotropic leaf movement in Siratro as a protective mechanism against drought-induced damage to primary photosynthetic reactions:Damage by excessive light and heat.Planta 161:505-518
Mart?n AC,Del Pozo JC,Iglesias J,Rubio V,Solano R,De La Pe~na A,Leyva A,Paz-Ares J(2000)Influence of cytokinins on the expression of phosphate starvation responsive genes in Arabidopsis.Plant J 24:559-567
Mok DW,Mok MC(1994)Cytokinins:Chemistry,Activity,and Function.CRC Press,Boca Raton.pp.1-15
Mok DW,Mok MC(2001)Cytokinin metabolism and action.Annu Rev Plant Biol 52:89-118
Negi J,Matsuda O,Nagasawa T,Oba Y,Takahashi H,Kawai-Yamada M,Uchimiya H,Hashimoto M,Iba K(2008)CO2regulator SLAC1 and its homologues are essential for anion homeostasis in plant cells.Nature 452:483-486
Niyogi KK(1999)Photoprotection revisited:Genetic and molecular approaches.Annu Rev Plant Biol 50:333-359
Ossowski S,Schwab R,Weigel D(2008)Gene silencing in plants using artificial micro RNAs and other small RNAs.Plant J 53:674-690
Ouyang SQ,Liu YF,Liu P,Lei G,He SJ,Ma B,Zhang WK,Zhang JS,Chen SY(2010)Receptor-like kinase Os SIK1 improves drought and salt stress tolerance in rice(Oryza sativa)plants.Plant J 62:316-329
Powles SB(1984)Photoinhibition of photosynthesis induced by visible light.Annu Rev Plant Physiol 35:15-44
Price AH,Atherton NM,Hendry GA(1989)Plants under droughtstress generate activated oxygen.Free Radical Res 8:61-66
Rhodes D(1987)Metabolic responses to stress.Biochem Plant 12:201-241
Sakakibara H,Suzuki M,Takei K,Deji A,Taniguchi M,Sugiyama T(1998)A response-regulator homologue possibly involved in nitrogen signal transduction mediated by cytokinin in maize.Plant J 14:337-344
Smyth GK(2005)Limma:Linear models for microarray data.In:Gentleman R,Carey VJ,Huber W,Irizarry RA,Dudoit S,eds.Bioinformatics and computational biology solutions using R and Bioconductor.Springer,pp.397-420
Takahashi S,Badger MR(2011)Photoprotection in plants:A new light on photosystem II damage.Trends Plant Sci 16:53-60
Tsuda K,Ito Y,Sato Y,Kurata N(2011)Positive autoregulation of a KNOX gene is essential for shoot apical meristem maintenance in rice.Plant Cell 23:4368-4381
Vahisalu T,Kollist H,Wang YF,Nishimura N,Chan WY,Valerio G,Lamminm€aki A,Brosch e M,Moldau H,Desikan R(2008)SLAC1 is required for plant guard cell S-type anion channel function in stomatal signalling.Nature 452:487-491
Wang HS,Yu C,Tang XF,Wang LY,Dong XC,Meng QW(2010)Antisense-mediated depletion of tomato endoplasmic reticulum omega-3 fatty acid desaturase enhances thermal tolerance.J Integr Plant Biol 52:568-577
Wang Z,Kang S,Jensen CR,Liu F(2011)Alternate partial root-zone irrigation reduces bundle-sheath cell leakage to CO2and enhances photosynthetic capacity in maize leaves.J Exp Bot10:e1093
Warthmann N,Chen H,Ossowski S,Weigel D,Herve P(2008)Highly specific gene silencing by artificial mi RNAs in rice.PLo S ONE 3:e1829
Wu C,Li X,Yuan W,Chen G,Kilian A,Li J,Xu C,Zhou DX,Wang S,Zhang Q(2003)Development of enhancer trap lines for functional analysis of the rice genome.Plant J 35:418-427
Yang X,Wang X,Wei M(2010)Response of photosynthesis in the leaves of cucumber seedlings to light intensity and CO2concentration under nitrate stress.Turk J Bot 34:303-310
Zhang J,Li C,Wu C,Xiong L,Chen G,Zhang Q,Wang S(2006)RMD:Arice mutant database for functional analysis of the rice genome.Nucleic Acids Res 34:D745-D748
Zhang L,Guo Q,Chang Q,Zhu Z,Liu L,Chen Y(2015)Chloroplast ultrastructure,photosynthesis and accumulation of secondary metabolites in Glechoma longituba in response to irradiance.Photosynthetica 53:144-153
Zhao KF,Song J,Fan H,Zhou S,Zhao M(2010)Growth response to ionic and osmotic stress of Na Cl in salt-tolerant and saltsensitive maize.J Integr Plant Biol 52:468-475
Zheng Q,Wang XJ(2008)GOEAST:A web-based software toolkit for Gene Ontology enrichment analysis.Nucleic Acids Res 36:W358-W363