异源过表达OsATG8b基因提高转基因拟南芥的氮/碳胁迫耐受性和产量
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摘要
氮素是参与植物生长发育的一种重要元素,对植物的产量和品质具有重要作用。自噬是真核生物中一种保守的细胞组分降解-循环再利用途径,在植物生长发育和籽粒形成期间的氮素再动员过程中发挥作用。我们鉴定到水稻(Oryza sativa)自噬核心基因OsATG8b,并获得2个独立的35S-OsATG8b转基因拟南芥(Arabidopsisthaliana)纯合株系。研究表明OsATG8b基因响应低氮胁迫处理,过表达OsATG8b基因促进转基因拟南芥的生长发育,使莲座叶增大,单株产量显著提高(15.16%)。进一步研究表明,过表达OsATG8b能够显著增强缺氮胁迫下转基因拟南芥叶片中的自噬活性,从而有效缓解氮胁迫和碳胁迫对转基因拟南芥造成的生长抑制。因此, OsATG8b是提高氮素利用效率和产量的候选基因。
Nitrogen is an essential element for plant growth and development and plays an important role in plant yield and quality. Autophagy is a conserved degradation-recycle pathway of cellular components in eukaryotes that plays an important role in nitrogen remobilization during plant growth and grain formation. We identified an autophagy core gene OsATG8b in rice and obtained 2 independent 35S-OsATG8b transgenic Arabidopsis homozygous lines. The expression of Os ATG8b responded to nitrogen starvation in rice. Overexpression of OsATG8b promoted the growth and development of transgenic Arabidopsis, with rosette leaves larger than wild-type leaves. In addition, the yield increased significantly, by 15.16%. In addition, overexpression of OsATG8b could significantly enhance autophagic activity in leaves of transgenic Arabidopsis under nitrogen deficiency and effectively alleviate the growth inhibition of transgenic Arabidopsis caused by nitrogen and carbon stress. OsATG8b may be a good candidate gene for increasing nitrogen use efficiency and yield.
Nitrogen is an essential element for plant growth and development and plays an important role in plant yield and quality. Autophagy is a conserved degradation-recycle pathway of cellular components in eukaryotes that plays an important role in nitrogen remobilization during plant growth and grain formation. We identified an autophagy core gene OsATG8b in rice and obtained 2 independent 35S-OsATG8b transgenic Arabidopsis homozygous lines. The expression of Os ATG8b responded to nitrogen starvation in rice. Overexpression of OsATG8b promoted the growth and development of transgenic Arabidopsis, with rosette leaves larger than wild-type leaves. In addition, the yield increased significantly, by 15.16%. In addition, overexpression of OsATG8b could significantly enhance autophagic activity in leaves of transgenic Arabidopsis under nitrogen deficiency and effectively alleviate the growth inhibition of transgenic Arabidopsis caused by nitrogen and carbon stress. OsATG8b may be a good candidate gene for increasing nitrogen use efficiency and yield.
引文
黄晓,李发强(2016).细胞自噬在植物细胞程序性死亡中的作用.植物学报51,859-862.
景红娟,周广舟,谭晓荣,平康康,任雪建(2012).活性氧对植物自噬调控的研究进展.植物学报47,534-542.
刘洋,张静,王秋玲,侯岁稳(2018).植物细胞自噬研究进展.植物学报53,5-16.
任晨霞,龚清秋(2014).细胞自噬在植物碳氮营养中作用的研究进展.中国细胞生物学学报36,407-414.
Arnon DI(1949).Copper enzymes in isolated chloroplasts.Polyphenoloxidase in Beta vulgaris.Plant Physiol 24,1-15.
Avila-Ospina L,Moison M,Yoshimoto K,MasclauxDaubresse C(2014).Autophagy,plant senescence,and nutrient recycling.J Exp Bot 65,3799-3811.
Biederbick A,Kern HF,Els?sser HP(1995).Monodansylcadaverine(MDC)is a specific in vivo marker for autophagic vacuoles.Eur J Cell Biol 66,3-14.
Bradford MM(1976).A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.Anal Biochem 72,248-254.
Breeze E,Harrison E,McHattie S,Hughes L,Hickman R,Hill C,Kiddle S,Kim YS,Penfold CA,Jenkins D,Zhang CJ,Morris K,Jenner C,Jackson S,Thomas B,Tabrett A,Legaie R,Moore JD,Wild DL,Ott S,Rand D,Beynon J,Denby K,Mead A,Buchanan-Wollaston V(2011).High-resolution temporal profiling of transcripts during Arabidopsis leaf senescence reveals a distinct chronology of processes and regulation.Plant Cell 23,873-894.
Chardon F,No?l V,Masclaux-Daubresse C(2012).Exploring NUE in crops and in Arabidopsis ideotypes to improve yield and seed quality.J Exp Bot 63,3401-3412.
Clough SJ,Bent AF(1998).Floral dip:a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.Plant J 16,735-743.
Contento AL,Xiong Y,Bassham DC(2005).Visualization of autophagy in Arabidopsis using the fluorescent dye monodansylcadaverine and a GFP-At ATG8e fusion protein.Plant J 42,598-608.
Feng YC,He D,Yao ZY,Klionsky DJ(2014).The machinery of macroautophagy.Cell Res 24,24-41.
Good AG,Shrawat AK,Muench DG(2004).Can less yield more?Is reducing nutrient input into the environment compatible with maintaining crop production?Trends Plant Sci 9,597-605.
Guiboileau A,Avila-Ospina L,Yoshimoto K,Soulay F,Azzopardi M,Marmagne A,Lothier J,MasclauxDaubresse C(2013).Physiological and metabolic consequences of autophagy deficiency for the management of nitrogen and protein resources in Arabidopsis leaves depending on nitrate availability.New Phytol 199,683-694.
Guiboileau A,Yoshimoto K,Soulay F,BatailléMP,Avice JC,Masclaux-Daubresse C(2012).Autophagy machinery controls nitrogen remobilization at the whole-plant level under both limiting and ample nitrate conditions in Arabidopsis.New Phytol 194,732-740.
Ishida H,Yoshimoto K,Izumi M,Reisen D,Yano Y,Makino A,Ohsumi Y,Hanson MR,Mae T(2008).Mobilization of rubisco and stroma-localized fluorescent proteins of chloroplasts to the vacuole by an ATGgene-dependent autophagic process.Plant Physiol 148,142-155.
Izumi M,Hidema J,Makino A,Ishida H(2013).Autophagy contributes to nighttime energy availability for growth in Arabidopsis.Plant Physiol 161,1682-1693.
Izumi M,Hidema J,Wada S,Kondo E,Kurusu T,Kuchitsu K,Makino A,Ishida H(2015).Establishment of monitoring methods for autophagy in rice reveals autophagic recycling of chloroplasts and root plastids during energy limitation.Plant Physiol 167,1307-1320.
Kichey T,Hirel B,Heumez E,Dubois F,Le Gouis J(2007).In winter wheat(Triticum aestivum L.),post-anthesis nitrogen uptake and remobilisation to the grain correlates with agronomic traits and nitrogen physiological markers.Field Crops Res 102,22-32.
Kraiser T,Gras DE,Gutiérrez AG,González B,Gutiérrez RA(2011).A holistic view of nitrogen acquisition in plants.J Exp Bot 62,1455-1466.
Krapp A(2015).Plant nitrogen assimilation and its regulation:a complex puzzle with missing pieces.Curr Opin Plant Biol 25,115-122.
Li FQ,Chung T,Pennington JG,Federico ML,Kaeppler HF,Kaeppler SM,Otegui MS,Vierstra RD(2015a).Autophagic recycling plays a central role in maize nitrogen remobilization.Plant Cell 27,1389-1408.
Li WW,Chen M,Wang EH,Hu LQ,Hawkesford MJ,Zhong L,Chen Z,Xu ZS,Li LC,Zhou YB,Guo CH,Ma YZ(2016).Genome-wide analysis of autophagy-associated genes in foxtail millet(Setaria italica L.)and characterization of the function of SiATG8a in conferring tolerance to nitrogen starvation in rice.BMC Genomics 17,797.
Li WW,Chen M,Zhong L,Liu JM,Xu ZS,Li LC,Zhou YB,Guo CH,Ma YZ(2015b).Overexpression of the autophagy-related gene SiATG8a from foxtail millet(Setaria italica L.)confers tolerance to both nitrogen starvation and drought stress in Arabidopsis.Biochem Biophys Res Commun 468,800-806.
Liu D,Gong QQ,Ma YY,Li PL,Li JP,Yang SH,Yuan LL,Yu YQ,Pan DD,Xu F,Wang NN(2010).Cpseca,a thylakoid protein translocase subunit,is essential for photosynthetic development in Arabidopsis.J Exp Bot 61,1655-1669.
Liu YM,Bassham DC(2012).Autophagy:pathways for self-eating in plant cells.Annu Rev Plant Biol 63,215-237.
Makino A,Osmond B(1991).Effects of nitrogen nutrition on nitrogen partitioning between chloroplasts and mitochondria in pea and wheat.Plant Physiol 96,355-362.
Masclaux-Daubresse C,Daniel-Vedele F,Dechorgnat J,Chardon F,Gaufichon L,Suzuki A(2010).Nitrogen uptake,assimilation and remobilization in plants:challenges for sustainable and productive agriculture.Ann Bot 105,1141-1157.
Masclaux-Daubresse C,Reisdorf-Cren M,Orsel M(2008).Leaf nitrogen remobilisation for plant development and grain filling.Plant Biol 10,23-36.
Meyer C,Stitt M(2001).Nitrate reduction and signaling.In:Lea PJ,Morot-Gaudry JF,eds.Plant Nitrogen.Berlin,Heidelberg:Springer.pp.37-59.
Moriyasu Y,Ohsumi Y(1996).Autophagy in tobacco suspension-cultured cells in response to sucrose starvation.Plant Physiol 111,1233-1241.
Ohsumi Y(2001).Molecular dissection of autophagy:two ubiquitin-like systems.Nat Rev Mol Cell Biol 2,211-216.
Otegui MS,Noh YS,Martínez DE,Vila Petroff MG,Staehelin LA,Amasino RM,Guiamet JJ(2005).Senescence-associated vacuoles with intense proteolytic activity develop in leaves of Arabidopsis and soybean.Plant J 41,831-844.
Patrick JW,Offler CE(2001).Compartmentation of transport and transfer events in developing seeds.J Exp Bot 52,551-564.
Rentsch D,Schmidt S,Tegeder M(2007).Transporters for uptake and allocation of organic nitrogen compounds in plants.FEBS Lett 581,2281-2289.
Roberts IN,Caputo C,Criado MV,Funk C(2012).Senescence-associated proteases in plants.Physiol Plant 145,130-139.
Slavikova S,Ufaz S,Avin-Wittenberg T,Levanony H,Galili G(2008).An autophagy-associated Atg8 protein is involved in the responses of Arabidopsis seedlings to hormonal controls and abiotic stresses.J Exp Bot 59,4029-4043.
Thompson AR,Doelling JH,Suttangkakul A,Vierstra RD(2005).Autophagic nutrient recycling in Arabidopsis directed by the ATG8 and ATG12 conjugation pathways.Plant Physiol 138,2097-2110.
Tsukada M,Ohsumi Y(1993).Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae.FEBS Lett 333,169-174.
Wada S,Hayashida Y,Izumi M,Kurusu T,Hanamata S,Kanno K,Kojima S,Yamaya T,Kuchitsu K,Makino A,Ishida H(2015).Autophagy supports biomass production and nitrogen use efficiency at the vegetative stage in rice.Plant Physiol 168,60-73.
Wada S,Ishida H,Izumi M,Yoshimoto K,Ohsumi Y,Mae T,Makino A(2009).Autophagy plays a role in chloroplast degradation during senescence in individually darkened leaves.Plant Physiol 149,885-893.
Walch-Liu P,Filleur S,Gan YB,Forde BG(2005).Signaling mechanisms integrating root and shoot responses to changes in the nitrogen supply.Photosynth Res 83,239-250.
Wang P,Sun X,Jia X,Wang N,Gong XQ,Ma FW(2016).Characterization of an autophagy-related gene Md ATG8i from apple.Front Plant Sci 7,720.
Wang Y,Yu BJ,Zhao JP,Guo JB,Li Y,Han SJ,Huang L,Du YM,Hong YG,Tang DZ,Liu YL(2013).Autophagy contributes to leaf starch degradation.Plant Cell 25,1383-1399.
Xia KF,Liu T,Ouyang J,Wang R,Fan T,Zhang MY(2011).Genome-wide identification,classification,and expression analysis of autophagy-associated gene homologues in rice(Oryza sativa L.).DNA Res 18,363-377.
Xia TM,Xiao D,Liu D,Chai WT,Gong QQ,Wang NN(2012).Heterologous expression of ATG8c from soybean confers tolerance to nitrogen deficiency and increases yield in Arabidopsis.PLoS One 7,e37217.
Yang XC,Bassham DC(2015).New insight into the mechanism and function of autophagy in plant cells.Int Rev Cell Mol Biol 320,1-40.
Yao ZY,Delorme-Axford E,Backues SK,Klionsky DJ(2015).Atg41/Icy2 regulates autophagosome formation.Autophagy 11,2288-2299.
Yoshimoto K(2012).Beginning to understand autophagy,an intracellular self-degradation system in plants.Plant Cell Physiol 53,1355-1365.
Yoshimoto K,Hanaoka H,Sato S,Kato T,Tabata S,Noda T,Ohsumi Y(2004).Processing of ATG8s,ubiquitin-like proteins,and their deconjugation by ATG4s are essential for plant autophagy.Plant Cell 16,2967-2983.
Yoshimoto K,Jikumaru Y,Kamiya Y,Kusano M,Consonni C,Panstruga R,Ohsumi Y,Shirasu K(2009).Autophagy negatively regulates cell death by controlling NPR1-dependent salicylic acid signaling during senescence and the innate immune response in Arabidopsis.Plant Cell 21,2914-2927.
景红娟,周广舟,谭晓荣,平康康,任雪建(2012).活性氧对植物自噬调控的研究进展.植物学报47,534-542.
刘洋,张静,王秋玲,侯岁稳(2018).植物细胞自噬研究进展.植物学报53,5-16.
任晨霞,龚清秋(2014).细胞自噬在植物碳氮营养中作用的研究进展.中国细胞生物学学报36,407-414.
Arnon DI(1949).Copper enzymes in isolated chloroplasts.Polyphenoloxidase in Beta vulgaris.Plant Physiol 24,1-15.
Avila-Ospina L,Moison M,Yoshimoto K,MasclauxDaubresse C(2014).Autophagy,plant senescence,and nutrient recycling.J Exp Bot 65,3799-3811.
Biederbick A,Kern HF,Els?sser HP(1995).Monodansylcadaverine(MDC)is a specific in vivo marker for autophagic vacuoles.Eur J Cell Biol 66,3-14.
Bradford MM(1976).A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.Anal Biochem 72,248-254.
Breeze E,Harrison E,McHattie S,Hughes L,Hickman R,Hill C,Kiddle S,Kim YS,Penfold CA,Jenkins D,Zhang CJ,Morris K,Jenner C,Jackson S,Thomas B,Tabrett A,Legaie R,Moore JD,Wild DL,Ott S,Rand D,Beynon J,Denby K,Mead A,Buchanan-Wollaston V(2011).High-resolution temporal profiling of transcripts during Arabidopsis leaf senescence reveals a distinct chronology of processes and regulation.Plant Cell 23,873-894.
Chardon F,No?l V,Masclaux-Daubresse C(2012).Exploring NUE in crops and in Arabidopsis ideotypes to improve yield and seed quality.J Exp Bot 63,3401-3412.
Clough SJ,Bent AF(1998).Floral dip:a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.Plant J 16,735-743.
Contento AL,Xiong Y,Bassham DC(2005).Visualization of autophagy in Arabidopsis using the fluorescent dye monodansylcadaverine and a GFP-At ATG8e fusion protein.Plant J 42,598-608.
Feng YC,He D,Yao ZY,Klionsky DJ(2014).The machinery of macroautophagy.Cell Res 24,24-41.
Good AG,Shrawat AK,Muench DG(2004).Can less yield more?Is reducing nutrient input into the environment compatible with maintaining crop production?Trends Plant Sci 9,597-605.
Guiboileau A,Avila-Ospina L,Yoshimoto K,Soulay F,Azzopardi M,Marmagne A,Lothier J,MasclauxDaubresse C(2013).Physiological and metabolic consequences of autophagy deficiency for the management of nitrogen and protein resources in Arabidopsis leaves depending on nitrate availability.New Phytol 199,683-694.
Guiboileau A,Yoshimoto K,Soulay F,BatailléMP,Avice JC,Masclaux-Daubresse C(2012).Autophagy machinery controls nitrogen remobilization at the whole-plant level under both limiting and ample nitrate conditions in Arabidopsis.New Phytol 194,732-740.
Ishida H,Yoshimoto K,Izumi M,Reisen D,Yano Y,Makino A,Ohsumi Y,Hanson MR,Mae T(2008).Mobilization of rubisco and stroma-localized fluorescent proteins of chloroplasts to the vacuole by an ATGgene-dependent autophagic process.Plant Physiol 148,142-155.
Izumi M,Hidema J,Makino A,Ishida H(2013).Autophagy contributes to nighttime energy availability for growth in Arabidopsis.Plant Physiol 161,1682-1693.
Izumi M,Hidema J,Wada S,Kondo E,Kurusu T,Kuchitsu K,Makino A,Ishida H(2015).Establishment of monitoring methods for autophagy in rice reveals autophagic recycling of chloroplasts and root plastids during energy limitation.Plant Physiol 167,1307-1320.
Kichey T,Hirel B,Heumez E,Dubois F,Le Gouis J(2007).In winter wheat(Triticum aestivum L.),post-anthesis nitrogen uptake and remobilisation to the grain correlates with agronomic traits and nitrogen physiological markers.Field Crops Res 102,22-32.
Kraiser T,Gras DE,Gutiérrez AG,González B,Gutiérrez RA(2011).A holistic view of nitrogen acquisition in plants.J Exp Bot 62,1455-1466.
Krapp A(2015).Plant nitrogen assimilation and its regulation:a complex puzzle with missing pieces.Curr Opin Plant Biol 25,115-122.
Li FQ,Chung T,Pennington JG,Federico ML,Kaeppler HF,Kaeppler SM,Otegui MS,Vierstra RD(2015a).Autophagic recycling plays a central role in maize nitrogen remobilization.Plant Cell 27,1389-1408.
Li WW,Chen M,Wang EH,Hu LQ,Hawkesford MJ,Zhong L,Chen Z,Xu ZS,Li LC,Zhou YB,Guo CH,Ma YZ(2016).Genome-wide analysis of autophagy-associated genes in foxtail millet(Setaria italica L.)and characterization of the function of SiATG8a in conferring tolerance to nitrogen starvation in rice.BMC Genomics 17,797.
Li WW,Chen M,Zhong L,Liu JM,Xu ZS,Li LC,Zhou YB,Guo CH,Ma YZ(2015b).Overexpression of the autophagy-related gene SiATG8a from foxtail millet(Setaria italica L.)confers tolerance to both nitrogen starvation and drought stress in Arabidopsis.Biochem Biophys Res Commun 468,800-806.
Liu D,Gong QQ,Ma YY,Li PL,Li JP,Yang SH,Yuan LL,Yu YQ,Pan DD,Xu F,Wang NN(2010).Cpseca,a thylakoid protein translocase subunit,is essential for photosynthetic development in Arabidopsis.J Exp Bot 61,1655-1669.
Liu YM,Bassham DC(2012).Autophagy:pathways for self-eating in plant cells.Annu Rev Plant Biol 63,215-237.
Makino A,Osmond B(1991).Effects of nitrogen nutrition on nitrogen partitioning between chloroplasts and mitochondria in pea and wheat.Plant Physiol 96,355-362.
Masclaux-Daubresse C,Daniel-Vedele F,Dechorgnat J,Chardon F,Gaufichon L,Suzuki A(2010).Nitrogen uptake,assimilation and remobilization in plants:challenges for sustainable and productive agriculture.Ann Bot 105,1141-1157.
Masclaux-Daubresse C,Reisdorf-Cren M,Orsel M(2008).Leaf nitrogen remobilisation for plant development and grain filling.Plant Biol 10,23-36.
Meyer C,Stitt M(2001).Nitrate reduction and signaling.In:Lea PJ,Morot-Gaudry JF,eds.Plant Nitrogen.Berlin,Heidelberg:Springer.pp.37-59.
Moriyasu Y,Ohsumi Y(1996).Autophagy in tobacco suspension-cultured cells in response to sucrose starvation.Plant Physiol 111,1233-1241.
Ohsumi Y(2001).Molecular dissection of autophagy:two ubiquitin-like systems.Nat Rev Mol Cell Biol 2,211-216.
Otegui MS,Noh YS,Martínez DE,Vila Petroff MG,Staehelin LA,Amasino RM,Guiamet JJ(2005).Senescence-associated vacuoles with intense proteolytic activity develop in leaves of Arabidopsis and soybean.Plant J 41,831-844.
Patrick JW,Offler CE(2001).Compartmentation of transport and transfer events in developing seeds.J Exp Bot 52,551-564.
Rentsch D,Schmidt S,Tegeder M(2007).Transporters for uptake and allocation of organic nitrogen compounds in plants.FEBS Lett 581,2281-2289.
Roberts IN,Caputo C,Criado MV,Funk C(2012).Senescence-associated proteases in plants.Physiol Plant 145,130-139.
Slavikova S,Ufaz S,Avin-Wittenberg T,Levanony H,Galili G(2008).An autophagy-associated Atg8 protein is involved in the responses of Arabidopsis seedlings to hormonal controls and abiotic stresses.J Exp Bot 59,4029-4043.
Thompson AR,Doelling JH,Suttangkakul A,Vierstra RD(2005).Autophagic nutrient recycling in Arabidopsis directed by the ATG8 and ATG12 conjugation pathways.Plant Physiol 138,2097-2110.
Tsukada M,Ohsumi Y(1993).Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae.FEBS Lett 333,169-174.
Wada S,Hayashida Y,Izumi M,Kurusu T,Hanamata S,Kanno K,Kojima S,Yamaya T,Kuchitsu K,Makino A,Ishida H(2015).Autophagy supports biomass production and nitrogen use efficiency at the vegetative stage in rice.Plant Physiol 168,60-73.
Wada S,Ishida H,Izumi M,Yoshimoto K,Ohsumi Y,Mae T,Makino A(2009).Autophagy plays a role in chloroplast degradation during senescence in individually darkened leaves.Plant Physiol 149,885-893.
Walch-Liu P,Filleur S,Gan YB,Forde BG(2005).Signaling mechanisms integrating root and shoot responses to changes in the nitrogen supply.Photosynth Res 83,239-250.
Wang P,Sun X,Jia X,Wang N,Gong XQ,Ma FW(2016).Characterization of an autophagy-related gene Md ATG8i from apple.Front Plant Sci 7,720.
Wang Y,Yu BJ,Zhao JP,Guo JB,Li Y,Han SJ,Huang L,Du YM,Hong YG,Tang DZ,Liu YL(2013).Autophagy contributes to leaf starch degradation.Plant Cell 25,1383-1399.
Xia KF,Liu T,Ouyang J,Wang R,Fan T,Zhang MY(2011).Genome-wide identification,classification,and expression analysis of autophagy-associated gene homologues in rice(Oryza sativa L.).DNA Res 18,363-377.
Xia TM,Xiao D,Liu D,Chai WT,Gong QQ,Wang NN(2012).Heterologous expression of ATG8c from soybean confers tolerance to nitrogen deficiency and increases yield in Arabidopsis.PLoS One 7,e37217.
Yang XC,Bassham DC(2015).New insight into the mechanism and function of autophagy in plant cells.Int Rev Cell Mol Biol 320,1-40.
Yao ZY,Delorme-Axford E,Backues SK,Klionsky DJ(2015).Atg41/Icy2 regulates autophagosome formation.Autophagy 11,2288-2299.
Yoshimoto K(2012).Beginning to understand autophagy,an intracellular self-degradation system in plants.Plant Cell Physiol 53,1355-1365.
Yoshimoto K,Hanaoka H,Sato S,Kato T,Tabata S,Noda T,Ohsumi Y(2004).Processing of ATG8s,ubiquitin-like proteins,and their deconjugation by ATG4s are essential for plant autophagy.Plant Cell 16,2967-2983.
Yoshimoto K,Jikumaru Y,Kamiya Y,Kusano M,Consonni C,Panstruga R,Ohsumi Y,Shirasu K(2009).Autophagy negatively regulates cell death by controlling NPR1-dependent salicylic acid signaling during senescence and the innate immune response in Arabidopsis.Plant Cell 21,2914-2927.