拟南芥聚ADP-核酸葡聚糖水解酶基因PARG1在抗病和抗逆反应中的作用研究
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摘要
聚ADP-核酸化是一类在哺乳动物系统中起重要作用的转录后蛋白修饰方式。最近研究表明,聚ADP-核酸化也参与了植物的生长发育调节和逆境反应。本文利用T-DNA插入突变体和过量表达转基因株系研究了拟南芥聚ADP-核酸葡聚糖水解酶1[poly(ADP-ribose)glycohydrolase 1, PARG1]基因在灰霉病(Botrytis cinerea, B. cinerea)抗性和非生物逆境反应中的作用。
RT-PCR分析结果表明,B. cinerea侵染拟南芥,植株叶片中PARG1转录水平逐渐增强；光照诱导拟南芥植株叶片中PARG1转录水平增强；黑暗条件下,以水杨酸(salicylic acid, SA)喷雾处理拟南芥植株,SA诱导拟南芥植株PARG1转录水平增强,但在处理SA时遇光照,PARG1基因下调表达。茉莉酸(jasmonic acid, JA)、乙烯前体1-氨基环丙烷-1-羧酸(1-aminocyclopropane-1-carboxylic acid, ACC)不诱导PARG1基因的表达。35S-GFP::PARG1结果显示,PARG1定位于细胞核和细胞质中。构建了PPARG1::GUS转基因株系,染色结果显示,PARG1在拟南芥植株的根尖、叶、花药内表达。
为了研究PARG1在抗病反应中的功能,筛选获得一个基于Ws-0生态型背景的T-DNA插入突变体parg1-3和一个基于Col-0生态型背景的T-DNA插入突变体parg1-4;构建了由CaMV 35S启动子驱动的基于parg1-3突变体背景的转PARG1基因过量表达系,PARG1-OE1/parg1-3和PARG1-OE2/parg1-3,与基于野生型Col-0背景的转PARG1基因过量表达系PARG1-OE1/Col-0和PARG1-OE2/Col-0。接着比较分析了上述突变体和过量表达转基因株系接种B. cinerea和番茄细菌性斑点病菌(Pseudomonas syringae pv. tomato DC3000, Pst DC3000)的病害表型。
喷雾接种B. cinerea或注射接种Pst DC3000后,parg1突变体的病害发病水平轻于野生型的病害发病水平,野生型的病害发病水平则轻于PARG1-OE株系的病害发病水平。接种病原菌后做菌量测试,parg1突变体叶片中B. cinerea生长量和Pst DC3000菌量均低于野生型中相应病菌菌量,野生型叶片中B. cinerea生长量和Pst DC3000菌量均低于PARG1-OE株系叶片的相应病菌菌量。B. cinerea侵染后,各株系病程相关蛋白基因(Pathogenesis-related protein gene,PR.)基因表达水平均无显著差异,说明PARG1调控拟南芥对B.cinerea抗病性不是通过调控PRs基因表达实现的。
考虑到活性氧和细胞死亡在B.cinerea侵染植物过程中的作用,以B.cinerea接种拟南芥,分析野生型、pargl和PARG1-OE株系的活性氧产生和细胞死亡状况。发现pargl突变体叶片中积累的活性氧含量比野生型叶片积累的活性氧含量少,而野生型叶片中活性氧的积累比PARG1-OE株系叶片中积累得少；同时发现在B.cinerea发病过程中,parg1植株叶片细胞的死亡数量比野生型叶片细胞的死亡数量少。为了进一步研究PARG1基因在细胞死亡中的功能,分别对拟南芥各株系接种Pst DC3000(avrRPM1)和高浓度Pst DC3000,PARG1-OE株系叶片细胞均比野生型叶片细胞易于死亡,而野生型叶片细胞均比parg1突变体叶片细胞易于死亡,说明PARG1参与过敏性细胞死亡的调控。考虑到聚ADP-核酸[poly(ADP-ribose),PAR]作为死亡信号的作用,应用PAR处理野生型、parg1突变体和PARG1-OE株系,发现PAR能诱导parg1突变体细胞凋亡,但并不引发细胞坏死,而caspase-3抑制剂Ac-DEVD-CHO能部分抑制PAR引发的细胞凋亡,表明受PARG1调控的胞内PAR能诱导细胞凋亡,其凋亡途径部分依赖caspase凋亡途径。
本文还比较分析了parg1-3突变体和转基因过量表达株系对干旱等非生物逆境的表型差异。基因表达结果表明,干旱和氧化胁迫处理,野生型拟南芥中的PARG1基因上调表达。在含甘露醇和甲基紫腈(methyl Viologen,MV)的培养基中进行种子萌发实验,模拟干旱和氧化胁迫逆境,发现parg1-3种子的发芽率比野生型种子发芽率降低,但以脱落酸(absisic acid,ABA)处理进行萌发实验,两者种子表现出相似的发芽率。在干旱、渗透和氧化胁迫下,parg1-3植株比野生型植株表现出较弱的忍耐力。在干旱逆境下,野生型植株叶片的气孔完全闭合,而parg1-3植株叶片的气孔不能完全闭合；但在ABA处理下,parg1-3植株叶片与野生型植株叶片的气孔闭合状况相似。此外,在干旱逆境中,parg1-3植株与野生型植株的干旱逆境／ABA反应基因表达水平相似。而在氧化胁迫下,parg1-3植株中的氧化胁迫相关基因,如交替氧化酶1(alternative oxidase 1,Aox1)和抗坏血酸过氧化物酶(ascorbate peroxidase 2,Apx2)下调表达。不论是干旱、渗透、氧化胁迫处理,还是ABA处理,PARG1的转基因过量表达株系均未表现出与野生型植株的差异。这些结果表明,PARG1基因在拟南芥对多种类型的逆境反应中起重要作用。
上述结果表明,PARG1基因可能通过调节细胞内的PAR含量,维持细胞内NAD+和ATP含量,在植物抗病和抗逆反应中起重要作用。研究结果对全面认识和理解拟南芥在抗病、逆境反应中的分子机制以及高等植物中聚ADP-核酸化的作用有积极的意义。
Poly(ADP-ribosyl)ation is a post-translational protein modification that plays important roles in many cellular processes in mammal systems. Emerging evidence indicates that poly(ADP-ribosyl)ation is also involved in regulation of growth/development, stress and defense response in plants. In this study, I studied the possible function of Arabidopsis poly(ADP-ribose) glycohydrolase 1 (PARG1) in disease resistance and abiotic stress responses using T-DNA insertional mutant and overexpression transgenic lines.
Bioinformatics analysis reveals that there are two genes encoding for poly(ADP-ribose) glycohydrolases. RT-PCR analysis showed that expression of PARG1 was up-regulated in Arabidopsis plants after inoculation with Botrytis cinerea(B. cinerea), a necrotrophic fungal pathogen. Similarly, expression of PARG1 was also significantly induced in Arabidopsis plants after treatment with salicylic acid (SA) or light. By contrast, the expression of PARG1 was reduced when Arabidopsis plants was treated with SA under the light. Expression of PARG1 in Arabidopsis was not be induced after treatment with jasmonic acid (JA) and 1-aminocyclopropane-l-carboxylic acid (ACC). PPARG1::GUS transgenic lines was generated and GUS staning showed that the PARG1 gene was expressed in root tips, leaves and anthers. Subcellular localization analysis using 35S-GFP::PARG1 showed that the PARG1 protein was localized in the nucleus and cytoplasm of Arabidopsis cells.
To study the function of PARG1 in disease resistance and abiotic stress responses, two T-DNA insertion line, parg1-3 in Ws-0 background and parg1-4 in Col-0 background were identified from genotyping screening. Meanwhile, transgenic lines overexpressing the PARG1 gene, driven by CaMV 35S promoter, in pargl-3 mutant and wild type Col-0 background were also generated. Homozygous lines with single copy of the PARG1 transgene were obtained through antibiotic resistance segregation screenings. Two independent transgenic lines overexpressing PARG1 gene in parg1-3 mutant background (PARG1-OE1/parg1-3 and PARG1-OE2/parg1-3) or wild type Col-0 background (PARG1-OE1/Col-0 and PARG1-OE2/Col-0) were selected for further studies. Disease phenotypes of the wild-type, pargl and PARG1-OE plants were compared after inoculation with B. cinerea or Pseudomonas syringae pv. tomato DC3000(Pst DC3000). As compared with the wild-type plants, the pargl plants showed increased resistance to B. cinerea and Pst DC3000. However, the transgenic PARG1-OE plants showed significant increased susceptibility to the above-mentioned pathogens. Furthermore, growth of B. cinerea and Pst DC3000 in leaves of the pargl plants was much less than in the wild-type plants; whereas growth of B. cinerea and Pst DC3000 in leaves of the PARG1-OE plants was significantly increased. After inoculation with B. cinerea, expression of Pathogenesis-related protein gene(PR) was similar in the wild-type, pargl and PARG1-OE plants. These results indicate that PARG1-mediated defense response against B. cinerea may be independent on PR genes. These data suggest that PARG1 plays an important role in Arabidopsis defense responses against both necrotrophic and biotrophic pathogens.
To further study the function of PARG1 in disease resistance response, we examined accumulation of reactive oxygen species and levels of apoptosis in Arabidopsis after inoculation with B. cinerea. It was observed that, after B. cinerea infection, PARG1-OE plants accumulated much more reactive oxygen species in leaves but the pargl plants accumulated less reactive oxygen species in leaves, when comopared with those in the wild-type plants. As compared with the wild-type plants, the pargl plants showed reduced level of apoptosis after B. cinerea infection, whereas the PARG1-OE plants showed accelerated cell death after inoculation with B. cinerea, Pst DC3000 (avrRPM1) or Pst DC3000. these results suggest that PARG1 may be also involved in regulation of cell death. Poly(ADP-ribose)(PAR) induces apoptosis in pargl plants, but did not induce cell necrosis. Ac-DEVD-CHO, a caspase3 inhibitor, inhibited partially PAR- induced apoptosis. These results demonstrate that PAR, which regulated by PARGl, can induce apoptosis, and this process is partially dependent on caspase-apoptosis signaling pathways.
I also examined the possible function of PARG1 in Arabidopsis abiotic stress tolerance using genetic mutant parg1-3 and transgenic PARG1-overexpressing plants. Expression of PARG1 in wild type plants was upregulated in response to drought and oxidative stress treatments. Germination rates of the parg1-3 seeds were reduced under mannitol or methyl viologen (MV) treatment as compared with the wild type seeds, but the parg1-3 seeds showed similar germination rate to the wild type seeds under ABA treatment. The parg1-3 plants showed reduced tolerance to drought, osmotic and oxidative stresses, with increased levels of cell damage under osmotic and oxidative stress and reduced survival rate under water-withholding drought stress, as compared with the wild type plants. Stomatal apertures of parg1-3 plants failed to close under water-withholding drought stress, but showed similar closure patterns to the wild type plants after ABA treatment. As compared with those in wild type plants, drought stress/ABA-responsive genes in parg1-3 plants showed comparable expression levels under drought stress condition, whereas expression level of some of oxidative stress-related genes in parg1-3 plants was reduced after MV treatment. Overexpression of PARG1 in parg1-3 mutant and wild type Col-0 background did not cause any phenotypical changes in response to drought, osmotic and oxidative stresses and ABA treatment. These results suggest that PARG1 plays important roles in abiotic stress tolerance.
Taken together, data presented in this thesis suggest that PARG1 plays important roles in disease resistance and abiotic stress responses.
RT-PCR分析结果表明,B. cinerea侵染拟南芥,植株叶片中PARG1转录水平逐渐增强；光照诱导拟南芥植株叶片中PARG1转录水平增强；黑暗条件下,以水杨酸(salicylic acid, SA)喷雾处理拟南芥植株,SA诱导拟南芥植株PARG1转录水平增强,但在处理SA时遇光照,PARG1基因下调表达。茉莉酸(jasmonic acid, JA)、乙烯前体1-氨基环丙烷-1-羧酸(1-aminocyclopropane-1-carboxylic acid, ACC)不诱导PARG1基因的表达。35S-GFP::PARG1结果显示,PARG1定位于细胞核和细胞质中。构建了PPARG1::GUS转基因株系,染色结果显示,PARG1在拟南芥植株的根尖、叶、花药内表达。
为了研究PARG1在抗病反应中的功能,筛选获得一个基于Ws-0生态型背景的T-DNA插入突变体parg1-3和一个基于Col-0生态型背景的T-DNA插入突变体parg1-4;构建了由CaMV 35S启动子驱动的基于parg1-3突变体背景的转PARG1基因过量表达系,PARG1-OE1/parg1-3和PARG1-OE2/parg1-3,与基于野生型Col-0背景的转PARG1基因过量表达系PARG1-OE1/Col-0和PARG1-OE2/Col-0。接着比较分析了上述突变体和过量表达转基因株系接种B. cinerea和番茄细菌性斑点病菌(Pseudomonas syringae pv. tomato DC3000, Pst DC3000)的病害表型。
喷雾接种B. cinerea或注射接种Pst DC3000后,parg1突变体的病害发病水平轻于野生型的病害发病水平,野生型的病害发病水平则轻于PARG1-OE株系的病害发病水平。接种病原菌后做菌量测试,parg1突变体叶片中B. cinerea生长量和Pst DC3000菌量均低于野生型中相应病菌菌量,野生型叶片中B. cinerea生长量和Pst DC3000菌量均低于PARG1-OE株系叶片的相应病菌菌量。B. cinerea侵染后,各株系病程相关蛋白基因(Pathogenesis-related protein gene,PR.)基因表达水平均无显著差异,说明PARG1调控拟南芥对B.cinerea抗病性不是通过调控PRs基因表达实现的。
考虑到活性氧和细胞死亡在B.cinerea侵染植物过程中的作用,以B.cinerea接种拟南芥,分析野生型、pargl和PARG1-OE株系的活性氧产生和细胞死亡状况。发现pargl突变体叶片中积累的活性氧含量比野生型叶片积累的活性氧含量少,而野生型叶片中活性氧的积累比PARG1-OE株系叶片中积累得少；同时发现在B.cinerea发病过程中,parg1植株叶片细胞的死亡数量比野生型叶片细胞的死亡数量少。为了进一步研究PARG1基因在细胞死亡中的功能,分别对拟南芥各株系接种Pst DC3000(avrRPM1)和高浓度Pst DC3000,PARG1-OE株系叶片细胞均比野生型叶片细胞易于死亡,而野生型叶片细胞均比parg1突变体叶片细胞易于死亡,说明PARG1参与过敏性细胞死亡的调控。考虑到聚ADP-核酸[poly(ADP-ribose),PAR]作为死亡信号的作用,应用PAR处理野生型、parg1突变体和PARG1-OE株系,发现PAR能诱导parg1突变体细胞凋亡,但并不引发细胞坏死,而caspase-3抑制剂Ac-DEVD-CHO能部分抑制PAR引发的细胞凋亡,表明受PARG1调控的胞内PAR能诱导细胞凋亡,其凋亡途径部分依赖caspase凋亡途径。
本文还比较分析了parg1-3突变体和转基因过量表达株系对干旱等非生物逆境的表型差异。基因表达结果表明,干旱和氧化胁迫处理,野生型拟南芥中的PARG1基因上调表达。在含甘露醇和甲基紫腈(methyl Viologen,MV)的培养基中进行种子萌发实验,模拟干旱和氧化胁迫逆境,发现parg1-3种子的发芽率比野生型种子发芽率降低,但以脱落酸(absisic acid,ABA)处理进行萌发实验,两者种子表现出相似的发芽率。在干旱、渗透和氧化胁迫下,parg1-3植株比野生型植株表现出较弱的忍耐力。在干旱逆境下,野生型植株叶片的气孔完全闭合,而parg1-3植株叶片的气孔不能完全闭合；但在ABA处理下,parg1-3植株叶片与野生型植株叶片的气孔闭合状况相似。此外,在干旱逆境中,parg1-3植株与野生型植株的干旱逆境／ABA反应基因表达水平相似。而在氧化胁迫下,parg1-3植株中的氧化胁迫相关基因,如交替氧化酶1(alternative oxidase 1,Aox1)和抗坏血酸过氧化物酶(ascorbate peroxidase 2,Apx2)下调表达。不论是干旱、渗透、氧化胁迫处理,还是ABA处理,PARG1的转基因过量表达株系均未表现出与野生型植株的差异。这些结果表明,PARG1基因在拟南芥对多种类型的逆境反应中起重要作用。
上述结果表明,PARG1基因可能通过调节细胞内的PAR含量,维持细胞内NAD+和ATP含量,在植物抗病和抗逆反应中起重要作用。研究结果对全面认识和理解拟南芥在抗病、逆境反应中的分子机制以及高等植物中聚ADP-核酸化的作用有积极的意义。
Poly(ADP-ribosyl)ation is a post-translational protein modification that plays important roles in many cellular processes in mammal systems. Emerging evidence indicates that poly(ADP-ribosyl)ation is also involved in regulation of growth/development, stress and defense response in plants. In this study, I studied the possible function of Arabidopsis poly(ADP-ribose) glycohydrolase 1 (PARG1) in disease resistance and abiotic stress responses using T-DNA insertional mutant and overexpression transgenic lines.
Bioinformatics analysis reveals that there are two genes encoding for poly(ADP-ribose) glycohydrolases. RT-PCR analysis showed that expression of PARG1 was up-regulated in Arabidopsis plants after inoculation with Botrytis cinerea(B. cinerea), a necrotrophic fungal pathogen. Similarly, expression of PARG1 was also significantly induced in Arabidopsis plants after treatment with salicylic acid (SA) or light. By contrast, the expression of PARG1 was reduced when Arabidopsis plants was treated with SA under the light. Expression of PARG1 in Arabidopsis was not be induced after treatment with jasmonic acid (JA) and 1-aminocyclopropane-l-carboxylic acid (ACC). PPARG1::GUS transgenic lines was generated and GUS staning showed that the PARG1 gene was expressed in root tips, leaves and anthers. Subcellular localization analysis using 35S-GFP::PARG1 showed that the PARG1 protein was localized in the nucleus and cytoplasm of Arabidopsis cells.
To study the function of PARG1 in disease resistance and abiotic stress responses, two T-DNA insertion line, parg1-3 in Ws-0 background and parg1-4 in Col-0 background were identified from genotyping screening. Meanwhile, transgenic lines overexpressing the PARG1 gene, driven by CaMV 35S promoter, in pargl-3 mutant and wild type Col-0 background were also generated. Homozygous lines with single copy of the PARG1 transgene were obtained through antibiotic resistance segregation screenings. Two independent transgenic lines overexpressing PARG1 gene in parg1-3 mutant background (PARG1-OE1/parg1-3 and PARG1-OE2/parg1-3) or wild type Col-0 background (PARG1-OE1/Col-0 and PARG1-OE2/Col-0) were selected for further studies. Disease phenotypes of the wild-type, pargl and PARG1-OE plants were compared after inoculation with B. cinerea or Pseudomonas syringae pv. tomato DC3000(Pst DC3000). As compared with the wild-type plants, the pargl plants showed increased resistance to B. cinerea and Pst DC3000. However, the transgenic PARG1-OE plants showed significant increased susceptibility to the above-mentioned pathogens. Furthermore, growth of B. cinerea and Pst DC3000 in leaves of the pargl plants was much less than in the wild-type plants; whereas growth of B. cinerea and Pst DC3000 in leaves of the PARG1-OE plants was significantly increased. After inoculation with B. cinerea, expression of Pathogenesis-related protein gene(PR) was similar in the wild-type, pargl and PARG1-OE plants. These results indicate that PARG1-mediated defense response against B. cinerea may be independent on PR genes. These data suggest that PARG1 plays an important role in Arabidopsis defense responses against both necrotrophic and biotrophic pathogens.
To further study the function of PARG1 in disease resistance response, we examined accumulation of reactive oxygen species and levels of apoptosis in Arabidopsis after inoculation with B. cinerea. It was observed that, after B. cinerea infection, PARG1-OE plants accumulated much more reactive oxygen species in leaves but the pargl plants accumulated less reactive oxygen species in leaves, when comopared with those in the wild-type plants. As compared with the wild-type plants, the pargl plants showed reduced level of apoptosis after B. cinerea infection, whereas the PARG1-OE plants showed accelerated cell death after inoculation with B. cinerea, Pst DC3000 (avrRPM1) or Pst DC3000. these results suggest that PARG1 may be also involved in regulation of cell death. Poly(ADP-ribose)(PAR) induces apoptosis in pargl plants, but did not induce cell necrosis. Ac-DEVD-CHO, a caspase3 inhibitor, inhibited partially PAR- induced apoptosis. These results demonstrate that PAR, which regulated by PARGl, can induce apoptosis, and this process is partially dependent on caspase-apoptosis signaling pathways.
I also examined the possible function of PARG1 in Arabidopsis abiotic stress tolerance using genetic mutant parg1-3 and transgenic PARG1-overexpressing plants. Expression of PARG1 in wild type plants was upregulated in response to drought and oxidative stress treatments. Germination rates of the parg1-3 seeds were reduced under mannitol or methyl viologen (MV) treatment as compared with the wild type seeds, but the parg1-3 seeds showed similar germination rate to the wild type seeds under ABA treatment. The parg1-3 plants showed reduced tolerance to drought, osmotic and oxidative stresses, with increased levels of cell damage under osmotic and oxidative stress and reduced survival rate under water-withholding drought stress, as compared with the wild type plants. Stomatal apertures of parg1-3 plants failed to close under water-withholding drought stress, but showed similar closure patterns to the wild type plants after ABA treatment. As compared with those in wild type plants, drought stress/ABA-responsive genes in parg1-3 plants showed comparable expression levels under drought stress condition, whereas expression level of some of oxidative stress-related genes in parg1-3 plants was reduced after MV treatment. Overexpression of PARG1 in parg1-3 mutant and wild type Col-0 background did not cause any phenotypical changes in response to drought, osmotic and oxidative stresses and ABA treatment. These results suggest that PARG1 plays important roles in abiotic stress tolerance.
Taken together, data presented in this thesis suggest that PARG1 plays important roles in disease resistance and abiotic stress responses.
引文
Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15:63-78.
Abramovitch RB, Anderson JC, Martin GB (2006) Bacterial elicitation and evasion of plant innate immunity. Nat Rev Mol Cell Biol 7:601-611.
Adams-Phillips L, Briggs AG, Bent AF (2010) Disruption of poly(ADP-ribosyl)ation mechanisms alters responses of Arabidopsis thaliana to biotic stress. Plant Physiol 152:261-280.
Adams-Phillips L, Wan J, Tan X, Dunning FM, Meyers BC, Michelmore RW, Bent AF (2008) Discovery of ADP-ribosylation and other plant defense pathway elements through expression profiling of four different Arabidopsis-Pseudomonas R-avr interactions. Mol Plant Microbe Interact 21: 646-665.
Ahel D, Horejsi Z, Wiechens N, Polo SE, Garcia-Wilson E, Ahel I, Flynn H, Skehel M, West SC, Jackson SP, Owen-Hughes T, Boulton SJ (2009) Poly(ADPribose)-dependent regulation of DNA repair by the chromatin remodeling enzyme ALC1. Science 325:1240-1243.
Ame JC, Apiou F, Jacobson EL, Jacobson MK (1999) Assignment of the poly(ADPribose) glycohydrolase gene (PARG) to human chromosome 10q11.23 and mouse chromosome 14B by in situ hybridization. Cytogenet Cell Genet 85: 269-270.
Ame JC, Spenlehauer C, de Murcia G (2004) The PARP superfamily. Bioessays 26: 882-893.
Ame JC, Rolli V, Schreiber V, Niedergang C, Apiou F, Decker P, Muller S, Hoger T, Menissier-de Murcia J, de Murcia G (1999) PARP-2, a novel mammalian DNA damagedependent poly(ADP-ribose) polymerase. J Biol Chem 274, 17860-17868.
Amor Y, Babiychuk E, Inze D, Levine A (1998) The involvement of poly(ADP-ribose) polymerase in the oxidative stress responses in plants. FEBS Lett 440:1-7.
Andrabi SA, Kim NS, Yu SW, Wang H, Koh DW, SasakiM, Klaus JA, Otsuka T, Zhang Z, Koehler RC, Hurn PD, Poirier GG, Dawson VL, Dawson TM (2006) Poly(ADP-ribose) (PAR) polymer is a death signal. Proc Natl Acad Sci USA 103: 18308-18313.
Andreasson E, Jenkins T, Brodersen P, Thorgrimsen S, Petersen NHT, Zhu S, Qiu JL, Micheelsen P, Rocher A, Petersen M, Newman MA, Bjorn Nielsen H, Hirt H, Somssich I, Mattsson O and Mundy J (2005) The MAP kinase substrate MKS1 is a regulator of plant defense responses. EMBO J 24:2579-2589.
Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez Gomez L, Boller T, Ausubel FM and Sheen J (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415:977-983.
Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24: 23-58.
Babiychuk E, Cottrill PB, Storozhenko S, Fuangthong M, Chen Y, O'Farrell MK, Van Montagu M, Inze D, Kushnir S (1998) Higher plants possess two structurally different poly(ADP-ribose) polymerases. Plant J 15:635-645.
Bargmann BOR and Munnik T (2006) The role of phospholipase D in plant stress responses. Curr Opin Plant Biol 9:515-522.
Bartsch M, Gobbato E, Bednarek P, Debey S, Schultze JL, Bautor J, Parker JE (2006) Salicylic acid-independent ENHANCED DISEASE SUSCEPTIBILITY 1 signaling in Arabidopsis immunity and cell death is regulated by the monooxygenase FMO1 and the Nudix hydrolase NUDT7. Plant Cell 18: 1038-1051.
Bessman MJ, Frick DN, O'Handley SF (1996) The MutT proteins or 'Nudix' hydrolases, a family of versatile, widely distributed,'housecleaning'enzymes. J Biol Chem 271:25059-25062.
Besson-Bard A, Pugin A, Wendehenne D (2008) New insights into nitric oxide signaling in plants. Annu Rev Plant Biol 59:21-39.
Blatt MR, Grabov A, Brearley J, Hammond-Kosack K and Jones JDG. (1999) K+ channels of Cf-9 transgenic tobacco guard cells as targets for Cladosporium fulvum Avr9 elicitor-dependent signal transduction. Plant J 19:453-462.
Blenn C, Althaus FR, Malanga M (2006) Poly(ADP-ribose)glycohydrolase silencing protects against H2O2-induced cell death. Biochem J 396:419-429.
Boller T (1995) Chemoperception of microbial signals in plant cells. Annu Rev Plant Physiol Plant Mol Biol 46:189-214.
Boller T and Felix G (2009) A Renaissance of elicitors:perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60:379-406.
Bonicalzi ME, Haince JF, Droit A, Poirier GG (2005) Regulation of poly(ADP-ribose) metabolism by poly(ADP-ribose)glycohydrolase:where and when? Cell Mol Life Sci 62:739-750.
Bonicalzi ME, Vodenicharov M, Coulombe M, Gagne JP, Poirier GG (2003) Alteration of poly(ADP-ribose) glycohydrolase nucleocytoplasmic shuttling characteristics upon cleavage by apoptotic proteases. Biol Cell 95:635-644.
Bryant HE, Schultz N, Thomas HD, Parker KM, Flower D, Lopez E, Kyle S, Meuth M, Curtin NJ, Helleday T (2005) Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 434:913-917.
Burkle A (2001) Physiology and pathophysiology of poly(ADP-ribosyl)ation. BioEssays 23:795-806.
Cabrera JC, Boland A, Messiaen J, Cambier P,Van Cutsem P (2008) Egg box conformation of oligogalacturonides:the time-dependent stabilization of the elicitor-active conformation increases its biological activity. Glycobiology 18: 473-482.
Caplan J, Padmanabhan M, Dinesh-Kumar SP (2008) Plant NB-LRR immune receptors:from recognition to transcriptional reprogramming. Cell Host Microbe 3:126-135.
Chang P, Coughlin M, Mitchison TJ (2005) Tankyrase-1 polymerization of poly(ADP-ribose) is required for spindle structure and function. Nat Cell Biol 7: 1133-1139.
Chang P, Coughlin M, Mitchison TJ (2009) Interaction between Poly(ADP-ribose) and NuMA contributes to mitotic spindle pole assembly. Mol Biol Cell 20: 4575-4585.
Chang P, Jacobson MK, Mitchison TJ (2004) Poly(ADP-ribose) is required for spindle assembly and structure. Nature 432:645-649.
Chen YM, Shall S, O'Farrell M (1994) Poly(ADP-ribose) polymerase in plant nuclei. Eur J Biochem 224:135-142.
Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nurnberger T, Jones JDG, Felix G. and Boller T (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448:497-500.
Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803-14.
Christmann A, Moes D, Himmelbach A, Yang Y, Tang Y, Grill E (2006) Integration of abscisic acid signalling into plant responses. Plant Biol 8:314-325.
Clough SJ, Bent AF (1998) Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743.
Colcombet J, Hirt H (2008) Arabidopsis MAPKs:a complex signaling network involved in multiple biological processes. Biochem J 413:217-226.
Cozzi A, Cipriani G, Fossati S, Faraco G, Formentini L, Min W, Cortes U, Wang ZQ, Moroni F, Chiarugi A (2006) Poly(ADP-ribose) accumulation and enhancement of postischemic brain damage in 110-kDa poly(ADP-ribose) glycohydrolase null mice. J Cereb Blood Flow Metab 26:684-695.
Cuzzocrea S, Di Paola R, Mazzon E, Cortes U, Genovese T, Muia C, Li W, Xu W, Li JH, Zhang J, Wang ZQ (2005) PARG activity mediates intestinal injury induced by splanchnic artery occlusion and reperfusion. FASEB J 19:558-566.
D'Amours D, Desnoyers S, D'Silva I, Poirier GG (1999) Poly(ADPribosyl)ation reactions in the regulation of nuclear functions. Biochem J 342:249-268.
De Block M, Verduyn C, De Brouwer D, Cornelissen M (2005) Poly(ADP-ribose) polymerase in plants affects energy homeostasis, cell death and stress tolerance. Plant J 41:95-106.
Devoto A, Turner JG. (2003) Regulation of jasmonate-mediated plant responses in Arabidopsis. Ann Bot (London) 92:329-337.
Dinesh-Kumar SP, Anandalakshmi R, Schiff M, Liu Y (2003) Virus-induced gene silencing. Methods in Mole Biol 236:287-294.
Doucet-Chabeaud G, Godon C, Brutesco C, de Murcia G, Kazmaier M (2001) Ionising radiation induces the expression of PARP-1 and PARP-2 genes in Arabidopsis. Mol Genet Genomics 265:954-963.
Durrant WE and Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185-209.
Dynek JN, Smith S (2004) Resolution of sister telomere association is required for progression through mitosis. Science 304:97-100.
Erdelyi K, Bai P, Kovacs I, Szabo E, Mocsar G, Kakuk A, Szabo C, Gergely P, Virag L (2009) Dual role of poly(ADP-ribose) glycohydrolase in the regulation of cell death in oxidatively stressed A549 cells. FASEB J 23:3553-3563.
Farmer H, McCabe N, Lord CJ, Tutt AN, Johnson DA, Richardson TB, Santarosa M, Dillon KJ, Hickson I, Knights C, Martin NM, Jackson SP, Smith GC, Ashworth A (2005) Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 434:917-921.
Fisher AE, Hochegger H, Takeda S, Caldecott KW (2007) Poly(ADPribose)polymerase 1 accelerates single-strand break repair in concert with poly(ADP-ribose) glycohydrolase. Mol Cell Biol 27:5597-5605.
Formentini L, Macchiarulo A, Cipriani G, Camaioni E, Rapizzi E, Pellicciari R, Moroni F, Chiarugi A (2009) Poly(ADP-ribose) catabolism triggers AMP-dependent mitochondrial energy failure. J Biol Chem 284:17668-17676.
Fu ZQ, Guo M, Jeong BR, Tian F, Elthon TE, Cerny RL, Staiger D, Alfano JR (2007) A type Ⅲ effector ADP-ribosylates RNA-binding proteins and quells plant immunity. Nature 447:284-288.
Fuglsang AT, Guo Y, Cuin TA, Qiu Q, Song C, Kristiansen KA, Bych K, Schulz A, Shabala S, Schumaker KS, Palmgren MG and Zhu JK (2007) Arabidopsis protein kinase PKS5 inhibits the plasma membrane H+-ATPase by preventing interaction with 14-3-3 protein. Plant Cell 19:1617-1634.
Gagne JP, Hendzel MJ, Droit A, Poirier GG (2006) The expanding role of poly(ADP-ribose) metabolism: Current challenges and new perspectives. Curr Opin Cell Biol 18:145-151.
Gao H, Coyle DL, Meyer-Ficca ML, Meyer RG, Jacobson EL, Wang ZQ, Jacobson MK (2007) Altered poly(ADP-ribose) metabolism impairs cellular responses to genotoxic stress in a hypomorphic mutant of poly(ADP-ribose) glycohydrolase. Exp Cell Res 313:984-996.
Garcia-Brugger A, Lamotte O, Vandelle E, Bourque S, Lecourieux D, Poinssot B, Wendehenne D, Pugin A (2006) Early signaling events induced by elicitors of plant defenses. Mol Plant Microbe Inter 19:711-724.
Ge X, Li GJ, Wang SB, Zhu H, Zhu T, Wang X, Xia Y (2007) AtNUDT7, a negative regulator of basal immunity in Arabidopsis, modulates two distinct defense response pathways and is involved in maintaining redox homeostasis. Plant Physiol 145:204-215.
Gelli A, Higgins VJ and Blumwald E (1997) Activation of plant plasma membrane Ca2+-permeable channels by race-specific fungal elicitors. Plant Physiol 113, 269-279.
Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205-227.
Govrin EM, Levine A.2000. The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Current Biology 10:751-757.
Grant M and Lamb C (2006) Systemic immunity. Curr Opin Plant Biol 9:414-420.
Haince JF, Ouellet ME, McDonald D, Hendzel MJ, Poirier GG (2006) Dynamic relocation of poly(ADP-ribose) glycohydrolase isoforms during radiation-induced DNA damage. Biochim Biophys Acta 1763:226-237.
Haince JF, Kozlov S, Dawson VL, Dawson TM, Hendzel MJ, Lavin MF, Poirier GG (2007) Ataxia telangiectasia mutated (ATM) signaling network is modulated by a novel poly(ADP-ribose)-dependent pathway in the early response to DNA-damaging agents. J Biol Chem 282:16441-16453.
Hanai S, Kanai M, Ohashi S, Okamoto K, Yamada M, Takahashi H, Miwa M (2004) Loss of poly(ADP-ribose) glycohydrolase causes progressive neurodegeneration in Drosophila melanogaster. Proc Natl Acad Sci USA 101:82-86.
Hashida SN, Takahashi H, Uchimiya H (2009) The role of NAD biosynthesis in plant development and stress responses. Ann Bot (Lond) 103:819-824.
Hassa PO, Hottiger MO (2008) The diverse biological roles of mammalian PARPs, a small but powerful family of poly-ADP-ribose polymerases. Front Biosci 13: 3046-3082.
Heeres JT and Hergenrother PJ (2007) Poly(ADP-ribose) makes a date with death. Curr Opin Chem Biol 11:644-653.
Heese A, Hann DR, Gimenez-Ibanez S, Jones AM, He K, Li J, Schroeder JI, Peck SC, Rathjen JP (2007) The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc Natl Acad Sci USA 104:12217-12222.
Hong JK, Hwang BK (2005) Induction of enhanced disease resistance and oxidative stress tolerance by complemention of pepper basic PR-1 gene in Arabidopsis. Physiol Plantarum 124:267-277.
Horvath EM, Szabo C (2007) Poly(ADP-ribose) polymerase as a drug target for cardiovascular disease and cancer: an update. Drug News Perspect 20:171-181.
Hunt L, Lerner F, Ziegler M (2004) NAD-new roles in signalling and gene regulation in plants. New Phytol 163:31-44.
Ishikawa K, Ogawa T, Hirosue E, Nakayama Y, Harada K, Fukusaki E, Yoshimura K, Shigeoka S (2009) Modulation of the poly(ADP-ribosyl)ation reaction via the Arabidopsis ADP-ribose/NADH pyrophosphohydrolase, AtNUDX7, is involved in the response to oxidative stress. Plant Physiol 151:741-754.
Jabs T (1999) Reactive oxygen intermediates as mediators of programmed cell death in plants and animals. Biochem Pharmacol 57:231-245.
Jagtap P and Szabo C (2005) Poly(ADP-ribose) polymerase and the therapeutic effects of its inhibitors. Nat Rev Drug Discov 4:421-440.
Jambunathan, N., and Mahalingam, R.2006. Analysis of Arabidopsis growth factor gene 1(GFG1) encoding a nudix hydrolase during oxidative signaling. Planta 224:1-11.
Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323-29.
Kabbage M, Dickman MB (2008) The BAG proteins:a ubiquitous family of chaperone regulators. Cell Mol Life Sci 65:1390-1402.
van Kan JAL (2006) Licensed to kill:The lifestyle of a necrotrophic plant pathogen. Trends Plant Sci 11:247-253.
Kang CH, Jung WY, Kang YH, Kim JY, Kim DG, Jeong JC, Baek DW, Jin JB, Lee JY, Kim MO, Chung WS, Mengiste T, Koiwa H, Kwak SS, Bahk JD, Lee SY, Nam JS, Yun DJ, Cho MJ (2006) AtBAG6, a novel calmodulin-binding protein, induces programmed cell death in yeast and plants. Cell Death Differ 13:84-95.
Katagirl F, Thilmony, He SY (2002) The Arabidopsis Thaliana-Pseudomonas Syringae Interaction. The Arabidopsis Book, doi:10.1199/tab.0039.
Kendrick MD, Chang C (2008) Ethylene signaling:new levels of complexity and regulation. Curr Opin Plant Biol 11:479-485.
Kersten B, Agrawal G.K, Iwahashi H, Rakwal R (2006) Plant phosphoproteomics:a long road ahead. Proteomics,6,5517-5528.
Kim MY, Zhang T, Kraus WL (2005) Poly(ADP-ribosyl)ation by PARP-1: 'PAR-laying' NAD+ into a nuclear signal. Genes Dev 19:1951-1967.
Koh DW, Lawler AM, Poitras MF, Sasaki M, Wattler S, Nehls MC, Stoger T, Poirier GG, Dawson VL, Dawson TM (2004) Failure to degrade poly(ADP-ribose) causes increased sensitivity to cytotoxicity and early embryonic lethality. Proc Natl Acad Sci USA 101:17699-17704.
Kolisek M, Beck A, Fleig A and Penner R (2005) Cyclic ADPribose and hydrogen peroxide synergize with ADP-ribose in the activation of TRPM2 channels. Mol Cell 18,61-69.
Kraus WL (2008) Transcriptional control by PARP-1:chromatin modulation, enhancer-binding, coregulation, and insulation. Curr Opin Cell Biol 20:294-302.
Kraus WL, Lis J (2003) PARP goes transcription. Cell 113:677-683.
Kunkel BN, Brooks DV (2002) Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol 5:325-331.
Lam E (2004) Controlled cell death, plant survival and development. Nat Rev Mol Cell Bio 5:305-315.
Laxalt AM and Munnik T (2002) Phospholipid signalling in plant defence. Curr Opin Plant Biol 5:332-333.
Leitner M, Vandelle E, Gaupels F, Bellin D, Delledonne M (2009) NO signals in the haze Nitric oxide signalling in plant defence. Curr Opin Plant Biol 12:451-458.
Li S, Assmann SM, Albert R (2006) Predicting essential components of signal transduction networks:A dynamic model of guard cell abscisic acid signaling. PLoS Biol 4:e312.
Liu Y and Zhang S (2004) Phosphorylation of 1-aminocyclopropane-l-carboxylic acid synthase by MPK6, a stress-responsive mitogen-activated protein kinase, induces ethylene biosynthesis in Arabidopsis. Plant Cell 16:3386-3399.
van Loon LC, Rep M, Pieterse CMJ (2006) Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44:135-162.
Lorenzo O, Solano R.2005. Molecular players regulating the jasmonate signalling network. Curr Opin Plant Bio 8:532-540.
Lucas JA (1998) Plant pathology and plant pathogens. Blackwell Science, Oxford, UK (Malden, MA, USA).
Ludwig AA, Saitoh H, Felix G, Freymark G, Miersch O, Wasternack C, Boller T, Jones JDG and Romeis T (2005) Ethylene-mediated cross-talk between calcium-dependent protein kinase and MAPK signaling controls stress responses in plants. Proc Natl Acad Sci USA 102:10736-10741.
Malanga M, Althaus FR (2005) The role of poly(ADP-ribose) in the DNA damage signaling network. Biochem Cell Biol 83:354-364.
Martin GB, Bogdanove AJ, Sessa G (2003) Understanding the functions of plant disease resistance proteins. Annu Rev Plant Biol 54:23-61.
Masson M, Niedergang C, Schreiber V, Muller S, Menissier-de Murcia J, de Murcia G (1998) XRCC1 is specifically associated with poly(ADP-ribose) polymerase and negatively regulates its activity following DNA damage. Mol Cell Biol 18: 3563-3571.
McDowell JM, Dangl JL (2000) Signal transduction in the plant immune response. Trends Biochem Sci 25:79-82.
Mengiste T, Chen X, Salmeron J, Dietrich R (2003) The BOTRYTIS SUSCEPTIBLEl gene encodes an R2R3MYB transcription factor protein that is required for biotic and abiotic stress responses in Arabidopsis. Plant Cell 15:2551-2565.
Menke FLH, Kang HG, Chen Z, Jeong MP, Kumar D and Klessig DF (2005) Tobacco transcription factor WRKY1 is phosphorylated by the MAP kinase SIPK and mediates HR-like cell death in tobacco. Mol Plant-Microbe Interact 18: 1027-1034.
Meyer-Ficca ML, Meyer RG, Coyle DL, Jacobson EL, Jacobson MK (2004) Human poly(ADP-ribose) glycohydrolase is expressed in alternative splice variants yielding isoforms that localize to different cell compartments. Exp Cell Res 297: 521-532.
Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) The reactive oxygen gene network of plants. Trends Plant Sci 9:490-498.
Modjtahedi N, Giordanetto F, Frank M Kroemer G (2006) Apoptosis-inducing factor: vital and lethal. Trends Cell Biol 16:264-272.
Moore T, Martineau B, Bostock RM, Lincoln JE and Gilchrist GD (1999) Molecular and genetic characterization of ethylene involvement in mycotoxins-induced plant cell death. Physiol Mol Plant Pathol 54:73-85.
Mur LA, Kenton P, Atzorn R, Miersch O Wasternack C (2006) The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiol 140:249-266.
Nimchuk Z, Eulgem T, Holt BE, Dangl JL (2003) Recognition and response in the plant immune system. Annu Rev Genet 37:579-609.
Oei SL, Keil C, Ziegler M (2005) Poly(ADP-ribosylation) and genomic stability. Biochem Cell Biol 83:263-269.
O'Farrell M (1995) ADP-ribosylation reactions in plants. Biochimie 77:486-491.
Ogawa T, Ishikawa K, Harada K, Fukusaki E, Yoshimura K, Shigeoka S (2009) Overexpression of an ADP-ribose pyrophosphatase, AtNUDX2, confers enhanced tolerance to oxidative stress in Arabidopsis plants. Plant J 57: 289-301.
Ogawa T, Ueda Y, Yoshimura K, Shigeoka S (2005) Comprehensive analysis of cytosolic Nudix hydrolases in Arabidopsis thaliana. J Biol Chem 280: 25277-25283.
Ohashi S, Kanai M, Hanai S, Uchiumi F, Maruta H, Tanuma S, Miwa M (2003) Subcellular localization of poly(ADP-ribose) glycohydrolase in mammalian cells. Biochem Biophys Res Commun 307:915-921.
Oirdi ME and Bouarab K (2007) Plant signalling components EDS1 and SGT1 enhance disease caused by the necrotrophic pathogen Botrytis cinerea. New Phytologist 175:131-139.
Oka S, Kato J, Moss J (2006) Identification and characterization of a mammalian 39-kDa Poly(ADP-ribose) glycohydrolase. JBiol Chem 281:705-713.
Olejnik K, Kraszewska E (2005) Cloning and characterization of an Arabidopsis thaliana Nudix hydrolase homologous to the mammalian GFG protein. Biochim Biophys Acta 1752:133-141.
Otto H, Reche PA, Bazan F, Dittmar K, Haag F, Koch-Nolte F (2005) In silico characterization of the family of PARP-like poly(ADP-ribosyl)transferases (pARTs). BMC Genomics 6:139.
Palmgren MG (2001) Plant plasme membrane H+-ATPases:powerhouses for nutrient uptake. Annu Rev Plant Physiol Plant Mol Biol 52:817-845.
Panda S, Poirier GG, Kay SA (2002) tej defines a role for poly(ADP-ribosyl)ation in establishing period length of the Arabidopsis circadian oscillator. Dev Cell 3: 51-61.
Patel NS, Cortes U, Di Poala R, Mazzon E, Mota-Filipe H, Cuzzocrea S, Wang ZQ, Thiemermann C (2005) Mice lacking the 110-kDa isoform of poly(ADP-ribose) glycohydrolase are protected against renal ischemia/reperfusion injury. J Am Soc Nephrol 16:712-719.
Pedley KF and Martin GB (2005) Role of mitogen-activated protein kinases in plant immunity. Curr Opin Plant Biol 8:541.
Perraud AL, Takanishi CL, Shen B, Kang S, Smith MK, Schmitz C, Knowles HM, Ferraris D, Li W, Zhang J, Stoddard BL, Scharenberg AM (2005) Accumulation of free ADP-ribose from mitochondria mediates oxidative stressinduced gating of TRPM2 cation channels. JBiol Chem 280:6138-6148.
Petrucco S (2003) Sensing DNA damage by PARP-like fingers. Nucleic Acids Res 31: 6689-6699.
Pitzschke A, Schikora A, Hirt H (2009) MAPK cascade signalling networks in plant defence. Curr Opin Plant Biol 12:421-426.
Pleschke JM, Kleczkowska HE, Strohm M, Althaus FR (2000) Poly(ADPribose) binds to specific domains in DNA damage checkpoint proteins. J Biol Chem 275: 40974-40980.
del Pozo O, Lam E.1998. Caspases and programmed cell death in the hypersensitive response of plants to pathogens. Current Biology 8:1129-1132.
del Pozo O, Lam E.2003. Expression of the baculovirus p35 protein in tobacco affects cell death progression and compromises N gene-mediated disease resistance response to Tobacco mosaic virus. Mole Plant-Microbe Interact 16: 485-494.
Qin F, Sakuma Y, Tran LS, Maruyama K, Kikodoro S, Fujita Y, Fujita M, Sawano Y, Miyazono K, Tanokura M, Shinozaki K, Yamaguchi-Shinozaki K (2008) Arabidopsis DREB2A-interacting proteins function as RING E3 ligases and negatively regulate plant drought stress-responsive gene expression. Plant Cell 20:1693-1707.
Qiu JL, Fiil BK, Petersen K, Nielsen HB, Botanga CJ, Thorgrimsen S, Palma K, Suarez-Rodriguez MC, Sandbech-Clausen S, Lichota J, Brodersen P, Grasser KD, Mattsson O, Glazebrook J, Mundy J, Petersen M (2008) Arabidopsis MAP kinase 4 regulates gene expression through transcription factor release in the nucleus. EMBO J 27:2214-2221.
Ratcliff F, Martin-Hernandez AM, Baulcombe DC (2001) Technical Advance. Tobacco rattle virus as a vector for analysis of gene function by silencing. Plant J25:237-245.
Robatzek S, Chinchilla D and Boller T (2006) Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev 20:537-542.
Roldan-Arjona T, Ariza RR (2009) Repair and tolerance of oxidative DNA damage in plants. Mutat Res 681:169-179.
Rongvaux A, Andris F, Van Gool F, Leo O (2003) Reconstructing eukaryotic NAD metabolism. BioEssays 25:683-690.
Rossi R, Montecucco A, Donzelli M, Denegri M, Biamonti G, Scovassi A (2002) DNA ligase I is dephosphorylated during the execution step of etoposide-induced apoptosis. Cell Death Differ 9:89-90.
Rouleau M, Aubin RA, Poirier GG (2004) Poly(ADPribosyl)ated chromatin domains: access granted. J Cell Sci 117:815-825.
Ryals JA, Neuenschwander UH., Willits MG, Molina A, Steiner HY, Hunt MD (1996) Systemic acquired resistance. Plant Cell 8:1809-1819.
Sakuma Y, Maruyama K, Qin F, Osakabe Y, Shinozaki K, Yamaguchi-Shinozaki K (2006) Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc Natl Acad Sci USA 103:18822-18827.
Schenk P M, Kazan K, Wilson I, Anderson JP, Richmond T, Somerville SC, Manners JM (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc Natl Acad Sci USA 97:11655-11660.
Schreiber V, Dantzer F, Ame JC, de Murcia G (2006) Poly(ADP-ribose):novel functions for an old molecule. Nat Rev Mol Cell Biol 7:517-528.
Schreiber, V. et al. (2002) Poly(ADP-ribose) polymerase-2 (PARP-2) is required for efficient base excision DNA repair in association with PARP-1 and XRCC1. J Biol Chem 277:23028-23036.
Seki M, Umezawa T,Urano K, Shinozaki K (2007) Regulatory metabolic networks in drought stress responses. Curr Opin Plant Biol 10:296-302.
Shan L, He P, Li J, Heese A, Peck SC, Nurnberger T, Martin GB, Sheen J (2008) Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity. Cell Host Microbe 4:17-27.
Sheikh S, O'Handley SF, Dunn CA, Bessman MJ (1998) Identification and characterization of the Nudix hydrolase from the Archaeon, Methanococcus jannaschii, as a highly specific ADP-ribose pyrophosphatase. J Biol Chem 273: 20924-20928.
Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. JExp Bot 58:221-227.
Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6: 410-417.
Simbulan-Rosenthal CM, Rosenthal DS, Luo R, Smulson ME (1999) Poly(ADPribosyl)ation of p53 during apoptosis in human osteosarcoma cells. Cancer Res 59:2190-2194.
Sokolovski S and Blatt MR (2004) Nitric oxide block of outwardrectifying K+ channels indicates direct control by protein nitrosylation in guard cells. Plant Physiol 136:4275-4284.
St-Laurent JF, Gagnon SN, Dequen F, Hardy I, Desnoyers S (2007) Altered DNA damage response in Caenorhabditis elegans with impaired poly(ADP-ribose) glycohydrolases genes expression. DNA Rep 6:329-343.
Straus MR, Rietz S, van Themaat EV, Bartsch M, Parker JE (2010) Salicylic acid antagonism of EDS1-driven cell death is important for immune and oxidative stress responses in Arabidopsis. Plant J doi:10.1111/j.1365-313X.2010.04178.x
Stulemeijer IJ and Joosten MH (2008) Post-translational modification of host proteins in pathogen-triggered defence signalling in plants. Mole Plant Pathol 9:545-560.
Tanaka Y, Sano T, Tamaoki M, Nakajima N, Kondo N, Hasezawa S (2005) Ethylene inhibits abscisic acid-induced stomatal closure in Arabidopsis. Plant Physiol 138: 2337-2343.
Tatsuki M and Mori H (2001) Phosphorylation of tomato 1-aminocyclopropane-1-carboxylic acid synthase, LE-ACS2, at the Cterminal region. JBiol Chem 276:28051-28057.
Testerink C and Munnik T (2005) Phosphatidic acid:A multifunctional stress signaling lipid in plants. Trends Plant Sci 10:368-375.
Tian R, Zhang GY, Yan CH, Dai YR (2000) Involvement of poly(ADP-ribose) polymerase and activation of caspase-3-like protease in heat shock-induced apoptosis in tobacco suspension cells. FEBS Lett 474:11-15.
Vanderauwera S, De Block M, Van de Steene N, van de Cotte B, Metzlaff M, Van Breusegem F (2007) Silencing of poly(ADP-ribose) polymerase in plants alters abiotic stress signal transduction. Proc Natl Acad Sci USA 104:15150-15155.
Van Wees SC, Van der Ent S, Pieterse CM (2008) Plant immune responses triggered by beneficial microbes. Curr Opin Plant Biol 11:443-448.
Veronese P, Nakagami H, Bluhm B, Abuqamar S, Chen X, Salmeron J, Dietrich R, Hirt H, Mengiste T (2006) The membrane-anchored BOTRYTIS-INDUCED KINASE1 plays distinct roles in Arabidopsis resistance to necrotrophic and biotrophic pathogens. Plant Cell 18:257-273.
Wang H, Li J, Bostock RM and Gilchrist DG (1996) Apoptosis:A functional paradigm for programmed plant cell death induced by a host-selective phytotoxin and invoked during development. Plant Cell 8,375-391.
Wang X, Kota U, He K, Blackburn K, Li J, Goshe MB, Huber SC, Clouse SD (2008) Sequential transphosphorylation of the BRI1/BAK1 receptor kinase complex impacts early events in brassinosteroid signaling. Dev Cell15:220-235.
Wang YS, Pi LY, Chen X, Chakrabarty PK, Jiang J, De Leon AL, Liu G.Z, Li A, Benny U, Oard J, Ronald PC and Song WY (2006) Rice XA21 binding protein 3 is a ubiquitin ligase required for full Xa21-mediated disease resistance. Plant Cell 18:3635-3646.
Wasilewska A, Vlad F, Sirichandra C, Redko Y, Jammes F, Valon C, Frei dit Frey N, Leung J (2008) An update on abscisic acid signaling in plants and more.... Mol Plant Ⅰ:198-217.
Watanabe N, Lam E (2006) Arabidopsis Bax inhibitor-1 functions as an attenuator of biotic and abiotic types of cell death. Plant J 45:884-894.
Watanabe N, Lam E (2008) BAX inhibitor-1 modulates endoplasmic reticulum stress-mediated programmed cell death in Arabidopsis. J Biol Chem 283: 3200-3210.
Watanabe N, Lam E (2009) Bax inhibitor-1, a conserved cell death suppressor, is a key molecular switch downstream from a variety of biotic and abiotic stress signals in plants. Int J Mol Sci 10:3149-3167.
Wilson ID, Neill SJ, Hancock JT (2008) Nitric oxide synthesis and signalling in plants. Plant Cell Environ 31:622-631.
Woon EC, Threadgill MD (2005) Poly(ADP-ribose)polymerase inhibition—where now? Curr Med Chem 12:2373-2392.
Woodhouse BC, Dianov GL (2008)Poly ADP-ribose polymerase-1:An international molecule of mystery. DNA repair 7:1077-1086.
Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14(Suppl):S165-S183.
Yamaguchi-Shinozaki K, Shinozaki K (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6:251-264.
Yoo SD, Cho YH, Tena G, Xiong Y, Sheen J (2008) Dual control of nuclear EIN3 by bifurcate MAPK cascades in C2H4 signalling. Nature 451:789-795.
Yu SW, Andrabi SA, Wang H, Kim NS, Poirier GG, Dawson TM, and. Dawson VL (2006) Apoptosis-inducing factor mediates poly(ADPribose) (PAR) polymer-induced cell death. Proc Natl Acad Sci USA 103:18314-18319.
Yu SW, Wang H, Poitras MF, Coombs C, Bowers WJ, Federoff HJ, Poirier GG, Dawson TM, Dawson VL (2002) Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science 297: 259-263.
Zeller G, Henz SR, Widmer CK, Sachsenberg T, Ratsch G, Weigel D, Laubinger S (2009) Stress-induced changes in the Arabidopsis thaliana transcriptome analyzed using whole-genome tiling arrays. Plant J 58:1068-1082
Ziegler M (2000) New functions of a long-known molecule:emerging roles of NAD in cellular signaling. Eur J Biochem 267:1550-1564.
Zhang T, Liu Y, Yang T, Zhang L, Xu S, Xue L and An L (2006) Diverse signals converge at MAPK cascades in plant. Plant Physiol Biochem 44:274-283.
Abramovitch RB, Anderson JC, Martin GB (2006) Bacterial elicitation and evasion of plant innate immunity. Nat Rev Mol Cell Biol 7:601-611.
Adams-Phillips L, Briggs AG, Bent AF (2010) Disruption of poly(ADP-ribosyl)ation mechanisms alters responses of Arabidopsis thaliana to biotic stress. Plant Physiol 152:261-280.
Adams-Phillips L, Wan J, Tan X, Dunning FM, Meyers BC, Michelmore RW, Bent AF (2008) Discovery of ADP-ribosylation and other plant defense pathway elements through expression profiling of four different Arabidopsis-Pseudomonas R-avr interactions. Mol Plant Microbe Interact 21: 646-665.
Ahel D, Horejsi Z, Wiechens N, Polo SE, Garcia-Wilson E, Ahel I, Flynn H, Skehel M, West SC, Jackson SP, Owen-Hughes T, Boulton SJ (2009) Poly(ADPribose)-dependent regulation of DNA repair by the chromatin remodeling enzyme ALC1. Science 325:1240-1243.
Ame JC, Apiou F, Jacobson EL, Jacobson MK (1999) Assignment of the poly(ADPribose) glycohydrolase gene (PARG) to human chromosome 10q11.23 and mouse chromosome 14B by in situ hybridization. Cytogenet Cell Genet 85: 269-270.
Ame JC, Spenlehauer C, de Murcia G (2004) The PARP superfamily. Bioessays 26: 882-893.
Ame JC, Rolli V, Schreiber V, Niedergang C, Apiou F, Decker P, Muller S, Hoger T, Menissier-de Murcia J, de Murcia G (1999) PARP-2, a novel mammalian DNA damagedependent poly(ADP-ribose) polymerase. J Biol Chem 274, 17860-17868.
Amor Y, Babiychuk E, Inze D, Levine A (1998) The involvement of poly(ADP-ribose) polymerase in the oxidative stress responses in plants. FEBS Lett 440:1-7.
Andrabi SA, Kim NS, Yu SW, Wang H, Koh DW, SasakiM, Klaus JA, Otsuka T, Zhang Z, Koehler RC, Hurn PD, Poirier GG, Dawson VL, Dawson TM (2006) Poly(ADP-ribose) (PAR) polymer is a death signal. Proc Natl Acad Sci USA 103: 18308-18313.
Andreasson E, Jenkins T, Brodersen P, Thorgrimsen S, Petersen NHT, Zhu S, Qiu JL, Micheelsen P, Rocher A, Petersen M, Newman MA, Bjorn Nielsen H, Hirt H, Somssich I, Mattsson O and Mundy J (2005) The MAP kinase substrate MKS1 is a regulator of plant defense responses. EMBO J 24:2579-2589.
Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez Gomez L, Boller T, Ausubel FM and Sheen J (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415:977-983.
Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24: 23-58.
Babiychuk E, Cottrill PB, Storozhenko S, Fuangthong M, Chen Y, O'Farrell MK, Van Montagu M, Inze D, Kushnir S (1998) Higher plants possess two structurally different poly(ADP-ribose) polymerases. Plant J 15:635-645.
Bargmann BOR and Munnik T (2006) The role of phospholipase D in plant stress responses. Curr Opin Plant Biol 9:515-522.
Bartsch M, Gobbato E, Bednarek P, Debey S, Schultze JL, Bautor J, Parker JE (2006) Salicylic acid-independent ENHANCED DISEASE SUSCEPTIBILITY 1 signaling in Arabidopsis immunity and cell death is regulated by the monooxygenase FMO1 and the Nudix hydrolase NUDT7. Plant Cell 18: 1038-1051.
Bessman MJ, Frick DN, O'Handley SF (1996) The MutT proteins or 'Nudix' hydrolases, a family of versatile, widely distributed,'housecleaning'enzymes. J Biol Chem 271:25059-25062.
Besson-Bard A, Pugin A, Wendehenne D (2008) New insights into nitric oxide signaling in plants. Annu Rev Plant Biol 59:21-39.
Blatt MR, Grabov A, Brearley J, Hammond-Kosack K and Jones JDG. (1999) K+ channels of Cf-9 transgenic tobacco guard cells as targets for Cladosporium fulvum Avr9 elicitor-dependent signal transduction. Plant J 19:453-462.
Blenn C, Althaus FR, Malanga M (2006) Poly(ADP-ribose)glycohydrolase silencing protects against H2O2-induced cell death. Biochem J 396:419-429.
Boller T (1995) Chemoperception of microbial signals in plant cells. Annu Rev Plant Physiol Plant Mol Biol 46:189-214.
Boller T and Felix G (2009) A Renaissance of elicitors:perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60:379-406.
Bonicalzi ME, Haince JF, Droit A, Poirier GG (2005) Regulation of poly(ADP-ribose) metabolism by poly(ADP-ribose)glycohydrolase:where and when? Cell Mol Life Sci 62:739-750.
Bonicalzi ME, Vodenicharov M, Coulombe M, Gagne JP, Poirier GG (2003) Alteration of poly(ADP-ribose) glycohydrolase nucleocytoplasmic shuttling characteristics upon cleavage by apoptotic proteases. Biol Cell 95:635-644.
Bryant HE, Schultz N, Thomas HD, Parker KM, Flower D, Lopez E, Kyle S, Meuth M, Curtin NJ, Helleday T (2005) Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 434:913-917.
Burkle A (2001) Physiology and pathophysiology of poly(ADP-ribosyl)ation. BioEssays 23:795-806.
Cabrera JC, Boland A, Messiaen J, Cambier P,Van Cutsem P (2008) Egg box conformation of oligogalacturonides:the time-dependent stabilization of the elicitor-active conformation increases its biological activity. Glycobiology 18: 473-482.
Caplan J, Padmanabhan M, Dinesh-Kumar SP (2008) Plant NB-LRR immune receptors:from recognition to transcriptional reprogramming. Cell Host Microbe 3:126-135.
Chang P, Coughlin M, Mitchison TJ (2005) Tankyrase-1 polymerization of poly(ADP-ribose) is required for spindle structure and function. Nat Cell Biol 7: 1133-1139.
Chang P, Coughlin M, Mitchison TJ (2009) Interaction between Poly(ADP-ribose) and NuMA contributes to mitotic spindle pole assembly. Mol Biol Cell 20: 4575-4585.
Chang P, Jacobson MK, Mitchison TJ (2004) Poly(ADP-ribose) is required for spindle assembly and structure. Nature 432:645-649.
Chen YM, Shall S, O'Farrell M (1994) Poly(ADP-ribose) polymerase in plant nuclei. Eur J Biochem 224:135-142.
Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nurnberger T, Jones JDG, Felix G. and Boller T (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448:497-500.
Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803-14.
Christmann A, Moes D, Himmelbach A, Yang Y, Tang Y, Grill E (2006) Integration of abscisic acid signalling into plant responses. Plant Biol 8:314-325.
Clough SJ, Bent AF (1998) Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743.
Colcombet J, Hirt H (2008) Arabidopsis MAPKs:a complex signaling network involved in multiple biological processes. Biochem J 413:217-226.
Cozzi A, Cipriani G, Fossati S, Faraco G, Formentini L, Min W, Cortes U, Wang ZQ, Moroni F, Chiarugi A (2006) Poly(ADP-ribose) accumulation and enhancement of postischemic brain damage in 110-kDa poly(ADP-ribose) glycohydrolase null mice. J Cereb Blood Flow Metab 26:684-695.
Cuzzocrea S, Di Paola R, Mazzon E, Cortes U, Genovese T, Muia C, Li W, Xu W, Li JH, Zhang J, Wang ZQ (2005) PARG activity mediates intestinal injury induced by splanchnic artery occlusion and reperfusion. FASEB J 19:558-566.
D'Amours D, Desnoyers S, D'Silva I, Poirier GG (1999) Poly(ADPribosyl)ation reactions in the regulation of nuclear functions. Biochem J 342:249-268.
De Block M, Verduyn C, De Brouwer D, Cornelissen M (2005) Poly(ADP-ribose) polymerase in plants affects energy homeostasis, cell death and stress tolerance. Plant J 41:95-106.
Devoto A, Turner JG. (2003) Regulation of jasmonate-mediated plant responses in Arabidopsis. Ann Bot (London) 92:329-337.
Dinesh-Kumar SP, Anandalakshmi R, Schiff M, Liu Y (2003) Virus-induced gene silencing. Methods in Mole Biol 236:287-294.
Doucet-Chabeaud G, Godon C, Brutesco C, de Murcia G, Kazmaier M (2001) Ionising radiation induces the expression of PARP-1 and PARP-2 genes in Arabidopsis. Mol Genet Genomics 265:954-963.
Durrant WE and Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185-209.
Dynek JN, Smith S (2004) Resolution of sister telomere association is required for progression through mitosis. Science 304:97-100.
Erdelyi K, Bai P, Kovacs I, Szabo E, Mocsar G, Kakuk A, Szabo C, Gergely P, Virag L (2009) Dual role of poly(ADP-ribose) glycohydrolase in the regulation of cell death in oxidatively stressed A549 cells. FASEB J 23:3553-3563.
Farmer H, McCabe N, Lord CJ, Tutt AN, Johnson DA, Richardson TB, Santarosa M, Dillon KJ, Hickson I, Knights C, Martin NM, Jackson SP, Smith GC, Ashworth A (2005) Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 434:917-921.
Fisher AE, Hochegger H, Takeda S, Caldecott KW (2007) Poly(ADPribose)polymerase 1 accelerates single-strand break repair in concert with poly(ADP-ribose) glycohydrolase. Mol Cell Biol 27:5597-5605.
Formentini L, Macchiarulo A, Cipriani G, Camaioni E, Rapizzi E, Pellicciari R, Moroni F, Chiarugi A (2009) Poly(ADP-ribose) catabolism triggers AMP-dependent mitochondrial energy failure. J Biol Chem 284:17668-17676.
Fu ZQ, Guo M, Jeong BR, Tian F, Elthon TE, Cerny RL, Staiger D, Alfano JR (2007) A type Ⅲ effector ADP-ribosylates RNA-binding proteins and quells plant immunity. Nature 447:284-288.
Fuglsang AT, Guo Y, Cuin TA, Qiu Q, Song C, Kristiansen KA, Bych K, Schulz A, Shabala S, Schumaker KS, Palmgren MG and Zhu JK (2007) Arabidopsis protein kinase PKS5 inhibits the plasma membrane H+-ATPase by preventing interaction with 14-3-3 protein. Plant Cell 19:1617-1634.
Gagne JP, Hendzel MJ, Droit A, Poirier GG (2006) The expanding role of poly(ADP-ribose) metabolism: Current challenges and new perspectives. Curr Opin Cell Biol 18:145-151.
Gao H, Coyle DL, Meyer-Ficca ML, Meyer RG, Jacobson EL, Wang ZQ, Jacobson MK (2007) Altered poly(ADP-ribose) metabolism impairs cellular responses to genotoxic stress in a hypomorphic mutant of poly(ADP-ribose) glycohydrolase. Exp Cell Res 313:984-996.
Garcia-Brugger A, Lamotte O, Vandelle E, Bourque S, Lecourieux D, Poinssot B, Wendehenne D, Pugin A (2006) Early signaling events induced by elicitors of plant defenses. Mol Plant Microbe Inter 19:711-724.
Ge X, Li GJ, Wang SB, Zhu H, Zhu T, Wang X, Xia Y (2007) AtNUDT7, a negative regulator of basal immunity in Arabidopsis, modulates two distinct defense response pathways and is involved in maintaining redox homeostasis. Plant Physiol 145:204-215.
Gelli A, Higgins VJ and Blumwald E (1997) Activation of plant plasma membrane Ca2+-permeable channels by race-specific fungal elicitors. Plant Physiol 113, 269-279.
Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205-227.
Govrin EM, Levine A.2000. The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Current Biology 10:751-757.
Grant M and Lamb C (2006) Systemic immunity. Curr Opin Plant Biol 9:414-420.
Haince JF, Ouellet ME, McDonald D, Hendzel MJ, Poirier GG (2006) Dynamic relocation of poly(ADP-ribose) glycohydrolase isoforms during radiation-induced DNA damage. Biochim Biophys Acta 1763:226-237.
Haince JF, Kozlov S, Dawson VL, Dawson TM, Hendzel MJ, Lavin MF, Poirier GG (2007) Ataxia telangiectasia mutated (ATM) signaling network is modulated by a novel poly(ADP-ribose)-dependent pathway in the early response to DNA-damaging agents. J Biol Chem 282:16441-16453.
Hanai S, Kanai M, Ohashi S, Okamoto K, Yamada M, Takahashi H, Miwa M (2004) Loss of poly(ADP-ribose) glycohydrolase causes progressive neurodegeneration in Drosophila melanogaster. Proc Natl Acad Sci USA 101:82-86.
Hashida SN, Takahashi H, Uchimiya H (2009) The role of NAD biosynthesis in plant development and stress responses. Ann Bot (Lond) 103:819-824.
Hassa PO, Hottiger MO (2008) The diverse biological roles of mammalian PARPs, a small but powerful family of poly-ADP-ribose polymerases. Front Biosci 13: 3046-3082.
Heeres JT and Hergenrother PJ (2007) Poly(ADP-ribose) makes a date with death. Curr Opin Chem Biol 11:644-653.
Heese A, Hann DR, Gimenez-Ibanez S, Jones AM, He K, Li J, Schroeder JI, Peck SC, Rathjen JP (2007) The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc Natl Acad Sci USA 104:12217-12222.
Hong JK, Hwang BK (2005) Induction of enhanced disease resistance and oxidative stress tolerance by complemention of pepper basic PR-1 gene in Arabidopsis. Physiol Plantarum 124:267-277.
Horvath EM, Szabo C (2007) Poly(ADP-ribose) polymerase as a drug target for cardiovascular disease and cancer: an update. Drug News Perspect 20:171-181.
Hunt L, Lerner F, Ziegler M (2004) NAD-new roles in signalling and gene regulation in plants. New Phytol 163:31-44.
Ishikawa K, Ogawa T, Hirosue E, Nakayama Y, Harada K, Fukusaki E, Yoshimura K, Shigeoka S (2009) Modulation of the poly(ADP-ribosyl)ation reaction via the Arabidopsis ADP-ribose/NADH pyrophosphohydrolase, AtNUDX7, is involved in the response to oxidative stress. Plant Physiol 151:741-754.
Jabs T (1999) Reactive oxygen intermediates as mediators of programmed cell death in plants and animals. Biochem Pharmacol 57:231-245.
Jagtap P and Szabo C (2005) Poly(ADP-ribose) polymerase and the therapeutic effects of its inhibitors. Nat Rev Drug Discov 4:421-440.
Jambunathan, N., and Mahalingam, R.2006. Analysis of Arabidopsis growth factor gene 1(GFG1) encoding a nudix hydrolase during oxidative signaling. Planta 224:1-11.
Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323-29.
Kabbage M, Dickman MB (2008) The BAG proteins:a ubiquitous family of chaperone regulators. Cell Mol Life Sci 65:1390-1402.
van Kan JAL (2006) Licensed to kill:The lifestyle of a necrotrophic plant pathogen. Trends Plant Sci 11:247-253.
Kang CH, Jung WY, Kang YH, Kim JY, Kim DG, Jeong JC, Baek DW, Jin JB, Lee JY, Kim MO, Chung WS, Mengiste T, Koiwa H, Kwak SS, Bahk JD, Lee SY, Nam JS, Yun DJ, Cho MJ (2006) AtBAG6, a novel calmodulin-binding protein, induces programmed cell death in yeast and plants. Cell Death Differ 13:84-95.
Katagirl F, Thilmony, He SY (2002) The Arabidopsis Thaliana-Pseudomonas Syringae Interaction. The Arabidopsis Book, doi:10.1199/tab.0039.
Kendrick MD, Chang C (2008) Ethylene signaling:new levels of complexity and regulation. Curr Opin Plant Biol 11:479-485.
Kersten B, Agrawal G.K, Iwahashi H, Rakwal R (2006) Plant phosphoproteomics:a long road ahead. Proteomics,6,5517-5528.
Kim MY, Zhang T, Kraus WL (2005) Poly(ADP-ribosyl)ation by PARP-1: 'PAR-laying' NAD+ into a nuclear signal. Genes Dev 19:1951-1967.
Koh DW, Lawler AM, Poitras MF, Sasaki M, Wattler S, Nehls MC, Stoger T, Poirier GG, Dawson VL, Dawson TM (2004) Failure to degrade poly(ADP-ribose) causes increased sensitivity to cytotoxicity and early embryonic lethality. Proc Natl Acad Sci USA 101:17699-17704.
Kolisek M, Beck A, Fleig A and Penner R (2005) Cyclic ADPribose and hydrogen peroxide synergize with ADP-ribose in the activation of TRPM2 channels. Mol Cell 18,61-69.
Kraus WL (2008) Transcriptional control by PARP-1:chromatin modulation, enhancer-binding, coregulation, and insulation. Curr Opin Cell Biol 20:294-302.
Kraus WL, Lis J (2003) PARP goes transcription. Cell 113:677-683.
Kunkel BN, Brooks DV (2002) Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol 5:325-331.
Lam E (2004) Controlled cell death, plant survival and development. Nat Rev Mol Cell Bio 5:305-315.
Laxalt AM and Munnik T (2002) Phospholipid signalling in plant defence. Curr Opin Plant Biol 5:332-333.
Leitner M, Vandelle E, Gaupels F, Bellin D, Delledonne M (2009) NO signals in the haze Nitric oxide signalling in plant defence. Curr Opin Plant Biol 12:451-458.
Li S, Assmann SM, Albert R (2006) Predicting essential components of signal transduction networks:A dynamic model of guard cell abscisic acid signaling. PLoS Biol 4:e312.
Liu Y and Zhang S (2004) Phosphorylation of 1-aminocyclopropane-l-carboxylic acid synthase by MPK6, a stress-responsive mitogen-activated protein kinase, induces ethylene biosynthesis in Arabidopsis. Plant Cell 16:3386-3399.
van Loon LC, Rep M, Pieterse CMJ (2006) Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44:135-162.
Lorenzo O, Solano R.2005. Molecular players regulating the jasmonate signalling network. Curr Opin Plant Bio 8:532-540.
Lucas JA (1998) Plant pathology and plant pathogens. Blackwell Science, Oxford, UK (Malden, MA, USA).
Ludwig AA, Saitoh H, Felix G, Freymark G, Miersch O, Wasternack C, Boller T, Jones JDG and Romeis T (2005) Ethylene-mediated cross-talk between calcium-dependent protein kinase and MAPK signaling controls stress responses in plants. Proc Natl Acad Sci USA 102:10736-10741.
Malanga M, Althaus FR (2005) The role of poly(ADP-ribose) in the DNA damage signaling network. Biochem Cell Biol 83:354-364.
Martin GB, Bogdanove AJ, Sessa G (2003) Understanding the functions of plant disease resistance proteins. Annu Rev Plant Biol 54:23-61.
Masson M, Niedergang C, Schreiber V, Muller S, Menissier-de Murcia J, de Murcia G (1998) XRCC1 is specifically associated with poly(ADP-ribose) polymerase and negatively regulates its activity following DNA damage. Mol Cell Biol 18: 3563-3571.
McDowell JM, Dangl JL (2000) Signal transduction in the plant immune response. Trends Biochem Sci 25:79-82.
Mengiste T, Chen X, Salmeron J, Dietrich R (2003) The BOTRYTIS SUSCEPTIBLEl gene encodes an R2R3MYB transcription factor protein that is required for biotic and abiotic stress responses in Arabidopsis. Plant Cell 15:2551-2565.
Menke FLH, Kang HG, Chen Z, Jeong MP, Kumar D and Klessig DF (2005) Tobacco transcription factor WRKY1 is phosphorylated by the MAP kinase SIPK and mediates HR-like cell death in tobacco. Mol Plant-Microbe Interact 18: 1027-1034.
Meyer-Ficca ML, Meyer RG, Coyle DL, Jacobson EL, Jacobson MK (2004) Human poly(ADP-ribose) glycohydrolase is expressed in alternative splice variants yielding isoforms that localize to different cell compartments. Exp Cell Res 297: 521-532.
Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) The reactive oxygen gene network of plants. Trends Plant Sci 9:490-498.
Modjtahedi N, Giordanetto F, Frank M Kroemer G (2006) Apoptosis-inducing factor: vital and lethal. Trends Cell Biol 16:264-272.
Moore T, Martineau B, Bostock RM, Lincoln JE and Gilchrist GD (1999) Molecular and genetic characterization of ethylene involvement in mycotoxins-induced plant cell death. Physiol Mol Plant Pathol 54:73-85.
Mur LA, Kenton P, Atzorn R, Miersch O Wasternack C (2006) The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiol 140:249-266.
Nimchuk Z, Eulgem T, Holt BE, Dangl JL (2003) Recognition and response in the plant immune system. Annu Rev Genet 37:579-609.
Oei SL, Keil C, Ziegler M (2005) Poly(ADP-ribosylation) and genomic stability. Biochem Cell Biol 83:263-269.
O'Farrell M (1995) ADP-ribosylation reactions in plants. Biochimie 77:486-491.
Ogawa T, Ishikawa K, Harada K, Fukusaki E, Yoshimura K, Shigeoka S (2009) Overexpression of an ADP-ribose pyrophosphatase, AtNUDX2, confers enhanced tolerance to oxidative stress in Arabidopsis plants. Plant J 57: 289-301.
Ogawa T, Ueda Y, Yoshimura K, Shigeoka S (2005) Comprehensive analysis of cytosolic Nudix hydrolases in Arabidopsis thaliana. J Biol Chem 280: 25277-25283.
Ohashi S, Kanai M, Hanai S, Uchiumi F, Maruta H, Tanuma S, Miwa M (2003) Subcellular localization of poly(ADP-ribose) glycohydrolase in mammalian cells. Biochem Biophys Res Commun 307:915-921.
Oirdi ME and Bouarab K (2007) Plant signalling components EDS1 and SGT1 enhance disease caused by the necrotrophic pathogen Botrytis cinerea. New Phytologist 175:131-139.
Oka S, Kato J, Moss J (2006) Identification and characterization of a mammalian 39-kDa Poly(ADP-ribose) glycohydrolase. JBiol Chem 281:705-713.
Olejnik K, Kraszewska E (2005) Cloning and characterization of an Arabidopsis thaliana Nudix hydrolase homologous to the mammalian GFG protein. Biochim Biophys Acta 1752:133-141.
Otto H, Reche PA, Bazan F, Dittmar K, Haag F, Koch-Nolte F (2005) In silico characterization of the family of PARP-like poly(ADP-ribosyl)transferases (pARTs). BMC Genomics 6:139.
Palmgren MG (2001) Plant plasme membrane H+-ATPases:powerhouses for nutrient uptake. Annu Rev Plant Physiol Plant Mol Biol 52:817-845.
Panda S, Poirier GG, Kay SA (2002) tej defines a role for poly(ADP-ribosyl)ation in establishing period length of the Arabidopsis circadian oscillator. Dev Cell 3: 51-61.
Patel NS, Cortes U, Di Poala R, Mazzon E, Mota-Filipe H, Cuzzocrea S, Wang ZQ, Thiemermann C (2005) Mice lacking the 110-kDa isoform of poly(ADP-ribose) glycohydrolase are protected against renal ischemia/reperfusion injury. J Am Soc Nephrol 16:712-719.
Pedley KF and Martin GB (2005) Role of mitogen-activated protein kinases in plant immunity. Curr Opin Plant Biol 8:541.
Perraud AL, Takanishi CL, Shen B, Kang S, Smith MK, Schmitz C, Knowles HM, Ferraris D, Li W, Zhang J, Stoddard BL, Scharenberg AM (2005) Accumulation of free ADP-ribose from mitochondria mediates oxidative stressinduced gating of TRPM2 cation channels. JBiol Chem 280:6138-6148.
Petrucco S (2003) Sensing DNA damage by PARP-like fingers. Nucleic Acids Res 31: 6689-6699.
Pitzschke A, Schikora A, Hirt H (2009) MAPK cascade signalling networks in plant defence. Curr Opin Plant Biol 12:421-426.
Pleschke JM, Kleczkowska HE, Strohm M, Althaus FR (2000) Poly(ADPribose) binds to specific domains in DNA damage checkpoint proteins. J Biol Chem 275: 40974-40980.
del Pozo O, Lam E.1998. Caspases and programmed cell death in the hypersensitive response of plants to pathogens. Current Biology 8:1129-1132.
del Pozo O, Lam E.2003. Expression of the baculovirus p35 protein in tobacco affects cell death progression and compromises N gene-mediated disease resistance response to Tobacco mosaic virus. Mole Plant-Microbe Interact 16: 485-494.
Qin F, Sakuma Y, Tran LS, Maruyama K, Kikodoro S, Fujita Y, Fujita M, Sawano Y, Miyazono K, Tanokura M, Shinozaki K, Yamaguchi-Shinozaki K (2008) Arabidopsis DREB2A-interacting proteins function as RING E3 ligases and negatively regulate plant drought stress-responsive gene expression. Plant Cell 20:1693-1707.
Qiu JL, Fiil BK, Petersen K, Nielsen HB, Botanga CJ, Thorgrimsen S, Palma K, Suarez-Rodriguez MC, Sandbech-Clausen S, Lichota J, Brodersen P, Grasser KD, Mattsson O, Glazebrook J, Mundy J, Petersen M (2008) Arabidopsis MAP kinase 4 regulates gene expression through transcription factor release in the nucleus. EMBO J 27:2214-2221.
Ratcliff F, Martin-Hernandez AM, Baulcombe DC (2001) Technical Advance. Tobacco rattle virus as a vector for analysis of gene function by silencing. Plant J25:237-245.
Robatzek S, Chinchilla D and Boller T (2006) Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev 20:537-542.
Roldan-Arjona T, Ariza RR (2009) Repair and tolerance of oxidative DNA damage in plants. Mutat Res 681:169-179.
Rongvaux A, Andris F, Van Gool F, Leo O (2003) Reconstructing eukaryotic NAD metabolism. BioEssays 25:683-690.
Rossi R, Montecucco A, Donzelli M, Denegri M, Biamonti G, Scovassi A (2002) DNA ligase I is dephosphorylated during the execution step of etoposide-induced apoptosis. Cell Death Differ 9:89-90.
Rouleau M, Aubin RA, Poirier GG (2004) Poly(ADPribosyl)ated chromatin domains: access granted. J Cell Sci 117:815-825.
Ryals JA, Neuenschwander UH., Willits MG, Molina A, Steiner HY, Hunt MD (1996) Systemic acquired resistance. Plant Cell 8:1809-1819.
Sakuma Y, Maruyama K, Qin F, Osakabe Y, Shinozaki K, Yamaguchi-Shinozaki K (2006) Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc Natl Acad Sci USA 103:18822-18827.
Schenk P M, Kazan K, Wilson I, Anderson JP, Richmond T, Somerville SC, Manners JM (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc Natl Acad Sci USA 97:11655-11660.
Schreiber V, Dantzer F, Ame JC, de Murcia G (2006) Poly(ADP-ribose):novel functions for an old molecule. Nat Rev Mol Cell Biol 7:517-528.
Schreiber, V. et al. (2002) Poly(ADP-ribose) polymerase-2 (PARP-2) is required for efficient base excision DNA repair in association with PARP-1 and XRCC1. J Biol Chem 277:23028-23036.
Seki M, Umezawa T,Urano K, Shinozaki K (2007) Regulatory metabolic networks in drought stress responses. Curr Opin Plant Biol 10:296-302.
Shan L, He P, Li J, Heese A, Peck SC, Nurnberger T, Martin GB, Sheen J (2008) Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity. Cell Host Microbe 4:17-27.
Sheikh S, O'Handley SF, Dunn CA, Bessman MJ (1998) Identification and characterization of the Nudix hydrolase from the Archaeon, Methanococcus jannaschii, as a highly specific ADP-ribose pyrophosphatase. J Biol Chem 273: 20924-20928.
Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. JExp Bot 58:221-227.
Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6: 410-417.
Simbulan-Rosenthal CM, Rosenthal DS, Luo R, Smulson ME (1999) Poly(ADPribosyl)ation of p53 during apoptosis in human osteosarcoma cells. Cancer Res 59:2190-2194.
Sokolovski S and Blatt MR (2004) Nitric oxide block of outwardrectifying K+ channels indicates direct control by protein nitrosylation in guard cells. Plant Physiol 136:4275-4284.
St-Laurent JF, Gagnon SN, Dequen F, Hardy I, Desnoyers S (2007) Altered DNA damage response in Caenorhabditis elegans with impaired poly(ADP-ribose) glycohydrolases genes expression. DNA Rep 6:329-343.
Straus MR, Rietz S, van Themaat EV, Bartsch M, Parker JE (2010) Salicylic acid antagonism of EDS1-driven cell death is important for immune and oxidative stress responses in Arabidopsis. Plant J doi:10.1111/j.1365-313X.2010.04178.x
Stulemeijer IJ and Joosten MH (2008) Post-translational modification of host proteins in pathogen-triggered defence signalling in plants. Mole Plant Pathol 9:545-560.
Tanaka Y, Sano T, Tamaoki M, Nakajima N, Kondo N, Hasezawa S (2005) Ethylene inhibits abscisic acid-induced stomatal closure in Arabidopsis. Plant Physiol 138: 2337-2343.
Tatsuki M and Mori H (2001) Phosphorylation of tomato 1-aminocyclopropane-1-carboxylic acid synthase, LE-ACS2, at the Cterminal region. JBiol Chem 276:28051-28057.
Testerink C and Munnik T (2005) Phosphatidic acid:A multifunctional stress signaling lipid in plants. Trends Plant Sci 10:368-375.
Tian R, Zhang GY, Yan CH, Dai YR (2000) Involvement of poly(ADP-ribose) polymerase and activation of caspase-3-like protease in heat shock-induced apoptosis in tobacco suspension cells. FEBS Lett 474:11-15.
Vanderauwera S, De Block M, Van de Steene N, van de Cotte B, Metzlaff M, Van Breusegem F (2007) Silencing of poly(ADP-ribose) polymerase in plants alters abiotic stress signal transduction. Proc Natl Acad Sci USA 104:15150-15155.
Van Wees SC, Van der Ent S, Pieterse CM (2008) Plant immune responses triggered by beneficial microbes. Curr Opin Plant Biol 11:443-448.
Veronese P, Nakagami H, Bluhm B, Abuqamar S, Chen X, Salmeron J, Dietrich R, Hirt H, Mengiste T (2006) The membrane-anchored BOTRYTIS-INDUCED KINASE1 plays distinct roles in Arabidopsis resistance to necrotrophic and biotrophic pathogens. Plant Cell 18:257-273.
Wang H, Li J, Bostock RM and Gilchrist DG (1996) Apoptosis:A functional paradigm for programmed plant cell death induced by a host-selective phytotoxin and invoked during development. Plant Cell 8,375-391.
Wang X, Kota U, He K, Blackburn K, Li J, Goshe MB, Huber SC, Clouse SD (2008) Sequential transphosphorylation of the BRI1/BAK1 receptor kinase complex impacts early events in brassinosteroid signaling. Dev Cell15:220-235.
Wang YS, Pi LY, Chen X, Chakrabarty PK, Jiang J, De Leon AL, Liu G.Z, Li A, Benny U, Oard J, Ronald PC and Song WY (2006) Rice XA21 binding protein 3 is a ubiquitin ligase required for full Xa21-mediated disease resistance. Plant Cell 18:3635-3646.
Wasilewska A, Vlad F, Sirichandra C, Redko Y, Jammes F, Valon C, Frei dit Frey N, Leung J (2008) An update on abscisic acid signaling in plants and more.... Mol Plant Ⅰ:198-217.
Watanabe N, Lam E (2006) Arabidopsis Bax inhibitor-1 functions as an attenuator of biotic and abiotic types of cell death. Plant J 45:884-894.
Watanabe N, Lam E (2008) BAX inhibitor-1 modulates endoplasmic reticulum stress-mediated programmed cell death in Arabidopsis. J Biol Chem 283: 3200-3210.
Watanabe N, Lam E (2009) Bax inhibitor-1, a conserved cell death suppressor, is a key molecular switch downstream from a variety of biotic and abiotic stress signals in plants. Int J Mol Sci 10:3149-3167.
Wilson ID, Neill SJ, Hancock JT (2008) Nitric oxide synthesis and signalling in plants. Plant Cell Environ 31:622-631.
Woon EC, Threadgill MD (2005) Poly(ADP-ribose)polymerase inhibition—where now? Curr Med Chem 12:2373-2392.
Woodhouse BC, Dianov GL (2008)Poly ADP-ribose polymerase-1:An international molecule of mystery. DNA repair 7:1077-1086.
Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14(Suppl):S165-S183.
Yamaguchi-Shinozaki K, Shinozaki K (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6:251-264.
Yoo SD, Cho YH, Tena G, Xiong Y, Sheen J (2008) Dual control of nuclear EIN3 by bifurcate MAPK cascades in C2H4 signalling. Nature 451:789-795.
Yu SW, Andrabi SA, Wang H, Kim NS, Poirier GG, Dawson TM, and. Dawson VL (2006) Apoptosis-inducing factor mediates poly(ADPribose) (PAR) polymer-induced cell death. Proc Natl Acad Sci USA 103:18314-18319.
Yu SW, Wang H, Poitras MF, Coombs C, Bowers WJ, Federoff HJ, Poirier GG, Dawson TM, Dawson VL (2002) Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science 297: 259-263.
Zeller G, Henz SR, Widmer CK, Sachsenberg T, Ratsch G, Weigel D, Laubinger S (2009) Stress-induced changes in the Arabidopsis thaliana transcriptome analyzed using whole-genome tiling arrays. Plant J 58:1068-1082
Ziegler M (2000) New functions of a long-known molecule:emerging roles of NAD in cellular signaling. Eur J Biochem 267:1550-1564.
Zhang T, Liu Y, Yang T, Zhang L, Xu S, Xue L and An L (2006) Diverse signals converge at MAPK cascades in plant. Plant Physiol Biochem 44:274-283.