小黑杨（Populus simonii×P.nigra）休眠顶芽的磷酸化和乙酰化蛋白质组学研究
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摘要
为了初步探索芽休眠的调控过程是否依赖磷酸化信号级联反应,以及Nα-乙酰化修饰在芽休眠的调控过程中可能的生物学意义,本文以杨树休眠顶芽为试材,应用nano-UPLC-MS/MS串联质谱结合磷酸化和乙酰化肽段富集的方法,进行了杨树休眠顶芽蛋白和核糖体P-蛋白的磷酸化蛋白质组研究,以及杨树休眠顶芽蛋白的乙酰化蛋白质组研究,分别得到了以下结论。
1.通过磷酸化蛋白质组鉴定和分析杨树休眠顶芽蛋白研究,鉴定了161个高信任值的磷酸化位点(131个pSer、28个pThr和2个pTyr),磷酸化共涉及到151个杨树蛋白。在这些磷酸化事件中,大部分磷酸化位点相对保守,表明依赖磷酸化的调控机制在杨树和拟南芥间是相对保守的；仅34个位点不保守,表明与草本植物相比其特有的依赖磷酸化调控机制也可能存在。应用Motif-X程序,获得四个显著富集的磷酸化基序,分别是脯氨酸引导的蛋白激酶(proline-directed protein kinase, PDPK)底物基序、未知磷酸化基序、酪氨酸激酶Ⅱ(casein kinases II, CK2)底物基序和14-3-3结合基序,该结果显示在杨树休眠期间PDPK和CK2应该是负责这些杨树蛋白磷酸化的主要蛋白激酶。此外,在杨树中还发现一些磷酸化蛋白与目前已知在其它植物物种中鉴定到的休眠相关候选基因产物同源,暗示了这些蛋白的磷酸化与休眠调控的相关性。这些结果将为未来理解和揭示杨树磷酸化调控顶芽休眠机理提供丰富的数据资源,也为人们提供了一个新的视角去探索木本植物休眠调控机理。
2.通过磷酸化蛋白质组鉴定和分析杨树休眠顶芽核糖体P-蛋白研究,相对完整地获得了休眠期间顶芽被修饰的全部磷酸化P-蛋白的状态。总共鉴定了5个Ser和1个Thr磷酸化位点,涉及到全部10个P-蛋白中的8个(2P0,2P1,3P2和1P3),且这些磷酸化都发生在它们保守的C-末端,表明休眠期间蛋白质的合成过程可能要通过磷酸化修饰大部分核糖体P-蛋白的C-末端来调控。序列分析显示发生在Ptr RPP2AC-末端的Thr磷酸化位点专门存在于木本植物的P2蛋白,同时此位点也被证明是新的磷酸化位点。鉴定的位于C-末端的全部磷酸化肽段具有一致的磷酸化基序(S/T)XX(D/E),且完好地与酪氨酸激酶Ⅱ(casein kinases II, CK2)底物基序相匹配,表明P-蛋白C-末端的磷酸化全部由CK2所介导。此外,进化分析显示P2蛋白的分歧(类型Ⅰ和Ⅱ)也出现在木本植物杨树中,此结果支持了目前P2蛋白具有分歧的学术观点。据了解,这是第一篇系统的表征木本植物P-蛋白磷酸化蛋白质组,此结果将为未来理解和揭示杨树P-蛋白磷酸化调控机理提供丰富的数据资源。
3.通过乙酰化蛋白质组鉴定和分析杨树休眠顶芽蛋白研究,共鉴定了51个高信任值的乙酰化位点,涉及到58个杨树Nα-乙酰化蛋白。它们的大部分(47,>81%)属于组(ii)依赖NME的Nα-乙酰化类型,其余小部分(11,～19%)属于组(i)非依赖NME的Nα-乙酰化类型,此类现象表明Na-乙酰化和NME代表了杨树蛋白普遍发生的NPM。全基因组鉴定和分析揭示,与拟南芥、酵母及人类等真核生物相类似,杨树基因组编码全部两种类型的MetAP, MetAP2s (Ptr MetAP2A和2B),MetAPls (Ptr MetAP1A-E),且杨树的Ptr MetAP1E在进化上与其它MetAP1s仍具一定的分歧,故将其考虑作为新的MetAP1s家族成员。TargetP亚细胞定位预测发现杨树的2个Ptr MetAP2s (Ptr MetAP2A和Ptr MetAP2B)专门定位到细胞质,而PtrMetAP1s既定位到细胞器(PtrMetAP1B-E)也定位到细胞质(PtrMetAP1A)。由于经历NME的全部组(ii)47个乙酰化蛋白均定位在细胞质,因此这些NME应该是由细胞质定位的杨树MetAPs (PtrMetAP1A, PtrMetAP2A和PtrMetAP2B)成员所介导。同时值得注意的是,这些经历NME的蛋白在位置2上的氨基酸完全被Ala(25/47),Ser(13/47),Gly(7/47),Thr(1/47)和Vla(1/47)残基占据,这些残基完全遵循真核生物蛋白普遍的NME规则。此外,全基因组鉴定和分析还揭示,杨树与拟南芥、酵母及人类具一致的Nats类酶系统,其基因组具编码全部Nats六个类型的所有催化和辅亚基基因。然而,也发现杨树的大部分类型的Nat催化亚基具备两个旁系同源异构体,相比之下,拟南芥、酵母及人类很少有这样的现象发生,此证据表明杨树中编码完整类型Nat催化亚基的基因是相对扩展的。基于全部Nats类型的所有催化和辅亚基的亚细胞定位信息,再结合乙酰化底物谱的分析结果揭示,在鉴定的58个乙酰化蛋白中,81%(47)蛋白乙酰化由杨树细胞质型的NatA异构体负责,其余的主要由细胞质型的NatB异构体负责乙酰化。总之,杨树与拟南芥、酵母及人类具一致的NME规则及Nat类型系统,表明包含杨树在内的真核生物具类似的NPM。此方法适合同时鉴定大量蛋白的乙酰化位点信息。此特异性位点乙酰化修饰数据将为进一步揭示杨树乙酰化蛋白功能提供了丰富的数据资源。据了解,这是第一次广泛调查木本植物蛋白Na-乙酰化的研究。然而在杨树休眠期间鉴定每个乙酰化蛋白的特定功能仍是当前所面临的挑战。
Although there has been considerable progress made towards understanding the molecular mechanisms of bud dormancy, the roles of protein phosphorylation in the process of dormancy regulation in woody plants remain unclear. We used mass spectrometry combined with TiO2phosphopeptide-enrichment strategies to investigate the phosphoproteome of dormant terminal buds (DTBs) in poplar(Populus simonii×P. nigra). There were161unique phosphorylated sites in161phosphopeptides from151proteins;141proteins have orthologs in Arabidopsis, and10proteins are unique to poplar. Only34sites in proteins in poplar did not match well with the equivalent phosphorylation sites of their orthologs in Arabidopsis, indicating that regulatory mechanisms are well conserved between poplar and Arabidopsis. Further functional classifications showed that most of these phosphoproteins were involved in binding and catalytic activity. Extraction of the phosphorylation motif using Motif-X indicated that proline-directed kinases are a major kinase group involved in protein phosphorylation in dormant poplar tissues. This study provides evidence about the significance of protein phosphorylation during dormancy, and will be useful for similar studies on other woody plants.
To better understand the role that reversible phosphorylation plays in woody plant ribosomal P-protein function, we initiated a phosphoproteomic investigation of P-proteins from Populus dormant terminal buds. Using gel-free (in-solution) protein digestion and phosphopeptide enrichment combined with a nanoUPLC-ESI-MS/MS strategy, we identified six phosphorylation sites on eight P-proteins from Populus dormant terminal buds. Among these, six Ser sites and one Thr site were identified in the highly conserved C-terminal region of eight P-proteins of various P-protein subfamilies, including two P0, two P1, three P2, and one P3protein. Among these, the Thr site was shown to be novel and has not been identified in any other organisms. Sequence analysis indicated that the phosphothreonine sites identified in the C-terminus of Ptr RPP2A exclusively occurred in woody species of Populus etc. The identified phosphopeptides shared a common phosphorylation motif of (S/T)XX(D/E) and may be phosphorylated in vivo by casein kinase2as suggested by using Scansite analysis. Furthermore, phylogenetic analysis suggested that divergence of P2also occurred in Populus, including Type Ⅰ and Type Ⅱ. To the best of our knowledge, this is the first systematic phosphoproteomic and phylogenetic analysis of P-proteins in woody plants, the results of which will provide a wealth of resources for future understanding and unraveling of the regulatory mechanisms of Populus P-protein phosphorylation during the maintenance of dormancy.
The N-terminal protein processing mechanism (NPM) represents a common protein modification process of eukaryotes, and involves the co-translational processes of N-terminal Met excision (NME) and N-terminal acetylation (Nα-acetylation). To reveal the NPM in poplar, we investigated the Nα-acetylation status of poplar proteins during dormancy by combining tandem mass spectrometry with TO2enrichment of acetylated peptides. We identified58N-terminally acetylated (Nα-acetylated) proteins. Most proteins (47,>81%) are subjected to Nα-acetylation following the N-terminal removal of Met, indicating that Nα-acetylation and NME could represent a common NPM of poplar proteins. Based on N-terminal features of these acetylated proteins, the NME in poplar was found to be similar to the NME process observed in yeast and humans. The poplar genome encodes cytosolic or organelle-targeted methionine aminopeptidase (MetAP), and NME of these identified poplar proteins is mediated by three cytosolic poplar MetAPs (PtrMetAP1A, PtrMetAP2A and PtrMetAP2B). A novel member of MetAP1s was identified and named Ptr MetAP1E because of its divergence with other known MetAP1s. We found that poplar possessed the entire N-terminal acetyltransferase (Nat) system composed of six Nats (NatA-F), however, one extended Nat system was also found in poplar, probably arising from multiple gene duplication events. Based on a comparison of these recognized substrate motifs of Nats found in yeast and humans with our extraction of substrate motifs, we predict that NatA and NatB represent the major Nats that acetylate the identified poplar proteins. This result reveals that poplar possesses analogous NPMs to those observed in eukaryotes.
1.通过磷酸化蛋白质组鉴定和分析杨树休眠顶芽蛋白研究,鉴定了161个高信任值的磷酸化位点(131个pSer、28个pThr和2个pTyr),磷酸化共涉及到151个杨树蛋白。在这些磷酸化事件中,大部分磷酸化位点相对保守,表明依赖磷酸化的调控机制在杨树和拟南芥间是相对保守的；仅34个位点不保守,表明与草本植物相比其特有的依赖磷酸化调控机制也可能存在。应用Motif-X程序,获得四个显著富集的磷酸化基序,分别是脯氨酸引导的蛋白激酶(proline-directed protein kinase, PDPK)底物基序、未知磷酸化基序、酪氨酸激酶Ⅱ(casein kinases II, CK2)底物基序和14-3-3结合基序,该结果显示在杨树休眠期间PDPK和CK2应该是负责这些杨树蛋白磷酸化的主要蛋白激酶。此外,在杨树中还发现一些磷酸化蛋白与目前已知在其它植物物种中鉴定到的休眠相关候选基因产物同源,暗示了这些蛋白的磷酸化与休眠调控的相关性。这些结果将为未来理解和揭示杨树磷酸化调控顶芽休眠机理提供丰富的数据资源,也为人们提供了一个新的视角去探索木本植物休眠调控机理。
2.通过磷酸化蛋白质组鉴定和分析杨树休眠顶芽核糖体P-蛋白研究,相对完整地获得了休眠期间顶芽被修饰的全部磷酸化P-蛋白的状态。总共鉴定了5个Ser和1个Thr磷酸化位点,涉及到全部10个P-蛋白中的8个(2P0,2P1,3P2和1P3),且这些磷酸化都发生在它们保守的C-末端,表明休眠期间蛋白质的合成过程可能要通过磷酸化修饰大部分核糖体P-蛋白的C-末端来调控。序列分析显示发生在Ptr RPP2AC-末端的Thr磷酸化位点专门存在于木本植物的P2蛋白,同时此位点也被证明是新的磷酸化位点。鉴定的位于C-末端的全部磷酸化肽段具有一致的磷酸化基序(S/T)XX(D/E),且完好地与酪氨酸激酶Ⅱ(casein kinases II, CK2)底物基序相匹配,表明P-蛋白C-末端的磷酸化全部由CK2所介导。此外,进化分析显示P2蛋白的分歧(类型Ⅰ和Ⅱ)也出现在木本植物杨树中,此结果支持了目前P2蛋白具有分歧的学术观点。据了解,这是第一篇系统的表征木本植物P-蛋白磷酸化蛋白质组,此结果将为未来理解和揭示杨树P-蛋白磷酸化调控机理提供丰富的数据资源。
3.通过乙酰化蛋白质组鉴定和分析杨树休眠顶芽蛋白研究,共鉴定了51个高信任值的乙酰化位点,涉及到58个杨树Nα-乙酰化蛋白。它们的大部分(47,>81%)属于组(ii)依赖NME的Nα-乙酰化类型,其余小部分(11,～19%)属于组(i)非依赖NME的Nα-乙酰化类型,此类现象表明Na-乙酰化和NME代表了杨树蛋白普遍发生的NPM。全基因组鉴定和分析揭示,与拟南芥、酵母及人类等真核生物相类似,杨树基因组编码全部两种类型的MetAP, MetAP2s (Ptr MetAP2A和2B),MetAPls (Ptr MetAP1A-E),且杨树的Ptr MetAP1E在进化上与其它MetAP1s仍具一定的分歧,故将其考虑作为新的MetAP1s家族成员。TargetP亚细胞定位预测发现杨树的2个Ptr MetAP2s (Ptr MetAP2A和Ptr MetAP2B)专门定位到细胞质,而PtrMetAP1s既定位到细胞器(PtrMetAP1B-E)也定位到细胞质(PtrMetAP1A)。由于经历NME的全部组(ii)47个乙酰化蛋白均定位在细胞质,因此这些NME应该是由细胞质定位的杨树MetAPs (PtrMetAP1A, PtrMetAP2A和PtrMetAP2B)成员所介导。同时值得注意的是,这些经历NME的蛋白在位置2上的氨基酸完全被Ala(25/47),Ser(13/47),Gly(7/47),Thr(1/47)和Vla(1/47)残基占据,这些残基完全遵循真核生物蛋白普遍的NME规则。此外,全基因组鉴定和分析还揭示,杨树与拟南芥、酵母及人类具一致的Nats类酶系统,其基因组具编码全部Nats六个类型的所有催化和辅亚基基因。然而,也发现杨树的大部分类型的Nat催化亚基具备两个旁系同源异构体,相比之下,拟南芥、酵母及人类很少有这样的现象发生,此证据表明杨树中编码完整类型Nat催化亚基的基因是相对扩展的。基于全部Nats类型的所有催化和辅亚基的亚细胞定位信息,再结合乙酰化底物谱的分析结果揭示,在鉴定的58个乙酰化蛋白中,81%(47)蛋白乙酰化由杨树细胞质型的NatA异构体负责,其余的主要由细胞质型的NatB异构体负责乙酰化。总之,杨树与拟南芥、酵母及人类具一致的NME规则及Nat类型系统,表明包含杨树在内的真核生物具类似的NPM。此方法适合同时鉴定大量蛋白的乙酰化位点信息。此特异性位点乙酰化修饰数据将为进一步揭示杨树乙酰化蛋白功能提供了丰富的数据资源。据了解,这是第一次广泛调查木本植物蛋白Na-乙酰化的研究。然而在杨树休眠期间鉴定每个乙酰化蛋白的特定功能仍是当前所面临的挑战。
Although there has been considerable progress made towards understanding the molecular mechanisms of bud dormancy, the roles of protein phosphorylation in the process of dormancy regulation in woody plants remain unclear. We used mass spectrometry combined with TiO2phosphopeptide-enrichment strategies to investigate the phosphoproteome of dormant terminal buds (DTBs) in poplar(Populus simonii×P. nigra). There were161unique phosphorylated sites in161phosphopeptides from151proteins;141proteins have orthologs in Arabidopsis, and10proteins are unique to poplar. Only34sites in proteins in poplar did not match well with the equivalent phosphorylation sites of their orthologs in Arabidopsis, indicating that regulatory mechanisms are well conserved between poplar and Arabidopsis. Further functional classifications showed that most of these phosphoproteins were involved in binding and catalytic activity. Extraction of the phosphorylation motif using Motif-X indicated that proline-directed kinases are a major kinase group involved in protein phosphorylation in dormant poplar tissues. This study provides evidence about the significance of protein phosphorylation during dormancy, and will be useful for similar studies on other woody plants.
To better understand the role that reversible phosphorylation plays in woody plant ribosomal P-protein function, we initiated a phosphoproteomic investigation of P-proteins from Populus dormant terminal buds. Using gel-free (in-solution) protein digestion and phosphopeptide enrichment combined with a nanoUPLC-ESI-MS/MS strategy, we identified six phosphorylation sites on eight P-proteins from Populus dormant terminal buds. Among these, six Ser sites and one Thr site were identified in the highly conserved C-terminal region of eight P-proteins of various P-protein subfamilies, including two P0, two P1, three P2, and one P3protein. Among these, the Thr site was shown to be novel and has not been identified in any other organisms. Sequence analysis indicated that the phosphothreonine sites identified in the C-terminus of Ptr RPP2A exclusively occurred in woody species of Populus etc. The identified phosphopeptides shared a common phosphorylation motif of (S/T)XX(D/E) and may be phosphorylated in vivo by casein kinase2as suggested by using Scansite analysis. Furthermore, phylogenetic analysis suggested that divergence of P2also occurred in Populus, including Type Ⅰ and Type Ⅱ. To the best of our knowledge, this is the first systematic phosphoproteomic and phylogenetic analysis of P-proteins in woody plants, the results of which will provide a wealth of resources for future understanding and unraveling of the regulatory mechanisms of Populus P-protein phosphorylation during the maintenance of dormancy.
The N-terminal protein processing mechanism (NPM) represents a common protein modification process of eukaryotes, and involves the co-translational processes of N-terminal Met excision (NME) and N-terminal acetylation (Nα-acetylation). To reveal the NPM in poplar, we investigated the Nα-acetylation status of poplar proteins during dormancy by combining tandem mass spectrometry with TO2enrichment of acetylated peptides. We identified58N-terminally acetylated (Nα-acetylated) proteins. Most proteins (47,>81%) are subjected to Nα-acetylation following the N-terminal removal of Met, indicating that Nα-acetylation and NME could represent a common NPM of poplar proteins. Based on N-terminal features of these acetylated proteins, the NME in poplar was found to be similar to the NME process observed in yeast and humans. The poplar genome encodes cytosolic or organelle-targeted methionine aminopeptidase (MetAP), and NME of these identified poplar proteins is mediated by three cytosolic poplar MetAPs (PtrMetAP1A, PtrMetAP2A and PtrMetAP2B). A novel member of MetAP1s was identified and named Ptr MetAP1E because of its divergence with other known MetAP1s. We found that poplar possessed the entire N-terminal acetyltransferase (Nat) system composed of six Nats (NatA-F), however, one extended Nat system was also found in poplar, probably arising from multiple gene duplication events. Based on a comparison of these recognized substrate motifs of Nats found in yeast and humans with our extraction of substrate motifs, we predict that NatA and NatB represent the major Nats that acetylate the identified poplar proteins. This result reveals that poplar possesses analogous NPMs to those observed in eukaryotes.
引文
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