百脉根结瘤信号途径中相关调控蛋白的功能和作用机制的研究
|
摘要
氮素是自然界中1植物生长的最主要的限制因子之一。豆科植物与根瘤菌之间的根瘤共生(RNS, root nodule symbiosis)固氮系统是自然界中氮素最直接和经济的来源,在农业生产中具有十分重要的意义。然而,共生固氮具有宿主专一性,仅限于豆科植物和极个别非豆科植物,目前想通过遗传工程的方法实现重要谷类作物的共生固氮仍面临巨大的挑战,有待于共生固氮分子机理的进一步揭示。
根瘤的形成过程可分为根瘤菌侵染和根瘤器官发生两个复杂的过程。近十年来,以模式豆科植物苜蓿(Medicago truncatula)和百脉根(Lotus japonicus)为材料,在宿主植物中鉴定出一系列与共生相关的基因,初步建立了共生信号转导模式图。其中依赖钙和钙调素的蛋白激酶(CCaMK)和两个GRAS类转录因子(NSP1和NSP2)同时控制根瘤菌侵染和根瘤器官发生两个过程,并预测CCaMK、NSP1和NSP2形成复合体行使功能,但缺乏明确的生物化学和分子生物学证据。本论文以百脉根为材料,围绕CCaMK、NSP1和NSP2三个基因开展了以下三个方而的工作：
1.分别以CCaMK, CCaMK自磷酸化位点突变形式CCaMK (T265I)和蛋白激酶结构域CCaMK (1-300aa)为诱饵,筛选百脉根AD-cDNA酵母双杂交文库。其中以蛋白激酶结构域为诱饵鉴定到一个新蛋白,命名为CIP73 (CCaMK interacting protein of approximately 73 kDa)。CIP73开放阅读框包含2,076个核苷酸,编码的蛋白质由691个氨基酸残基组成,分子量约为73kD。蛋白质序列分析显示CIP73的N端含有一个和泛素(ubiquitin)同源的类似Scythe_N结构域的区域。只有当CCaMK的C端钙调素结合结构域和EF hand结构域去除后CCaMK才能与CIP73在酵母细胞中相互作用。进一步的缺失突变分析显示CCaMK的N端80个氨基酸(residues80-160)是与CIP73相互作用所必需的。虽然全长的CCaMK与CIP73在酵母细胞中没有检测到相互作用,但体外蛋白Pull-down和体内双分子荧光互补(BiFC)实验证明全长CCaMK与CIP73之间存在相互作用。通过半定量RT-PCR,检查了CIP73和CCaMK在百脉根不同器官中的表达情况。相对于茎和叶,CIP73和CCaMK在根中都大量表达,不同的是CIP73在根瘤中仅检测到微弱的表达,而CCaMK在根瘤中大量表达。接种了根瘤菌后CIP73的表达和CCaMK相似,有一个有明显的表达量下降的过程。CIP73的C端CIP73(486-691)与GFP的融合蛋白在洋葱表皮细胞和百脉根毛根细胞的细胞核中能检测到很强的荧光。更重要的是,在钙离子和钙调素存在的条件下,CCaMK在体外能够磷酸化CIP73的N端(1-413aa)区域。RNA干扰(RNAi)降低CIP73的表达能抑制结瘤,但对菌根共生没有明显的影响,表明CIP73在结瘤过程中行使重要功能。
2.百脉根CCaMK的自磷酸化位点突变后,在没有根瘤菌的情况下能形成自发根瘤。另一方面,水稻的CCaMK能够互补百脉根CCaMK失去功能的突变表型,并且水稻CCaMK突变影响菌根共生。为了研究CCaMK在水稻中的共生效应,分别构建了水稻和百脉根CCaMK的自磷酸化位点突变Os T263A和Lj T265I的超表达(双CaMV35S)和自身启动子表达载体,并转入水稻中,收获了T1代转基因种子。PCR扩增目标基因和GUS染色鉴定每个片段均有20多个阳性转基因系,但其共生效应还有待于进一步实验验证。
3.以NSP2的GRAS结构域为诱饵,在百脉根AD-cDNA酵母双杂交文库中鉴定到一个与NSP2相互作用的新蛋白,命名为IPN2 (Interacting Protein of NSP2)。IPN2开放阅读框包含1,074个核苷酸,编码的蛋白质由358个氨基酸残基组成,分子量约为40 kD。蛋白质序列分析显示IPN2的N端含有一个单个重复的MYB类结合DNA结构域和一个预测的coiled-coil结构域。在酵母中,NSP2的GRAS结构域是和IPN2相互作用所必需的,而IPN2的coiled-coil结构域是和NSP2相互作用所必需的。另外通过体外蛋白Pull-down和体内双分子荧光互补(BiFC)实验进一步证实了NSP2与IPN2之间的相互作用。而且,NSP2与IPN2共定位于百脉根毛根细胞的细胞核中。IPN2在酵母细胞中有很强的转录激活作用,并且能结合NIN的启动子。IPN2的mRNA在百脉根不同器官中广泛表达,并且其启动子在转基因毛根的韧皮部特异表达。IPN2的超表达能促进结瘤,而RNAi降低IPN2的表达则抑制结瘤,表明IPN2在结瘤过程中行使重要功能。
Nitrogen is one of the limiting factors required for plant growth. The root nodule symbiosis (RNS) between legume plants and rhizobia is the most efficient and productive source of fixed nitrogen, and has critical importance in agriculture. But this endosymbiosis is specific for host plant and is restricted to legume plants and occasionally some nonlegume plants. Engineering nitrogen-fixing cereals like rice, wheat or maize is a highly topic challenge, and more efforts will further be required to reveal the molecular mechanisms of nitrogen fixing.
The formation of nitrogen-fixing nodules requires the coordinated development of rhizobial infection and nodule organogenisis, which can be separated genetically. During the past decade, a lot of genes have been cloned from various symbiotic mutants of the two model legumes:Lotus japonicus and Medicago truncatula. A model of early symbiotic signaling cascade has been built based on these studies. Evidence is emerging that CCaMK, NSP1 and NSP2 form a complex on DNA, which need to be further confirmed. Here, we got some results as follows:
1. Using the kinase domain of CCaMK as a bait in yeast two-hybrid screening, we identify a novel protein, CIP73 (CCaMK interacting protein of approximately 73 kDa), that interacts with CCaMK. CIP73 contains a Scythe_N ubiquitin-like domain and belongs to the large ubiquitin superfamily. Deletion and mutagenesis analysis demonstrate that CIP73 could only interact with CCaMK when the calmodulin-binding domain and three EF hand motifs are removed from the kinase domain. The N terminus 80 amino acid residues (80-160) of CCaMK are required for interacting with CIP73 in yeast cells. On the other hand, protein pull down assay and BiFC assay in Nicotiana benthamiana show that the full-length CCaMK could interact with CIP73 in vitro and in planta. Importantly, CCaMK phosphorylates the N-terminus of CIP73 in a Ca2+/calmodulin dependent manner in vitro. CIP73 transcripts are preferentially expressed in roots, and very low expression is detected in leaves, stems and nodules. The expression in roots is significantly decreased after inoculation of Mesorhizobium loti. RNA interference (RNAi) knockdown of CIP 73 expression by hairy root transformation in Lotus japonicus led to decreased nodule formation, suggesting that CIP73 performed an essential role in nodulation.
2. In L. japonicus, snf1, a gain-of-function CCaMK (T265I) point mutation, which resides in the autophosphorylation site of the kinase domain, develops spontaneous nodules in the absence of rhizobia. The rice ortholog OsCCaMK mutant has defect in arbuscular mycorrhiza (AM) symbiosis. Moreover, molecular transfection of OsCCaMK could fully complement symbiosis defects in the corresponding Lotus mutant lines for both the AM and RN symbioses. To explore the symbiotic effects of CCaMK in rice, we transformed the OsCCaMK (T263A) or LjCCaMK (T265I) point mutation to rice, which was drived by the CaMV 35S or their native promoter respectively. The transgenic plants were identified by PCR amplification and GUS staining, but the symbiotic effects need to be further tested in the future.
3. Using yeast two-hybrid (Y2H) screening, we identified a novel MYB coiled-coil transcription factor, referred as IPN2, which interacts with NSP2 in Lotus japonicus. This interaction was confirmed by protein pull-down assay and BiFC assay in Nicotiana benthamiana. Moreover, IPN2 and NSP2 were co-localized in nuclei of L. japonicus hairy roots. The Y2H assay showed that the GRAS domain of NSP2 was required for interacting with IPN2, while the coiled-coil domain of IPN2 was necessary and sufficient for interacting with NSP2. IPN2 showed strong transcriptional activation activity in yeast cells, and it bound to the NIN promoter in vivo and in vitro. IPN2 was widely expressed in various organs, and showed phloem-specific expression within the vasculature of transgenic hairy roots. Overexpression of IPN2 promoted nodulation, while RNA interference (RNAi) knockdown of IPN2 expression led to decreased nodule formation in L. japonicus. Take together, our results strongly suggest that IPN2 plays an essential role in nodulation.
根瘤的形成过程可分为根瘤菌侵染和根瘤器官发生两个复杂的过程。近十年来,以模式豆科植物苜蓿(Medicago truncatula)和百脉根(Lotus japonicus)为材料,在宿主植物中鉴定出一系列与共生相关的基因,初步建立了共生信号转导模式图。其中依赖钙和钙调素的蛋白激酶(CCaMK)和两个GRAS类转录因子(NSP1和NSP2)同时控制根瘤菌侵染和根瘤器官发生两个过程,并预测CCaMK、NSP1和NSP2形成复合体行使功能,但缺乏明确的生物化学和分子生物学证据。本论文以百脉根为材料,围绕CCaMK、NSP1和NSP2三个基因开展了以下三个方而的工作：
1.分别以CCaMK, CCaMK自磷酸化位点突变形式CCaMK (T265I)和蛋白激酶结构域CCaMK (1-300aa)为诱饵,筛选百脉根AD-cDNA酵母双杂交文库。其中以蛋白激酶结构域为诱饵鉴定到一个新蛋白,命名为CIP73 (CCaMK interacting protein of approximately 73 kDa)。CIP73开放阅读框包含2,076个核苷酸,编码的蛋白质由691个氨基酸残基组成,分子量约为73kD。蛋白质序列分析显示CIP73的N端含有一个和泛素(ubiquitin)同源的类似Scythe_N结构域的区域。只有当CCaMK的C端钙调素结合结构域和EF hand结构域去除后CCaMK才能与CIP73在酵母细胞中相互作用。进一步的缺失突变分析显示CCaMK的N端80个氨基酸(residues80-160)是与CIP73相互作用所必需的。虽然全长的CCaMK与CIP73在酵母细胞中没有检测到相互作用,但体外蛋白Pull-down和体内双分子荧光互补(BiFC)实验证明全长CCaMK与CIP73之间存在相互作用。通过半定量RT-PCR,检查了CIP73和CCaMK在百脉根不同器官中的表达情况。相对于茎和叶,CIP73和CCaMK在根中都大量表达,不同的是CIP73在根瘤中仅检测到微弱的表达,而CCaMK在根瘤中大量表达。接种了根瘤菌后CIP73的表达和CCaMK相似,有一个有明显的表达量下降的过程。CIP73的C端CIP73(486-691)与GFP的融合蛋白在洋葱表皮细胞和百脉根毛根细胞的细胞核中能检测到很强的荧光。更重要的是,在钙离子和钙调素存在的条件下,CCaMK在体外能够磷酸化CIP73的N端(1-413aa)区域。RNA干扰(RNAi)降低CIP73的表达能抑制结瘤,但对菌根共生没有明显的影响,表明CIP73在结瘤过程中行使重要功能。
2.百脉根CCaMK的自磷酸化位点突变后,在没有根瘤菌的情况下能形成自发根瘤。另一方面,水稻的CCaMK能够互补百脉根CCaMK失去功能的突变表型,并且水稻CCaMK突变影响菌根共生。为了研究CCaMK在水稻中的共生效应,分别构建了水稻和百脉根CCaMK的自磷酸化位点突变Os T263A和Lj T265I的超表达(双CaMV35S)和自身启动子表达载体,并转入水稻中,收获了T1代转基因种子。PCR扩增目标基因和GUS染色鉴定每个片段均有20多个阳性转基因系,但其共生效应还有待于进一步实验验证。
3.以NSP2的GRAS结构域为诱饵,在百脉根AD-cDNA酵母双杂交文库中鉴定到一个与NSP2相互作用的新蛋白,命名为IPN2 (Interacting Protein of NSP2)。IPN2开放阅读框包含1,074个核苷酸,编码的蛋白质由358个氨基酸残基组成,分子量约为40 kD。蛋白质序列分析显示IPN2的N端含有一个单个重复的MYB类结合DNA结构域和一个预测的coiled-coil结构域。在酵母中,NSP2的GRAS结构域是和IPN2相互作用所必需的,而IPN2的coiled-coil结构域是和NSP2相互作用所必需的。另外通过体外蛋白Pull-down和体内双分子荧光互补(BiFC)实验进一步证实了NSP2与IPN2之间的相互作用。而且,NSP2与IPN2共定位于百脉根毛根细胞的细胞核中。IPN2在酵母细胞中有很强的转录激活作用,并且能结合NIN的启动子。IPN2的mRNA在百脉根不同器官中广泛表达,并且其启动子在转基因毛根的韧皮部特异表达。IPN2的超表达能促进结瘤,而RNAi降低IPN2的表达则抑制结瘤,表明IPN2在结瘤过程中行使重要功能。
Nitrogen is one of the limiting factors required for plant growth. The root nodule symbiosis (RNS) between legume plants and rhizobia is the most efficient and productive source of fixed nitrogen, and has critical importance in agriculture. But this endosymbiosis is specific for host plant and is restricted to legume plants and occasionally some nonlegume plants. Engineering nitrogen-fixing cereals like rice, wheat or maize is a highly topic challenge, and more efforts will further be required to reveal the molecular mechanisms of nitrogen fixing.
The formation of nitrogen-fixing nodules requires the coordinated development of rhizobial infection and nodule organogenisis, which can be separated genetically. During the past decade, a lot of genes have been cloned from various symbiotic mutants of the two model legumes:Lotus japonicus and Medicago truncatula. A model of early symbiotic signaling cascade has been built based on these studies. Evidence is emerging that CCaMK, NSP1 and NSP2 form a complex on DNA, which need to be further confirmed. Here, we got some results as follows:
1. Using the kinase domain of CCaMK as a bait in yeast two-hybrid screening, we identify a novel protein, CIP73 (CCaMK interacting protein of approximately 73 kDa), that interacts with CCaMK. CIP73 contains a Scythe_N ubiquitin-like domain and belongs to the large ubiquitin superfamily. Deletion and mutagenesis analysis demonstrate that CIP73 could only interact with CCaMK when the calmodulin-binding domain and three EF hand motifs are removed from the kinase domain. The N terminus 80 amino acid residues (80-160) of CCaMK are required for interacting with CIP73 in yeast cells. On the other hand, protein pull down assay and BiFC assay in Nicotiana benthamiana show that the full-length CCaMK could interact with CIP73 in vitro and in planta. Importantly, CCaMK phosphorylates the N-terminus of CIP73 in a Ca2+/calmodulin dependent manner in vitro. CIP73 transcripts are preferentially expressed in roots, and very low expression is detected in leaves, stems and nodules. The expression in roots is significantly decreased after inoculation of Mesorhizobium loti. RNA interference (RNAi) knockdown of CIP 73 expression by hairy root transformation in Lotus japonicus led to decreased nodule formation, suggesting that CIP73 performed an essential role in nodulation.
2. In L. japonicus, snf1, a gain-of-function CCaMK (T265I) point mutation, which resides in the autophosphorylation site of the kinase domain, develops spontaneous nodules in the absence of rhizobia. The rice ortholog OsCCaMK mutant has defect in arbuscular mycorrhiza (AM) symbiosis. Moreover, molecular transfection of OsCCaMK could fully complement symbiosis defects in the corresponding Lotus mutant lines for both the AM and RN symbioses. To explore the symbiotic effects of CCaMK in rice, we transformed the OsCCaMK (T263A) or LjCCaMK (T265I) point mutation to rice, which was drived by the CaMV 35S or their native promoter respectively. The transgenic plants were identified by PCR amplification and GUS staining, but the symbiotic effects need to be further tested in the future.
3. Using yeast two-hybrid (Y2H) screening, we identified a novel MYB coiled-coil transcription factor, referred as IPN2, which interacts with NSP2 in Lotus japonicus. This interaction was confirmed by protein pull-down assay and BiFC assay in Nicotiana benthamiana. Moreover, IPN2 and NSP2 were co-localized in nuclei of L. japonicus hairy roots. The Y2H assay showed that the GRAS domain of NSP2 was required for interacting with IPN2, while the coiled-coil domain of IPN2 was necessary and sufficient for interacting with NSP2. IPN2 showed strong transcriptional activation activity in yeast cells, and it bound to the NIN promoter in vivo and in vitro. IPN2 was widely expressed in various organs, and showed phloem-specific expression within the vasculature of transgenic hairy roots. Overexpression of IPN2 promoted nodulation, while RNA interference (RNAi) knockdown of IPN2 expression led to decreased nodule formation in L. japonicus. Take together, our results strongly suggest that IPN2 plays an essential role in nodulation.
引文
1. Amor B B, Shaw S L, Oldroyd G E, Mai I let F, Penmetsa R V, Cook D, Long S R, Denarie J and Gough C. The NFP locus of Medicago truncatula controls an early step of Nod factor signal transduction upstream of a rapid calcium flux and root hair deformation. Plant J,2003,34: 495-506.
2. Andriankaja A, Boisson-Dernier A, Frances L, Sauviac L, Jauneau A, Barker D G, and de Carvalho-Niebel F. AP2-ERF transcription factors mediate Nod factor dependent Mt ENOD11 activation in root hairs via a novel cis-regulatory motif. Plant Cell,2007,19:2866-2885.
3. Ane J M, Kiss G B, Riely B K, Penmetsa R V, Oldroyd G E, Ayax C, Levy J, Debelle F, Baek J M, Kalo P, Rosenberg C, Roe B A, Long S R, Denarie J, and Cook D R. Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science,2004,303:1364-1367.
4. Ardourel M, Demont N, Debelle F, Maillet F, de Billy F, Prome J C, Denarie J, and Truchet G. Rhizobium meliloti lipooligosaccharide nodulation factors:different structural requirements for bacterial entry into target root hair cells and induction of plant symbiotic developmental responses. Plant Cell,1994,6:1357-1374.
5. Arrighi J F, Barre A, Ben Amor B, Bersoult A, Soriano L C, Mirabella R, de Carvalho-Niebel F, Journet E P, Gherardi M, Huguet T, Geurts R, Denarie J, Rouge P, and Gough C. The Medicago truncatula lysin [corrected] motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiol,2006,142:265-279.
6. Asamizu E, Shimoda Y, Kouchi H, Tabata S, and Sato S. A positive regulatory role for LjERFl in the nodulation process is revealed by systematic analysis of nodule-associated transcription factors of Lotus japonicus. Plant Physiol,2008,147:2030-2040.
7. Banba M, Gutjahr C, Miyao A, Hirochika H, Paszkowski U, Kouchi H, and Imaizumi-Anraku H. Divergence of evolutionary ways among common sym genes:CASTOR and CCaMK show functional conservation between two symbiosis systems and constitute the root of a common signaling pathway. Plant Cell Physiol,2008,49:1659-1671.
8. Banerji J, Sands J, Strominger J L, and Spies T. A gene pair from the human major histocompatibility complex encodes large proline-rich proteins with multiple repeated motifs and a single ubiquitin-like domain. Proc Natl Acad Sci U S A,1990,87:2374-2378.
9. Baranowskij N, Frohberg C, Prat S, and Willmitzer L. A novel DNA binding protein with homology to Myb oncoproteins containing only one repeat can function as a transcriptional activator. EMBO J,1994,13:5383-5392.
10. Boisson-Dernier A, Chabaud M, Garcia F, Becard G, Rosenberg C and Barker D G. Agrobacterium rhizogenes-transformed roots of Medicago truncatula for the study of nitrogen-fixing and endomycorrhizal symbiotic associations. Mol Plant Microbe Interact,2001, 14:695-700.
11. Bolle C. The role of GRAS proteins in plant signal transduction and development. Planta,2004, 218:683-692.
12. Bonke M, Thitamadee S, Mahonen A P, Hauser M T, and Helariutta Y. APL regulates vascular tissue identity in Arabidopsis. Nature,2003,426:181-186.
13. Borisov A Y, Madsen L H, Tsyganov V E, Umehara Y, Voroshilova V A, Batagov A O, Sandal N, Mortensen A, Schauser L, Ellis N, Tikhonovich I A and Stougaard J. The Sym35 gene required for root nodule development in pea is an ortholog of Nin from Lotus japonicus. Plant Physiol, 2003,131:1009-1017.
14. Briarty L. The development of root nodule xylem transfer cells in Trifolium repens. Journal of Experimental Botany,1978,29:735.
15. Caetano-Anollcs G, and Gresshoff P M. Early induction of feedback regulatory responses governing nodulation in soybean. Plant Science,1990,71:69-81.
16. Caetano-Anolles G, and Gresshoff P M. Plant genetic control of nodulation. Annu Rev Microbiol, 1991,45:345-382.
17. Capoen W, Den Herder J, Sun J, Verplancke C, De Keyser A, De Rycke R, Goormachtig S, Oldroyd G E, Holsters M. Calcium spiking patterns and the role of the calcium/calmodulin-dependent kinase CCaMK in lateral root base nodulation of Sesbania rostrata. Plant Cell,2009,21 (5):1526-1540.
18. Carroll B J, McNeil D L, and Gresshoff P M. A Supernodulation and Nitrate-Tolerant Symbiotic (nts) Soybean Mutant. Plant Physiol,1985,78:34-40.
19. Catoira R, Galera C, de Billy F, Penmetsa R V, Journet E P, Maillet F, Rosenberg C, Cook D, Gough C and Denarie J. Four genes of Medicago truncatula controlling components of a nod factor transduction pathway. Plant Cell,2000,12:1647-1666.
20. Charpentier M, and Oldroyd G. How close are we to nitrogen-fixing cereals? Curr Opin Plant Biol,2010,13,556-564.
21. Chen C, Ane J M, and Zhu H. OsIPD3, an ortholog of the Medicago truncatula DMI3 interacting protein IPD3, is required for mycorrhizal symbiosis in rice. New Phytol,2008,180,311-315.
22. Chen C, Gao M, Liu J, and Zhu H. Fungal symbiosis in rice requires an ortholog of a legume common symbiosis gene encoding a Ca2+/calmodulin-dependent protein kinase. Plant Physiol, 2007,145,1619-1628.
23. Ciechanover A. The ubiquitin-proteasome pathway:on protein death and cell life. EMBOJ,1998, 17:7151-7160.
24. Combier J P, Frugier F, de Billy F, Boualem A, El-Yahyaoui F, Moreau S, Vernie T, Ott T, Gamas P, Crespi M, and Niebel A. MtHAP2-1 is a key transcriptional regulator of symbiotic nodule development regulated by microRNA169 in Medicago truncatula. Genes Dev,2006,20: 3084-3088.
25. Complainville A, Brocard L, Roberts I, Dax E, Sever N, Sauer N, Kondorosi A, Wolf S, Oparka K, and Crespi M. Nodule initiation involves the creation of a new symplasmic field in specific root cells of medicago species. Plant Cell,2003,15:2778-2791.
26. Corduan A, Lecomte S, Martin C, Michel D, and Desmots F. Sequential interplay between BAG6 and HSP70 upon heat shock. Cell Mol Life Sci,2009,66:1998-2004.
27. Crdenas L, Vidali L, Domnguez J, Prez H, Snchez F, Hepler P K and Quinto C. Rearrangement of actin microfilaments in plant root hairs responding to rhizobium etli nodulation signals. Plant Physiol,1998,116:871-877.
28. Cui H, Levesque M P, Vernoux T, Jung J W, Paquette A J, Gallagher K L, Wang J Y, Blilou I, Scheres B, and Benfey PN. An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science,2007,316:421-425.
29. de Lucas M, Daviere J M, Rodriguez-Falcon M, Pontin M, Iglesias-Pedraz J M, Lorrain S, Fankhauser C, Blazquez M A, Titarenko E, and Prat S. A molecular framework for light and gibberellin control of cell elongation. Nature,2008,451:480-484.
30. D'Haeze W and Holsters M. Nod factor structures, responses, and perception during initiation of nodule development. Glycobiology,2002,12:79R-105R.
31. Denarie J and Cullimore J. Lipo-oligosaccharide nodulation factors:a minireview new class of signaling molecules mediating recognition and morphogenesis. Cell,1993,74:951-954.
32. Desmots F, Russell H R, Lee Y, Boyd K, and McKinnon P J. The reaper-binding protein scythe modulates apoptosis and proliferation during mammalian development. Mol Cell Biol,2005,25: 10329-10337.
33. Ding Y, Kalo P, Yendrek C, Sun J, Liang Y, Marsh J F, Harris J M, and Oldroyd G E. Abscisic acid coordinates nod factor and cytokinin signaling during the regulation of nodulation in Medicago truncatula. Plant Cell,2008,20:2681-2695.
34. Ehrhardt D W, Atkinson E M and Long S R. Depolarization of alfalfa root hair membrane potential by Rhizobium meliloti Nod factors. Science,1992,256:998-1000.
35. Ehrhardt D W, Wais R and Long S R. Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell,1996,85:673-681.
36. Endre G, Kereszt A, Kevei Z, Mihacea S, Kalo P and Kiss G B. A receptor kinase gene regulating symbiotic nodule development. Nature,2002,417:962-966.
37. Felle H H, Kondorosi E, Kondorosi A, and Schultze M. Elevation of the cytosolic free [Ca2+] is indispensable for the transduction of the Nod factor signal in alfalfa. Plant Physiol,1999,121: 273-280.
38. Ferguson B J, Indrasumunar A, Hayashi S, Lin M H, Lin Y H, Reid D E, and Gresshoff P M. Molecular analysis of legume nodule development and autoregulation. J Integr Plant Biol,2010, 52:61-76.
39. Fisher R F and Long S R. Rhizobium--plant signal exchange. Nature,1992,357:655-660.
40. Foucher F, and Kondorosi E. Cell cycle regulation in the course of nodule organogenesis in Medicago. Plant Mol Biol,2000,43:773-786.
41. Frugier F, Kosuta S, Murray J D, Crespi M, and Szczyglowski K. Cytokinin:secret agent of symbiosis. Trends Plant Sci,2008,13:115-120.
42. Fukuzawa M, Zhukovskaya N V, Yamada Y, Araki T, and Williams J G. Regulation of Dictyostelium prestalk-specific gene expression by a SHAQKY family MYB transcription factor. Development,2006,133:1715-1724.
43. Gage D J. Infection and Invasion of Roots by Symbiotic, Nitrogen-Fixing Rhizobia during Nodulation of Temperate Legumes. Microbiology and Molecular Biology Reviews,2004,68: 280-300.
44. Gallagher K L, and Benfey P N. Both the conserved GRAS domain and nuclear localization are required for SHORT-ROOT movement. Plant J,2009,57:785-797.
45. Geurts R and Bisseling T. Rhizobium nod factor perception and signalling. Plant Cell,2002,14 Suppl:S239-249.
46. Geurts R, Fedorova E and Bisseling T. Nod factor signaling genes and their function in the early stages of Rhizobium infection. Curr Opin Plant Biol,2005,8:346-352.
47. Gherbi H, Markmann K, Svistoonoff S, Estevan J, Autran D, Giczey G, Auguy F, Peret B, Laplaze L, Franche C, Parniske M and Bogusz D. SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankiabacteria. Proc Natl Acad Sci U S A,2008,105:4928-4932.
48. Gietz R D, Schiestl R H, Willems A R, and Woods R A. Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast,1995,11:355-360.
49. Godfroy O, Debelle F, Timmers T, and Rosenberg C. A rice calcium-and calmodulin-dependent protein kinase restores nodulation to a legume mutant. Mol Plant Microbe Interact,2006,19: 495-501.
50. Gonzalez-Rizzo S, Crespi M and Frugier F. The Medicago truncatula CRE1 cytokinin receptor regulates lateral root development and early symbiotic interaction with Sinorhizobium meliloti. Plant Cell,2006,18:2680-269
51. Gronlund M, Roussis A, Flemetakis E, Quaedvlieg N E, Schlaman H R, Umehara Y, Katinakis P, Stougaard J and Spaink H P. Analysis of promoter activity of the early nodulin Enod40 in Lotus japonicus. Mol Plant Microbe Interact,2005,18:414-427.
52. Groth M, Takeda N, Perry J, Uchida H, Draxl S, Brachmann A, Sato S, Tabata S, Kawaguchi M, Wang T L, and Parniske M. NENA, a Lotus japonicus Homolog of Sec 13, Is Required for Rhizodermal Infection by Arbuscular Mycorrhiza Fungi and Rhizobia but Dispensable for Cortical Endosymbiotic Development. Plant Cell,2010,22:2509-2526.
53. Gutjahr C, Banba M, Crose V, An K, Miyao A, An G, Hirochika H, Imaizumi-Anraku H, and Paszkowski U. Arbuscular mycorrhiza-specific signaling in rice transcends the common symbiosis signaling pathway. Plant Cell,2008,20:2989-3005.
54. Hall L N, Rossini L, Cribb L, and Langdale J A. GOLDEN 2:a novel transcriptional regulator of cellular differentiation in the maize leaf. Plant Cell,1998,10:925-936.
55. Harper J F, Breton G, and Harmon A. Decoding Ca(2+) signals through plant protein kinases. Annu Rev Plant Biol,2004,55,263-288.
56. Harper J F and Harmon A. Plants, symbiosis and parasites:a calcium signalling connection. Nat Rev Mol Cell Biol,2005,6:555-566.
57. Hayashi T, Banba M, Shimoda Y, Kouchi H, Hayashi M, Imaizumi-Anraku H. A dominant function of CCaMK in intracellular accommodation of bacterial and fungal endosymbionts. Plant J,2010,63:141-154
58. Hazen S P, Schultz T F, Pruneda-Paz J L, Borevitz J O, Ecker J R, and Kay S A. LUX ARRHYTHMO encodes a Myb domain protein essential for circadian rhythms. Proc Natl Acad Sci USA,2005,102:10387-10392.
59. Heckmann A B, Lombardo F, Miwa H, Perry J A, Bunnewell S, Parniske M, Wang T L and Downie J A. Lotus japonicus nodulation requires two GRAS domain regulators, one of which is functionally conserved in a non-legume. Plant Physiol,2006,142:1739-1750.
60. Heidstra R and Bisseling T. Nod factor-induced host responses and mechanisms of Nod factor perception. New Phytol,1996,133:25-43.
61. Heidstra R, Geurts R, Franssen H, Spaink H P, Van Kammen A and Bisseling T. Root hair deformation activity of nodulation factors and their fate on Vicia sativa. Plant Physiol,1994,105: 787-797.
62. Higuchi R, Krummel B, and Saiki R K. A general method of in vitro preparation and specific mutagenesis of DNA fragments:study of protein and DNA interactions. Nucleic Acids Res,1998, 16:7351-7367.
63. Hirsch A M, Lum M R, and Downie J A. What makes the rhizobia-legume symbiosis so special? Plant Physiol,2001,127:1484-1492.
64. Hirsch S, Kim J, Munoz A, Heckmann A B, Downie J A, and Oldroyd G E. GRAS proteins form a DNA binding complex to induce gene expression during nodulation signaling in Medicago truncatula. Plant Cell,2009,21:545-557.
65. Ho S N, Hunt H D, Horton R M, Pullen J K, and Pease L R. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene,1989,77:51-59.
66. Horton P, Park K J, Obayashi T, Fujita N, Harada H, Adams-Collier C J, and Nakai K. WoLF PSORT:protein localization predictor. Nucleic Acids Res,2007,35:585-587.
67. Hosoda K, Imamura A, Katoh E, Hatta T, Tachiki M, Yamada H, Mizuno T, and Yamazaki T. Molecular structure of the GARP family of plant Myb-related DNA binding motifs of the Arabidopsis response regulators. Plant Cell,2002,14:2015-2029.
68. Hudmon A, and Schulman H. Neuronal Ca2+/calmodulin-dependent protein kinase Ⅱ:the role of structure and autoregulation in cellular function. Annu Rev Biochem,2002,71:473-510.
69. Imaizumi-Anraku H, Takeda N, Charpentier M, Perry J, Miwa H, Umehara Y, Kouchi H, Murakami Y, Mulder L, Vickers K, Pike J, Downie J A, Wang T, Sato S, Asamizu E, Tabata S, Yoshikawa M, Murooka Y, Wu G J, Kawaguchi M, et al. Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots. Nature,2005,433:527-531.
70. Imamura A, Hanaki N, Nakamura A, Suzuki T, Taniguchi M, Kiba T, Ueguchi C, Sugiyama T, and Mizuno T. Compilation and characterization of Arabidopsis thaliana response regulators implicated in His-Asp phosphorelay signal transduction. Plant Cell Physiol,1999,40:733-742.
71. Inoue T, Higuchi M, Hashimoto Y, Seki M, Kobayashi M, Kato T, Tabata S, Shinozaki K, and Kakimoto T. Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature,2001,409: 1060-1063.
72. Jaworski K, Szmidt-Jaworska A, and Kopcewicz J. Plant protein kinases stimulated by calcium. Postepy Biochem,2005,51,188-197.
73. Jentsch S, and Pyrowolakis G. Ubiquitin and its kin:how close are the family ties? Trends Cell Biol,2000,10:335-342.
74. Jones K M, Kobayashi H, Davies B W, Taga M E and Walker G C. How rhizobial symbionts invade plants:the Sinorhizobium-Medicago model. Nat Rev Microbiol,2007,5:619-633.
75. Kalo P, Gleason C, Edwards A, Marsh J, Mitra R M, Hirsch S, Jakab J, Sims S, Long S R, Rogers J, Kiss G B, Downie J A and Oldroyd G E. Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science,2005,308: 1786-1789.
76. Kanamori N, Madsen L H, Radutoiu S, Frantescu M, Quistgaard E M, Miwa H, Downie J A, James E K, Felle H H, Haaning L L, Jensen T H, Sato S, Nakamura Y, Tabata S, Sandal N and Stougaard J. A nucleoporin is required for induction of Ca2+spiking in legume nodule development and essential for rhizobial and fungal symbiosis. Proc Natl Acad Sci U S A,2006, 103:359-364.
77. Kaye F J, Modi S, Ivanovska I, Koonin E V, Thress K, Kubo A, Kornbluth S, and Rose M D. A family of ubiquitin-like proteins binds the ATPase domain of Hsp70-like Stch. FEBS Lett,2000, 467:348-355.
78. Kerstetter R, Bollman K, Taylor R, Bomblies K, and Poethig R. KANADI regulates organ polarity in Arabidopsis. Nature,2001,411:706-709.
79. Kevei Z, Lougnon G, Mergaert P, Horvath G V, Kereszt A, Jayaraman D, Zaman N, Marcel F, Regulski K, Kiss G B, Kondorosi A, Endre G, Kondorosi E and Ane J M. 3-hydroxy-3-methylglutaryl coenzyme a reductase 1 interacts with NORK and is crucial for nodulation in Medicago truncatula. Plant Cell,2007,19:3974-3989.
80. Kiss E, Olah B, Kalo P, Morales M, Heckmann A B, Borbola A, Lozsa A, Kontar K, Middleton P, Downie J A, Oldroyd G E, and Endre G. LIN, a novel type of U-box/WD40 protein, controls early infection by rhizobia in legumes. Plant Physiol,2009,151:1239-1249.
81. Kistner C, Winzer T, Pitzschke A, Mulder L, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J, Webb K J, Szczyglowski K, and Parniske M. Seven Lotus japonicus genes required for transcriptional reprogramming of the root during fungal and bacterial symbiosis. Plant Cell, 2005,17,2217-2229.
82. Kistner C, and Parniske M. Evolution of signal transduction in intracellular symbiosis. Trends Plant Sci,2002,7:511-518.
83. Kondorosi E, Redondo-Nieto M, and Kondorosi A. Ubiquitin-mediated proteolysis. To be in the right place at the right moment during nodule development. Plant Physiol,2005,137: 1197-1204.
84. Kouchi H, Imaizumi-Anraku H, Hayashi M, Hakoyama T, Nakagawa T, Umehara Y, Suganuma N, and Kawaguchi M. How many peas in a pod? Legume genes responsible for mutualistic symbioses underground. Plant Cell Physiol,2010,51,1381-1397.
85. Kumagai H, and Kouchi H. Gene silencing by expression of hairpin RNA in Lotus japonicus roots and root nodules. Mol Plant Microbe Interact,2003,16:663-668.
86. Lee S S, Cho H S, Yoon G M, Ahn J W, Kim H H, and Pai H S. Interaction of NtCDPKl calcium-dependent protein kinase with NtRpn3 regulatory subunit of the 26S proteasome in Nicotiana tabacum. Plant J,2003,33:825-840.
87. Lerouge P, Roche P, Faucher C, Maillet F, Truchet G, Prome J C and Denarie J. Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature,1990,344:781-784.
88. Levy J, Bres C, Geurts R, Chalhoub B, Kulikova O, Due G, Journet E P, Ane J M, Lauber E, Bisseling T, Denarie J, Rosenberg C, and Debelle F. A putative Ca2+and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science,2004,303:1361-1364.
89. Li J and Chory J. A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell,1997,90:929-938.
90. Lohar D P, Schaff J E, Laskey J G, Kieber J J, Bilyeu K D and Bird D M. Cytokinins play opposite roles in lateral root formation, and nematode and Rhizobial symbioses. Plant J,2004, 38:203-214.
91. Lohar D P, Sharopova N, Endre G, Penuela S, Samac D, Town C, Silverstein K A and VandenBosch K A. Transcript analysis of early nodulation events in Medicago truncatula. Plant Physiol,2006,140:221-234.
92. Lorteau M A, Ferguson B J and Guinel F C. Effects of cytokinin on ethylene production and nodulation in pea(Pisum sativum) cv. Sparkle. Physiol Plant,2001,112:421-428.
93. Lupas A, Van Dyke M, and Stock J. Predicting coiled coils from protein sequences. Science, 1991,252:1162-1164.
94. Madsen E B, Antolin-Llovera M, Grossmann C, Ye J, Vieweg S, Broghammer A, Krusell L, Radutoiu S, Jensen O N, Stougaard J, and Parniske M. Autophosphorylation is essential for the in vivo function of the Lotus japonicus Nod factor receptor 1 and receptor-mediated signalling in cooperation with Nod factor receptor 5. Plant J,2011,65,404-417.
95. Madsen E B, Madsen L H, Radutoiu S, Olbryt M, Rakwalska M, Szczyglowski K, Sato S, Kaneko T, Tabata S, Sandal N and Stougaard J. A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature,2003,425:637-640.
96. Madsen L, Tirichine L, Jurkiewicz A, Sullivan J, Heckmann A, Bek A, Ronson C, James E, Stougaard. The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nature Communications,2010,1:1-12.
97. Maekawa T, Maekawa-Yoshikawa M, Takeda N, Imaizumi-Anraku H, Murooka Y, and Hayashi M. Gibberellin controls the nodulation signaling pathway in Lotus japonicus. Plant J,2009,58, 183-194.
98. Mahonen A R, Bonke M, Kauppinen L, Riikonen M, Benfey P N, and Helariutta Y. A novel two-component hybrid molecule regulates vascular morphogenesis of the Arabidopsis root. Genes Dev,2000,14:2938-2943.
99. Maillet F, Poinsot V, Andre O, Puech-Pages V, Haouy A, Gueunier M, Cromer L, Giraudet D, Formey D, Niebel A, Martinez E A, Driguez H, Becard G, and Denarie J. Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature,2011,469:58-63.
100. Majello B, Kenyon L C, and Dalla-Favera R. Human c-myb protooncogene:nucleotide sequence of cDNA and organization of the genomic locus. Proc Natl Acad Sci U S A,1986,83:9636-9640.
101. Marian C O, Bordoli S J, Goltz M, Santarella R A, Jackson L P, Danilevskaya O, Beckstette M, Meeley R, and Bass H W. The maize Single myb histone 1 gene, Smhl, belongs to a novel gene family and encodes a protein that binds telomere DNA repeats in vitro. Plant Physiol,2003,133: 1336-1350.
102. Markmann K, Giczey G and Parniske M. Functional adaptation of a plant receptor-kinase paved the way for the evolution of intracellular root symbioses with bacteria. PLoS Biol,2008,6:e68.
103. Marsh J F, Rakocevic A, Mitra R M, Brocard L, Sun J, Eschstruth A, Long S R, Schultze M, Ratet P and Oldroyd G E. Medicago truncatula NIN is essential for rhizobial-independent nodule organogenesis induced by autoactive calcium/calmodulin-dependent protein kinase. Plant Physiol,2007,144:324-335.
104. Mathesius U, Charon C, Rolfe B G, Kondorosi A and Crespi M. Temporal and spatial order of events during the induction of cortical cell divisions in white clover by Rhizobium leguminosarum bv. trifolii inoculation or localized cytokinin addition. Mol Plant Microbe Interact,2000,13(6):617-628.
105. Mathesius U, Schlaman H R, Spaink H P, Of Sautter C, Rolfe B G and Djordjevic M A. Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides. Plant J,1998,14(1):23-34.
106. McGonigle T, Miller M, Evans D, Fairchild G, and Swan J. A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytologist,1990,115:495-501.
107. Messinese E, Mun J H, Yeun L H, Jayaraman D, Rouge P, Barre A, Lougnon G, Schornack S, Bono J J, Cook D R, and Ane J M. A novel nuclear protein interacts with the symbiotic DMI3 calcium-and calmodulin-dependent protein kinase of Medicago truncatula. Mol Plant Microbe Interact,2007,20:912-921.
108. Middleton P H, Jakab J, Penmetsa R V, Starker C G, Doll J, Kalo P, Prabhu R, Marsh J F, Mitra R M, Kereszt A, Dudas B, VandenBosch K, Long S R, Cook D R, Kiss G B, and Oldroyd G E. An ERF transcription factor in Medicago truncatula that is essential for Nod factor signal transduction. Plant Cell,2007,19:1221-1234.
109. Mitra R M, Gleason C A, Edwards A, Hadfield J, Downie J A, Oldroyd G E, and Long S R. A Ca2+/calmodulin-dependent protein kinase required for symbiotic nodule development:Gene identification by transcript-based cloning. Proc Natl Acad Sci USA,2004,101:4701-4705.
110. Miwa H, Sun J, Oldroyd G E and Downie J A. Analysis of Nod-factor-induced calcium signaling in root hairs of symbiotically defective mutants of Lotus japonicus. Mol Plant Microbe Interact, 2006,19:914-92.
111. Miyazawa H, Oka-Kira E, Sato N, Takahashi H, Wu G J, Sato S, Hayashi M, Betsuyaku S, Nakazono M, Tabata S, Harada K, Sawa S, Fukuda H, and Kawaguchi M. The receptor-like kinase KLAVIER mediates systemic regulation of nodulation and non-symbiotic shoot development in Lotus japonicus. Development,2010,137:4317-4325.
112. Murakami Y, Miwa H, Imaizumi-Anraku H, Kouchi H, Downie J A, Kawaguchi M and Kawasaki S. Positional cloning identifies Lotus japonicus NSP2, a putative transcription factor of the GRAS family, required for N1N and ENOD40 gene expression in nodule initiation. DNA Res,2006,13:255-265.
113. Murray J D, Karas B J, Sato S, Tabata S, Amyot L, and Szczyglowski K. A cytokinin perception mutant colonized by Rhizobium in the absence of nodule organogenesis. Science,2007,315: 101-104.
114. Mylona P, Pawlowski K and Bisseling T. Symbiotic Nitrogen Fixation. Plant Cell,1995,7: 869-885.
115. Nam K H and Li J. BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell, 2002,110:203-212.
116. Nishimura R, Ohmori M, Fujita H, and Kawaguchi M. A Lotus basic leucine zipper protein with a RING-finger motif negatively regulates the developmental program of nodulation. Proc Natl Acad Sci USA,2002,99:15206-15210.
117. Nontachaiyapoom S, Scott P T, Men A E, Kinkema M, Schenk P M, and Gresshoff P M. Promoters of orthologous Glycine max and Lotus japonicus nodulation autoregulation genes interchangeably drive phloem-specific expression in transgenic plants. Mol Plant Microbe Interact,2007,20:769-780.
118.Norbert C A, Ruijter d, Bisseling T and Emons A M C. Rhizobium Nod Factors Induce an Increase in Sub-apical Fine Bundles of Actin Filaments in Vicia sativa Root Hairs within Minutes. Mol Plant Microbe Interact,1999,12:829-832.
119. Ogata K, Hojo H, Aimoto S, Nakai T, Nakamura H, Sarai A, Ishii S, and Nishimura Y. Solution structure of a DNA-binding unit of Myb:a helix-turn-helix-related motif with conserved tryptophans forming a hydrophobic core. Proc Natl Acad Sci USA,1992,89:6428-6432.
120. Oka-Kira E, and Kawaguchi M. Long-distance signaling to control root nodule number. Curr Opin Plant Biol,2006,9:496-502.
121. Oldroyd G E. Plant science. Nodules and hormones. Science,2007,315:52-53.
122. Oldroyd G E and Downie J A. Calcium, kinases and nodulation signalling in legumes. Nat Rev Mol Cell Biol,2004,5:566-576.
123. Oldroyd G E and Downie J A. Nuclear calcium changes at the core of symbiosis signalling. Curr Opin Plant Biol,2006,9:351-357.
124. Oldroyd G E, and Downie J A. Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol,2008,59:519-546.
125. Oldroyd G E, Harrison M J and Udvardi M. Peace talks and trade deals. Keys to long-term harmony in legume-microbe symbioses. Plant Physiol,2005,137:1205-1210.
126. Op den Camp R, Streng A, De Mita S, Cao Q, Polone E, Liu W, Ammiraju J S, Kudrna D, Wing R, Untergasser A, Bisseling T, and Geurts R. LysM-Type Mycorrhizal Receptor Recruited for Rhizobium Symbiosis in Nonlegume Parasponia. Science,2011,331:909-912.
127. Pacios-Bras C, Schlaman H R, Boot K, Admiraal P, Langerak J M, Stougaard J and Spaink H P. Auxin distribution in Lotus japonicus during root nodule development. Plant Mol Biol,2003,52: 1169-1180.
128. Parniske M. Arbuscular mycorrhiza:the mother of plant root endosymbioses. Nat Rev Microbiol, 2008,6:763-775
129. Parniske M and Downie J A. Plant biology:locks, keys and symbioses. Nature,2003,425: 569-570.
130. Parry D A, Fraser R D, and Squire J M. Fifty years of coiled-coils and alpha-helical bundles:a close relationship between sequence and structure. J Struct Biol,2008,163:258-269.
131. Pate J, Gunning B, and Briarty L. Ultrastructure and functioning of the transport system of the leguminous root nodule. Planta,1969,85:11-34.
132. Patharkar O R, and Cushman J C. A stress-induced calcium-dependent protein kinase from Mesembryanthemum crystallinum phosphorylates a two-component pseudo-response regulator. Plant J,2000,24:679-691.
133. Patil S, Takezawa D, and Poovaiah B W. Chimeric plant calcium/calmodulin-dependent protein kinase gene with a neural visinin-like calcium-binding domain. Proc Natl Acad Sci U S A,1995, 92:4897-4901.
134. Pawlowski K and Bisseling T. Rhizobial and Actinorhizal Symbioses:What Are the Shared Features? Plant Cell,1996,8:1899-1913.
135. Penmetsa R V, Frugoli J A, Smith L S, Long S R, and Cook D R. Dual genetic pathways controlling nodule number in Medicago truncatula. Plant Physiol,2003,131:998-1008.
136. Penmetsa R V, Uribe P, Anderson J, Lichtenzveig J, Gish J C, Nam Y W, Engstrom E, Xu K, Sckisel G, Pereira M, Baek J M, Lopez-Meyer M, Long S R, Harrison M J, Singh K B, Kiss G B, and Cook D R. The Medicago truncatula ortholog of Arabidopsis EIN2, sickle, is a negative regulator of symbiotic and pathogenic microbial associations. Plant J,2008,55:580-595.
137. Perret X, Staehelin C and Broughton W J. Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev,2000,64:180-201.
138. Pickart C M. Back to the future with ubiquitin. Cell,2004,116:181-190.
139. Poovaiah B W, Xia M, Liu Z, Wang W, Yang T, Sathyanarayanan P V, and Franceschi V R. Developmental regulation of the gene for chimeric calcium/calmodulin-dependent protein kinase in anthers. Planta,1999,209:161-171.
140. Pueppke S G. The genetic and biochemical basis for nodulation of legumes by rhizobia. Crit Rev Biotechnol,1996,16:1-51.
141. Pysh L D, Wysocka-Diller J W, Camilleri C, Bouchez D and Benfey P N. The GRAS gene family in Arabidopsis:sequence characterization and basic expression analysis of the SCARECROW-LIKE genes. Plant J,1999,18:111-119.
142. Radutoiu S, Madsen L H, Madsen E B, Felle H H, Umehara Y, Gronlund M, Sato S, Nakamura Y, Tabata S, Sandal N and Stougaard J. Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature,2003,425:585-592.
143. Ramachandiran S, Takezawa D, Wang W, and Poovaiah B W. Functional domains of plant chimeric calcium/calmodulin-dependent protein kinase:regulation by autoinhibitory and visinin-like domains. J Biol Chem,1997,121:984-990.
144. Richards D E, Peng J, and Harberd N P. Plant GRAS and metazoan STATs:one family? Bioessays,2000,22:573-577.
145. Ridge R W. A model of legume root hair growth and Rhizobium infection. Symbiosis,1993,14: 359-373.
146. Riechmann J, Heard J, Martin G, Reuber L, Jiang C, Keddie J, Adam L, Pineda O, Ratcliffe O J, Samaha R R, Creelman R, Pilgrim M, Broun P, Zhang J Z, Ghandehari D, Sherman B K, and Yu G. Arabidopsis transcription factors:genome-wide comparative analysis among eukaryotes. Science,2000,290:2105-2110.
147. Riely B K, Mun J H and Ane J M. Unravelling the molecular basis for symbiotic signal transduction in legumes. Mol. Plant Pathol,2006,7:197-207.
148. Roche R, Lerouge P, Ponthus C and Prome J C. Structural determination of bacterial nodulation factors involved in the Rhizobium meliloti-alfalfa symbiosis. J Biol Chem,1991,266: 10933-10940.
149. Rodriguez Milla M A, Uno Y, Chang I F, Townsend J, Maher E A, Quilici D, and Cushman J C. A novel yeast two-hybrid approach to identify CDPK substrates:characterization of the interaction between AtCPK11 and AtDi19, a nuclear zinc finger protein. FEBS Lett,2006,580: 904-911.
150. Rubio V, Linhares F, Solano R, Martin A C, Iglesias J, Leyva A, and Paz-Ares J. A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev,2001,15:2122-2133.
151. Ruijter N C A d, Rook M B, Bisseling T and Emons A M C. Lipochito-oligosaccharides re-initiate root hair tip growth in Vicia sativa with high calcium and spectrin-like antigen at the tip. Plant J,1998,13:341-350.
152. Saito K, Yoshikawa M, Yano K, Miwa H, Uchida H, Asamizu E, Sato S, Tabata S, Imaizumi-Anraku H, Umehara Y, Kouchi H, Murooka Y, Szczyglowski K, Downie J A, Parniske M, Hayashi M and Kawaguchi M. NUCLEOPORIN85 is required for calcium spiking, fungal and bacterial symbioses, and seed production in Lotus japonicus. Plant Cell,2007,19:610-624.
153.Saitou N, and Nei M. The neighbor-joining method:a new method for reconstructing phylogenetic trees. Mol Biol Evol,1987,4:406-425.
154. Sasaki T, Marcon E, McQuire T, Arai Y, Moens P B, and Okada H. Bat3 deficiency accelerates the degradation of Hsp70-2/HspA2 during spermatogenesis. J Cell Biol,2008,182:449-458.
155. Sathyanarayanan P V, Cremo C R, and Poovaiah B W. Plant chimeric Ca2+/Calmodulin-dependent protein kinase. Role of the neural visinin-like domain in regulating autophosphorylation and calmodulin affinity. J Biol Chem,2000,275:30417-30422.
156. Sathyanarayanan P V, Siems W F, Jones J P, and Poovaiah B W. Calcium-stimulated autophosphorylation site of plant chimeric calcium/calmodulin-dependent protein kinase. J Biol Chem,2001,276:32940-32947.
157. Savoure A, Magyar Z, Pierre M, Brown S, Schultze M, Dudits D, Kondorosi A and Kondorosi E. Activation of the cell cycle machinery and the isoflavonoid biosynthesis pathway by active Rhizobium meliloti Nod signal molecules in Medicago microcallus suspensions. EMBO J,1994, 13:1093-1102.
158. Schaffer R, Ramsay N, Samach A, Corden S, Putterill J, Carre I A, and Coupland G.. The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell,1998,93:1219-1229.
159. Schauser L, Roussis A, Stiller J and Stougaard J. A plant regulator controlling development of symbiotic root nodules. Nature,1999,402:191-195.
160. Schneider A, Walker S A, Poyser S, Sagan M, Ellis T H and Downie J A. Genetic mapping and functional analysis of a nodulation-defective mutant (sym19) of pea (Pisum sativum L.). Mol Gen Genet,1999,262:1-11.
161. Schwikowski B, Uetz P and Fields S. A network of protein-protein interactions in yeast. Nat Biotechnol,2000,18:1257-1261.
162. Searle I R, Men A E, Laniya T S, Buzas D M, Iturbe-Ormaetxe I, Carroll B J and Gresshoff P M. Long-distance signaling in nodulation directed by a CLAVATA1-like receptor kinase. Science, 2003,299:109-112.
163. Shimomura K, Nomura M, Tajima S and Kouchi H. LjnsRING, a novel RING finger protein, is required for symbiotic interactions between Mesorhizobium loti and Lotus japonicus. Plant Cell Physiol,2006,47:1572-1581.
164. Sinharoy S, DasGupta M. RNA interference highlights the role of CCaMK in dissemination of endosymbionts in the Aeschynomeneae legume Arachis. Mol Plant Microbe Interact,2009,22: 1466-1475.
165. Smit G, Kijne J W and Lugtenberg B J. Roles of flagella, lipopolysaccharide, and a Ca2+-dependent cell surface protein in attachment of Rhizobium leguminosarum biovar viciae to pea root hair tips. JBacteriol,1989a,171:569-572.
166. Smit G, Logman T J, Boerrigter M E, Kijne J W and Lugtenberg B J. Purification and partial characterization of the Rhizobium leguminosarum biovar viciae Ca2+-dependent adhesin, which mediates the first step in attachment of cells of the family Rhizobiaceae to plant root hair tips. J Bacteriol,1989b,171:4054-4062.
167. Smit P, Limpens E, Geurts R, Fedorova E, Dolgikh E, Gough C and Bisseling T. Medicago LYK3, an entry receptor in rhizobial nodulation factor signaling. Plant Physiol,2007,145: 183-191.
168. Smit P, Raedts J, Portyanko V, Debelle F, Gough C, Bisseling T and Geurts R. NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science,2005, 308:1789-1791.
169. Sprent, J I. Evolving ideas of legume evolution and diversity:a taxonomic perspective on the occurrence of nodulation. New Phytol,2007,174,11-25.
170. Stacey G, Libault M, Brechenmacher L, Wan J, and May G. D. Genetics and functional genomics of legume nodulation. Curr Opin Plant Biol,2006,9:110-121.
171. Staehelin C, Granado J, Muller J, Wiemken A, Mellor R B, Felix G, Regenass M, Broughton W J and Boller T. Perception of Rhizobium nodulation factors by tomato cells and inactivation by root chitinases. Proc Natl Acad Sci USA,1994,91:2196-2200.
172. Stracke R, Werber M, and Weisshaar B. The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol,2001,4:447-456.
173. Stracke S, Kistner C, Yoshida S, Mulder L, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J, Szczyglowski K and Parniske M. A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature,2002,417:959-962.
174. Subramanian S, Stacey G and Yu O. Endogenous isoflavones are essential for the establishment of symbiosis between soybean and Bradyrhizobium japonicum. Plant J,2006,48:261-273.
175. Sun J, Cardoza V, Mitchell D M, Bright L, Oldroyd G and Harris J M. Crosstalk between jasmonic acid, ethylene and Nod factor signaling allows integration of diverse inputs for regulation of nodulation. Plant J,2006,46:961-970.
176. Suzuki T, Miwa K, Ishikawa K, Yamada H, Aiba H, and Mizuno T. The Arabidopsis sensor His-kinase, AHk4, can respond to cytokinins. Plant Cell Physiot,2001,42:107-113.
177. Takezawa D, Ramachandiran S, Paranjape V, and Poovaiah B W. Dual regulation of a chimeric plant serine/threonine kinase by calcium and calcium/calmodulin. J Biol Chem,1996,271: 8126-8132.
178. Tamura K, Dudley J, Nei M, and Kumar S. MEGA4:Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol,2007,24:1596-1599.
179. Tansengco M L, Hayashi M, Kawaguchi M, Imaizumi-Anraku H, and Murooka Y. crinkle, a novel symbiotic mutant that affects the infection thread growth and alters the root hair, trichome, and seed development in Lotus japonicus. Plant Physiol,2003,131:1054-1063.
180. Thompson J D, Gibson T J, Plewniak F, Jeanmougin F, and Higgins D G. The CLUSTAL_X windows interface:flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res,1997,25:4876-4882.
181. Thress K, Henzel W, Shillinglaw W, and Kornbluth S. Scythe:a novel reaper-binding apoptotic regulator. EMBOJ,1998,17:6135-6143.
182. Thress K, Song J, Morimoto R I, and Kornbluth S. Reversible inhibition of Hsp70 chaperone function by Scythe and Reaper. EMBOJ,2001,20:1033-1041.
183. Tian C, Wan P, Sun S, Li J, and Chen M. Genome-wide analysis of the GRAS gene family in rice and Arabidopsis. Plant Mol Biol,2004,54:519-532.
184. Timmers A C, Auriac M C and Truchet G. Refined analysis of early symbiotic steps of the Rhizobium-Medicago interaction in relationship with microtubular cytoskeleton rearrangements. Development,1999,126:3617-3628.
185. Tirichine L, Imaizumi-Anraku H, Yoshida S, Murakami Y, Madsen L H, Miwa H, Nakagawa T, Sandal N, Albrektsen A S, Kawaguchi M, Downie A, Sato S, Tabata S, Kouchi H, Parniske M, Kawasaki S and Stougaard J. Deregulation of a Ca27calmodulin-dependent kinase leads to spontaneous nodule development. Nature,2006,441:1153-1156.
186. Tirichine L, Sandal N, Madsen L H, Radutoiu S, Albrektsen A S, Sato S, Asamizu E, Tabata S and Stougaard J. A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis. Science,2007,315:104-107.
187. Uno Y, Rodriguez Milla M A, Maher E, and Cushman J C. Identification of proteins that interact with catalytically active calcium-dependent protein kinases from Arabidopsis. Mol Genet Genomics,2009,281:375-390.
188. van-Batenburg F H D, Jonker R and Kijne J W. Rhizobium induces marked root hair curling by redirection of tip growth:a computer simulation. Physiol Plant,1986,66:476-480.
189. van Brussel A A, Bakhuizen R, van Spronsen P C, Spaink H P, Tak T, Lugtenberg B J and Kijne J W. Induction of Pre-Infection Thread Structures in the Leguminous Host Plant by Mitogenic Lipo-Oligosaccharides of Rhizobium. Science,1992,257:70-72.
190. Vijn I, das Nevas L, van Kammen A, Franssen H and Bisseling T. Nod factors and nodulation in plants. Science,1993,260:1764-1765.
191. Waadt R, Schmidt L K, Lohse M, Hashimoto K, Bock R, and Kudla J. Multicolor bimolecular fluorescence complementation reveals simultaneous formation of alternative CBL/CIPK complexes in planta. Plant J,2008,56:505-516.
192. Walter M, Chaban C, Schutze K, Batistic O, Weckermann K, Nake C, Blazevic D, Grefen C, Schumacher K, Oecking C, Harter K, and Kudla J. Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J,2004,40:428-438.
193. Wang D, Harper J F, Gribskov M. Systematic trans-genomic comparison of protein kinases between Arabidopsis and Saccharomyces cerevisiae. Plant Physiol,2003,132:2152-2165.
194. Wang Z Y, Kenigsbuch D, Sun L, Harel E, Ong M S, and Tobin E M. A Myb-related transcription factor is involved in the phytochrome regulation of an Arabidopsis Lhcb gene. Plant Cell,1997, 9:491-507.
195. Wang W, and Poovaiah B W. Interaction of plant chimeric calcium/calmodulin-dependent protein kinase with a homolog of eukaryotic elongation factor-1 alpha. J Biol Chem,1999,274: 12001-12008.
196. Webb K J, Skot L, Nicholson M N, Jorgensen B, and Mizen S. Mesorhizobium loti increases root-specific expression of a calcium-binding protein homologue identified by promoter tagging in Lotus japonicus. Mol Plant Microbe Interact,2000,13:606-616.
197. Wopereis J, Pajuelo E, Dazzo F B, Jiang Q, Gresshoff P M, De Bruijn F J, Stougaard J, and Szczyglowski K. Short root mutant of Lotus japonicus with a dramatically altered symbiotic phenotype. Plant J,2000,23:97-114.
198. Wykoff D D, Grossman A R, Weeks D P, Usuda H, and Shimogawara K. Psrl, a nuclear localized protein that regulates phosphorus metabolism in Chlamydomonas. Proc Natl Acad Sci USA,1999,96:15336-15341.
199. Yang T, and Poovaiah B W. Calcium/calmodulin-mediated signal network in plants. Trends Plant Sci,2003,8:505-512.
200. Yokota K, Soyano T, Kouchi H, and Hayashi M. Function of GRAS proteins in root nodule symbiosis is retained in homologs of a non-legume, rice. Plant Cell Physiol,2010,51: 1436-1442.
201.Yano K, Shibata S, Chen W L, Sato S, Kaneko T, Jurkiewicz A, Sandal N, Banba M, Imaizumi-Anraku H, Kojima T, Ohtomo R, Szczyglowski K, Stougaard J, Tabata S, Hayashi M, Kouchi H, and Umehara Y CERBERUS, a novel U-box protein containing WD-40 repeats, is required for formation of the infection thread and nodule development in the legume-Rhizobium symbiosis. Plant J,2009,60:168-180.
202. Yano K, Yoshida S, Muller J, Singh S, Banba M, Vickers K, Markmann K, White C, Schuller B, Sato S, Asamizu E, Tabata S, Murooka Y, Perry J, Wang T L, Kawaguchi M, Imaizumi-Anraku H, Hayashi M, and Parniske M. CYCLOPS, a mediator of symbiotic intracellular accommodation. Proc Natl Acad Sci U S A,2008,105:20540-20545.
203. Yoshida S and Parniske M. Regulation of plant symbiosis receptor kinase through serine and threonine phosphorylation. J Biol Chem,2005,280:9203-9209.
204. Zhu H, Chen T, Zhu M, Fang Q, Kang H, Hong Z, and Zhang Z. A novel ARID DNA-binding protein interacts with SymRK and is expressed during early nodule development in Lotus japonicus. Plant Physiol,2008,148:337-347.
2. Andriankaja A, Boisson-Dernier A, Frances L, Sauviac L, Jauneau A, Barker D G, and de Carvalho-Niebel F. AP2-ERF transcription factors mediate Nod factor dependent Mt ENOD11 activation in root hairs via a novel cis-regulatory motif. Plant Cell,2007,19:2866-2885.
3. Ane J M, Kiss G B, Riely B K, Penmetsa R V, Oldroyd G E, Ayax C, Levy J, Debelle F, Baek J M, Kalo P, Rosenberg C, Roe B A, Long S R, Denarie J, and Cook D R. Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science,2004,303:1364-1367.
4. Ardourel M, Demont N, Debelle F, Maillet F, de Billy F, Prome J C, Denarie J, and Truchet G. Rhizobium meliloti lipooligosaccharide nodulation factors:different structural requirements for bacterial entry into target root hair cells and induction of plant symbiotic developmental responses. Plant Cell,1994,6:1357-1374.
5. Arrighi J F, Barre A, Ben Amor B, Bersoult A, Soriano L C, Mirabella R, de Carvalho-Niebel F, Journet E P, Gherardi M, Huguet T, Geurts R, Denarie J, Rouge P, and Gough C. The Medicago truncatula lysin [corrected] motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiol,2006,142:265-279.
6. Asamizu E, Shimoda Y, Kouchi H, Tabata S, and Sato S. A positive regulatory role for LjERFl in the nodulation process is revealed by systematic analysis of nodule-associated transcription factors of Lotus japonicus. Plant Physiol,2008,147:2030-2040.
7. Banba M, Gutjahr C, Miyao A, Hirochika H, Paszkowski U, Kouchi H, and Imaizumi-Anraku H. Divergence of evolutionary ways among common sym genes:CASTOR and CCaMK show functional conservation between two symbiosis systems and constitute the root of a common signaling pathway. Plant Cell Physiol,2008,49:1659-1671.
8. Banerji J, Sands J, Strominger J L, and Spies T. A gene pair from the human major histocompatibility complex encodes large proline-rich proteins with multiple repeated motifs and a single ubiquitin-like domain. Proc Natl Acad Sci U S A,1990,87:2374-2378.
9. Baranowskij N, Frohberg C, Prat S, and Willmitzer L. A novel DNA binding protein with homology to Myb oncoproteins containing only one repeat can function as a transcriptional activator. EMBO J,1994,13:5383-5392.
10. Boisson-Dernier A, Chabaud M, Garcia F, Becard G, Rosenberg C and Barker D G. Agrobacterium rhizogenes-transformed roots of Medicago truncatula for the study of nitrogen-fixing and endomycorrhizal symbiotic associations. Mol Plant Microbe Interact,2001, 14:695-700.
11. Bolle C. The role of GRAS proteins in plant signal transduction and development. Planta,2004, 218:683-692.
12. Bonke M, Thitamadee S, Mahonen A P, Hauser M T, and Helariutta Y. APL regulates vascular tissue identity in Arabidopsis. Nature,2003,426:181-186.
13. Borisov A Y, Madsen L H, Tsyganov V E, Umehara Y, Voroshilova V A, Batagov A O, Sandal N, Mortensen A, Schauser L, Ellis N, Tikhonovich I A and Stougaard J. The Sym35 gene required for root nodule development in pea is an ortholog of Nin from Lotus japonicus. Plant Physiol, 2003,131:1009-1017.
14. Briarty L. The development of root nodule xylem transfer cells in Trifolium repens. Journal of Experimental Botany,1978,29:735.
15. Caetano-Anollcs G, and Gresshoff P M. Early induction of feedback regulatory responses governing nodulation in soybean. Plant Science,1990,71:69-81.
16. Caetano-Anolles G, and Gresshoff P M. Plant genetic control of nodulation. Annu Rev Microbiol, 1991,45:345-382.
17. Capoen W, Den Herder J, Sun J, Verplancke C, De Keyser A, De Rycke R, Goormachtig S, Oldroyd G E, Holsters M. Calcium spiking patterns and the role of the calcium/calmodulin-dependent kinase CCaMK in lateral root base nodulation of Sesbania rostrata. Plant Cell,2009,21 (5):1526-1540.
18. Carroll B J, McNeil D L, and Gresshoff P M. A Supernodulation and Nitrate-Tolerant Symbiotic (nts) Soybean Mutant. Plant Physiol,1985,78:34-40.
19. Catoira R, Galera C, de Billy F, Penmetsa R V, Journet E P, Maillet F, Rosenberg C, Cook D, Gough C and Denarie J. Four genes of Medicago truncatula controlling components of a nod factor transduction pathway. Plant Cell,2000,12:1647-1666.
20. Charpentier M, and Oldroyd G. How close are we to nitrogen-fixing cereals? Curr Opin Plant Biol,2010,13,556-564.
21. Chen C, Ane J M, and Zhu H. OsIPD3, an ortholog of the Medicago truncatula DMI3 interacting protein IPD3, is required for mycorrhizal symbiosis in rice. New Phytol,2008,180,311-315.
22. Chen C, Gao M, Liu J, and Zhu H. Fungal symbiosis in rice requires an ortholog of a legume common symbiosis gene encoding a Ca2+/calmodulin-dependent protein kinase. Plant Physiol, 2007,145,1619-1628.
23. Ciechanover A. The ubiquitin-proteasome pathway:on protein death and cell life. EMBOJ,1998, 17:7151-7160.
24. Combier J P, Frugier F, de Billy F, Boualem A, El-Yahyaoui F, Moreau S, Vernie T, Ott T, Gamas P, Crespi M, and Niebel A. MtHAP2-1 is a key transcriptional regulator of symbiotic nodule development regulated by microRNA169 in Medicago truncatula. Genes Dev,2006,20: 3084-3088.
25. Complainville A, Brocard L, Roberts I, Dax E, Sever N, Sauer N, Kondorosi A, Wolf S, Oparka K, and Crespi M. Nodule initiation involves the creation of a new symplasmic field in specific root cells of medicago species. Plant Cell,2003,15:2778-2791.
26. Corduan A, Lecomte S, Martin C, Michel D, and Desmots F. Sequential interplay between BAG6 and HSP70 upon heat shock. Cell Mol Life Sci,2009,66:1998-2004.
27. Crdenas L, Vidali L, Domnguez J, Prez H, Snchez F, Hepler P K and Quinto C. Rearrangement of actin microfilaments in plant root hairs responding to rhizobium etli nodulation signals. Plant Physiol,1998,116:871-877.
28. Cui H, Levesque M P, Vernoux T, Jung J W, Paquette A J, Gallagher K L, Wang J Y, Blilou I, Scheres B, and Benfey PN. An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science,2007,316:421-425.
29. de Lucas M, Daviere J M, Rodriguez-Falcon M, Pontin M, Iglesias-Pedraz J M, Lorrain S, Fankhauser C, Blazquez M A, Titarenko E, and Prat S. A molecular framework for light and gibberellin control of cell elongation. Nature,2008,451:480-484.
30. D'Haeze W and Holsters M. Nod factor structures, responses, and perception during initiation of nodule development. Glycobiology,2002,12:79R-105R.
31. Denarie J and Cullimore J. Lipo-oligosaccharide nodulation factors:a minireview new class of signaling molecules mediating recognition and morphogenesis. Cell,1993,74:951-954.
32. Desmots F, Russell H R, Lee Y, Boyd K, and McKinnon P J. The reaper-binding protein scythe modulates apoptosis and proliferation during mammalian development. Mol Cell Biol,2005,25: 10329-10337.
33. Ding Y, Kalo P, Yendrek C, Sun J, Liang Y, Marsh J F, Harris J M, and Oldroyd G E. Abscisic acid coordinates nod factor and cytokinin signaling during the regulation of nodulation in Medicago truncatula. Plant Cell,2008,20:2681-2695.
34. Ehrhardt D W, Atkinson E M and Long S R. Depolarization of alfalfa root hair membrane potential by Rhizobium meliloti Nod factors. Science,1992,256:998-1000.
35. Ehrhardt D W, Wais R and Long S R. Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell,1996,85:673-681.
36. Endre G, Kereszt A, Kevei Z, Mihacea S, Kalo P and Kiss G B. A receptor kinase gene regulating symbiotic nodule development. Nature,2002,417:962-966.
37. Felle H H, Kondorosi E, Kondorosi A, and Schultze M. Elevation of the cytosolic free [Ca2+] is indispensable for the transduction of the Nod factor signal in alfalfa. Plant Physiol,1999,121: 273-280.
38. Ferguson B J, Indrasumunar A, Hayashi S, Lin M H, Lin Y H, Reid D E, and Gresshoff P M. Molecular analysis of legume nodule development and autoregulation. J Integr Plant Biol,2010, 52:61-76.
39. Fisher R F and Long S R. Rhizobium--plant signal exchange. Nature,1992,357:655-660.
40. Foucher F, and Kondorosi E. Cell cycle regulation in the course of nodule organogenesis in Medicago. Plant Mol Biol,2000,43:773-786.
41. Frugier F, Kosuta S, Murray J D, Crespi M, and Szczyglowski K. Cytokinin:secret agent of symbiosis. Trends Plant Sci,2008,13:115-120.
42. Fukuzawa M, Zhukovskaya N V, Yamada Y, Araki T, and Williams J G. Regulation of Dictyostelium prestalk-specific gene expression by a SHAQKY family MYB transcription factor. Development,2006,133:1715-1724.
43. Gage D J. Infection and Invasion of Roots by Symbiotic, Nitrogen-Fixing Rhizobia during Nodulation of Temperate Legumes. Microbiology and Molecular Biology Reviews,2004,68: 280-300.
44. Gallagher K L, and Benfey P N. Both the conserved GRAS domain and nuclear localization are required for SHORT-ROOT movement. Plant J,2009,57:785-797.
45. Geurts R and Bisseling T. Rhizobium nod factor perception and signalling. Plant Cell,2002,14 Suppl:S239-249.
46. Geurts R, Fedorova E and Bisseling T. Nod factor signaling genes and their function in the early stages of Rhizobium infection. Curr Opin Plant Biol,2005,8:346-352.
47. Gherbi H, Markmann K, Svistoonoff S, Estevan J, Autran D, Giczey G, Auguy F, Peret B, Laplaze L, Franche C, Parniske M and Bogusz D. SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankiabacteria. Proc Natl Acad Sci U S A,2008,105:4928-4932.
48. Gietz R D, Schiestl R H, Willems A R, and Woods R A. Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast,1995,11:355-360.
49. Godfroy O, Debelle F, Timmers T, and Rosenberg C. A rice calcium-and calmodulin-dependent protein kinase restores nodulation to a legume mutant. Mol Plant Microbe Interact,2006,19: 495-501.
50. Gonzalez-Rizzo S, Crespi M and Frugier F. The Medicago truncatula CRE1 cytokinin receptor regulates lateral root development and early symbiotic interaction with Sinorhizobium meliloti. Plant Cell,2006,18:2680-269
51. Gronlund M, Roussis A, Flemetakis E, Quaedvlieg N E, Schlaman H R, Umehara Y, Katinakis P, Stougaard J and Spaink H P. Analysis of promoter activity of the early nodulin Enod40 in Lotus japonicus. Mol Plant Microbe Interact,2005,18:414-427.
52. Groth M, Takeda N, Perry J, Uchida H, Draxl S, Brachmann A, Sato S, Tabata S, Kawaguchi M, Wang T L, and Parniske M. NENA, a Lotus japonicus Homolog of Sec 13, Is Required for Rhizodermal Infection by Arbuscular Mycorrhiza Fungi and Rhizobia but Dispensable for Cortical Endosymbiotic Development. Plant Cell,2010,22:2509-2526.
53. Gutjahr C, Banba M, Crose V, An K, Miyao A, An G, Hirochika H, Imaizumi-Anraku H, and Paszkowski U. Arbuscular mycorrhiza-specific signaling in rice transcends the common symbiosis signaling pathway. Plant Cell,2008,20:2989-3005.
54. Hall L N, Rossini L, Cribb L, and Langdale J A. GOLDEN 2:a novel transcriptional regulator of cellular differentiation in the maize leaf. Plant Cell,1998,10:925-936.
55. Harper J F, Breton G, and Harmon A. Decoding Ca(2+) signals through plant protein kinases. Annu Rev Plant Biol,2004,55,263-288.
56. Harper J F and Harmon A. Plants, symbiosis and parasites:a calcium signalling connection. Nat Rev Mol Cell Biol,2005,6:555-566.
57. Hayashi T, Banba M, Shimoda Y, Kouchi H, Hayashi M, Imaizumi-Anraku H. A dominant function of CCaMK in intracellular accommodation of bacterial and fungal endosymbionts. Plant J,2010,63:141-154
58. Hazen S P, Schultz T F, Pruneda-Paz J L, Borevitz J O, Ecker J R, and Kay S A. LUX ARRHYTHMO encodes a Myb domain protein essential for circadian rhythms. Proc Natl Acad Sci USA,2005,102:10387-10392.
59. Heckmann A B, Lombardo F, Miwa H, Perry J A, Bunnewell S, Parniske M, Wang T L and Downie J A. Lotus japonicus nodulation requires two GRAS domain regulators, one of which is functionally conserved in a non-legume. Plant Physiol,2006,142:1739-1750.
60. Heidstra R and Bisseling T. Nod factor-induced host responses and mechanisms of Nod factor perception. New Phytol,1996,133:25-43.
61. Heidstra R, Geurts R, Franssen H, Spaink H P, Van Kammen A and Bisseling T. Root hair deformation activity of nodulation factors and their fate on Vicia sativa. Plant Physiol,1994,105: 787-797.
62. Higuchi R, Krummel B, and Saiki R K. A general method of in vitro preparation and specific mutagenesis of DNA fragments:study of protein and DNA interactions. Nucleic Acids Res,1998, 16:7351-7367.
63. Hirsch A M, Lum M R, and Downie J A. What makes the rhizobia-legume symbiosis so special? Plant Physiol,2001,127:1484-1492.
64. Hirsch S, Kim J, Munoz A, Heckmann A B, Downie J A, and Oldroyd G E. GRAS proteins form a DNA binding complex to induce gene expression during nodulation signaling in Medicago truncatula. Plant Cell,2009,21:545-557.
65. Ho S N, Hunt H D, Horton R M, Pullen J K, and Pease L R. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene,1989,77:51-59.
66. Horton P, Park K J, Obayashi T, Fujita N, Harada H, Adams-Collier C J, and Nakai K. WoLF PSORT:protein localization predictor. Nucleic Acids Res,2007,35:585-587.
67. Hosoda K, Imamura A, Katoh E, Hatta T, Tachiki M, Yamada H, Mizuno T, and Yamazaki T. Molecular structure of the GARP family of plant Myb-related DNA binding motifs of the Arabidopsis response regulators. Plant Cell,2002,14:2015-2029.
68. Hudmon A, and Schulman H. Neuronal Ca2+/calmodulin-dependent protein kinase Ⅱ:the role of structure and autoregulation in cellular function. Annu Rev Biochem,2002,71:473-510.
69. Imaizumi-Anraku H, Takeda N, Charpentier M, Perry J, Miwa H, Umehara Y, Kouchi H, Murakami Y, Mulder L, Vickers K, Pike J, Downie J A, Wang T, Sato S, Asamizu E, Tabata S, Yoshikawa M, Murooka Y, Wu G J, Kawaguchi M, et al. Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots. Nature,2005,433:527-531.
70. Imamura A, Hanaki N, Nakamura A, Suzuki T, Taniguchi M, Kiba T, Ueguchi C, Sugiyama T, and Mizuno T. Compilation and characterization of Arabidopsis thaliana response regulators implicated in His-Asp phosphorelay signal transduction. Plant Cell Physiol,1999,40:733-742.
71. Inoue T, Higuchi M, Hashimoto Y, Seki M, Kobayashi M, Kato T, Tabata S, Shinozaki K, and Kakimoto T. Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature,2001,409: 1060-1063.
72. Jaworski K, Szmidt-Jaworska A, and Kopcewicz J. Plant protein kinases stimulated by calcium. Postepy Biochem,2005,51,188-197.
73. Jentsch S, and Pyrowolakis G. Ubiquitin and its kin:how close are the family ties? Trends Cell Biol,2000,10:335-342.
74. Jones K M, Kobayashi H, Davies B W, Taga M E and Walker G C. How rhizobial symbionts invade plants:the Sinorhizobium-Medicago model. Nat Rev Microbiol,2007,5:619-633.
75. Kalo P, Gleason C, Edwards A, Marsh J, Mitra R M, Hirsch S, Jakab J, Sims S, Long S R, Rogers J, Kiss G B, Downie J A and Oldroyd G E. Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science,2005,308: 1786-1789.
76. Kanamori N, Madsen L H, Radutoiu S, Frantescu M, Quistgaard E M, Miwa H, Downie J A, James E K, Felle H H, Haaning L L, Jensen T H, Sato S, Nakamura Y, Tabata S, Sandal N and Stougaard J. A nucleoporin is required for induction of Ca2+spiking in legume nodule development and essential for rhizobial and fungal symbiosis. Proc Natl Acad Sci U S A,2006, 103:359-364.
77. Kaye F J, Modi S, Ivanovska I, Koonin E V, Thress K, Kubo A, Kornbluth S, and Rose M D. A family of ubiquitin-like proteins binds the ATPase domain of Hsp70-like Stch. FEBS Lett,2000, 467:348-355.
78. Kerstetter R, Bollman K, Taylor R, Bomblies K, and Poethig R. KANADI regulates organ polarity in Arabidopsis. Nature,2001,411:706-709.
79. Kevei Z, Lougnon G, Mergaert P, Horvath G V, Kereszt A, Jayaraman D, Zaman N, Marcel F, Regulski K, Kiss G B, Kondorosi A, Endre G, Kondorosi E and Ane J M. 3-hydroxy-3-methylglutaryl coenzyme a reductase 1 interacts with NORK and is crucial for nodulation in Medicago truncatula. Plant Cell,2007,19:3974-3989.
80. Kiss E, Olah B, Kalo P, Morales M, Heckmann A B, Borbola A, Lozsa A, Kontar K, Middleton P, Downie J A, Oldroyd G E, and Endre G. LIN, a novel type of U-box/WD40 protein, controls early infection by rhizobia in legumes. Plant Physiol,2009,151:1239-1249.
81. Kistner C, Winzer T, Pitzschke A, Mulder L, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J, Webb K J, Szczyglowski K, and Parniske M. Seven Lotus japonicus genes required for transcriptional reprogramming of the root during fungal and bacterial symbiosis. Plant Cell, 2005,17,2217-2229.
82. Kistner C, and Parniske M. Evolution of signal transduction in intracellular symbiosis. Trends Plant Sci,2002,7:511-518.
83. Kondorosi E, Redondo-Nieto M, and Kondorosi A. Ubiquitin-mediated proteolysis. To be in the right place at the right moment during nodule development. Plant Physiol,2005,137: 1197-1204.
84. Kouchi H, Imaizumi-Anraku H, Hayashi M, Hakoyama T, Nakagawa T, Umehara Y, Suganuma N, and Kawaguchi M. How many peas in a pod? Legume genes responsible for mutualistic symbioses underground. Plant Cell Physiol,2010,51,1381-1397.
85. Kumagai H, and Kouchi H. Gene silencing by expression of hairpin RNA in Lotus japonicus roots and root nodules. Mol Plant Microbe Interact,2003,16:663-668.
86. Lee S S, Cho H S, Yoon G M, Ahn J W, Kim H H, and Pai H S. Interaction of NtCDPKl calcium-dependent protein kinase with NtRpn3 regulatory subunit of the 26S proteasome in Nicotiana tabacum. Plant J,2003,33:825-840.
87. Lerouge P, Roche P, Faucher C, Maillet F, Truchet G, Prome J C and Denarie J. Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature,1990,344:781-784.
88. Levy J, Bres C, Geurts R, Chalhoub B, Kulikova O, Due G, Journet E P, Ane J M, Lauber E, Bisseling T, Denarie J, Rosenberg C, and Debelle F. A putative Ca2+and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science,2004,303:1361-1364.
89. Li J and Chory J. A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell,1997,90:929-938.
90. Lohar D P, Schaff J E, Laskey J G, Kieber J J, Bilyeu K D and Bird D M. Cytokinins play opposite roles in lateral root formation, and nematode and Rhizobial symbioses. Plant J,2004, 38:203-214.
91. Lohar D P, Sharopova N, Endre G, Penuela S, Samac D, Town C, Silverstein K A and VandenBosch K A. Transcript analysis of early nodulation events in Medicago truncatula. Plant Physiol,2006,140:221-234.
92. Lorteau M A, Ferguson B J and Guinel F C. Effects of cytokinin on ethylene production and nodulation in pea(Pisum sativum) cv. Sparkle. Physiol Plant,2001,112:421-428.
93. Lupas A, Van Dyke M, and Stock J. Predicting coiled coils from protein sequences. Science, 1991,252:1162-1164.
94. Madsen E B, Antolin-Llovera M, Grossmann C, Ye J, Vieweg S, Broghammer A, Krusell L, Radutoiu S, Jensen O N, Stougaard J, and Parniske M. Autophosphorylation is essential for the in vivo function of the Lotus japonicus Nod factor receptor 1 and receptor-mediated signalling in cooperation with Nod factor receptor 5. Plant J,2011,65,404-417.
95. Madsen E B, Madsen L H, Radutoiu S, Olbryt M, Rakwalska M, Szczyglowski K, Sato S, Kaneko T, Tabata S, Sandal N and Stougaard J. A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature,2003,425:637-640.
96. Madsen L, Tirichine L, Jurkiewicz A, Sullivan J, Heckmann A, Bek A, Ronson C, James E, Stougaard. The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nature Communications,2010,1:1-12.
97. Maekawa T, Maekawa-Yoshikawa M, Takeda N, Imaizumi-Anraku H, Murooka Y, and Hayashi M. Gibberellin controls the nodulation signaling pathway in Lotus japonicus. Plant J,2009,58, 183-194.
98. Mahonen A R, Bonke M, Kauppinen L, Riikonen M, Benfey P N, and Helariutta Y. A novel two-component hybrid molecule regulates vascular morphogenesis of the Arabidopsis root. Genes Dev,2000,14:2938-2943.
99. Maillet F, Poinsot V, Andre O, Puech-Pages V, Haouy A, Gueunier M, Cromer L, Giraudet D, Formey D, Niebel A, Martinez E A, Driguez H, Becard G, and Denarie J. Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature,2011,469:58-63.
100. Majello B, Kenyon L C, and Dalla-Favera R. Human c-myb protooncogene:nucleotide sequence of cDNA and organization of the genomic locus. Proc Natl Acad Sci U S A,1986,83:9636-9640.
101. Marian C O, Bordoli S J, Goltz M, Santarella R A, Jackson L P, Danilevskaya O, Beckstette M, Meeley R, and Bass H W. The maize Single myb histone 1 gene, Smhl, belongs to a novel gene family and encodes a protein that binds telomere DNA repeats in vitro. Plant Physiol,2003,133: 1336-1350.
102. Markmann K, Giczey G and Parniske M. Functional adaptation of a plant receptor-kinase paved the way for the evolution of intracellular root symbioses with bacteria. PLoS Biol,2008,6:e68.
103. Marsh J F, Rakocevic A, Mitra R M, Brocard L, Sun J, Eschstruth A, Long S R, Schultze M, Ratet P and Oldroyd G E. Medicago truncatula NIN is essential for rhizobial-independent nodule organogenesis induced by autoactive calcium/calmodulin-dependent protein kinase. Plant Physiol,2007,144:324-335.
104. Mathesius U, Charon C, Rolfe B G, Kondorosi A and Crespi M. Temporal and spatial order of events during the induction of cortical cell divisions in white clover by Rhizobium leguminosarum bv. trifolii inoculation or localized cytokinin addition. Mol Plant Microbe Interact,2000,13(6):617-628.
105. Mathesius U, Schlaman H R, Spaink H P, Of Sautter C, Rolfe B G and Djordjevic M A. Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides. Plant J,1998,14(1):23-34.
106. McGonigle T, Miller M, Evans D, Fairchild G, and Swan J. A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytologist,1990,115:495-501.
107. Messinese E, Mun J H, Yeun L H, Jayaraman D, Rouge P, Barre A, Lougnon G, Schornack S, Bono J J, Cook D R, and Ane J M. A novel nuclear protein interacts with the symbiotic DMI3 calcium-and calmodulin-dependent protein kinase of Medicago truncatula. Mol Plant Microbe Interact,2007,20:912-921.
108. Middleton P H, Jakab J, Penmetsa R V, Starker C G, Doll J, Kalo P, Prabhu R, Marsh J F, Mitra R M, Kereszt A, Dudas B, VandenBosch K, Long S R, Cook D R, Kiss G B, and Oldroyd G E. An ERF transcription factor in Medicago truncatula that is essential for Nod factor signal transduction. Plant Cell,2007,19:1221-1234.
109. Mitra R M, Gleason C A, Edwards A, Hadfield J, Downie J A, Oldroyd G E, and Long S R. A Ca2+/calmodulin-dependent protein kinase required for symbiotic nodule development:Gene identification by transcript-based cloning. Proc Natl Acad Sci USA,2004,101:4701-4705.
110. Miwa H, Sun J, Oldroyd G E and Downie J A. Analysis of Nod-factor-induced calcium signaling in root hairs of symbiotically defective mutants of Lotus japonicus. Mol Plant Microbe Interact, 2006,19:914-92.
111. Miyazawa H, Oka-Kira E, Sato N, Takahashi H, Wu G J, Sato S, Hayashi M, Betsuyaku S, Nakazono M, Tabata S, Harada K, Sawa S, Fukuda H, and Kawaguchi M. The receptor-like kinase KLAVIER mediates systemic regulation of nodulation and non-symbiotic shoot development in Lotus japonicus. Development,2010,137:4317-4325.
112. Murakami Y, Miwa H, Imaizumi-Anraku H, Kouchi H, Downie J A, Kawaguchi M and Kawasaki S. Positional cloning identifies Lotus japonicus NSP2, a putative transcription factor of the GRAS family, required for N1N and ENOD40 gene expression in nodule initiation. DNA Res,2006,13:255-265.
113. Murray J D, Karas B J, Sato S, Tabata S, Amyot L, and Szczyglowski K. A cytokinin perception mutant colonized by Rhizobium in the absence of nodule organogenesis. Science,2007,315: 101-104.
114. Mylona P, Pawlowski K and Bisseling T. Symbiotic Nitrogen Fixation. Plant Cell,1995,7: 869-885.
115. Nam K H and Li J. BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell, 2002,110:203-212.
116. Nishimura R, Ohmori M, Fujita H, and Kawaguchi M. A Lotus basic leucine zipper protein with a RING-finger motif negatively regulates the developmental program of nodulation. Proc Natl Acad Sci USA,2002,99:15206-15210.
117. Nontachaiyapoom S, Scott P T, Men A E, Kinkema M, Schenk P M, and Gresshoff P M. Promoters of orthologous Glycine max and Lotus japonicus nodulation autoregulation genes interchangeably drive phloem-specific expression in transgenic plants. Mol Plant Microbe Interact,2007,20:769-780.
118.Norbert C A, Ruijter d, Bisseling T and Emons A M C. Rhizobium Nod Factors Induce an Increase in Sub-apical Fine Bundles of Actin Filaments in Vicia sativa Root Hairs within Minutes. Mol Plant Microbe Interact,1999,12:829-832.
119. Ogata K, Hojo H, Aimoto S, Nakai T, Nakamura H, Sarai A, Ishii S, and Nishimura Y. Solution structure of a DNA-binding unit of Myb:a helix-turn-helix-related motif with conserved tryptophans forming a hydrophobic core. Proc Natl Acad Sci USA,1992,89:6428-6432.
120. Oka-Kira E, and Kawaguchi M. Long-distance signaling to control root nodule number. Curr Opin Plant Biol,2006,9:496-502.
121. Oldroyd G E. Plant science. Nodules and hormones. Science,2007,315:52-53.
122. Oldroyd G E and Downie J A. Calcium, kinases and nodulation signalling in legumes. Nat Rev Mol Cell Biol,2004,5:566-576.
123. Oldroyd G E and Downie J A. Nuclear calcium changes at the core of symbiosis signalling. Curr Opin Plant Biol,2006,9:351-357.
124. Oldroyd G E, and Downie J A. Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol,2008,59:519-546.
125. Oldroyd G E, Harrison M J and Udvardi M. Peace talks and trade deals. Keys to long-term harmony in legume-microbe symbioses. Plant Physiol,2005,137:1205-1210.
126. Op den Camp R, Streng A, De Mita S, Cao Q, Polone E, Liu W, Ammiraju J S, Kudrna D, Wing R, Untergasser A, Bisseling T, and Geurts R. LysM-Type Mycorrhizal Receptor Recruited for Rhizobium Symbiosis in Nonlegume Parasponia. Science,2011,331:909-912.
127. Pacios-Bras C, Schlaman H R, Boot K, Admiraal P, Langerak J M, Stougaard J and Spaink H P. Auxin distribution in Lotus japonicus during root nodule development. Plant Mol Biol,2003,52: 1169-1180.
128. Parniske M. Arbuscular mycorrhiza:the mother of plant root endosymbioses. Nat Rev Microbiol, 2008,6:763-775
129. Parniske M and Downie J A. Plant biology:locks, keys and symbioses. Nature,2003,425: 569-570.
130. Parry D A, Fraser R D, and Squire J M. Fifty years of coiled-coils and alpha-helical bundles:a close relationship between sequence and structure. J Struct Biol,2008,163:258-269.
131. Pate J, Gunning B, and Briarty L. Ultrastructure and functioning of the transport system of the leguminous root nodule. Planta,1969,85:11-34.
132. Patharkar O R, and Cushman J C. A stress-induced calcium-dependent protein kinase from Mesembryanthemum crystallinum phosphorylates a two-component pseudo-response regulator. Plant J,2000,24:679-691.
133. Patil S, Takezawa D, and Poovaiah B W. Chimeric plant calcium/calmodulin-dependent protein kinase gene with a neural visinin-like calcium-binding domain. Proc Natl Acad Sci U S A,1995, 92:4897-4901.
134. Pawlowski K and Bisseling T. Rhizobial and Actinorhizal Symbioses:What Are the Shared Features? Plant Cell,1996,8:1899-1913.
135. Penmetsa R V, Frugoli J A, Smith L S, Long S R, and Cook D R. Dual genetic pathways controlling nodule number in Medicago truncatula. Plant Physiol,2003,131:998-1008.
136. Penmetsa R V, Uribe P, Anderson J, Lichtenzveig J, Gish J C, Nam Y W, Engstrom E, Xu K, Sckisel G, Pereira M, Baek J M, Lopez-Meyer M, Long S R, Harrison M J, Singh K B, Kiss G B, and Cook D R. The Medicago truncatula ortholog of Arabidopsis EIN2, sickle, is a negative regulator of symbiotic and pathogenic microbial associations. Plant J,2008,55:580-595.
137. Perret X, Staehelin C and Broughton W J. Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev,2000,64:180-201.
138. Pickart C M. Back to the future with ubiquitin. Cell,2004,116:181-190.
139. Poovaiah B W, Xia M, Liu Z, Wang W, Yang T, Sathyanarayanan P V, and Franceschi V R. Developmental regulation of the gene for chimeric calcium/calmodulin-dependent protein kinase in anthers. Planta,1999,209:161-171.
140. Pueppke S G. The genetic and biochemical basis for nodulation of legumes by rhizobia. Crit Rev Biotechnol,1996,16:1-51.
141. Pysh L D, Wysocka-Diller J W, Camilleri C, Bouchez D and Benfey P N. The GRAS gene family in Arabidopsis:sequence characterization and basic expression analysis of the SCARECROW-LIKE genes. Plant J,1999,18:111-119.
142. Radutoiu S, Madsen L H, Madsen E B, Felle H H, Umehara Y, Gronlund M, Sato S, Nakamura Y, Tabata S, Sandal N and Stougaard J. Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature,2003,425:585-592.
143. Ramachandiran S, Takezawa D, Wang W, and Poovaiah B W. Functional domains of plant chimeric calcium/calmodulin-dependent protein kinase:regulation by autoinhibitory and visinin-like domains. J Biol Chem,1997,121:984-990.
144. Richards D E, Peng J, and Harberd N P. Plant GRAS and metazoan STATs:one family? Bioessays,2000,22:573-577.
145. Ridge R W. A model of legume root hair growth and Rhizobium infection. Symbiosis,1993,14: 359-373.
146. Riechmann J, Heard J, Martin G, Reuber L, Jiang C, Keddie J, Adam L, Pineda O, Ratcliffe O J, Samaha R R, Creelman R, Pilgrim M, Broun P, Zhang J Z, Ghandehari D, Sherman B K, and Yu G. Arabidopsis transcription factors:genome-wide comparative analysis among eukaryotes. Science,2000,290:2105-2110.
147. Riely B K, Mun J H and Ane J M. Unravelling the molecular basis for symbiotic signal transduction in legumes. Mol. Plant Pathol,2006,7:197-207.
148. Roche R, Lerouge P, Ponthus C and Prome J C. Structural determination of bacterial nodulation factors involved in the Rhizobium meliloti-alfalfa symbiosis. J Biol Chem,1991,266: 10933-10940.
149. Rodriguez Milla M A, Uno Y, Chang I F, Townsend J, Maher E A, Quilici D, and Cushman J C. A novel yeast two-hybrid approach to identify CDPK substrates:characterization of the interaction between AtCPK11 and AtDi19, a nuclear zinc finger protein. FEBS Lett,2006,580: 904-911.
150. Rubio V, Linhares F, Solano R, Martin A C, Iglesias J, Leyva A, and Paz-Ares J. A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev,2001,15:2122-2133.
151. Ruijter N C A d, Rook M B, Bisseling T and Emons A M C. Lipochito-oligosaccharides re-initiate root hair tip growth in Vicia sativa with high calcium and spectrin-like antigen at the tip. Plant J,1998,13:341-350.
152. Saito K, Yoshikawa M, Yano K, Miwa H, Uchida H, Asamizu E, Sato S, Tabata S, Imaizumi-Anraku H, Umehara Y, Kouchi H, Murooka Y, Szczyglowski K, Downie J A, Parniske M, Hayashi M and Kawaguchi M. NUCLEOPORIN85 is required for calcium spiking, fungal and bacterial symbioses, and seed production in Lotus japonicus. Plant Cell,2007,19:610-624.
153.Saitou N, and Nei M. The neighbor-joining method:a new method for reconstructing phylogenetic trees. Mol Biol Evol,1987,4:406-425.
154. Sasaki T, Marcon E, McQuire T, Arai Y, Moens P B, and Okada H. Bat3 deficiency accelerates the degradation of Hsp70-2/HspA2 during spermatogenesis. J Cell Biol,2008,182:449-458.
155. Sathyanarayanan P V, Cremo C R, and Poovaiah B W. Plant chimeric Ca2+/Calmodulin-dependent protein kinase. Role of the neural visinin-like domain in regulating autophosphorylation and calmodulin affinity. J Biol Chem,2000,275:30417-30422.
156. Sathyanarayanan P V, Siems W F, Jones J P, and Poovaiah B W. Calcium-stimulated autophosphorylation site of plant chimeric calcium/calmodulin-dependent protein kinase. J Biol Chem,2001,276:32940-32947.
157. Savoure A, Magyar Z, Pierre M, Brown S, Schultze M, Dudits D, Kondorosi A and Kondorosi E. Activation of the cell cycle machinery and the isoflavonoid biosynthesis pathway by active Rhizobium meliloti Nod signal molecules in Medicago microcallus suspensions. EMBO J,1994, 13:1093-1102.
158. Schaffer R, Ramsay N, Samach A, Corden S, Putterill J, Carre I A, and Coupland G.. The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell,1998,93:1219-1229.
159. Schauser L, Roussis A, Stiller J and Stougaard J. A plant regulator controlling development of symbiotic root nodules. Nature,1999,402:191-195.
160. Schneider A, Walker S A, Poyser S, Sagan M, Ellis T H and Downie J A. Genetic mapping and functional analysis of a nodulation-defective mutant (sym19) of pea (Pisum sativum L.). Mol Gen Genet,1999,262:1-11.
161. Schwikowski B, Uetz P and Fields S. A network of protein-protein interactions in yeast. Nat Biotechnol,2000,18:1257-1261.
162. Searle I R, Men A E, Laniya T S, Buzas D M, Iturbe-Ormaetxe I, Carroll B J and Gresshoff P M. Long-distance signaling in nodulation directed by a CLAVATA1-like receptor kinase. Science, 2003,299:109-112.
163. Shimomura K, Nomura M, Tajima S and Kouchi H. LjnsRING, a novel RING finger protein, is required for symbiotic interactions between Mesorhizobium loti and Lotus japonicus. Plant Cell Physiol,2006,47:1572-1581.
164. Sinharoy S, DasGupta M. RNA interference highlights the role of CCaMK in dissemination of endosymbionts in the Aeschynomeneae legume Arachis. Mol Plant Microbe Interact,2009,22: 1466-1475.
165. Smit G, Kijne J W and Lugtenberg B J. Roles of flagella, lipopolysaccharide, and a Ca2+-dependent cell surface protein in attachment of Rhizobium leguminosarum biovar viciae to pea root hair tips. JBacteriol,1989a,171:569-572.
166. Smit G, Logman T J, Boerrigter M E, Kijne J W and Lugtenberg B J. Purification and partial characterization of the Rhizobium leguminosarum biovar viciae Ca2+-dependent adhesin, which mediates the first step in attachment of cells of the family Rhizobiaceae to plant root hair tips. J Bacteriol,1989b,171:4054-4062.
167. Smit P, Limpens E, Geurts R, Fedorova E, Dolgikh E, Gough C and Bisseling T. Medicago LYK3, an entry receptor in rhizobial nodulation factor signaling. Plant Physiol,2007,145: 183-191.
168. Smit P, Raedts J, Portyanko V, Debelle F, Gough C, Bisseling T and Geurts R. NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science,2005, 308:1789-1791.
169. Sprent, J I. Evolving ideas of legume evolution and diversity:a taxonomic perspective on the occurrence of nodulation. New Phytol,2007,174,11-25.
170. Stacey G, Libault M, Brechenmacher L, Wan J, and May G. D. Genetics and functional genomics of legume nodulation. Curr Opin Plant Biol,2006,9:110-121.
171. Staehelin C, Granado J, Muller J, Wiemken A, Mellor R B, Felix G, Regenass M, Broughton W J and Boller T. Perception of Rhizobium nodulation factors by tomato cells and inactivation by root chitinases. Proc Natl Acad Sci USA,1994,91:2196-2200.
172. Stracke R, Werber M, and Weisshaar B. The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol,2001,4:447-456.
173. Stracke S, Kistner C, Yoshida S, Mulder L, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J, Szczyglowski K and Parniske M. A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature,2002,417:959-962.
174. Subramanian S, Stacey G and Yu O. Endogenous isoflavones are essential for the establishment of symbiosis between soybean and Bradyrhizobium japonicum. Plant J,2006,48:261-273.
175. Sun J, Cardoza V, Mitchell D M, Bright L, Oldroyd G and Harris J M. Crosstalk between jasmonic acid, ethylene and Nod factor signaling allows integration of diverse inputs for regulation of nodulation. Plant J,2006,46:961-970.
176. Suzuki T, Miwa K, Ishikawa K, Yamada H, Aiba H, and Mizuno T. The Arabidopsis sensor His-kinase, AHk4, can respond to cytokinins. Plant Cell Physiot,2001,42:107-113.
177. Takezawa D, Ramachandiran S, Paranjape V, and Poovaiah B W. Dual regulation of a chimeric plant serine/threonine kinase by calcium and calcium/calmodulin. J Biol Chem,1996,271: 8126-8132.
178. Tamura K, Dudley J, Nei M, and Kumar S. MEGA4:Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol,2007,24:1596-1599.
179. Tansengco M L, Hayashi M, Kawaguchi M, Imaizumi-Anraku H, and Murooka Y. crinkle, a novel symbiotic mutant that affects the infection thread growth and alters the root hair, trichome, and seed development in Lotus japonicus. Plant Physiol,2003,131:1054-1063.
180. Thompson J D, Gibson T J, Plewniak F, Jeanmougin F, and Higgins D G. The CLUSTAL_X windows interface:flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res,1997,25:4876-4882.
181. Thress K, Henzel W, Shillinglaw W, and Kornbluth S. Scythe:a novel reaper-binding apoptotic regulator. EMBOJ,1998,17:6135-6143.
182. Thress K, Song J, Morimoto R I, and Kornbluth S. Reversible inhibition of Hsp70 chaperone function by Scythe and Reaper. EMBOJ,2001,20:1033-1041.
183. Tian C, Wan P, Sun S, Li J, and Chen M. Genome-wide analysis of the GRAS gene family in rice and Arabidopsis. Plant Mol Biol,2004,54:519-532.
184. Timmers A C, Auriac M C and Truchet G. Refined analysis of early symbiotic steps of the Rhizobium-Medicago interaction in relationship with microtubular cytoskeleton rearrangements. Development,1999,126:3617-3628.
185. Tirichine L, Imaizumi-Anraku H, Yoshida S, Murakami Y, Madsen L H, Miwa H, Nakagawa T, Sandal N, Albrektsen A S, Kawaguchi M, Downie A, Sato S, Tabata S, Kouchi H, Parniske M, Kawasaki S and Stougaard J. Deregulation of a Ca27calmodulin-dependent kinase leads to spontaneous nodule development. Nature,2006,441:1153-1156.
186. Tirichine L, Sandal N, Madsen L H, Radutoiu S, Albrektsen A S, Sato S, Asamizu E, Tabata S and Stougaard J. A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis. Science,2007,315:104-107.
187. Uno Y, Rodriguez Milla M A, Maher E, and Cushman J C. Identification of proteins that interact with catalytically active calcium-dependent protein kinases from Arabidopsis. Mol Genet Genomics,2009,281:375-390.
188. van-Batenburg F H D, Jonker R and Kijne J W. Rhizobium induces marked root hair curling by redirection of tip growth:a computer simulation. Physiol Plant,1986,66:476-480.
189. van Brussel A A, Bakhuizen R, van Spronsen P C, Spaink H P, Tak T, Lugtenberg B J and Kijne J W. Induction of Pre-Infection Thread Structures in the Leguminous Host Plant by Mitogenic Lipo-Oligosaccharides of Rhizobium. Science,1992,257:70-72.
190. Vijn I, das Nevas L, van Kammen A, Franssen H and Bisseling T. Nod factors and nodulation in plants. Science,1993,260:1764-1765.
191. Waadt R, Schmidt L K, Lohse M, Hashimoto K, Bock R, and Kudla J. Multicolor bimolecular fluorescence complementation reveals simultaneous formation of alternative CBL/CIPK complexes in planta. Plant J,2008,56:505-516.
192. Walter M, Chaban C, Schutze K, Batistic O, Weckermann K, Nake C, Blazevic D, Grefen C, Schumacher K, Oecking C, Harter K, and Kudla J. Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J,2004,40:428-438.
193. Wang D, Harper J F, Gribskov M. Systematic trans-genomic comparison of protein kinases between Arabidopsis and Saccharomyces cerevisiae. Plant Physiol,2003,132:2152-2165.
194. Wang Z Y, Kenigsbuch D, Sun L, Harel E, Ong M S, and Tobin E M. A Myb-related transcription factor is involved in the phytochrome regulation of an Arabidopsis Lhcb gene. Plant Cell,1997, 9:491-507.
195. Wang W, and Poovaiah B W. Interaction of plant chimeric calcium/calmodulin-dependent protein kinase with a homolog of eukaryotic elongation factor-1 alpha. J Biol Chem,1999,274: 12001-12008.
196. Webb K J, Skot L, Nicholson M N, Jorgensen B, and Mizen S. Mesorhizobium loti increases root-specific expression of a calcium-binding protein homologue identified by promoter tagging in Lotus japonicus. Mol Plant Microbe Interact,2000,13:606-616.
197. Wopereis J, Pajuelo E, Dazzo F B, Jiang Q, Gresshoff P M, De Bruijn F J, Stougaard J, and Szczyglowski K. Short root mutant of Lotus japonicus with a dramatically altered symbiotic phenotype. Plant J,2000,23:97-114.
198. Wykoff D D, Grossman A R, Weeks D P, Usuda H, and Shimogawara K. Psrl, a nuclear localized protein that regulates phosphorus metabolism in Chlamydomonas. Proc Natl Acad Sci USA,1999,96:15336-15341.
199. Yang T, and Poovaiah B W. Calcium/calmodulin-mediated signal network in plants. Trends Plant Sci,2003,8:505-512.
200. Yokota K, Soyano T, Kouchi H, and Hayashi M. Function of GRAS proteins in root nodule symbiosis is retained in homologs of a non-legume, rice. Plant Cell Physiol,2010,51: 1436-1442.
201.Yano K, Shibata S, Chen W L, Sato S, Kaneko T, Jurkiewicz A, Sandal N, Banba M, Imaizumi-Anraku H, Kojima T, Ohtomo R, Szczyglowski K, Stougaard J, Tabata S, Hayashi M, Kouchi H, and Umehara Y CERBERUS, a novel U-box protein containing WD-40 repeats, is required for formation of the infection thread and nodule development in the legume-Rhizobium symbiosis. Plant J,2009,60:168-180.
202. Yano K, Yoshida S, Muller J, Singh S, Banba M, Vickers K, Markmann K, White C, Schuller B, Sato S, Asamizu E, Tabata S, Murooka Y, Perry J, Wang T L, Kawaguchi M, Imaizumi-Anraku H, Hayashi M, and Parniske M. CYCLOPS, a mediator of symbiotic intracellular accommodation. Proc Natl Acad Sci U S A,2008,105:20540-20545.
203. Yoshida S and Parniske M. Regulation of plant symbiosis receptor kinase through serine and threonine phosphorylation. J Biol Chem,2005,280:9203-9209.
204. Zhu H, Chen T, Zhu M, Fang Q, Kang H, Hong Z, and Zhang Z. A novel ARID DNA-binding protein interacts with SymRK and is expressed during early nodule development in Lotus japonicus. Plant Physiol,2008,148:337-347.
© 2004-2018 中国地质图书馆版权所有 京ICP备05064691号 京公网安备11010802017129号 地址：北京市海淀区学院路29号 邮编：100083 电话：办公室：(+86 10)66554848；文献借阅、咨询服务、科技查新：66554700 |