Advertisement

Journal of Plant Biology

, Volume 58, Issue 5, pp 271–284 | Cite as

Molecular insights into the function of ankyrin proteins in plants

  • Kieu Thi Xuan Vo
  • Chi-Yeol Kim
  • Anil Kumar Nalini Chandran
  • Ki-Hong Jung
  • Gynheung An
  • Jong-Seong JeonEmail author
Review Article

Abstract

Ankyrin (ANK) repeat domain-containing proteins comprise one of the largest known protein superfamilies in all species including plants. Recently, several genomeanalysis studies have provided valuable information on the structure of ANK proteins in plants. Among the 13 subgroups based on the presence of various additional domains in addition to the ANK domain, the E3 ubiquitin ligase activity and transcriptional regulation functions of ANK-RF and ANK-ZF subgroup members, respectively, are relatively well understood. NPR1 (nonexpressor of pathogenesis-related1), a key regulator of systemic acquired resistance in Arabidopsis, is a noteworthy member of the ANK-BTB subgroup; however, ANK-M and ANK-TM, the two main subgroups, have been less functionally characterized. With the ability to mediate protein-protein interactions, the majority of plant ANK proteins play crucial roles in defense responses and, on occasion, functions in growth and development. In this review, we summarize on the current knowledge of plant ANK superfamily members and focus on ANK proteins involved in defense responses. In addition, we provide a valuable framework for the future functional characterization of ANK genes with current unknown function in rice, a model crop species.

Keywords

Ankyrin Defense Function Gene expression Mutant Rice Subcellular localization 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Supplementary material

12374_2015_228_MOESM1_ESM.pdf (552 kb)
Supplementary material, approximately 309 KB.

References

  1. AbuQamar S, Chen X, Dhawan R, Bluhm B, Salmeron J, Lam S, Dietrich RA, Mengiste T (2006) Expression profiling and mutant analysis reveals complex regulatory networks involved in Arabidopsis response to Botrytis infection. Plant J 48:28–44PubMedCrossRefGoogle Scholar
  2. Albert S, Després B, Guilleminot J, Bechtold N, Pelletier G, Delseny M, Devic M (1999) TheEMB506 gene encodes a novel ankyrin repeat containing protein that is essential for the normal development of Arabidopsis embryos. Plant J 17:169–179PubMedCrossRefGoogle Scholar
  3. Bae W, Lee YJ, Kim DH, Lee J, Kim S, Sohn EJ, Hwang I (2008) AKR2A-mediated import of chloroplast outer membrane proteins is essential for chloroplast biogenesis. Nat Cell Biol 10: 220–227PubMedCrossRefGoogle Scholar
  4. Bardwell VJ, Treisman R (1994) The POZ domain: a conserved protein-protein interaction motif. Genes Dev 8:1664–1677PubMedCrossRefGoogle Scholar
  5. Batistiè O (2012) Genomics and localization of the Arabidopsis DHHC-cysteine-rich domain S-acyltransferase protein family. Plant Physiol 160:1597–1612CrossRefGoogle Scholar
  6. Becerra C, Jahrmann T, Puigdomènech P, Vicient CM (2004) Ankyrin repeat-containing proteins in Arabidopsis: characterization of a novel and abundant group of genes coding ankyrin-transmembrane proteins. Gene 340:111–121PubMedCrossRefGoogle Scholar
  7. Blanvillain R, Wei S, Wei P, Kim JH, Ow DW (2011) Stress tolerance to stress escape in plants: role of the OXS2 zinc-finger transcription factor family. EMBO J 30:3812–3822PubMedCentralPubMedCrossRefGoogle Scholar
  8. Borden KL (2000) RING domains: master builders of molecular scaffolds? J Mol Biol 295:1103–1112PubMedCrossRefGoogle Scholar
  9. Böttner S, Iven T, Carsjens CS, Dröge-Laser W (2009) Nuclear accumulation of the ankyrin repeat protein ANK1 enhances the auxin-mediated transcription accomplished by the bZIP transcription factors BZI-1 and BZI-2. Plant J 58:914–926PubMedCrossRefGoogle Scholar
  10. Bouché N, Scharlat A, Snedden W, Bouchez D, Fromm H (2002) A novel family of calmodulin-binding transcription activators in multicellular organisms. J Biol Chem 277:21851–21861PubMedCrossRefGoogle Scholar
  11. Breeden L, Nasmyth K (1987) Similarity between cell-cycle genes of budding yeast and fission yeast and the Notch gene of Drosophila. Nature 329:651–659PubMedCrossRefGoogle Scholar
  12. Canet JV, Dobón A, Fajmonová J, Tornero P (2012) The BLADEON-PETIOLE genes of Arabidopsis are essential for resistance induced by methyl jasmonate. BMC Plant Biol 12:199PubMedCentralPubMedCrossRefGoogle Scholar
  13. Cao H, Bowling SA, Gordon AS, Dong X (1994) Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6:1583–1592PubMedCentralPubMedCrossRefGoogle Scholar
  14. Cao H, Glazebrook J, Clarke JD, Volko S, Dong X (1997) The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88:57–63PubMedCrossRefGoogle Scholar
  15. Cao H, Li X, Dong X (1998) Generation of broad-spectrum disease resistance by overexpression of an essential regulatory gene in systemic acquired resistance. Proc Natl Acad Sci USA 95:6531–6536PubMedCentralPubMedCrossRefGoogle Scholar
  16. Carvalho SD, Saraiva R, Maia TM, Abreu IA, Duque P (2012) XBAT35, a Novel Arabidopsis RING E3 Ligase Exhibiting Dual Targeting of Its Splice Isoforms, Is Involved in Ethylene-Mediated Regulation of Apical Hook Curvature. Mol Plant 5: 1295–1309PubMedCrossRefGoogle Scholar
  17. Chern M, Bai W, Ruan D, Oh T, Chen X, Ronald PC (2014) Interaction specificity and coexpression of rice NPR1 homologs 1 and 3 (NH1 and NH3), TGA transcription factors and Negative Regulator of Resistance (NRR) proteins. BMC Genomics 15: 461PubMedCentralPubMedCrossRefGoogle Scholar
  18. Chern M, Fitzgerald HA, Canlas PE, Navarre DA, Ronald PC (2005) Overexpression of a rice NPR1 homolog leads to constitutive activation of defense response and hypersensitivity to light. Mol Plant-Microbe Interact 18:511–520PubMedCrossRefGoogle Scholar
  19. Cui Y-L, Jia Q-S, Yin Q-Q, Lin G-N, Kong M-M, Yang Z-N (2011) The GDC1 gene encodes a novel ankyrin domain-containing protein that is essential for grana formation in Arabidopsis. Plant Physiol 155:130–141PubMedCentralPubMedCrossRefGoogle Scholar
  20. Deng-wei J, Min C, Qing Y (2014) Cloning and characterization of a Solanum torvum NPR1 gene involved in regulating plant resistance to Verticillium dahliae. Acta Physiol Plant 36:2999–3011CrossRefGoogle Scholar
  21. Després C, DeLong C, Glaze S, Liu E, Fobert PR (2000) The Arabidopsis NPR1/NIM1 protein enhances the DNA binding activity of a subgroup of the TGA family of bZIP transcription factors. Plant Cell 12:279–290PubMedCentralPubMedCrossRefGoogle Scholar
  22. Dong X (2004a) NPR1, all things considered. Curr Opin Plant Biol 7: 547–552PubMedCrossRefGoogle Scholar
  23. Dong X (2004b) The role of membrane-bound ankyrin-repeat protein ACD6 in programmed cell death and plant defense. Sci STKE 2004:pe6PubMedGoogle Scholar
  24. Du ZY, Chen MX, Chen QF, Xiao S, Chye ML (2013) Arabidopsis acyl-CoA-binding protein ACBP1 participates in the regulation of seed germination and seedling development. Plant J 74:294–309PubMedCrossRefGoogle Scholar
  25. Fan W, Dong X (2002) In vivo interaction between NPR1 and transcription factor TGA2 leads to salicylic acid–mediated gene activation in Arabidopsis. Plant Cell 14:1377–1389PubMedCentralPubMedCrossRefGoogle Scholar
  26. Feys BJ, Moisan LJ, Newman MA, Parker JE (2001) Direct interaction between the Arabidopsis disease resistance signaling proteins, EDS1 and PAD4. EMBO J 20:5400–5411PubMedCentralPubMedCrossRefGoogle Scholar
  27. Fitzgerald HA, Chern M-S, Navarre R, Ronald PC (2004) Overexpression of (At) NPR1 in rice leads to a BTH-and environment-induced lesion-mimic/cell death phenotype. Mol Plant-Microbe Interact 17:140–151PubMedCrossRefGoogle Scholar
  28. Fridborg I, Grainger J, Page A, Coleman M, Findlay K, Angell S (2003) TIP, a novel host factor linking callose degradation with the cell-to-cell movement of Potato virus X. Mol Plant-Microbe Interact 16:132–140PubMedCrossRefGoogle Scholar
  29. Fu ZQ, Yan S, Saleh A, Wang W, Ruble J, Oka N, Mohan R, Spoel SH, Tada Y, Zheng N (2012) NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature 486:228–232PubMedCentralPubMedGoogle Scholar
  30. Galon Y, Nave R, Boyce JM, Nachmias D, Knight MR, Fromm H (2008) Calmodulin-binding transcription activator (CAMTA) 3 mediates biotic defense responses in Arabidopsis. FEBS Lett 582:943–948PubMedCrossRefGoogle Scholar
  31. Gao W, Li H-Y, Xiao S, Chye M-L (2010a) Protein interactors of acyl-CoA-binding protein ACBP2 mediate cadmium tolerance in Arabidopsis. Plant Signal Behav 5:1025–1027PubMedCentralPubMedCrossRefGoogle Scholar
  32. Gao W, Li HY, Xiao S, Chye ML (2010b) Acyl-CoA-binding protein 2 binds lysophospholipase 2 and lysoPC to promote tolerance to cadmium-induced oxidative stress in transgenic Arabidopsis. Plant J 62:989–1003PubMedGoogle Scholar
  33. Garcion C, Guilleminot J, Kroj T, Parcy F, Giraudat J, Devic M (2006) AKRP and EMB506 are two ankyrin repeat proteins essential for plastid differentiation and plant development in Arabidopsis. Plant J 48:895–906PubMedCrossRefGoogle Scholar
  34. Hartje S, Zimmermann S, Klonus D, Mueller-Roeber B (2000) Functional characterisation of LKT1, a K+ uptake channel from tomato root hairs, and comparison with the closely related potato inwardly rectifying K+ channel SKT1 after expression in Xenopus oocytes. Planta 210:723–731PubMedCrossRefGoogle Scholar
  35. Hemsley PA, Kemp AC, Grierson CS (2005) The TIP GROWTH DEFECTIVE1 S-acyl transferase regulates plant cell growth in Arabidopsis. Plant Cell 17:2554–2563PubMedCentralPubMedCrossRefGoogle Scholar
  36. Hirsch RE, Lewis BD, Spalding EP, Sussman MR (1998) A role for the AKT1 potassium channel in plant nutrition. Science 280: 918–921PubMedCrossRefGoogle Scholar
  37. Huang J, Chen F, Del Casino C, Autino A, Shen M, Yuan S, Peng J, Shi H, Wang C, Cresti M (2006) An ankyrin repeat-containing protein, characterized as a ubiquitin ligase, is closely associated with membrane-enclosed organelles and required for pollen germination and pollen tube growth in lily. Plant Physiol 140: 1374–1383PubMedCentralPubMedCrossRefGoogle Scholar
  38. Huang J, Zhao X, Yu H, Ouyang Y, Wang L, Zhang Q (2009) The ankyrin repeat gene family in rice: genome-wide identification, classification and expression profiling. Plant Mol Biol 71:207–226PubMedCrossRefGoogle Scholar
  39. Jaru-Ampornpan P, Liang F-C, Nisthal A, Nguyen TX, Wang P, Shen K, Mayo SL, Shan SO (2013) Mechanism of an ATP-independent protein disaggregase II. Distinct molecular interactions drive multiple steps during aggregate disassembly. J Biol Chem 288: 13431–13445PubMedCentralPubMedCrossRefGoogle Scholar
  40. Jeon JS, Lee S, Jung KH, Jun SH, Jeong DH, Lee J, Kim C, Jang S, Lee S, Yang K (2000) T-DNA insertional mutagenesis for functional genomics in rice. Plant J 22:561–570PubMedCrossRefGoogle Scholar
  41. Jiang H, Wu Q, Jin J, Sheng L, Yan H, Cheng B, Zhu S (2013a) Genome-wide identification and expression profiling of ankyrinrepeat gene family in maize. Dev Genes Evol 223:303–318PubMedCrossRefGoogle Scholar
  42. Jiang Y, Chen X, Ding X, Wang Y, Chen Q, Song WY (2013b) The XA21 binding protein XB25 is required for maintaining XA21- mediated disease resistance. Plant J 73:814–823PubMedCrossRefGoogle Scholar
  43. Johnson C, Boden E, Arias J (2003) Salicylic acid and NPR1 induce the recruitment of trans-activating TGA factors to a defense gene promoter in Arabidopsis. Plant Cell 15:1846–1858PubMedCentralPubMedCrossRefGoogle Scholar
  44. Kim DH, Park M-J, Gwon GH, Silkov A, Xu Z-Y, Yang EC, Song S, Song K, Kim Y, Yoon HS (2014) Chloroplast targeting factor AKR2 evolved from an ankyrin repeat domain coincidentally binds two chloroplast lipids. Dev Cell 30:598–609PubMedCentralPubMedCrossRefGoogle Scholar
  45. Kim DH, Xu Z-Y, Na YJ, Yoo Y-J, Lee J, Sohn E-J, Hwang I (2011) Small heat shock protein Hsp17.8 functions as an AKR2A cofactor in the targeting of chloroplast outer membrane proteins in Arabidopsis. Plant Physiol 157:132–146PubMedCentralPubMedCrossRefGoogle Scholar
  46. Kohl A, Binz HK, Forrer P, Stumpp MT, Plückthun A, Grütter MG (2003) Designed to be stable: crystal structure of a consensus ankyrin repeat protein. Proc Natl Acad Sci USA 100:1700–1705PubMedCentralPubMedCrossRefGoogle Scholar
  47. Koizumi K, Naramoto S, Sawa S, Yahara N, Ueda T, Nakano A, Sugiyama M, Fukuda H (2005) VAN3 ARF–GAP-mediated vesicle transport is involved in leaf vascular network formation. Development 132:1699–1711PubMedCrossRefGoogle Scholar
  48. Krishna SS, Majumdar I, Grishin NV (2003) SURVEY AND SUMMARY: Structural classification of zinc fingers. Nucleic Acids Res 31:532–550PubMedCentralPubMedCrossRefGoogle Scholar
  49. Kuhlmann M, Horvay K, Strathmann A, Heinekamp T, Fischer U, Böttner S, Dröge-Laser W (2003) The a-helical D1 domain of the tobacco bZIP transcription factor BZI-1 interacts with the ankyrin-repeat protein ANK1 and is important for BZI-1 function, both in auxin signaling and pathogen response. J Biol Chem 278:8786–8794PubMedCrossRefGoogle Scholar
  50. Kumagai H, Hakoyama T, Umehara Y, Sato S, Kaneko T, Tabata S, Kouchi H (2007) A novel ankyrin-repeat membrane protein, IGN1, is required for persistence of nitrogen-fixing symbiosis in root nodules of Lotus japonicus. Plant Physiol 143:1293–1305PubMedCentralPubMedCrossRefGoogle Scholar
  51. Lin W-C, Lu C-F, Wu J-W, Cheng M-L, Lin Y-M, Yang N-S, Black L, Green SK, Wang J-F, Cheng C-P (2004) Transgenic tomato plants expressing the Arabidopsis NPR1 gene display enhanced resistance to a spectrum of fungal and bacterial diseases. Transgenic Res 13:567–581PubMedCrossRefGoogle Scholar
  52. Liu W, Triplett L, Liu J, Leach JE, Wang G-L (2014) Novel Insights into Rice Innate Immunity against Bacterial and Fungal Pathogens. Annu Rev Phytopathol 52:213–241PubMedCrossRefGoogle Scholar
  53. Lorick KL, Jensen JP, Fang S, Ong AM, Hatakeyama S, Weissman AM (1999) RING fingers mediate ubiquitin-conjugating enzyme (E2)-dependent ubiquitination. Proc Natl Acad Sci USA 96: 11364–11369PubMedCentralPubMedCrossRefGoogle Scholar
  54. Lu H, Liu Y, Greenberg JT (2005) Structure–function analysis of the plasma membrane-localized Arabidopsis defense component ACD6. Plant J 44:798–809PubMedCrossRefGoogle Scholar
  55. Lu H, Rate DN, Song JT, Greenberg JT (2003) ACD6, a novel ankyrin protein, is a regulator and an effector of salicylic acid signaling in the Arabidopsis defense response. Plant Cell 15: 2408–2420PubMedCentralPubMedCrossRefGoogle Scholar
  56. Lu H, Salimian S, Gamelin E, Wang G, Fedorowski J, LaCourse W, Greenberg JT (2009) Genetic analysis of acd6–1 reveals complex defense networks and leads to identification of novel defense genes in Arabidopsis. Plant J 58:401–412PubMedCentralPubMedCrossRefGoogle Scholar
  57. Lyzenga WJ, Booth JK, Stone SL (2012) The Arabidopsis RINGtype E3 ligase XBAT32 mediates the proteasomal degradation of the ethylene biosynthetic enzyme, 1-aminocyclopropane-1-carboxylate synthase 7. Plant J 71:23–34PubMedCrossRefGoogle Scholar
  58. Lyzenga WJ, Liu H, Schofield A, Muise-Hennessey A, Stone SL (2013) Arabidopsis CIPK26 interacts with KEG, components of the ABA signalling network and is degraded by the ubiquitin–proteasome system. J Exp Bot 64:2779–2791PubMedCentralPubMedCrossRefGoogle Scholar
  59. Maldonado-Bonilla LD, Eschen-Lippold L, Gago-Zachert S, Tabassum N, Bauer N, Scheel D, Lee J (2014) The Arabidopsis tandem zinc finger 9 protein binds RNA and mediates pathogen-associated molecular pattern-triggered immune responses. Plant Cell Physiol 55:412–425PubMedCrossRefGoogle Scholar
  60. Matthews BF, Beard H, Brewer E, Kabir S, MacDonald MH, Youssef RM (2014) Arabidopsis genes, AtNPR1, AtTGA2 and AtPR-5, confer partial resistance to soybean cyst nematode (Heterodera glycines) when overexpressed in transgenic soybean roots. BMC Plant Biol 14:96PubMedCentralPubMedCrossRefGoogle Scholar
  61. Michaely P, Bennett V (1992) The ANK repeat: a ubiquitous motif involved in macromolecular recognition. Trends Cell Biol 2: 127–129PubMedCrossRefGoogle Scholar
  62. Mosavi LK, Cammett TJ, Desrosiers DC, Peng Zy (2004) The ankyrin repeat as molecular architecture for protein recognition. Protein Sci 13:1435–1448PubMedCentralPubMedCrossRefGoogle Scholar
  63. Mosavi LK, Minor DL, Peng Z-y (2002) Consensus-derived structural determinants of the ankyrin repeat motif. Proc Natl Acad Sci USA 99:16029–16034PubMedCentralPubMedCrossRefGoogle Scholar
  64. Mou S, Liu Z, Guan D, Qiu A, Lai Y, He S (2013) Functional Analysis and Expressional Characterization of rice ankyrin repeat-containing protein, OsPIANK1, in basal defense against Magnaporthe oryzae attack. PloS one 8:e59699PubMedCentralPubMedCrossRefGoogle Scholar
  65. Mou Z, Fan W, Dong X (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113:935–944PubMedCrossRefGoogle Scholar
  66. Naramoto S, Kleine-Vehn J, Robert S, Fujimoto M, Dainobu T, Paciorek T, Ueda T, Nakano A, Van Montagu MC, Fukuda H (2010) ADP-ribosylation factor machinery mediates endocytosis in plant cells. Proc Natl Acad Sci USA 107:21890–21895PubMedCentralPubMedCrossRefGoogle Scholar
  67. Nguyen TX, Jaru-Ampornpan P, Lam VQ, Cao P, Piszkiewicz S, Hess S, Shan SO (2013) Mechanism of an ATP-independent protein disaggregase I. Structure of a membrane protein aggregate reveals a mechanism of recognition by its chaperone. J Biol Chem 288:13420–13430PubMedCentralPubMedCrossRefGoogle Scholar
  68. Nieves-Cordones M, Caballero F, Martínez V, Rubio F (2012) Disruption of the Arabidopsis thaliana inward-rectifier K+ channel AKT1 improves plant responses to water stress. Plant Cell Physiol 53:423–432PubMedCrossRefGoogle Scholar
  69. Nodzon LA, Xu WH, Wang Y, Pi LY, Chakrabarty PK, Song WY (2004) The ubiquitin ligase XBAT32 regulates lateral root development in Arabidopsis. Plant J 40:996–1006PubMedCrossRefGoogle Scholar
  70. Pandey N, Ranjan A, Pant P, Tripathi RK, Ateek F, Pandey HP, Patre UV, Sawant SV (2013) CAMTA 1 regulates drought responses in Arabidopsis thaliana. BMC Genomics 14:216PubMedCentralPubMedCrossRefGoogle Scholar
  71. Peck SC, Nühse TS, Hess D, Iglesias A, Meins F, Boller T (2001) Directed proteomics identifies a plant-specific protein rapidly phosphorylated in response to bacterial and fungal elicitors. Plant Cell 13:1467–1475PubMedCentralPubMedCrossRefGoogle Scholar
  72. Prasad BD, Goel S, Krishna P (2010a) In silico identification of carboxylate clamp type tetratricopeptide repeat proteins in Arabidopsis and rice as putative co-chaperones of Hsp90/Hsp70. PloS one 5:e12761PubMedCentralPubMedCrossRefGoogle Scholar
  73. Prasad ME, Schofield A, Lyzenga W, Liu H, Stone SL (2010b) Arabidopsis RING E3 ligase XBAT32 regulates lateral root production through its role in ethylene biosynthesis. Plant Physiol 153:1587–1596PubMedCentralPubMedCrossRefGoogle Scholar
  74. Prasad ME, Stone SL (2010) Further analysis of XBAT32, an Arabidopsis RING E3 ligase, involved in ethylene biosynthesis. Plant Signal Behav 5:1425–1429PubMedCentralPubMedCrossRefGoogle Scholar
  75. Priya DB, Somasekhar N, Prasad J, Kirti P (2011) Transgenic tobacco plants constitutively expressing Arabidopsis NPR1 show enhanced resistance to root-knot nematode, Meloidogyne incognita. BMC research notes 4:231PubMedCentralPubMedCrossRefGoogle Scholar
  76. Rate DN, Cuenca JV, Bowman GR, Guttman DS, Greenberg JT (1999) The gain-of-function Arabidopsis acd6 mutant reveals novel regulation and function of the salicylic acid signaling pathway in controlling cell death, defenses, and cell growth. Plant Cell 11:1695–1708PubMedCentralPubMedCrossRefGoogle Scholar
  77. Reddy AS, Ali GS, Celesnik H, Day IS (2011) Coping with stresses: roles of calcium-and calcium/calmodulin-regulated gene expression. Plant Cell 23:2010–2032PubMedCentralPubMedCrossRefGoogle Scholar
  78. Rubtsov AM, Lopina OD (2000) Ankyrins. FEBS Lett 482:1–5PubMedCrossRefGoogle Scholar
  79. Ryan E, Grierson CS, Cavell A, Steer M, Dolan L (1998) TIP1 is required for both tip growth and non-tip growth in Arabidopsis. New Phytol 138:49–58CrossRefGoogle Scholar
  80. Sakamoto H, Matsuda O, Iba K (2008) ITN1, a novel gene encoding an ankyrin-repeat protein that affects the ABA-mediated production of reactive oxygen species and is involved in saltstress tolerance in Arabidopsis thaliana. Plant J 56:411–422PubMedCrossRefGoogle Scholar
  81. Sedgwick SG, Smerdon SJ (1999) The ankyrin repeat: a diversity of interactions on a common structural framework. Trends Biochem Sci 24:311–316PubMedCrossRefGoogle Scholar
  82. Seong ES, Cho HS, Choi D, Joung YH, Lim CK, Hur JH, Wang M-H (2007a) Tomato plants overexpressing CaKR1 enhanced tolerance to salt and oxidative stress. Biochem Biophys Res Commun 363: 983–988PubMedCrossRefGoogle Scholar
  83. Seong ES, Choi D, Cho HS, Lim CK, Cho HJ, Wang M (2007b) Characterization of a stress-responsive ankyrin repeat-containing zinc finger protein of Capsicum annuum (CaKR1). J Biochem Mol Biol 40:952–958PubMedCrossRefGoogle Scholar
  84. Shen G, Kuppu S, Venkataramani S, Wang J, Yan J, Qiu X, Zhang H (2010) ANKYRIN REPEAT-CONTAINING PROTEIN 2A is an essential molecular chaperone for peroxisomal membranebound ASCORBATE PEROXIDASE3 in Arabidopsis. Plant Cell 22:811–831PubMedCentralPubMedCrossRefGoogle Scholar
  85. Shi Z, Maximova SN, Liu Y, Verica J, Guiltinan MJ (2010) Functional analysis of the Theobroma cacao NPR1 gene in Arabidopsis. BMC Plant Biol 10:248PubMedCentralPubMedCrossRefGoogle Scholar
  86. Song W-Y, Wang G-L, Chen L-L, Kim H-S, Pi L-Y, Holsten T, Gardner J, Wang B, Zhai W-X, Zhu L-H (1995) A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270:1804–1806PubMedCrossRefGoogle Scholar
  87. Spoel SH, Koornneef A, Claessens SM, Korzelius JP, Van Pelt JA, Mueller MJ, Buchala AJ, Métraux J-P, Brown R, Kazan K (2003) NPR1 modulates cross-talk between salicylate-and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15:760–770PubMedCentralPubMedCrossRefGoogle Scholar
  88. Spoel SH, Mou Z, Tada Y, Spivey NW, Genschik P, Dong X (2009) Proteasome-mediated turnover of the transcription co-activator NPR1 plays dual roles in regulating plant immunity. Cell 137: 860–872PubMedCentralPubMedCrossRefGoogle Scholar
  89. Stone JM, Liang X, Nekl ER, Stiers JJ (2005a) Arabidopsis AtSPL14, a plant-specific SBP-domain transcription factor, participates in plant development and sensitivity to fumonisin B1. Plant J 41: 744–754PubMedCrossRefGoogle Scholar
  90. Stone SL, Hauksdóttir H, Troy A, Herschleb J, Kraft E, Callis J (2005b) Functional analysis of the RING-type ubiquitin ligase family of Arabidopsis. Plant Physiol 137:13–30PubMedCentralPubMedCrossRefGoogle Scholar
  91. Sugano S, Jiang C-J, Miyazawa S-I, Masumoto C, Yazawa K, Hayashi N, Shimono M, Nakayama A, Miyao M, Takatsuji H (2010) Role of OsNPR1 in rice defense program as revealed by genome-wide expression analysis. Plant Mol Biol 74:549–562PubMedCrossRefGoogle Scholar
  92. Sun J, Jiang H, Xu Y, Li H, Wu X, Xie Q, Li C (2007) The CCCHtype zinc finger proteins AtSZF1 and AtSZF2 regulate salt stress responses in Arabidopsis. Plant Cell Physiol 48:1148–1158PubMedCrossRefGoogle Scholar
  93. Takatsuji H (1998) Zinc-finger transcription factors in plants. Cell Mol Life Sci 54:582–596PubMedCrossRefGoogle Scholar
  94. Vernoud V, Horton AC, Yang Z, Nielsen E (2003) Analysis of the small GTPase gene superfamily of Arabidopsis. Plant Physiol 131:1191–1208PubMedCentralPubMedCrossRefGoogle Scholar
  95. Wang Y-S, Pi L-Y, Chen X, Chakrabarty PK, Jiang J, De Leon AL, Liu G-Z, Li L, Benny U, Oard J (2006) Rice XA21 binding protein 3 is a ubiquitin ligase required for full Xa21-mediated disease resistance. Plant Cell 18:3635–3646PubMedCentralPubMedCrossRefGoogle Scholar
  96. Wingenter K, Trentmann O, Winschuh I, Hörmiller II, Heyer AG, Reinders J, Schulz A, Geiger D, Hedrich R, Neuhaus HE (2011) A member of the mitogen-activated protein 3-kinase family is involved in the regulation of plant vacuolar glucose uptake. Plant J 68:890–900PubMedCrossRefGoogle Scholar
  97. Wirdnam C, Motoyama A, Arn-Bouldoires E, van Eeden S, Iglesias A, Meins F (2004) Altered expression of an ankyrin-repeat protein results in leaf abnormalities, necrotic lesions, and the elaboration of a systemic signal. Plant Mol Biol 56:717–730PubMedCrossRefGoogle Scholar
  98. Wu Q, Wang XZ, Tang YY, Yu HT, Ding YF, De Yang C, Cui FG, Zhang JC, Wang CT (2014) Molecular cloning and characterization of NPR1 gene from Arachis hypogaea. Mol Biol Rep 41:1–10CrossRefGoogle Scholar
  99. Wu T, Tian Z, Liu J, Yao C, Xie C (2009) A novel ankyrin repeat-rich gene in potato, Star, involved in response to late blight. Biochem Genet 47:439–450PubMedCrossRefGoogle Scholar
  100. Xiao S, Chye M-L (2011) New roles for acyl-CoA-binding proteins (ACBPs) in plant development, stress responses and lipid metabolism. Prog Lipid Res 50:141–151PubMedCrossRefGoogle Scholar
  101. Xu X, Jiang C-Z, Donnelly L, Reid MS (2007) Functional analysis of a RING domain ankyrin repeat protein that is highly expressed during flower senescence. J Exp Bot 58:3623–3630PubMedCrossRefGoogle Scholar
  102. Xue Y, Xiao S, Kim J, Lung S-C, Chen L, Tanner JA, Suh MC, Chye M-L (2014) Arabidopsis membrane-associated acyl-CoA-binding protein ACBP1 is involved in stem cuticle formation. J Exp Bot 65:5473–5483PubMedCentralPubMedCrossRefGoogle Scholar
  103. Yan J, Wang J, Zhang H (2002) An ankyrin repeat-containing protein plays a role in both disease resistance and antioxidation metabolism. Plant J 29:193–202PubMedCrossRefGoogle Scholar
  104. Yang T, Poovaiah B (2002) A calmodulin-binding/CGCG box DNAbinding protein family involved in multiple signaling pathways in plants. J Biol Chem 277:45049–45058PubMedCrossRefGoogle Scholar
  105. Yang X, Sun C, Hu Y, Lin Z (2008) Molecular cloning and characterization of a gene encoding RING zinc finger ankyrin protein from drought-tolerant Artemisia desertorum. J Biosci 33: 103–112PubMedCrossRefGoogle Scholar
  106. Yang Y, Zhang Y, Ding P, Johnson K, Li X, Zhang Y (2012) The ankyrin-repeat transmembrane protein BDA1 functions downstream of the receptor-like protein SNC2 to regulate plant immunity. Plant Physiol 159:1857–1865PubMedCentralPubMedCrossRefGoogle Scholar
  107. Yoo J, Shin DH, Cho MH, Kim TL, Bhoo SH, Hahn TR (2011) An ankyrin repeat protein is involved in anthocyanin biosynthesis in Arabidopsis. Physiol Plant 142:314–325PubMedCrossRefGoogle Scholar
  108. Yu F, Shi J, Zhou J, Gu J, Chen Q, Li J, Cheng W, Mao D, Tian L, Buchanan BB (2010) ANK6, a mitochondrial ankyrin repeat protein, is required for male-female gamete recognition in Arabidopsis thaliana. Proc Natl Acad Sci USA 107:22332–22337PubMedCentralPubMedCrossRefGoogle Scholar
  109. Yuan X, Zhang S, Liu S, Yu M, Su H, Shu H, Li X (2013a) Global analysis of ankyrin repeat domain C3HC4-type RING finger gene family in plants. PloS one 8:e58003PubMedCentralPubMedCrossRefGoogle Scholar
  110. Yuan X, Zhang S, Qing X, Sun M, Liu S, Su H, Shu H, Li X (2013b) Superfamily of ankyrin repeat proteins in tomato. Gene 523: 126–136PubMedCrossRefGoogle Scholar
  111. Yuan Y, Zhong S, Li Q, Zhu Z, Lou Y, Wang L, Wang J, Wang M, Li Q, Yang D (2007) Functional analysis of rice NPR1-like genes reveals that OsNPR1/NH1 is the rice orthologue conferring disease resistance with enhanced herbivore susceptibility. Plant Biotech J 5:313–324CrossRefGoogle Scholar
  112. Zhang H, Scheirer DC, Fowle WH, Goodman HM (1992) Expression of antisense or sense RNA of an ankyrin repeat-containing gene blocks chloroplast differentiation in Arabidopsis. Plant Cell 4: 1575–1588PubMedCentralPubMedCrossRefGoogle Scholar
  113. Zhang Y, Cheng YT, Qu N, Zhao Q, Bi D, Li X (2006) Negative regulation of defense responses in Arabidopsis by two NPR1 paralogs. Plant J 48:647–656PubMedCrossRefGoogle Scholar
  114. Zhou J-M, Trifa Y, Silva H, Pontier D, Lam E, Shah J, Klessig DF (2000) NPR1 differentially interacts with members of the TGA/ OBF family of transcription factors that bind an element of the PR-1 gene required for induction by salicylic acid. Mol Plant- Microbe Interact 13:191–202PubMedCrossRefGoogle Scholar

Copyright information

© Korean Society of Plant Biologists and Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Kieu Thi Xuan Vo
    • 1
  • Chi-Yeol Kim
    • 1
  • Anil Kumar Nalini Chandran
    • 1
  • Ki-Hong Jung
    • 1
  • Gynheung An
    • 1
  • Jong-Seong Jeon
    • 1
    Email author
  1. 1.Graduate School of Biotechnology & Crop Biotech InstituteKyung Hee UniversityYonginKorea

Personalised recommendations