Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Bioinformatic studies of the wheat glutaredoxin gene family and functional analysis of the ROXY1 orthologues

Mark Ziemann A C D , Mrinal Bhave A and Sabine Zachgo B C E
+ Author Affiliations
- Author Affiliations

A Environment and Biotechnology Centre, Faculty of Life and Social Sciences, Swinburne University of Technology, Hawthorn, Vic. 3122, Australia.

B Department of Botany, University of Osnabrück, 49076 Osnabrück, Germany.

C Max Planck Institute for Plant Breeding Research, Plant Molecular Genetics, 50829 Cologne, Germany.

D Present address: Baker IDI Heart and Diabetes Institute, Melbourne, Vic. 3004, Australia.

E Corresponding author. Email: sabine.zachgo@biologie.uni-osnabrueck.de

Functional Plant Biology 38(1) 25-34 https://doi.org/10.1071/FP10185
Submitted: 7 September 2010  Accepted: 28 October 2010   Published: 17 December 2010

Abstract

CC-type glutaredoxins comprise a large land plant-specific class of oxidoreductases. Previous research shows roles for two such proteins in developmental processes in Arabidopsis; ROXY1 mediates petal initiation and morphogenesis, and ROXY1 and ROXY2 are required for normal anther development. In the present work, the broader glutaredoxin family was investigated in hexaploid wheat with bioinformatic methods, revealing a large and multifunctional gene family. With a PCR based method, three wheat ROXY homeoalleles were isolated. Complementation analyses show that these three isoforms fully complemented the roxy1 mutation in Arabidopsis. Further, yeast two-hybrid experiments demonstrate that one such wheat ROXY protein interacts strongly with TGA3, an Arabidopsis TGA transcription factor previously shown to associate with ROXY1. Deletion analyses show that TaROXY3 docks to a glutamine rich region of TGA3, a putative transcriptional activation domain. These results suggest a conserved molecular role of Arabidopsis and wheat ROXY proteins in inflorescence/spike development, most likely in the post-translational regulation of TGA proteins including HBP-1b (the wheat PERIANTHIA orthologue), which likely exerts also a developmental function by activating histone gene transcription in highly proliferating tissues such as the SAM and root tip.

Additional keywords: CC-type GRX class, flower development, GRX, ROXY.


References

Ball L, Accotto GP, Bechtold U, Creissen G, Funck D, et al (2004) Evidence for a direct link between glutathione biosynthesis and stress defense gene expression in Arabidopsis. The Plant Cell 16, 2448–2462.
Evidence for a direct link between glutathione biosynthesis and stress defense gene expression in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvVartbg%3D&md5=bd90b06c2093ec71b70843ecbd10fea5CAS | 15308753PubMed |

Benfey PN, Ren L, Chua NH (1990) Tissue-specific expression from CaMV 35S enhancer subdomains in early stages of plant development. EMBO Journal 9, 1677–1684.

Bouchez D, Tokuhisa JG, Llewellyn DJ, Dennis ES, Ellis JG (1989) The OCS-element is a component of the promoters of several T-DNA and plant viral genes. EMBO Journal 8, 4197–4204.

Cheng NH, Liu JZ, Brock A, Nelson RS, Hirschi KD (2006) AtGRXcp, an Arabidopsis chloroplastic glutaredoxin, is critical for protection against protein oxidative damage. Journal of Biological Chemistry 281, 26 280–26 288.
AtGRXcp, an Arabidopsis chloroplastic glutaredoxin, is critical for protection against protein oxidative damage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XovFyqtrw%3D&md5=e861d40ef819b2a7d43db689e71b8c60CAS |

Childs KL, Hamilton JP, Zhu W, Ly E, Cheung F, Wu H, Rabinowicz PD, Town CD, Buell CR, Chan AP (2007) The TIGR plant transcript assemblies database. Nucleic Acids Research 35, D846–D851.
The TIGR plant transcript assemblies database.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXivFGnsw%3D%3D&md5=7b3eb2d21a29af3d894dac6393f780ecCAS | 17088284PubMed |

Clarke J (2002) Cetyltrimethyl ammonium bromide (CTAB) DNA miniprep for plant DNA isolation. Cold Spring Harbor Protocols 2009, 40–42.

Couturier J, Jacquot JP, Rouhier N (2009) Evolution and diversity of glutaredoxins in photosynthetic organisms. Cellular and Molecular Life Sciences 66, 2539–2557.
Evolution and diversity of glutaredoxins in photosynthetic organisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXos1egsLg%3D&md5=f34ee01f75c943a2b919b8fcf98ded63CAS | 19506802PubMed |

Dietz KJ (2003) Redox control, redox signaling, and redox homeostasis in plant cells. International Review of Cytology 228, 141–193.
Redox control, redox signaling, and redox homeostasis in plant cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXktlejtw%3D%3D&md5=ffe3ef0c29b9513fe5892694f89d03c1CAS | 14667044PubMed |

Fernandes AP, Fladvad M, Berndt C, Andresen C, Lillig CH, Neubauer P, Sunnerhagen M, Holmgren A, Vlamis-Gardikas A (2005) A novel monothiol glutaredoxin (Grx4) from Escherichia coli can serve as a substrate for thioredoxin reductase. Journal of Biological Chemistry 280, 24 544–24 552.
A novel monothiol glutaredoxin (Grx4) from Escherichia coli can serve as a substrate for thioredoxin reductase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlsFyrurc%3D&md5=0b45fbf9713cddab56f0a68c000084caCAS |

Fromm H, Katagiri F, Chua NH (1989) An octopine synthase enhancer element directs tissue-specific expression and binds ASF-1, a factor from tobacco nuclear extracts. The Plant Cell 1, 977–984.

Hepworth SR, Zhang Y, McKim S, Li X, Haughn GW (2005) BLADE-ON-PETIOLE-dependent signaling controls leaf and floral patterning in Arabidopsis. The Plant Cell 17, 1434–1448.
BLADE-ON-PETIOLE-dependent signaling controls leaf and floral patterning in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXksVKks7w%3D&md5=9b17fd73639b74b93c10479fa7a88aa2CAS | 15805484PubMed |

Holmgren A (1979) Glutathione-dependent synthesis of deoxyribonucleotides. Characterization of the enzymatic mechanism of Escherichia coli glutaredoxin. Journal of Biological Chemistry 254, 3672–3678.

Huang X, Madan A (1999) CAP3: A DNA sequence assembly program. Genome Research 9, 868–877.
CAP3: A DNA sequence assembly program.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmslKgs7Y%3D&md5=a34f04b30844f4276c52a4d2e1d92d6dCAS | 10508846PubMed |

Jupin I, Chua NH (1996) Activation of the CaMV as-1 cis-element by salicylic acid: differential DNA-binding of a factor related to TGA1a. EMBO Journal 15, 5679–5689.

Kawata T, Imada T, Shiraishi H, Okada K, Shimura Y, Iwabuchi M (1992) A cDNA clone encoding HBP-1b homologue in Arabidopsis thaliana. Nucleic Acids Research 20, 1141
A cDNA clone encoding HBP-1b homologue in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXit1Krtrs%3D&md5=fe20c8f850293592d166655fb8ca0680CAS | 1549479PubMed |

Lemaire SD (2004) The glutaredoxin family in oxygenic photosynthetic organisms. Photosynthesis Research 79, 305–318.
The glutaredoxin family in oxygenic photosynthetic organisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhsV2quro%3D&md5=3d9d47f0b438d0d5f9548c6dc4c94443CAS | 16328797PubMed |

Li S, Zachgo S (2009) Glutaredoxins in development and stress responses of plants. Advances in Botanical Research 52, 333–361.
Glutaredoxins in development and stress responses of plants.Crossref | GoogleScholarGoogle Scholar |

Li S, Lauri A, Ziemann M, Busch A, Bhave M, Zachgo S (2009) Nuclear activity of ROXY1, a glutaredoxin interacting with TGA factors, is required for petal development in Arabidopsis thaliana. The Plant Cell 21, 429–441.
Nuclear activity of ROXY1, a glutaredoxin interacting with TGA factors, is required for petal development in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXksVKrtr8%3D&md5=1f6682d92b15706bee7aaa0107ffc2fbCAS | 19218396PubMed |

Martin JL (1995) Thioredoxin – a fold for all reasons. Structure 3, 245–250.
Thioredoxin – a fold for all reasons.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXksFyntLg%3D&md5=3e283d88f640f5c4a58b582c1ce4f6eaCAS | 7788290PubMed |

Meyer AJ, Brach T, Marty L, Kreye S, Rouhier N, Jacquot JP, Hell R (2007) Redox-sensitive GFP in Arabidopsis thaliana is a quantitative biosensor for the redox potential of the cellular glutathione redox buffer. The Plant Journal 52, 973–986.
Redox-sensitive GFP in Arabidopsis thaliana is a quantitative biosensor for the redox potential of the cellular glutathione redox buffer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVGls77O&md5=072689e22836ee3bc491b9f460b4004bCAS | 17892447PubMed |

Mikami K, Tabata T, Kawata T, Nakayama T, Iwabuchi M (1987) Nuclear protein(s) binding to the conserved DNA hexameric sequence postulated to regulate transcription of wheat histone genes. FEBS Letters 223, 273–278.
Nuclear protein(s) binding to the conserved DNA hexameric sequence postulated to regulate transcription of wheat histone genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXhslSquw%3D%3D&md5=8951da4886f0c98f80bd95ebab073fd4CAS | 2822486PubMed |

Mikami K, Sakamoto A, Takase H, Tabata T, Iwabuchi M (1989) Wheat nuclear protein HBP-1 binds to the hexameric sequence in the promoter of various plant genes. Nucleic Acids Research 17, 9707–9717.
Wheat nuclear protein HBP-1 binds to the hexameric sequence in the promoter of various plant genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXntFCmtA%3D%3D&md5=17890c75b235fb533776730c33f86f9cCAS | 2602142PubMed |

Murmu J, Bush MJ, DeLong C, Li S, Xu M, Khan M, Malcolmson C, Fobert PR, Zachgo S, Hepworth S (2010) Arabidopsis bZIP transcription factors TGA9 and TGA10 interact with floral glutaredoxins ROXY1 and ROXY2 and are redundantly required for anther development. Plant Physiology 154, 1492–1504.
Arabidopsis bZIP transcription factors TGA9 and TGA10 interact with floral glutaredoxins ROXY1 and ROXY2 and are redundantly required for anther development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsV2ntr3M&md5=f097df3d5888214539810920d19dfe7eCAS | 20805327PubMed |

Ndamukong I, Abdallat AA, Thurow C, Fode B, Zander M, Weigel R, Gatz C (2007) SA-inducible Arabidopsis glutaredoxin interacts with TGA factors and suppresses JA-responsive PDF1.2 transcription. The Plant Journal 52, 128–139.
SA-inducible Arabidopsis glutaredoxin interacts with TGA factors and suppresses JA-responsive PDF1.2 transcription.Crossref | GoogleScholarGoogle Scholar |

Overbeek R, Fonstein M, D’Souza M, Pusch GD, Maltsev N (1999) The use of gene clusters to infer functional coupling. Proceedings of the National Academy of Sciences of the United States of America 96, 2896–2901.
The use of gene clusters to infer functional coupling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhvFyks7s%3D&md5=c368d7081e53b6129a6de06c38e8ce7cCAS | 10077608PubMed |

Parisy V, Poinssot B, Owsianowski L, Buchala A, Glazebrook J, Mauch F (2007) Identification of PAD2 as a γ-glutamylcysteine synthetase highlights the importance of glutathione in disease resistance of Arabidopsis. The Plant Journal 49, 159–172.
Identification of PAD2 as a γ-glutamylcysteine synthetase highlights the importance of glutathione in disease resistance of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnvVyqug%3D%3D&md5=3c8fe51e2bba1839df5bc84efcae9527CAS | 17144898PubMed |

Sorrells ME, La Rota M, Bermudez-Kandianis CE, Greene RA, Kantety R, et al (2003) Comparative DNA sequence analysis of wheat and rice genomes. Genome Research 13, 1818–1827.

Tabata T, Takase H, Takayama S, Mikami K, Nakatsuka A, Kawata T, Nakayama T, Iwabuchi M (1989) A protein that binds to a cis-acting element of wheat histone genes has a leucine zipper motif. Science 245, 965–967.
A protein that binds to a cis-acting element of wheat histone genes has a leucine zipper motif.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXhvFeqt7Y%3D&md5=5e33b92641e94a6ad2f9b462bd97beffCAS | 2772648PubMed |

Tabata T, Nakayama T, Mikami K, Iwabuchi M (1991) HBP-1a and HBP-1b: leucine zipper-type transcription factors of wheat. EMBO Journal 10, 1459–1467.

Walsh J, Waters CA, Freeling M (1998) The maize gene LIGULELESS2 encodes a basic leucine zipper protein involved in the establishment of the leaf blade-sheath boundary. Genes & Development 12, 208–218.
The maize gene LIGULELESS2 encodes a basic leucine zipper protein involved in the establishment of the leaf blade-sheath boundary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnsV2gsw%3D%3D&md5=42edc5ce08ac3be8f69ba06e5dc3cdf2CAS | 9490265PubMed |

Wang Z, Xing S, Birkenbihl RP, Zachgo S (2009) Conserved functions of Arabidopsis and rice CC-type glutaredoxins in flower development and pathogen response. Molecular Plant 2, 323–335.
Conserved functions of Arabidopsis and rice CC-type glutaredoxins in flower development and pathogen response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjvVWhsbc%3D&md5=5a9354db1eae4758c086e620b2cdfe89CAS | 19825617PubMed |

Xing S, Zachgo S (2008) ROXY1 and ROXY2, two Arabidopsis glutaredoxin genes, are required for anther development. The Plant Journal 53, 790–801.
ROXY1 and ROXY2, two Arabidopsis glutaredoxin genes, are required for anther development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjsFyjs7k%3D&md5=c24273e096f7cbadc6423e56ef3973e4CAS | 18036205PubMed |

Xing S, Rosso MG, Zachgo S (2005) ROXY1, a member of the plant glutaredoxin family, is required for petal development in Arabidopsis thaliana. Development 132, 1555–1565.
ROXY1, a member of the plant glutaredoxin family, is required for petal development in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjslGlsrc%3D&md5=8e238000c4299941e777dfc9537b44deCAS | 15728668PubMed |

Xing S, Lauri A, Zachgo S (2006) Redox regulation and flower development: a novel function for glutaredoxins. Plant Biology 8, 547–555.
Redox regulation and flower development: a novel function for glutaredoxins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFSktbjI&md5=85df5b95da2c25c633f9933c4988348cCAS | 16883479PubMed |

Zhang B, Singh KB (1994) OCS element promoter sequences are activated by auxin and salicylic acid in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 91, 2507–2511.
OCS element promoter sequences are activated by auxin and salicylic acid in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXjtFOisL0%3D&md5=779d7499cf6f13276f6faeb9dec08051CAS | 8146146PubMed |

Ziemann M, Ramalingam A, Bhave M (2008) Evidence of physical interactions of puroindoline proteins using the yeast two-hybrid system. Plant Science 175, 307–311.
Evidence of physical interactions of puroindoline proteins using the yeast two-hybrid system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXptVeksLo%3D&md5=753f5b435049297079f9e881fbf04a2fCAS |

Ziemann M, Bhave M, Zachgo S (2009) Origin and diversification of land plant CC-type glutaredoxins. Genome Biology and Evolution 2009, 265–277.
Origin and diversification of land plant CC-type glutaredoxins.Crossref | GoogleScholarGoogle Scholar |