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

Global gene expression analysis of in vitro root formation in Medicago truncatula

Peta Holmes A , Michael A. Djordjevic A and Nijat Imin B C
+ Author Affiliations
- Author Affiliations

A ARC Centre of Excellence for Integrative Legume Research, Plant Science Division, Research School of Biology, Australian National University, Canberra, ACT 2601, Australia.

B Nijat Imin, Plant Science Division, Research School of Biology, Australian National University, Canberra, ACT 2601, Australia.

C Corresponding author. Email: nijat.imin@anu.edu.au

Functional Plant Biology 37(12) 1117-1131 https://doi.org/10.1071/FP10159
Submitted: 3 August 2010  Accepted: 17 September 2010   Published: 17 November 2010

Abstract

Medicago truncatula Gaertn. can generate roots in vitro through the formation of root stem cells from leaf explants cultured with auxin. To identify key genes involved in the early processes of root initiation, we compared gene expression in root-forming cultures (RFC) enriched for root stem cells with non-root-forming cultures (NRFC) and untreated leaves using the Affymetrix Medicago GeneChip. Comparing RFC (at 1 week, before root primordium formation) to normal leaf tissue, we identified 904 and 993 up- and downregulated probe sets. Comparing RFC and NRFC, we identified 92 and 182 up- and downregulated probe sets. By comparing all the samples we identified a set of 76 and 42 probe sets up- and downregulated that may be crucial to root stem cell formation and subsequent root initiation. Upregulated probe sets in RFC include Arabidopsis orthologs that are involved in root stem cell formation and root initiation. To validate the GeneChip results, quantitative real-time RT–PCR analysis was used to examine the expression of specific up- and downregulated genes, all of which positively correlated with the microarray data. We used bioinformatic tools developed to functionally annotate the Medicago genome array. This showed significant changes in metabolism, signalling and the expression of transcription factors including some with described roles in root organogenesis and other genes not previously linked to this process. This data facilitates the mapping of regulatory and metabolic networks in M. truncatula and provides candidates for further functional analysis of root initiation in vitro and in planta.

Additional keywords: microarray analysis, real time RT-PCR, root stem cell niche formation.


References

Agusti J, Merelo P, Cercos M, Tadeo FR, Talon M (2008) Ethylene-induced differential gene expression during abscission of citrus leaves. Journal of Experimental Botany 59, 2717–2733.
Ethylene-induced differential gene expression during abscission of citrus leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXot1WitrY%3D&md5=873b78b32c258cccb44c585006cc0493CAS | 18515267PubMed |

Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C, Nussaume L, Noh Y-S, Amasino R, Scheres B (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119, 109–120.
The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXotlyqu7o%3D&md5=189f6c3664052617d39ad03d8e527169CAS | 15454085PubMed |

Altschul S, Gish W, Miller W, Myers E, Lipman D (1990) Basic local alignment search tool. Journal of Molecular Biology 215, 403–410.

Ané J-M, Zhu H, Frugoli J (2008) Recent advances in Medicago truncatula genomics. International Journal of Plant Genomics
Recent advances in Medicago truncatula genomics.Crossref | GoogleScholarGoogle Scholar | 18288239PubMed |

Benedito VA, Torres-Jerez I, Murray JD, Andriankaja A, Allen S, et al (2008) A gene expression atlas of the model legume Medicago truncatula. The Plant Journal 55, 504–513.
A gene expression atlas of the model legume Medicago truncatula.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVSrtrbN&md5=4a83e5985dea133e25c3a464ced01bbcCAS | 18410479PubMed |

Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate – a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B, Statistical Methodology 57, 289–300.

Benková E, Hejátko J (2009) Hormone interactions at the root apical meristem. Plant Molecular Biology 69, 383–396.
Hormone interactions at the root apical meristem.Crossref | GoogleScholarGoogle Scholar | 18807199PubMed |

Buer CS, Muday GK, Djordjevic MA (2007) Flavonoids are differentially taken up and transported long distances in Arabidopsis. Plant Physiology 145, 478–490.
Flavonoids are differentially taken up and transported long distances in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1SjsLrK&md5=5c6d9813affa4270b8a7e26dedd8febfCAS | 17720762PubMed |

Buer CS, Imin N, Djordjevic MA (2010) Flavonoids: new roles for old molecules. Journal of Integrative Plant Biology 52, 98–111.
Flavonoids: new roles for old molecules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitVOhsLc%3D&md5=9cc45d176d7074c403a0bb2e38b088aaCAS | 20074144PubMed |

Callow MJ, Dudoit S, Gong EL, Speed TP, Rubin EM (2000) Microarray expression profiling identifies genes with altered expression in HDL-deficient mice. Genome Research 10, 2022–2029.
Microarray expression profiling identifies genes with altered expression in HDL-deficient mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjs10%3D&md5=54287a1623bddc9939e30a73c7ab33cdCAS | 11116096PubMed |

Casamitjana-Martinez E (2003) Receptor kinase signaling in Arabidopsis root meristem maintenance. PhD thesis, University of Utrecht, Utrecht.

Casamitjana-Martinez E, Hofhuis HF, Xu J, Liu C-M, Heidstra R, Scheres B (2003) Root-Specific CLE19 overexpression and the sol1/2: suppressors implicate a CLV-like pathway in the control of Arabidopsis root meristem maintenance. Current Biology 13, 1435–1441.
Root-Specific CLE19 overexpression and the sol1/2: suppressors implicate a CLV-like pathway in the control of Arabidopsis root meristem maintenance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmslentbk%3D&md5=b96becb1b7339fe9ae0c30c506d250feCAS | 12932329PubMed |

Chang C, Damiani I, Puppo A, Frendo P (2009) Redox changes during the legume-rhizobium symbiosis. Molecular Plant 2, 370–377.
Redox changes during the legume-rhizobium symbiosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtlyitLo%3D&md5=380e1a9152de25a9ed2effc8b4aa38c2CAS | 19825622PubMed |

Che P, Lall S, Nettleton D, Howell SH (2006) Gene expression programs during shoot, root, and callus development in Arabidopsis tissue culture. Plant Physiology 141, 620–637.
Gene expression programs during shoot, root, and callus development in Arabidopsis tissue culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xmt1aktLw%3D&md5=81f290e390738b687082e3945ccc8c09CAS | 16648215PubMed |

Chen SK, Kurdyukov S, Kereszt A, Wang XD, Gresshoff PM, Rose RJ (2009) The association of homeobox gene expression with stem cell formation and morphogenesis in cultured Medicago truncatula. Planta 230, 827–840.
The association of homeobox gene expression with stem cell formation and morphogenesis in cultured Medicago truncatula.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVait7zL&md5=a5f4bce1bd866665fbf729a112401c61CAS | 19639337PubMed |

Cho RJ, Huang M, Huang M, Campbell MJ, Dong H, Steinmetz L, Sapinoso L, Hampton G, Elledge SJ, Davis RW, Lockhart DJ (2001) Transcriptional regulation and function during the human cell cycle. Nature Genetics 27, 48–54.
Transcriptional regulation and function during the human cell cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXis1yksQ%3D%3D&md5=67e62da872afde5146981859768bb522CAS | 11137997PubMed |

Claus W, Otto M, Robert K, Bettina H, Jane W, Michael B, Wilhelm B, Benno P, Ivo F (1998) Jasmonic acid: biosynthesis, signal transduction, gene expression. European Journal of Lipid Science and Technology 100, 139–146.

D’Haeze W, De Rycke R, Mathis R, Goormachtig S, Pagnotta S, Verplancke C, Capoen W, Holsters M (2003) Reactive oxygen species and ethylene play a positive role in lateral root base nodulation of a semiaquatic legume. Proceedings of the National Academy of Sciences of the United States of America 100, 11 789–11 794.
Reactive oxygen species and ethylene play a positive role in lateral root base nodulation of a semiaquatic legume.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXotFKmurk%3D&md5=b62cc4262b5abc420f470ee03800d329CAS |

Dalton DA, Boniface C, Turner Z, Lindahl A, Kim HJ, Jelinek L, Govindarajulu M, Finger RE, Taylor CG (2009) Physiological roles of glutathione-S-transferases in soybean root nodules. Plant Physiology 150, 521–530.
Physiological roles of glutathione-S-transferases in soybean root nodules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlvFahsbo%3D&md5=5472a2399b6a6b09eda5aa570c220a30CAS | 19279195PubMed |

Dello Ioio R, Linhares FS, Scacchi E, Casamitjana-Martinez E, Heidstra R, Costantino P, Sabatini S (2007) Cytokinins determine Arabidopsis root-meristem size by controlling cell differentiation. Current Biology 17, 678–682.
Cytokinins determine Arabidopsis root-meristem size by controlling cell differentiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkt1ahsLk%3D&md5=0cfad785a8f26e55df26efc2eab25a8bCAS | 17363254PubMed |

Dolferus R, De Bruxelles G, Dennis ES, Peacock WJ (1994) Regulation of the Arabidopsis Adh gene by anaerobic and other environmental stresses. Annals of Botany 74, 301–308.
Regulation of the Arabidopsis Adh gene by anaerobic and other environmental stresses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXhvVKgsb8%3D&md5=48fbc92b3f36617cb2b4fe09cd962e89CAS |

Ermel FF, Vizoso S, Charpentier JP, Jay-Allemand C, Catesson AM, Couee I (2000) Mechanisms of primordium formation during adventitious root development from walnut cotyledon explants. Planta 211, 563–574.
Mechanisms of primordium formation during adventitious root development from walnut cotyledon explants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmt12itr8%3D&md5=cc8b4a39add24af600e5c921dd3bd123CAS | 11030556PubMed |

Frendo P, Harrison J, Norman C, Jimenez MJH, Van de Sype G, Gilabert A, Puppo A (2005) Glutathione and homoglutathione play a critical role in the nodulation process of Medicago truncatula. Molecular Plant-Microbe Interactions 18, 254–259.
Glutathione and homoglutathione play a critical role in the nodulation process of Medicago truncatula.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhs1eltbg%3D&md5=aacea4c00cc3696917664a815a50dc0dCAS | 15782639PubMed |

Frickey T, Weiller G (2007) http://bioinfoserver.rsbs.anu.edu.au/utils/affytrees/

Frickey T, Benedito VA, Udvardi M, Weiller G (2008) AffyTrees: facilitating comparative analysis of Affymetrix plant microarray chips. Plant Physiology 146, 377–386.
AffyTrees: facilitating comparative analysis of Affymetrix plant microarray chips.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjtFCmtro%3D&md5=cca2a16b49770b03e58c1703272bdf2bCAS | 18065560PubMed |

Fukuda T, Yokoyama J, Nakamura T, Song I-J, Ito T, Ochiai T, Kanno A, Kameya T, Maki M (2005) Molecular phylogeny and evolution of alcohol dehydrogenase (Adh) genes in legumes. BMC Plant Biology 5, 6
Molecular phylogeny and evolution of alcohol dehydrogenase (Adh) genes in legumes.Crossref | GoogleScholarGoogle Scholar | 15836788PubMed |

Galinha C, Hofhuis H, Luijten M, Willemsen V, Blilou I, Heidstra R, Scheres B (2007) PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature 449, 1053–1057.
PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1Wgtr3K&md5=5737514fa026fc1449d34ce204aaa952CAS | 17960244PubMed |

Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, et al (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biology 5, R80
Bioconductor: open software development for computational biology and bioinformatics.Crossref | GoogleScholarGoogle Scholar | 15461798PubMed |

Goffard N, Weiller G (2006) GeneBins: a database for classifying gene expression data. Available at http://bioinfoserver.rsbs.anu.edu.au/utils/GeneBins/ [Verified 21 October 2010]

Goffard N, Weiller G (2007a) GeneBins: a database for classifying gene expression data, with application to plant genome arrays. BMC Bioinformatics 8, 87
GeneBins: a database for classifying gene expression data, with application to plant genome arrays.Crossref | GoogleScholarGoogle Scholar | 17349060PubMed |

Goffard N, Weiller G (2007b) PathExpress: Exploring the metabolic network to interpret post-genomic data. Available at http://bioinfoserver.rsbs.anu.edu.au/utils/PathExpress/ [Verified 21 October 2010]

Goffard N, Weiller G (2007c) PathExpress: a web-based tool to identify relevant pathways in gene expression data. Nucleic Acids Research 35, W176–W181.
PathExpress: a web-based tool to identify relevant pathways in gene expression data.Crossref | GoogleScholarGoogle Scholar | 17586825PubMed |

Goffard N, Frickey T, Weiller G (2009) PathExpress update: the enzyme neighbourhood method of associating gene-expression data with metabolic pathways. Nucleic Acids Research 37, W335–W339.

Gong H, Jiao Y, Hu W-w, Pua E-C (2005) Expression of glutathione-S-transferase and its role in plant growth and development in vivo and shoot morphogenesis in vitro. Plant Molecular Biology 57, 53–66.
Expression of glutathione-S-transferase and its role in plant growth and development in vivo and shoot morphogenesis in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjtV2hurg%3D&md5=c293ecea6b0999ac428a06972798989cCAS | 15821868PubMed |

Guo A, He K, Liu D, Bai S, Gu X, Wei L, Luo J (2005) DATF: a database of Arabidopsis transcription factors. Bioinformatics 21, 2568–2569.
DATF: a database of Arabidopsis transcription factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXktl2qsrc%3D&md5=518f7622ad0aa52455467f932af79ce4CAS | 15731212PubMed |

Hayashi S, Gresshoff PM, Kinkema M (2008) Molecular analysis of lipoxygenases associated with nodule development in soybean. Molecular Plant-Microbe Interactions 21, 843–853.
Molecular analysis of lipoxygenases associated with nodule development in soybean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmtlejtbk%3D&md5=980da191baa97d5330ee1cba22b85885CAS | 18624647PubMed |

Hernández I, Alegre L, Van Breusegem F, Munné-Bosch S (2009) How relevant are flavonoids as antioxidants in plants? Trends in Plant Science 14, 125–132.
How relevant are flavonoids as antioxidants in plants?Crossref | GoogleScholarGoogle Scholar | 19230744PubMed |

Holmes P, Goffard N, Weiller GF, Rolfe BG, Imin N (2008) Transcriptional profiling of Medicago truncatula meristematic root cells. BMC Plant Biology 8, 21
Transcriptional profiling of Medicago truncatula meristematic root cells.Crossref | GoogleScholarGoogle Scholar | 18302802PubMed |

Imin N, Nizamidin M, Daniher D, Nolan KE, Rose RJ, Rolfe BG (2005) Proteomic analysis of somatic embryogenesis in Medicago truncatula. Explant cultures grown under 6-benzylaminopurine and 1-naphthaleneacetic acid treatments. Plant Physiology 137, 1250–1260.
Proteomic analysis of somatic embryogenesis in Medicago truncatula. Explant cultures grown under 6-benzylaminopurine and 1-naphthaleneacetic acid treatments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjslaqurw%3D&md5=20f874989859c5d07da06ebd3d39a9a3CAS | 15749990PubMed |

Imin N, Nizamidin M, Wu T, Rolfe BG (2007) Factors involved in root formation in Medicago truncatula. Journal of Experimental Botany 58, 439–451.
Factors involved in root formation in Medicago truncatula.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhvFWlsLY%3D&md5=daf448e094e40c9987ec2d6711b0b94fCAS | 17158109PubMed |

Imin N, Goffard N, Nizamidin M, Rolfe B (2008) Genome-wide transcriptional analysis of super-embryogenic Medicago truncatula explant cultures. BMC Plant Biology 8, 110
Genome-wide transcriptional analysis of super-embryogenic Medicago truncatula explant cultures.Crossref | GoogleScholarGoogle Scholar | 18950541PubMed |

Inukai Y, Sakamoto T, Ueguchi-Tanaka M, Shibata Y, Gomi K, Umemura I, Hasegawa Y, Ashikari M, Kitano H, Matsuoka M (2005) Crown rootless1, which is essential for crown root formation in rice, is a target of an AUXIN RESPONSE FACTOR in auxin signaling. The Plant Cell 17, 1387–1396.
Crown rootless1, which is essential for crown root formation in rice, is a target of an AUXIN RESPONSE FACTOR in auxin signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXksVKksrY%3D&md5=672da62eedf2ff9c547c2c9b8ed40262CAS | 15829602PubMed |

Joo JH, Yoo HJ, Hwang I, Lee JS, Nam KH, Bae YS (2005) Auxin-induced reactive oxygen species production requires the activation of phosphatidylinositol 3-kinase. FEBS Letters 579, 1243–1248.
Auxin-induced reactive oxygen species production requires the activation of phosphatidylinositol 3-kinase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlOnt7c%3D&md5=247663b92eb873a6a0656bc52b501cfbCAS | 15710420PubMed |

Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M (2004) The KEGG resource for deciphering the genome. Nucleic Acids Research 32, D277–D280.
The KEGG resource for deciphering the genome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtVSrurvO&md5=635a3ffb6bdfab8d7b478b9018c5e051CAS | 14681412PubMed |

Kwak JM, Nguyen V, Schroeder JI (2006) The role of reactive oxygen species in hormonal responses. Plant Physiology 141, 323–329.
The role of reactive oxygen species in hormonal responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xmt1aksLk%3D&md5=e9482ee43ead015908232b7bf60cf63bCAS | 16760482PubMed |

Lee HW, Kim NY, Lee DJ, Kim J (2009) LBD18/ASL20 regulates lateral root formation in combination with LBD16/ASL18 downstream of ARF7 and ARF19 in Arabidopsis. Plant Physiology 151, 1377–1389.
LBD18/ASL20 regulates lateral root formation in combination with LBD16/ASL18 downstream of ARF7 and ARF19 in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVCjsbnN&md5=cad27f0106aa26db7acc9c0d5252fa29CAS | 19717544PubMed |

Liu HJ, Wang SF, Yu XB, Yu J, He XW, Zhang SL, Shou HX, Wu P (2005) ARL1, a LOB-domain protein required for adventitious root formation in rice. The Plant Journal 43, 47–56.
ARL1, a LOB-domain protein required for adventitious root formation in rice.Crossref | GoogleScholarGoogle Scholar | 15960615PubMed |

Mathesius U (2001) Flavonoids induced in cells undergoing nodule organogenesis in white clover are regulators of auxin breakdown by peroxidase. Journal of Experimental Botany 52, 419–426.

Million T, Jiangqi W, He J, Tu H, Kwak Y, et al (2008) Large-scale insertional mutagenesis using the Tnt1 retrotransposon in the model legume Medicago truncatula. The Plant Journal 54, 335–347.
Large-scale insertional mutagenesis using the Tnt1 retrotransposon in the model legume Medicago truncatula.Crossref | GoogleScholarGoogle Scholar | 18208518PubMed |

Nolan KE, Rose RJ, Gorst JR (1989) Regeneration of Medicago truncatula from tissue culture: increased somatic embryogenesis from regenerated plants. Plant Cell Reports 8, 278–281.
Regeneration of Medicago truncatula from tissue culture: increased somatic embryogenesis from regenerated plants.Crossref | GoogleScholarGoogle Scholar |

Nolan KE, Irwanto RR, Rose RJ (2003) Auxin up-regulates MtSERK1 expression in both Medicago truncatula root-forming and embryogenic cultures. Plant Physiology 133, 218–230.
Auxin up-regulates MtSERK1 expression in both Medicago truncatula root-forming and embryogenic cultures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntlaitb0%3D&md5=1f86917b962fe336873518fa0708bc59CAS | 12970488PubMed |

Passarinho P, Ketelaar T, Xing M, van Arkel J, Maliepaard C, et al (2008) BABY BOOM target genes provide diverse entry points into cell proliferation and cell growth pathways. Plant Molecular Biology 68, 225–237.
BABY BOOM target genes provide diverse entry points into cell proliferation and cell growth pathways.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVahu7%2FP&md5=e8efd4fe7d30172806227d21f66eda25CAS | 18663586PubMed |

Penmetsa RV, Cook DR (1997) A legume ethylene-insensitive mutant hyperinfected by its rhizobial symbiont. Science 275, 527–530.
A legume ethylene-insensitive mutant hyperinfected by its rhizobial symbiont.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXnvVekuw%3D%3D&md5=b9cb2847c455aacd7596a0a552c88025CAS | 8999796PubMed |

Penmetsa RV, Uribe P, Anderson J, Lichtenzveig J, Gish J-C, et al (2008) The Medicago truncatula ortholog of Arabidopsis EIN2, sickle, is a negative regulator of symbiotic and pathogenic microbial associations. The Plant Journal 55, 580–595.
The Medicago truncatula ortholog of Arabidopsis EIN2, sickle, is a negative regulator of symbiotic and pathogenic microbial associations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVyltb7K&md5=591b89c06151e6d44191924febe4489eCAS | 18435823PubMed |

Porceddu A, Panara F, Calderini O, Molinari L, Taviani P, et al (2008) An Italian functional genomic resource for Medicago truncatula. BMC Research Notes 1, 129
An Italian functional genomic resource for Medicago truncatula.Crossref | GoogleScholarGoogle Scholar | 19077311PubMed |

Rhee SY, Beavis W, Berardini TZ, Chen G, Dixon D, et al (2003) The Arabidopsis Information Resource (TAIR): a model organism database providing a centralized, curated gateway to Arabidopsis biology, research materials and community. Nucleic Acids Research 31, 224–228.
The Arabidopsis Information Resource (TAIR): a model organism database providing a centralized, curated gateway to Arabidopsis biology, research materials and community.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhvFSnurk%3D&md5=3ddd39e7c3acdf04c46656663b5d36a6CAS | 12519987PubMed |

Rice-Evans C, Miller N, Paganga G (1997) Antioxidant properties of phenolic compounds. Trends in Plant Science 2, 152–159.
Antioxidant properties of phenolic compounds.Crossref | GoogleScholarGoogle Scholar |

Rose RJ, Wang XD, Nolan KE, Rolfe BG (2006) Root meristems in Medicago truncatula tissue culture arise from vascular-derived procambial-like cells in a process regulated by ethylene. Journal of Experimental Botany 57, 2227–2235.
Root meristems in Medicago truncatula tissue culture arise from vascular-derived procambial-like cells in a process regulated by ethylene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnvF2mu74%3D&md5=2ccac13c4fd9a078a8d66eccf748884eCAS | 16714308PubMed |

Sánchez-Fernández R, Fricker M, Corben LB, White NS, Sheard N, Leaver CJ, Van Montagu M, Inzé D, May MJ (1997) Cell proliferation and hair tip growth in the Arabidopsis root are under mechanistically different forms of redox control. Proceedings of the National Academy of Sciences of the United States of America 94, 2745–2750.
Cell proliferation and hair tip growth in the Arabidopsis root are under mechanistically different forms of redox control.Crossref | GoogleScholarGoogle Scholar | 11038608PubMed |

Sarkar AK, Luijten M, Miyashima S, Lenhard M, Hashimoto T, Nakajima K, Scheres B, Heidstra R, Laux T (2007) Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446, 811–814.
Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXktVeqtLs%3D&md5=c0c4e6cf3be7ba7fa8857487b4097c55CAS | 17429400PubMed |

Skoog F, Miller CO (1957) Chemical regulation of growth and organ formation in plant tissues cultured in vitro. Symposia of the Society for Experimental Biology 54, 116–130.

Smith DL, Fedoroff NV (1995) LRP1, a gene expressed in lateral and adventitious root primordia of Arabidopsis. The Plant Cell 7, 735–745.

Söderman E, Mattsson J, Svenson M, Borkird C, Engström P (1994) Expression patterns of novel genes encoding homeodomain leucine-zipper proteins in Arabidopsis thaliana. Plant Molecular Biology 26, 145–154.
Expression patterns of novel genes encoding homeodomain leucine-zipper proteins in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 7948864PubMed |

Song Y, Joo J, Ryu H, Lee J, Bae Y, Nam K (2007) Reactive oxygen species mediate IAA-lnduced ethylene production in mungbean (Vigna radiata L.) hypocotyls. Journal of Plant Biology 50, 18–23.
Reactive oxygen species mediate IAA-lnduced ethylene production in mungbean (Vigna radiata L.) hypocotyls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXktleitLw%3D&md5=2987ad984f50e994819cdcab2cd61521CAS |

Soyano T, Thitamadee S, Machida Y, Chua NH (2008) ASYMMETRIC LEAVES2-LIKE19/LATERAL ORGAN BOUNDARIES DOMAIN30 and ASL20/LBD18 regulate tracheary element differentiation in Arabidopsis. The Plant Cell 20, 3359–3373.
ASYMMETRIC LEAVES2-LIKE19/LATERAL ORGAN BOUNDARIES DOMAIN30 and ASL20/LBD18 regulate tracheary element differentiation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXitVarurg%3D&md5=56a66cd6b021f79f4b501fc78b49d66bCAS | 19088331PubMed |

Sturaro M, Hartings H, Schmelzer E, Velasco R, Salamini F, Motto M (2005) Cloning and characterization of GLOSSY1, a maize gene involved in cuticle membrane and wax production. Plant Physiology 138, 478–489.
Cloning and characterization of GLOSSY1, a maize gene involved in cuticle membrane and wax production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXks12hs7o%3D&md5=e8b725d852c2511e5a30398056775918CAS | 15849306PubMed |

TAIR (2006) http://www.arabidopsis.org/browse/genefamily/index.jsp

Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, Krüger P, Selbig J, Müller LA, Rhee SY, Stitt M (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. The Plant Journal 37, 914–939.
MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjtFChu78%3D&md5=d9d5c13b1336be4985ea2d4d15d2d342CAS | 14996223PubMed |

Thomas MR, Johnson LB, White FF (1990) Selection of interspecific somatic hybrids of Medicago truncatula by using Agrobacterium-transformed tissues. Plant Science 69, 189–198.
Selection of interspecific somatic hybrids of Medicago truncatula by using Agrobacterium-transformed tissues.Crossref | GoogleScholarGoogle Scholar |

Tian C, Muto H, Higuchi K, Matamura T, Tatematsu K, Koshiba T, Yamamoto KT (2004) Disruption and overexpression of auxin response factor 8 gene of Arabidopsis affect hypocotyl elongation and root growth habit, indicating its possible involvement in auxin homeostasis in light condition. The Plant Journal 40, 333–343.
Disruption and overexpression of auxin response factor 8 gene of Arabidopsis affect hypocotyl elongation and root growth habit, indicating its possible involvement in auxin homeostasis in light condition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVShurjF&md5=d2736716b86a8ccdcbdd476d41409dd9CAS | 15469491PubMed |

Tognolli M, Penel C, Greppin H, Simon P (2002) Analysis and expression of the class III peroxidase large gene family in Arabidopsis thaliana. Gene 288, 129–138.
Analysis and expression of the class III peroxidase large gene family in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjvFGiur8%3D&md5=a89e596cd6d7feffb6f435c27fb1ed16CAS | 12034502PubMed |

Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proceedings of the National Academy of Sciences of the United States of America 98, 5116–5121.
Significance analysis of microarrays applied to the ionizing radiation response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjt1Ons7w%3D&md5=540c767f7b18d4d2268a63d8d302fcf1CAS | 11309499PubMed |

Ubeda-Tomás S, Swarup R, Coates J, Swarup K, Laplaze L, Beemster GTS, Hedden P, Bhalerao R, Bennett MJ (2008) Root growth in Arabidopsis requires gibberellin/DELLA signalling in the endodermis. Nature Cell Biology 10, 625–628.
Root growth in Arabidopsis requires gibberellin/DELLA signalling in the endodermis.Crossref | GoogleScholarGoogle Scholar | 18425113PubMed |

van Noorden GE, Ross JJ, Reid JB, Rolfe BG, Mathesius U (2006) Defective long-distance auxin transport regulation in the Medicago truncatula super numeric nodules mutant. Plant Physiology 140, 1494–1506.
Defective long-distance auxin transport regulation in the Medicago truncatula super numeric nodules mutant.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjsl2js78%3D&md5=ef912bbf229d2c43891e90d33982f540CAS | 16489131PubMed |

Vernoux T, Wilson RC, Seeley KA, Reichheld J-P, Muroy S, et al (2000) The ROOT MERISTEMLESS1/CADMIUM SENSITIVE2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during postembryonic root development. The Plant Cell 12, 97–110.

Veronico P, Giannino D, Melillo MT, Leone A, Reyes A, Kennedy MW, Bleve-Zacheo T (2006) A novel lipoxygenase in pea roots. Its function in wounding and biotic stress. Plant Physiology 141, 1045–1055.
A novel lipoxygenase in pea roots. Its function in wounding and biotic stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xnt1Ogtrg%3D&md5=21013bc8263f159fd0d1e15ed9da2ebeCAS | 16679421PubMed |

Wasson AP, Pellerone FI, Mathesius U (2006) Silencing the flavonoid pathway in Medicago truncatula inhibits root nodule formation and prevents auxin transport regulation by rhizobia. The Plant Cell 18, 1617–1629.
Silencing the flavonoid pathway in Medicago truncatula inhibits root nodule formation and prevents auxin transport regulation by rhizobia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmvV2qt7s%3D&md5=82d203bd09740ba48d1b5b1006b39aefCAS | 16751348PubMed |

Wasson AP, Ramsay K, Jones MGK, Mathesius U (2009) Differing requirements for flavonoids during the formation of lateral roots, nodules and root knot nematode galls in Medicago truncatula. New Phytologist 183, 167–179.
Differing requirements for flavonoids during the formation of lateral roots, nodules and root knot nematode galls in Medicago truncatula.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosFCrsr8%3D&md5=6b79a62823d11002b435b74ccc4bc38bCAS | 19402878PubMed |

Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ (2007) An ‘electronic fluorescent pictograph’ browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2, e718
An ‘electronic fluorescent pictograph’ browser for exploring and analyzing large-scale biological data sets.Crossref | GoogleScholarGoogle Scholar | 17684564PubMed |

Wisniewski J-P, Gardner C, Brewin N (1999) Isolation of lipoxygenase cDNA clones from pea nodule mRNA. Plant Molecular Biology 39, 775–783.
Isolation of lipoxygenase cDNA clones from pea nodule mRNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjtFSqs7g%3D&md5=3184e1dc4423fcd15f14a3a54697fed3CAS | 10350091PubMed |

Wu Z, Irizarry RA, Gentleman R, Murillo FM, Spencer F (2004) A model based background adjustment for oligonucleotide expression arrays. Technical report. Department of Biostatistics Working Papers, John Hopkins University, Baltimore, MD, USA.

Yaxley JR, Ross JJ, Sherriff LJ, Reid JB (2001) Gibberellin biosynthesis mutations and root development in pea. Plant Physiology 125, 627–633.
Gibberellin biosynthesis mutations and root development in pea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhs1Kls7g%3D&md5=2eae5644303427ca05646e01bf4c94d5CAS | 11161020PubMed |

Yoko M, Hidekazu I, Yasunori M, Chiyoko M (2009) Characterization of genes in the ASYMMETRIC LEAVES2/LATERAL ORGAN BOUNDARIES (AS2/LOB) family in Arabidopsis thaliana, and functional and molecular comparisons between AS2 and other family members. The Plant Journal 58, 525–537.
Characterization of genes in the ASYMMETRIC LEAVES2/LATERAL ORGAN BOUNDARIES (AS2/LOB) family in Arabidopsis thaliana, and functional and molecular comparisons between AS2 and other family members.Crossref | GoogleScholarGoogle Scholar | 19154202PubMed |