Overexpression of miR160 affects root growth and nitrogen-fixing nodule number in Medicago truncatula
Pilar Bustos-Sanmamed A , Guohong Mao B , Ying Deng B , Morgane Elouet A , Ghazanfar Abbas Khan A , Jérémie Bazin A C , Marie Turner D , Senthil Subramanian D , Oliver Yu B , Martin Crespi A E and Christine Lelandais-Brière A C
+ Author Affiliations
- Author Affiliations
A Institut des Sciences du Végétal (ISV), Centre National de la Recherche Scientifique (CNRS), Gif sur Yvette F-91198 Gif-sur-Yvette Cedex, France.
B Donald Danforth Plant Science Center, St Louis, MO 63132, USA.
C Université Paris Diderot, Sorbonne Paris Cité, F-75205 Paris Cedex 13, France.
D Department of Plant Science, Department of Biology and Microbiology, South Dakota State University, Brookings, SD 57007, USA.
E Corresponding author. Email: crespi@isv.cnrs-gif.fr
This paper originates from a presentation at the ‘VI International Conference on Legume Genetics and Genomics (ICLGG)’ Hyderabad, India, 2–7 October 2012.
Functional Plant Biology 40(12) 1208-1220 https://doi.org/10.1071/FP13123
Submitted: 1 May 2013 Accepted: 21 August 2013 Published: 7 October 2013
Abstract
Auxin action is mediated by a complex signalling pathway involving transcription factors of the auxin response factor (ARF) family. In Arabidopsis, microRNA160 (miR160) negatively regulates three ARF genes (ARF10/ARF16/ARF17) and therefore controls several developmental processes, including primary and lateral root growth. Here, we analysed the role of miR160 in root development and nodulation in Medicago truncatula Gaertn. Bioinformatic analyses identified two main mtr-miR160 variants (mtr-miR160abde and mtr-miR160c) and 17 predicted ARF targets. The miR160-dependent cleavage of four predicted targets in roots was confirmed by analysis of parallel analysis of RNA ends (PARE) data and RACE-PCR experiments. Promoter-GUS analyses for mtr-miR160d and mtr-miR160c genes revealed overlapping but distinct expression profiles during root and nodule development. In addition, the early miR160 activation in roots during symbiotic interaction was not observed in mutants of the nodulation signalling or autoregulation pathways. Composite plants that overexpressed mtr-miR160a under two different promoters exhibited distinct defects in root growth and nodulation: the p35S:miR160a construct led to reduced root length associated to a severe disorganisation of the RAM, whereas pCsVMV:miR160a roots showed gravitropism defects and lower nodule numbers. Our results suggest that a regulatory loop involving miR160/ARFs governs root and nodule organogenesis in M. truncatula.
Additional keywords: auxin, legume, miRNA, root development, symbiotic nodulation.
References
Addo-Quaye C, Miller W, Axtell MJ (2009) CleaveLand: a pipeline for using degradome data to find cleaved small RNA targets. Bioinformatics 25, 130–131.| CleaveLand: a pipeline for using degradome data to find cleaved small RNA targets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmvFWl&md5=6f8da2a490c34a272e3d1e5c50eedf64CAS | 19017659PubMed |
Allen ON, Allen EK (1953) Morphogenesis of the leguminous root nodule. Brookhaven Symposia in Biology 6, 209–232.
Amor BB, Shaw SL, Oldroyd GE, Maillet F, Penmetsa RV, Cook D, Long SR, Dénarié J, Gough C (2003) 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. The Plant Journal 34, 495–506.
| 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.Crossref | GoogleScholarGoogle Scholar | 12753588PubMed |
Ané JM, Kiss GB, Penmetsa RV, Oldroyd GED, Ayax C, Lévy J, Debellé F, Baek J-M, Kalo P, Rosenberg C, Roe BA, Long SR, Dénarié J, Cook DR (2004) Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303, 1364–1367.
| Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes.Crossref | GoogleScholarGoogle Scholar | 14963334PubMed |
Band LR, Darren MW, Larrieu A, Sun J, Middleton AM, French AP, Brunoud G, Mendocilla Sato E, Wilson MH, Péret B, et al (2012) Root gravitropism is regulated by a transient lateral auxin gradient controlled by a tipping-point mechanism. Proceedings of the National Academy of Sciences of the United States of America
| Root gravitropism is regulated by a transient lateral auxin gradient controlled by a tipping-point mechanism.Crossref | GoogleScholarGoogle Scholar | 22523244PubMed |
Benková E, Bielach A (2010) Lateral root organogenesis – from cell to organ. Current Opinion in Plant Biology 13, 677–683.
| Lateral root organogenesis – from cell to organ.Crossref | GoogleScholarGoogle Scholar | 20934368PubMed |
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 |
Boisson-Dernier A, Chabaud M, Garcia F, Bécard G, Rosenberg C, Barker DG (2001) Agrobacterium rhizogenes-transformed roots of Medicago truncatula for the study of nitrogen-fixing and endomycorrhizal symbiotic associations. Molecular Plant-Microbe Interactions 14, 695–700.
| Agrobacterium rhizogenes-transformed roots of Medicago truncatula for the study of nitrogen-fixing and endomycorrhizal symbiotic associations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjvVSjsLw%3D&md5=602d9514862ce3a1cdfa00cb9f6b16b5CAS | 11386364PubMed |
Brodersen P, Voinnet O (2009) Revisiting the principles of microRNA target recognition and mode of action. Nature Reviews. Molecular Cell Biology 10, 141–148.
| Revisiting the principles of microRNA target recognition and mode of action.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltFWqtg%3D%3D&md5=547e836dd38eab1f2edb3a84201bfd9dCAS | 19145236PubMed |
Chen X (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303, 2022–2025.
| A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXisVGlt7g%3D&md5=80a1019af1b626a4f3d5cc98e9b9e07cCAS | 12893888PubMed |
Collier R, Fuchs B, Walter N, Kevin Lutke W, Taylor CG (2005) Ex vitro composite plants: an inexpensive, rapid method for root biology. The Plant Journal 43, 449–457.
| Ex vitro composite plants: an inexpensive, rapid method for root biology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXnsVCjurg%3D&md5=1cf4370a0e6a2209b799ef6dcc46ea70CAS | 16045479PubMed |
Crespi M, Frugier F (2008) De novo organ formation from differentiated cells: root nodule organogenesis. Science Signaling 1, re11
| De novo organ formation from differentiated cells: root nodule organogenesis.Crossref | GoogleScholarGoogle Scholar | 19066400PubMed |
D’haeseleer K, Den Herder G, Laffont C, Plet J, Mortier V, Lelandais-Brière C, De Bodt S, De Keyser A, Crespi M, Holsters M, Frugier F, Goormachtig S (2011) Transcriptional and post-transcriptional regulation of a NAC1 transcription factor in Medicago truncatula roots. New Phytologist 191, 647–661.
| Transcriptional and post-transcriptional regulation of a NAC1 transcription factor in Medicago truncatula roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFWjtL%2FL&md5=0a6d0bfefdc0c9203ae68b68da5498d2CAS | 21770944PubMed |
de Billy F, Grosjean C, May S, Bennett M, Cullimore JV (2001) Expression studies on AUX1-like genes in Medicago truncatula suggest that auxin is required at two steps in early nodule development. Molecular Plant-Microbe Interactions 14, 267–277.
| Expression studies on AUX1-like genes in Medicago truncatula suggest that auxin is required at two steps in early nodule development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhsVKgsLw%3D&md5=f9d7bb47efadc36f62c2f46d70a7ec60CAS | 11277424PubMed |
de Lorenzo L, Merchan F, Laporte P, Thompson R, Clarke J, Sousa C, Crespi M (2009) A novel plant leucine-rich repeat receptor kinase regulates the response of Medicago truncatula roots to salt stress. The Plant Cell 21, 668–680.
| A novel plant leucine-rich repeat receptor kinase regulates the response of Medicago truncatula roots to salt stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXksVKrt7k%3D&md5=ff9987a32d9c46a711e8e95616cddca8CAS | 19244136PubMed |
De Rybel B, Vassileva V, Parizot B, Demeulenaere M, Grunewald W, Audenaert D, Van Campenhout J, Overvoorde P, Jansen L, Vanneste S, et al (2010) A novel aux/IAA28 signaling cascade activates GATA23-dependent specification of lateral root founder cell identity. Current Biology 20, 1697–1706.
| A novel aux/IAA28 signaling cascade activates GATA23-dependent specification of lateral root founder cell identity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1OmtrjO&md5=e4fd8da4bcdeb147cc2db2252126b1efCAS | 20888232PubMed |
De Smet I (2012) Lateral root initiation: one step at a time. New Phytologist 193, 867–873.
| Lateral root initiation: one step at a time.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XivVyht7s%3D&md5=befb5680c96ced60ddf281da67468000CAS | 22403823PubMed |
Devers EA, Branscheid A, May P, Krajinski F (2011) Stars and symbiosis: microRNA- and microRNA*-mediated transcript cleavage involved in arbuscular mycorrhizal symbiosis. Plant Physiology 156, 1990–2010.
| Stars and symbiosis: microRNA- and microRNA*-mediated transcript cleavage involved in arbuscular mycorrhizal symbiosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVOrur3M&md5=f253045c73b2f06de3c179b9ed9083c3CAS | 21571671PubMed |
Dharmasiri N, Estelle M (2004) Auxin signaling and regulated protein degradation. Trends in Plant Science 9, 302–308.
| Auxin signaling and regulated protein degradation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXksVemur0%3D&md5=9dfb2e3f243253ac273b69be9c3c7c60CAS | 15165562PubMed |
Ding Z, Friml J (2010) Auxin regulates distal stem cell differentiation in Arabidopsis roots. Proceedings of the National Academy of Sciences of the United States of America 107, 12 046–12 051.
| Auxin regulates distal stem cell differentiation in Arabidopsis roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXovVartbk%3D&md5=fbf24f8c82e89990e1b0ef891b191c69CAS |
Ding Y, Oldroyd GE (2009) Positioning the nodule, the hormone dictum. Plant Signaling & Behavior 4, 89–93.
| Positioning the nodule, the hormone dictum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpsVyqtr0%3D&md5=c2ef015386a264e2bc0396f2e7ee8f29CAS |
Fukaki H, Tasaka M (2009) Hormone interactions during lateral root formation. Plant Molecular Biology 69, 437–449.
| Hormone interactions during lateral root formation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhvVOisLw%3D&md5=b3dd72a7153790b1b1f0717fa98757f4CAS | 18982413PubMed |
Govindarajulu M, Elmore JM, Fester T, Taylor CG (2008) Evaluation of constitutive viral promoters in transgenic soybean roots and nodules. Molecular Plant-Microbe Interactions 21, 1027–1035.
| Evaluation of constitutive viral promoters in transgenic soybean roots and nodules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXos1Citbg%3D&md5=29e3cd3920a3216135cfc90e810571c7CAS | 18616399PubMed |
Graham TL, Graham MY, Subramanian S, Yu O (2007) RNAi silencing of genes for elicitation or biosynthesis of 5-deoxyisoflavonoids suppresses race-specific resistance and hypersensitive cell death in Phytophthora sojae infected tissues. Plant Physiology 144, 728–740.
| RNAi silencing of genes for elicitation or biosynthesis of 5-deoxyisoflavonoids suppresses race-specific resistance and hypersensitive cell death in Phytophthora sojae infected tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmvValtr8%3D&md5=35cdd1d2e4dd8b85e058ac8b207d9809CAS | 17416637PubMed |
Guilfoyle TJ, Hagen G (2007) Auxin response factors. Current Opinion in Plant Biology 10, 453–460.
| Auxin response factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFekurvE&md5=56251421ab2c382b08dfdf2677299b4aCAS | 17900969PubMed |
Gutierrez L, Bussell JD, Pacurar DI, Schwambach J, Pacurar M, Bellini C (2009) Phenotypic plasticity of adventitious rooting in Arabidopsis is controlled by complex regulation of AUXIN RESPONSE FACTOR transcripts and microRNA abundance. The Plant Cell 21, 3119–3132.
| Phenotypic plasticity of adventitious rooting in Arabidopsis is controlled by complex regulation of AUXIN RESPONSE FACTOR transcripts and microRNA abundance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFOgsLvE&md5=70da1b8809c17ccc1195d643452db121CAS | 19820192PubMed |
Gutierrez L, Mongelard G, Floková K, Pacurar DI, Novák O, Staswick P, Kowalczyk M, Pacurar M, Demailly H, Geiss G, Bellini C (2012) Auxin controls Arabidopsis adventitious root initiation by regulating jasmonic acid homeostasis. The Plant Cell 24, 2515–2527.
| Auxin controls Arabidopsis adventitious root initiation by regulating jasmonic acid homeostasis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1Wjs7fF&md5=a46b8e4ed786a47080e1275bc51a8dc7CAS | 22730403PubMed |
Hayashi K (2012) The interaction and integration of auxin signaling components. Plant & Cell Physiology 53, 965–975.
| The interaction and integration of auxin signaling components.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XotlelsLY%3D&md5=e8703e1df8ce46411432ebca3543720cCAS |
Hirsch AM, Bhuvaneswari TV, Torrey JG, Bisseling T (1989) Early nodulin genes are induced in alfalfa root outgrowths elicited by auxin transport inhibitors. Proceedings of the National Academy of Sciences of the United States of America 86, 1244–1248.
| Early nodulin genes are induced in alfalfa root outgrowths elicited by auxin transport inhibitors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXhvV2mtrs%3D&md5=e70edc860932a00e460fa94637e7dbc3CAS | 16594017PubMed |
Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Molecular Cell 14, 787–799.
| Computational identification of plant microRNAs and their targets, including a stress-induced miRNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlslemtrs%3D&md5=701f817f29fc015c7b9c8b2e9f36abe5CAS | 15200956PubMed |
Karimi M, Inzé D, Depicker A (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends in Plant Science 7, 193–195.
| GATEWAY vectors for Agrobacterium-mediated plant transformation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xjtl2ktrk%3D&md5=dae9df422526bdbb4256673c46cfc730CAS | 11992820PubMed |
Khan GA, Declerck M, Sorin C, Hartmann C, Crespi M, Lelandais-Brière C (2011) MicroRNAs as regulators of root development and architecture. Plant Molecular Biology 77, 47–58.
| MicroRNAs as regulators of root development and architecture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVKjtrvN&md5=3c1c2cb03856f0e74086f9fd38278ef0CAS | 21607657PubMed |
Kondorosi E, Schultze M, Savoure A, Hoffmann B, Dudits D, Pierre M, Allison L, Bauer P, Kiss GB, Kondorosi A (1993) Control of nodule induction and plant cell growth by Nod factors. In ‘Advances in molecular-genetics of plant–microbe interactions’. (Eds EW Nester, DPS Verma) pp. 143–150. (Kluwer Academic Publishers: Dordrecht, The Netherlands)
Kuppusamy KT, Ivashuta S, Bucciarelli B, Vance CP, Gantt JS, Vandenbosch KA (2009) Knockdown of CELL DIVISION CYCLE16 reveals an inverse relationship between lateral root and nodule numbers and a link to auxin in Medicago truncatula. Plant Physiology 151, 1155–1166.
| Knockdown of CELL DIVISION CYCLE16 reveals an inverse relationship between lateral root and nodule numbers and a link to auxin in Medicago truncatula.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVCjsbvO&md5=25a4010b4514c4c727915b405a06acf8CAS | 19789288PubMed |
Lelandais-Brière C, Naya L, Sallet E, Calenge F, Frugier F, Hartmann C, Gouzy J, Crespi M (2009) Genome-wide Medicago truncatula small RNA analysis revealed novel microRNAs and isoforms differentially regulated in roots and nodules. The Plant Cell 21, 2780–2796.
| Genome-wide Medicago truncatula small RNA analysis revealed novel microRNAs and isoforms differentially regulated in roots and nodules.Crossref | GoogleScholarGoogle Scholar | 19767456PubMed |
Lewis DR, Miller ND, Splitt BL, Wu G, Spalding EP (2007) Separating the roles of acropetal and basipetal auxin transport on gravitropism with mutations in two Arabidopsis multidrug resistance-like ABC transporter genes. The Plant Cell 19, 1838–1850.
| Separating the roles of acropetal and basipetal auxin transport on gravitropism with mutations in two Arabidopsis multidrug resistance-like ABC transporter genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXptFKnsro%3D&md5=98fc48fd5ac7e75cd4f05811a685deabCAS | 17557805PubMed |
Li H, Deng Y, Wu T, Subramanian S, Yu O (2010) Misexpression of miR482, miR1512, and miR1515 increases soybean nodulation. Plant Physiology 153, 1759–1770.
| Misexpression of miR482, miR1512, and miR1515 increases soybean nodulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVCrsrzP&md5=9555882f1bd9c5cf720f353873b86906CAS | 20508137PubMed |
Liu PP, Montgomery TA, Fahlgren N, Kasschau KD, Nonogaki H, Carrington JC (2007) Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages. The Plant Journal 52, 133–146.
| Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1SjsLzO&md5=b8cf6b8ef09146bf8bdfe52ebb38e9c0CAS | 17672844PubMed |
Maekawa T, Maekawa-Yoshikawa M, Takeda N, Imaizumi-Anraku H, Murooka Y, Hayashi M (2009) Gibberellin controls the nodulation signaling pathway in Lotus japonicus. The Plant Journal 58, 183–194.
| Gibberellin controls the nodulation signaling pathway in Lotus japonicus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlsVWltLk%3D&md5=7d23cc1be65d1592eb60bb145f4cb41eCAS | 19121107PubMed |
Mallory AC, Bartel DP, Bartel B (2005) MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes. The Plant Cell 17, 1360–1375.
| MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXksVKksrg%3D&md5=2fb456f7f363cdaec363ed2b34da5a51CAS | 15829600PubMed |
Mathesius U, Schlaman HR, Spaink HP, Of Sautter C, Rolfe BG, Djordjevic MA (1998) Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides. The Plant Journal 14, 23–34.
| Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjtV2is7o%3D&md5=26de7cf5f45a4234cc0224acdb413f15CAS | 15494052PubMed |
Mathesius U, Charon C, Rolfe BG, Kondorosi A, Crespi M (2000) 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. Molecular Plant-Microbe Interactions 13, 617–628.
| 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.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjsFensbc%3D&md5=402e977fe1aa46d55af038a41f149db2CAS | 10830261PubMed |
Meng Y, Ma X, Chen D, Wu P, Chen M (2010) MicroRNA-mediated signaling involved in plant root development. Biochemical and Biophysical Research Communications 393, 345–349.
| MicroRNA-mediated signaling involved in plant root development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjt1GrsL0%3D&md5=75f68c62f8bc05b86669378e186e650bCAS | 20138828PubMed |
Mun JH, Yu HJ, Shin JY, Oh M, Hwang HJ, Chung H (2012) Auxin response factor gene family in Brassica rapa: genomic organization, divergence, expression, and evolution. Molecular Genetics and Genomics 287, 765–784.
| Auxin response factor gene family in Brassica rapa: genomic organization, divergence, expression, and evolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVSntrbE&md5=530b60e7297073cb3a1b4e83046feb5cCAS | 22915303PubMed |
Notredame C, Higgins DG, Heringa J (2000) T-Coffee: a novel method for fast and accurate multiple sequence alignment. Journal of Molecular Biology 302, 205–217.
| T-Coffee: a novel method for fast and accurate multiple sequence alignment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmtVGntr8%3D&md5=0e38c8dea722b5e90b9a2d23ed06045cCAS | 10964570PubMed |
Overvoorde P, Fukaki H, Beeckman T (2010) Auxin control of root development. Cold Spring Harbor Perspectives in Biology 2, a001537
| Auxin control of root development.Crossref | GoogleScholarGoogle Scholar | 20516130PubMed |
Patriarca EJ, Tatè R, Ferraioli S, Iaccarino M (2004) Organogenesis of legume root nodules. International Review of Cytology 234, 201–262.
| Organogenesis of legume root nodules.Crossref | GoogleScholarGoogle Scholar | 15066376PubMed |
Péret B, De Rybel B, Casimiro I, Benková E, Swarup R, Laplaze L, Beeckman T, Bennett MJ (2009) Arabidopsis lateral root development: an emerging story. Trends in Plant Science 14, 399–408.
| Arabidopsis lateral root development: an emerging story.Crossref | GoogleScholarGoogle Scholar | 19559642PubMed |
Perilli S, Di Mambro R, Sabatini S (2012) Growth and development of the root apical meristem. Current Opinion in Plant Biology 15, 17–23.
| Growth and development of the root apical meristem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsFCrs7w%3D&md5=e7673149937f65b545e1cd51f7ad5008CAS | 22079783PubMed |
Petersson SV, Johansson AI, Kowalczyk M, Makoveychuk A, Wang JY, Moritz T, Grebe M, Benfey PN, Sandberg G, Ljung K (2009) An auxin gradient and maximum in the Arabidopsis root apex shown by high-resolution cell-specific analysis of IAA distribution and synthesis. The Plant Cell 21, 1659–1668.
| An auxin gradient and maximum in the Arabidopsis root apex shown by high-resolution cell-specific analysis of IAA distribution and synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpvFOksrk%3D&md5=1951367e9e9b1ac2026aa52f4d2bae82CAS | 19491238PubMed |
Rashotte AM, Brady SR, Reed RC, Ante SJ, Muday GK (2000) Basipetal auxin transport is required for gravitropism in roots of Arabidopsis. Plant Physiology 122, 481–490.
| Basipetal auxin transport is required for gravitropism in roots of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXktFCjtb8%3D&md5=8dce081caf9a8f044201153ec4ad017eCAS | 10677441PubMed |
Reed RC, Brady SR, Muday GK (1998) Inhibition of auxin movement from the shoot into the root inhibits lateral root development in Arabidopsis. Plant Physiology 118, 1369–1378.
| Inhibition of auxin movement from the shoot into the root inhibits lateral root development in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhtlQ%3D&md5=abcf59b4d98bc76780a3a343d3116b42CAS | 9847111PubMed |
Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In ‘Bioinformatics methods and protocols: methods in molecular biology’. (Eds S Krawetz, S Misener) pp. 365–386. (Humana Press: Totowa, NJ, USA)
Samac DA, Tesfaye M, Dornbusch M, Saruul P, Temple SJ (2004) A comparison of constitutive promoters for expression of transgenes in alfalfa (Medicago sativa). Transgenic Research 13, 349–361.
| A comparison of constitutive promoters for expression of transgenes in alfalfa (Medicago sativa).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXntFGms70%3D&md5=05fceddec9009e44cc51eb91b5a084eeCAS | 15517994PubMed |
Schnabel E, Etienne-Pascal J, de Carvalho-Niebel F, Gerard D, Frugoli J (2005) The Medicago truncatula SUNN gene encodes a CLV1-like leucine-rich repeat receptor kinase that regulates nodule number and root length. Plant Molecular Biology 58, 809–822.
| The Medicago truncatula SUNN gene encodes a CLV1-like leucine-rich repeat receptor kinase that regulates nodule number and root length.Crossref | GoogleScholarGoogle Scholar | 16240175PubMed |
Stougaard J (2000) Regulators and regulation of legume root nodule development. Plant Physiology 124, 531–540.
| Regulators and regulation of legume root nodule development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnsF2rs70%3D&md5=659c84cccb4359d349978143ca2285e8CAS | 11027704PubMed |
Su YH, Liu YB, Zhang XS (2011) Auxin-cytokinin interaction regulates meristem development. Molecular Plant 4, 616–625.
| Auxin-cytokinin interaction regulates meristem development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXps1Orsbw%3D&md5=307a2903695c924a32cfa8bdb90624fdCAS | 21357646PubMed |
Subramanian S, Stacey G, Yu O (2006) Endogenous isoflavones are essential for the establishment of symbiosis between soybean and Bradyrhizobium japonicum. The Plant Journal 48, 261–273.
| Endogenous isoflavones are essential for the establishment of symbiosis between soybean and Bradyrhizobium japonicum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFGhsr3N&md5=3ff2f477dfd4b8cf031a02ec2438ae72CAS | 17018035PubMed |
Subramanian S, Stacey G, Yu O (2007) Distinct, crucial roles of flavonoids during legume nodulation. Trends in Plant Science 12, 282–285.
| Distinct, crucial roles of flavonoids during legume nodulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnslWlu70%3D&md5=35ce9e0cb94e428af6730f127e315773CAS | 17591456PubMed |
Subramanian S, Fu Y, Sunkar R, Barbazuk WB, Zhu JK, Yu O (2008) Novel and nodulation-regulated microRNAs in soybean roots. BMC Genomics 9, 160
| Novel and nodulation-regulated microRNAs in soybean roots.Crossref | GoogleScholarGoogle Scholar | 18402695PubMed |
Suzaki T, Yano K, Ito M, Umehara Y, Suganuma N, Kawaguchi M (2012) Positive and negative regulation of cortical cell division during root nodule development in Lotus japonicus is accompanied by auxin response. Development 139, 3997–4006.
| Positive and negative regulation of cortical cell division during root nodule development in Lotus japonicus is accompanied by auxin response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVaksbnP&md5=c100506a1b44ebe757ac87af923b869aCAS | 23048184PubMed |
Suzaki T, Ito M, Kawaguchi M (2013) Genetic basis of cytokinin and auxin functions during root nodule development. Frontiers in Plant Science 4, 42
| Genetic basis of cytokinin and auxin functions during root nodule development.Crossref | GoogleScholarGoogle Scholar | 23483805PubMed |
Truernit E, Bauby H, Dubreucq B, Grandjean O, Runions J, Barthélémy J, Palauqui JC (2008) High-resolution whole-mount imaging of three-dimensional tissue organization and gene expression enables the study of phloem development and structure in Arabidopsis. The Plant Cell 20, 1494–1503.
| High-resolution whole-mount imaging of three-dimensional tissue organization and gene expression enables the study of phloem development and structure in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpvVOisLo%3D&md5=20d96397bb9690e2f50b8b90a7a82ea4CAS | 18523061PubMed |
Turner M, Nizampatnam NR, Baron M, Coppin S, Damodaran S, Adhikari S, Arunachalam S, Yu O, Subramanian S (2013) Ectopic expression of miR160 results in auxin hypersensitivity, cytokinin hyposensitivity, and inhibition of symbiotic nodule development in soybean. Plant Physiology
| Ectopic expression of miR160 results in auxin hypersensitivity, cytokinin hyposensitivity, and inhibition of symbiotic nodule development in soybean.Crossref | GoogleScholarGoogle Scholar | 23796794PubMed |
Ulmasov T, Hagen G, Guilfoyle TJ (1999) Activation and repression of transcription by auxin-response factors. Proceedings of the National Academy of Sciences of the United States of America 96, 5844–5849.
| Activation and repression of transcription by auxin-response factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjtFCnu7s%3D&md5=89e25d5fe8982cff1f2ad64a21b50625CAS | 10318972PubMed |
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=f8da7e468a2d35a21af0d9187c77344fCAS | 16489131PubMed |
van Noorden GE, Kerim T, Goffard N, Wiblin R, Pellerone FI, Rolfe BG, Mathesius U (2007) Overlap of proteome changes in Medicago truncatula in response to auxin and Sinorhizobium meliloti. Plant Physiology 144, 1115–1131.
| Overlap of proteome changes in Medicago truncatula in response to auxin and Sinorhizobium meliloti.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmvValtbw%3D&md5=8a90b05507791334c2acbf21d697dc97CAS | 17468210PubMed |
Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3, research0034–research0034.11.
| Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes.Crossref | GoogleScholarGoogle Scholar | 12184808PubMed |
Vanstraelen M, Benková E (2012) Hormonal interactions in the regulation of plant development. Annual Review of Cell and Developmental Biology 28, 463–487.
| Hormonal interactions in the regulation of plant development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslagtbrL&md5=6dffbda995dacde117ea3b2436be8170CAS | 22856461PubMed |
Varkonyi-Gasic E, Hellens RP (2011) Quantitative stem-loop RT-PCR for detection of microRNAs. Methods in Molecular Biology 744, 145–157.
| Quantitative stem-loop RT-PCR for detection of microRNAs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXotFWkurc%3D&md5=54251e4f44f97982be670f0f2b45a8f8CAS | 21533691PubMed |
Wang JW, Wang LJ, Mao YB, Cai WJ, Xue HW, Chen XY (2005) Control of root cap formation by microRNA-targeted auxin response factors in Arabidopsis. The Plant Cell 17, 2204–2216.
| Control of root cap formation by microRNA-targeted auxin response factors in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpsFGjs7c%3D&md5=2e138965e9a98c7175f24a404a8fa581CAS | 16006581PubMed |
Wang D, Pei K, Fu Y, Sun Z, Li S, Liu H, Tang K, Han B, Tao Y (2007) Genome-wide analysis of the auxin response factors (ARF) gene family in rice (Oryza sativa). Gene 394, 13–24.
| Genome-wide analysis of the auxin response factors (ARF) gene family in rice (Oryza sativa).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXksVelur8%3D&md5=00be7a0da633798da754556f32c1d930CAS | 17408882PubMed |
Wang Y, Deng D, Shi Y, Miao N, Bian Y, Yin Z (2012) Diversification, phylogeny and evolution of auxin response factor (ARF) family: insights gained from analyzing maize ARF genes. Molecular Biology Reports 39, 2401–2415.
| Diversification, phylogeny and evolution of auxin response factor (ARF) family: insights gained from analyzing maize ARF genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVWmtrw%3D&md5=d19ba9f54d31969db36ec4bf1c3e7c39CAS | 21667107PubMed |
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=817a84a53facca1828d421f8ee202339CAS | 16751348PubMed |
Zhang J, Subramanian S, Stacey G, Yu O (2009) Flavones and flavonols play distinct critical roles during nodulation of Medicago truncatula by Sinorhizobium meliloti. The Plant Journal 57, 171–183.
| Flavones and flavonols play distinct critical roles during nodulation of Medicago truncatula by Sinorhizobium meliloti.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFOiu7s%3D&md5=7ce318a48d7e2ae3d16408dfcb95b181CAS | 18786000PubMed |
