A systems biology approach identifies new regulators of poplar root development under low nitrogen

Dash, Madhumita; Yordanov, Yordan S.; Georgieva, Tatyana; Kumari, Sapna; Wei, Hairong; Busov, Victor

doi:10.1111/tpj.13002

Title: A systems biology approach identifies new regulators of poplar root development under low nitrogen

Journal Article · Thu Oct 08 00:00:00 EDT 2015 · The Plant Journal

DOI:https://doi.org/10.1111/tpj.13002· OSTI ID:1401156

Dash, Madhumita ^[1]; Yordanov, Yordan S. ^[2]; Georgieva, Tatyana ^[1]; Kumari, Sapna ^[1]; Wei, Hairong ^[1]; Busov, Victor ^[1]

Forest Resources and Environmental Science Michigan Technological University Houghton MI 49931 USA
Department of Biological Sciences Eastern Illinois University Charleston IL 61920 USA

Summary In Populus , low nitrogen ( LN ) elicits rapid and vigorous lateral root ( LR ) proliferation, which is closely mirrored by corresponding transcriptomic changes. Using transcriptomic data, we built a genetic network encompassing a large proportion of the differentially regulated transcriptome. The network is organized in a hierarchical fashion, centered on 11 genes. Transgenic manipulations of only three of the 11 genes had a strong impact on root development under LN . These three genes encoded an F‐box protein similar to Hawaiian Skirt ( Pta HWS ) and two transcription factors ( Pta RAP 2.11 and Pta NAC 1 ). Up‐ and downregulation of the three genes caused increased and decreased root proliferation under LN conditions, respectively. The transgenic manipulations had a strong positive effect on growth under greenhouse conditions including increased shoot and root biomass. The three genes appeared to encompass a putative yet‐unknown mechanism that underlies root development under LN . Specifically, the genes are predominantly expressed in roots and have a similar temporal response to LN . More importantly, transgenic manipulation for each of the three genes had a highly significant impact on the expression of the other two. The transgenic manipulations appear to also affect the expression of the regulatory mi RNA ( Ptami RNA 164e ) of one of the transcription factors ( Pta NAC 1 ), albeit in an opposite fashion. Consistent with a putative function of Pta HWS in proteasome degradation, treatment with proteasome inhibitor reversed the expression changes in the transgenic plants. The insights from this study will allow genetic modifications of root architecture for more efficient and dynamic nitrogen foraging in biofuel crops like poplar.

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Sponsoring Organization:: USDOE

OSTI ID:: 1401156

Journal Information:: The Plant Journal, Journal Name: The Plant Journal Vol. 84 Journal Issue: 2; ISSN 0960-7412

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United Kingdom

Language:: English

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Cited by: 21 works

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References (58)

A DNA Transformation–Competent Arabidopsis Genomic Library in Agrobacterium Lazo, Gerard R.; Stein, Pascal A.; Ludwig, Robert A. Bio/Technology, Vol. 9, Issue 10 https://doi.org/10.1038/nbt1091-963	journal	October 1991
Manipulation of microRNA expression to improve nitrogen use efficiency Fischer, Jeffrey J.; Beatty, Perrin H.; Good, Allen G. Plant Science, Vol. 210 https://doi.org/10.1016/j.plantsci.2013.05.009	journal	September 2013
Mutants of Arabidopsis thaliana with pleiotropic effects on the expression of the gene for beta-amylase and on the accumulation of anthocyanin that are inducible by sugars Mita, Satoru; Murano, Nobuhito; Akaike, Mikiko The Plant Journal, Vol. 11, Issue 4 https://doi.org/10.1046/j.1365-313X.1997.11040841.x	journal	April 1997
The nodule inception-like protein 7 modulates nitrate sensing and metabolism in Arabidopsis Castaings, Loren; Camargo, Antonio; Pocholle, Delphine The Plant Journal, Vol. 57, Issue 3 https://doi.org/10.1111/j.1365-313X.2008.03695.x	journal	February 2009
Activation Tagging of a Dominant Gibberellin Catabolism Gene ( GA 2-oxidase ) from Poplar That Regulates Tree Stature Busov, Victor B.; Meilan, Richard; Pearce, David W. Plant Physiology, Vol. 132, Issue 3 https://doi.org/10.1104/pp.103.020354	journal	June 2003
Nutritional regulation of ANR1 and other root-expressed MADS-box genes in Arabidopsis thaliana Gan, Yinbo; Filleur, Sophie; Rahman, Azizur Planta, Vol. 222, Issue 4 https://doi.org/10.1007/s00425-005-0020-3	journal	July 2005
Expression and Interaction Analysis of Arabidopsis Skp1-Related Genes Takahashi, Naoki; Kuroda, Hirofumi; Kuromori, Takashi Plant and Cell Physiology, Vol. 45, Issue 1 https://doi.org/10.1093/pcp/pch009	journal	January 2004
HAWAIIAN SKIRT : An F-Box Gene That Regulates Organ Fusion and Growth in Arabidopsis González-Carranza, Zinnia H.; Rompa, Unchalee; Peters, Janny L. Plant Physiology, Vol. 144, Issue 3 https://doi.org/10.1104/pp.106.092288	journal	May 2007
MicroRNA regulation of the CUC genes is required for boundary size control in Arabidopsis meristems Laufs, P. Development, Vol. 131, Issue 17 https://doi.org/10.1242/dev.01320	journal	September 2004
Functions of microRNAs in plant stress responses Sunkar, Ramanjulu; Li, Yong-Fang; Jagadeeswaran, Guru Trends in Plant Science, Vol. 17, Issue 4 https://doi.org/10.1016/j.tplants.2012.01.010	journal	April 2012
Flavonoids as antioxidants in plants: Location and functional significance Agati, Giovanni; Azzarello, Elisa; Pollastri, Susanna Plant Science, Vol. 196 https://doi.org/10.1016/j.plantsci.2012.07.014	journal	November 2012
Systems approach identifies TGA1 and TGA4 transcription factors as important regulatory components of the nitrate response of Arabidopsis thaliana roots Alvarez, José M.; Riveras, Eleodoro; Vidal, Elena A. The Plant Journal, Vol. 80, Issue 1 https://doi.org/10.1111/tpj.12618	journal	August 2014
Enhancer trapping in woody plants: Isolation of the ET304 gene encoding a putative AT-hook motif transcription factor and characterization of the expression patterns conferred by its promoter in transgenic Populus and Arabidopsis Filichkin, Sergei A.; Wu, Qian; Busov, Victor Plant Science, Vol. 171, Issue 2 https://doi.org/10.1016/j.plantsci.2006.03.011	journal	August 2006
GATEWAY™ vectors for Agrobacterium-mediated plant transformation Karimi, Mansour; Inzé, Dirk; Depicker, Ann Trends in Plant Science, Vol. 7, Issue 5, p. 193-195 https://doi.org/10.1016/S1360-1385(02)02251-3	journal	May 2002
Involvement of miR169 in the nitrogen-starvation responses in Arabidopsis Zhao, Meng; Ding, Hong; Zhu, Jian-Kang New Phytologist, Vol. 190, Issue 4 https://doi.org/10.1111/j.1469-8137.2011.03647.x	journal	February 2011
Mechanisms and function of substrate recruitment by F-box proteins Skaar, Jeffrey R.; Pagan, Julia K.; Pagano, Michele Nature Reviews Molecular Cell Biology, Vol. 14, Issue 6 https://doi.org/10.1038/nrm3582	journal	May 2013
Nitrate transporters and peptide transporters Tsay, Yi-Fang; Chiu, Chi-Chou; Tsai, Chyn-Bey FEBS Letters, Vol. 581, Issue 12 https://doi.org/10.1016/j.febslet.2007.04.047	journal	April 2007
Understanding plant response to nitrogen limitation for the improvement of crop nitrogen use efficiency Kant, S.; Bi, Y. -M.; Rothstein, S. J. Journal of Experimental Botany, Vol. 62, Issue 4 https://doi.org/10.1093/jxb/erq297	journal	October 2010
Adaptation of Arabidopsis to nitrogen limitation involves induction of anthocyanin synthesis which is controlled by the NLA gene Peng, M.; Hudson, D.; Schofield, A. Journal of Experimental Botany, Vol. 59, Issue 11 https://doi.org/10.1093/jxb/ern148	journal	June 2008
The SCF Ubiquitin Ligase Jackson, Peter K.; Eldridge, Adam G. Molecular Cell, Vol. 9, Issue 5 https://doi.org/10.1016/S1097-2765(02)00538-5	journal	May 2002
Gene expression, localization, and protein–protein interaction of Arabidopsis SKP1-like (ASK) 20A and 20B Ogura, Yasunobu; Ihara, Norihisa; Komatsu, Akihiro Plant Science, Vol. 174, Issue 5 https://doi.org/10.1016/j.plantsci.2008.02.010	journal	May 2008
F-Box Proteins Are Receptors that Recruit Phosphorylated Substrates to the SCF Ubiquitin-Ligase Complex Skowyra, Dorota; Craig, Karen L.; Tyers, Mike Cell, Vol. 91, Issue 2 https://doi.org/10.1016/S0092-8674(00)80403-1	journal	October 1997
Members of the LBD Family of Transcription Factors Repress Anthocyanin Synthesis and Affect Additional Nitrogen Responses in Arabidopsis Rubin, Grit; Tohge, Takayuki; Matsuda, Fumio The Plant Cell, Vol. 21, Issue 11 https://doi.org/10.1105/tpc.109.067041	journal	November 2009
The Arabidopsis NRT1.1 transporter participates in the signaling pathway triggering root colonization of nitrate-rich patches Remans, T.; Nacry, P.; Pervent, M. Proceedings of the National Academy of Sciences, Vol. 103, Issue 50 https://doi.org/10.1073/pnas.0605275103	journal	December 2006
NIH Image to ImageJ: 25 years of image analysis Schneider, Caroline A.; Rasband, Wayne S.; Eliceiri, Kevin W. Nature Methods, Vol. 9, Issue 7 https://doi.org/10.1038/nmeth.2089	journal	June 2012
Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana Vidal, E. A.; Araus, V.; Lu, C. Proceedings of the National Academy of Sciences, Vol. 107, Issue 9 https://doi.org/10.1073/pnas.0909571107	journal	February 2010
An Agrobacterium tumefaciens transformation protocol effective on a variety of cottonwood hybrids (genus Populus) Han, K.-H.; Meilan, R.; Ma, C. Plant Cell Reports, Vol. 19, Issue 3, p. 315-320 https://doi.org/10.1007/s002990050019	journal	January 2000
A new mathematical model for relative quantification in real-time RT-PCR Pfaffl, M. W. Nucleic Acids Research, Vol. 29, Issue 9 https://doi.org/10.1093/nar/29.9.e45	journal	May 2001
Genetic Regulation by NLA and MicroRNA827 for Maintaining Nitrate-Dependent Phosphate Homeostasis in Arabidopsis Kant, Surya; Peng, Mingsheng; Rothstein, Steven J. PLoS Genetics, Vol. 7, Issue 3 https://doi.org/10.1371/journal.pgen.1002021	journal	March 2011
Flavonoids Act as Negative Regulators of Auxin Transport in Vivo in Arabidopsis Brown, Dana E.; Rashotte, Aaron M.; Murphy, Angus S. Plant Physiology, Vol. 126, Issue 2 https://doi.org/10.1104/pp.126.2.524	journal	June 2001
Nitrogen-use efficiency in maize (Zea mays L.): from 'omics' studies to metabolic modelling Simons, M.; Saha, R.; Guillard, L. Journal of Experimental Botany, Vol. 65, Issue 19 https://doi.org/10.1093/jxb/eru227	journal	May 2014
Systems approaches map regulatory networks downstream of the auxin receptor AFB3 in the nitrate response of Arabidopsis thaliana roots Vidal, E. A.; Moyano, T. C.; Riveras, E. Proceedings of the National Academy of Sciences, Vol. 110, Issue 31 https://doi.org/10.1073/pnas.1310937110	journal	July 2013
Transcriptome response to nitrogen starvation in rice Cai, Hongmei; Lu, Yongen; Xie, Weibo Journal of Biosciences, Vol. 37, Issue 4 https://doi.org/10.1007/s12038-012-9242-2	journal	August 2012
NITROGEN LIMITATION ADAPTATION, a Target of MicroRNA827, Mediates Degradation of Plasma Membrane–Localized Phosphate Transporters to Maintain Phosphate Homeostasis in Arabidopsis Lin, Wei-Yi; Huang, Teng-Kuei; Chiou, Tzyy-Jen The Plant Cell, Vol. 25, Issue 10 https://doi.org/10.1105/tpc.113.116012	journal	October 2013
Learning Bayesian Networks with the bnlearn R Package Scutari, Marco Journal of Statistical Software, Vol. 35, Issue 3 https://doi.org/10.18637/jss.v035.i03	journal	January 2010
ARACNE: An Algorithm for the Reconstruction of Gene Regulatory Networks in a Mammalian Cellular Context Margolin, Adam A.; Nemenman, Ilya; Basso, Katia BMC Bioinformatics, Vol. 7, Issue S1 https://doi.org/10.1186/1471-2105-7-S1-S7	journal	March 2006
A mutation in NLA, which encodes a RING-type ubiquitin ligase, disrupts the adaptability of Arabidopsis to nitrogen limitation: NLA required for adaptability to nitrogen limitation Peng, Mingsheng; Hannam, Carol; Gu, Honglan The Plant Journal, Vol. 50, Issue 2 https://doi.org/10.1111/j.1365-313X.2007.03050.x	journal	March 2007
MicroRNA Regulation of NAC-Domain Targets Is Required for Proper Formation and Separation of Adjacent Embryonic, Vegetative, and Floral Organs Mallory, Allison C.; Dugas, Diana V.; Bartel, David P. Current Biology, Vol. 14, Issue 12 https://doi.org/10.1016/j.cub.2004.06.022	journal	June 2004
Uptake, allocation and signaling of nitrate Wang, Ya-Yun; Hsu, Po-Kai; Tsay, Yi-Fang Trends in Plant Science, Vol. 17, Issue 8 https://doi.org/10.1016/j.tplants.2012.04.006	journal	August 2012
Cloning and Characterization of Maize miRNAs Involved in Responses to Nitrogen Deficiency Zhao, Meng; Tai, Huanhuan; Sun, Suzhen PLoS ONE, Vol. 7, Issue 1 https://doi.org/10.1371/journal.pone.0029669	journal	January 2012
Lateral root development in Arabidopsis: fifty shades of auxin Lavenus, Julien; Goh, Tatsuaki; Roberts, Ianto Trends in Plant Science, Vol. 18, Issue 8 https://doi.org/10.1016/j.tplants.2013.04.006	journal	August 2013
Gene Expression Biomarkers Provide Sensitive Indicators of in Planta Nitrogen Status in Maize Yang, Xiaofeng S.; Wu, Jingrui; Ziegler, Todd E. Plant Physiology, Vol. 157, Issue 4 https://doi.org/10.1104/pp.111.187898	journal	October 2011
Nitrogen deprivation promotes Populus root growth through global transcriptome reprogramming and activation of hierarchical genetic networks Wei, Hairong; Yordanov, Yordan S.; Georgieva, Tatyana New Phytologist, Vol. 200, Issue 2 https://doi.org/10.1111/nph.12375	journal	June 2013
Plant Nitrogen Assimilation and Use Efficiency Xu, Guohua; Fan, Xiaorong; Miller, Anthony J. Annual Review of Plant Biology, Vol. 63, Issue 1 https://doi.org/10.1146/annurev-arplant-042811-105532	journal	June 2012
The Arabidopsis AP2/ERF Transcription Factor RAP2.11 Modulates Plant Response to Low-Potassium Conditions Kim, Min Jung; Ruzicka, Daniel; Shin, Ryoung Molecular Plant, Vol. 5, Issue 5 https://doi.org/10.1093/mp/sss003	journal	September 2012
Nitrogen use efficiency of rice reconsidered: What are the key constraints? Cassman, K. G.; Kropff, M. J.; Gaunt, J. Plant and Soil, Vol. 155-156, Issue 1 https://doi.org/10.1007/BF00025057	journal	October 1993
Flavonoids and auxin transport: modulators or regulators? Peer, Wendy Ann; Murphy, Angus S. Trends in Plant Science, Vol. 12, Issue 12 https://doi.org/10.1016/j.tplants.2007.10.003	journal	December 2007
Members of the LATERAL ORGAN BOUNDARIES DOMAIN Transcription Factor Family Are Involved in the Regulation of Secondary Growth in Populus Yordanov, Yordan S.; Regan, Sharon; Busov, Victor The Plant Cell, Vol. 22, Issue 11 https://doi.org/10.1105/tpc.110.078634	journal	November 2010
Signalling mechanisms underlying the morphological responses of the root system to nitrogen in Arabidopsis thaliana Zhang, H.; Rong, H.; Pilbeam, D. Journal of Experimental Botany, Vol. 58, Issue 9 https://doi.org/10.1093/jxb/erm114	journal	March 2007
Estimation of total phenols and flavonoids in extracts of actaea spicata roots and antioxidant activity studies Madaan, R.; Kumar, S.; Bansal, G. Indian Journal of Pharmaceutical Sciences, Vol. 73, Issue 6 https://doi.org/10.4103/0250-474X.100242	journal	January 2011
Plant hormones and nutrient signaling Rubio, Vicente; Bustos, Regla; Irigoyen, María Luisa Plant Molecular Biology, Vol. 69, Issue 4 https://doi.org/10.1007/s11103-008-9380-y	journal	August 2008
Genome-Wide Identification of MicroRNAs in Response to Low Nitrate Availability in Maize Leaves and Roots Xu, Zhenhua; Zhong, Sihui; Li, Xinhai PLoS ONE, Vol. 6, Issue 11 https://doi.org/10.1371/journal.pone.0028009	journal	November 2011
An Arabidopsis MADS Box Gene That Controls Nutrient-Induced Changes in Root Architecture Zhang, H. Science, Vol. 279, Issue 5349 https://doi.org/10.1126/science.279.5349.407	journal	January 1998
Systems analysis of transcriptome data provides new hypotheses about Arabidopsis root response to nitrate treatments Canales, Javier; Moyano, Tomás C.; Villarroel, Eva Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00022	journal	January 2014
MicroRNA Directs mRNA Cleavage of the Transcription Factor NAC1 to Downregulate Auxin Signals for Arabidopsis Lateral Root Development Guo, Hui-Shan; Xie, Qi; Fei, Ji-Feng The Plant Cell, Vol. 17, Issue 5 https://doi.org/10.1105/tpc.105.030841	journal	April 2005
Genome-wide characterization of new and drought stress responsive microRNAs in Populus euphratica Li, Bosheng; Qin, Yurong; Duan, Hui Journal of Experimental Botany, Vol. 62, Issue 11 https://doi.org/10.1093/jxb/err051	journal	April 2011
Regulation of Flower Development in Arabidopsis by SCF Complexes Ni, Weimin; Xie, Daoxin; Hobbie, Lawrence Plant Physiology, Vol. 134, Issue 4 https://doi.org/10.1104/pp.103.031971	journal	March 2004
Auxin biosynthetic gene TAR2 is involved in low nitrogen-mediated reprogramming of root architecture in Arabidopsis Ma, Wenying; Li, Jingjuan; Qu, Baoyuan The Plant Journal, Vol. 78, Issue 1 https://doi.org/10.1111/tpj.12448	journal	March 2014

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