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

Abstract

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 tomore » 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.« less

Authors:
 [1];  [2];  [1];  [1];  [1];  [1]
  1. Forest Resources and Environmental Science Michigan Technological University Houghton MI 49931 USA
  2. Department of Biological Sciences Eastern Illinois University Charleston IL 61920 USA
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1401156
Resource Type:
Publisher's Accepted Manuscript
Journal Name:
The Plant Journal
Additional Journal Information:
Journal Name: The Plant Journal Journal Volume: 84 Journal Issue: 2; Journal ID: ISSN 0960-7412
Publisher:
Wiley-Blackwell
Country of Publication:
United Kingdom
Language:
English

Citation Formats

Dash, Madhumita, Yordanov, Yordan S., Georgieva, Tatyana, Kumari, Sapna, Wei, Hairong, and Busov, Victor. A systems biology approach identifies new regulators of poplar root development under low nitrogen. United Kingdom: N. p., 2015. Web. doi:10.1111/tpj.13002.
Dash, Madhumita, Yordanov, Yordan S., Georgieva, Tatyana, Kumari, Sapna, Wei, Hairong, & Busov, Victor. A systems biology approach identifies new regulators of poplar root development under low nitrogen. United Kingdom. https://doi.org/10.1111/tpj.13002
Dash, Madhumita, Yordanov, Yordan S., Georgieva, Tatyana, Kumari, Sapna, Wei, Hairong, and Busov, Victor. Thu . "A systems biology approach identifies new regulators of poplar root development under low nitrogen". United Kingdom. https://doi.org/10.1111/tpj.13002.
@article{osti_1401156,
title = {A systems biology approach identifies new regulators of poplar root development under low nitrogen},
author = {Dash, Madhumita and Yordanov, Yordan S. and Georgieva, Tatyana and Kumari, Sapna and Wei, Hairong and Busov, Victor},
abstractNote = {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.},
doi = {10.1111/tpj.13002},
journal = {The Plant Journal},
number = 2,
volume = 84,
place = {United Kingdom},
year = {Thu Oct 08 00:00:00 EDT 2015},
month = {Thu Oct 08 00:00:00 EDT 2015}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1111/tpj.13002

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Cited by: 21 works
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Works referenced in this record:

A DNA Transformation–Competent Arabidopsis Genomic Library in Agrobacterium
journal, October 1991

  • Lazo, Gerard R.; Stein, Pascal A.; Ludwig, Robert A.
  • Bio/Technology, Vol. 9, Issue 10
  • DOI: 10.1038/nbt1091-963

Manipulation of microRNA expression to improve nitrogen use efficiency
journal, September 2013


The nodule inception-like protein 7 modulates nitrate sensing and metabolism in Arabidopsis
journal, February 2009


Activation Tagging of a Dominant Gibberellin Catabolism Gene ( GA 2-oxidase ) from Poplar That Regulates Tree Stature
journal, June 2003

  • Busov, Victor B.; Meilan, Richard; Pearce, David W.
  • Plant Physiology, Vol. 132, Issue 3
  • DOI: 10.1104/pp.103.020354

Nutritional regulation of ANR1 and other root-expressed MADS-box genes in Arabidopsis thaliana
journal, July 2005


Expression and Interaction Analysis of Arabidopsis Skp1-Related Genes
journal, January 2004

  • Takahashi, Naoki; Kuroda, Hirofumi; Kuromori, Takashi
  • Plant and Cell Physiology, Vol. 45, Issue 1
  • DOI: 10.1093/pcp/pch009

HAWAIIAN SKIRT : An F-Box Gene That Regulates Organ Fusion and Growth in Arabidopsis
journal, May 2007

  • González-Carranza, Zinnia H.; Rompa, Unchalee; Peters, Janny L.
  • Plant Physiology, Vol. 144, Issue 3
  • DOI: 10.1104/pp.106.092288

Functions of microRNAs in plant stress responses
journal, April 2012


Flavonoids as antioxidants in plants: Location and functional significance
journal, November 2012


Systems approach identifies TGA1 and TGA4 transcription factors as important regulatory components of the nitrate response of Arabidopsis thaliana roots
journal, August 2014

  • Alvarez, José M.; Riveras, Eleodoro; Vidal, Elena A.
  • The Plant Journal, Vol. 80, Issue 1
  • DOI: 10.1111/tpj.12618

GATEWAY™ vectors for Agrobacterium-mediated plant transformation
journal, May 2002


Involvement of miR169 in the nitrogen-starvation responses in Arabidopsis
journal, February 2011


Mechanisms and function of substrate recruitment by F-box proteins
journal, May 2013

  • Skaar, Jeffrey R.; Pagan, Julia K.; Pagano, Michele
  • Nature Reviews Molecular Cell Biology, Vol. 14, Issue 6
  • DOI: 10.1038/nrm3582

Nitrate transporters and peptide transporters
journal, April 2007


Understanding plant response to nitrogen limitation for the improvement of crop nitrogen use efficiency
journal, October 2010

  • Kant, S.; Bi, Y. -M.; Rothstein, S. J.
  • Journal of Experimental Botany, Vol. 62, Issue 4
  • DOI: 10.1093/jxb/erq297

Adaptation of Arabidopsis to nitrogen limitation involves induction of anthocyanin synthesis which is controlled by the NLA gene
journal, June 2008

  • Peng, M.; Hudson, D.; Schofield, A.
  • Journal of Experimental Botany, Vol. 59, Issue 11
  • DOI: 10.1093/jxb/ern148

The SCF Ubiquitin Ligase
journal, May 2002


Gene expression, localization, and protein–protein interaction of Arabidopsis SKP1-like (ASK) 20A and 20B
journal, May 2008


F-Box Proteins Are Receptors that Recruit Phosphorylated Substrates to the SCF Ubiquitin-Ligase Complex
journal, October 1997


Members of the LBD Family of Transcription Factors Repress Anthocyanin Synthesis and Affect Additional Nitrogen Responses in Arabidopsis
journal, November 2009


The Arabidopsis NRT1.1 transporter participates in the signaling pathway triggering root colonization of nitrate-rich patches
journal, December 2006

  • Remans, T.; Nacry, P.; Pervent, M.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 50
  • DOI: 10.1073/pnas.0605275103

NIH Image to ImageJ: 25 years of image analysis
journal, June 2012

  • Schneider, Caroline A.; Rasband, Wayne S.; Eliceiri, Kevin W.
  • Nature Methods, Vol. 9, Issue 7
  • DOI: 10.1038/nmeth.2089

Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana
journal, February 2010

  • Vidal, E. A.; Araus, V.; Lu, C.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 9
  • DOI: 10.1073/pnas.0909571107

An Agrobacterium tumefaciens transformation protocol effective on a variety of cottonwood hybrids (genus Populus)
journal, January 2000

  • Han, K.-H.; Meilan, R.; Ma, C.
  • Plant Cell Reports, Vol. 19, Issue 3, p. 315-320
  • DOI: 10.1007/s002990050019

A new mathematical model for relative quantification in real-time RT-PCR
journal, May 2001


Genetic Regulation by NLA and MicroRNA827 for Maintaining Nitrate-Dependent Phosphate Homeostasis in Arabidopsis
journal, March 2011


Flavonoids Act as Negative Regulators of Auxin Transport in Vivo in Arabidopsis
journal, June 2001

  • Brown, Dana E.; Rashotte, Aaron M.; Murphy, Angus S.
  • Plant Physiology, Vol. 126, Issue 2
  • DOI: 10.1104/pp.126.2.524

Nitrogen-use efficiency in maize (Zea mays L.): from 'omics' studies to metabolic modelling
journal, May 2014

  • Simons, M.; Saha, R.; Guillard, L.
  • Journal of Experimental Botany, Vol. 65, Issue 19
  • DOI: 10.1093/jxb/eru227

Systems approaches map regulatory networks downstream of the auxin receptor AFB3 in the nitrate response of Arabidopsis thaliana roots
journal, July 2013

  • Vidal, E. A.; Moyano, T. C.; Riveras, E.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 31
  • DOI: 10.1073/pnas.1310937110

Transcriptome response to nitrogen starvation in rice
journal, August 2012


Learning Bayesian Networks with the bnlearn R Package
journal, January 2010


ARACNE: An Algorithm for the Reconstruction of Gene Regulatory Networks in a Mammalian Cellular Context
journal, March 2006


MicroRNA Regulation of NAC-Domain Targets Is Required for Proper Formation and Separation of Adjacent Embryonic, Vegetative, and Floral Organs
journal, June 2004


Uptake, allocation and signaling of nitrate
journal, August 2012


Cloning and Characterization of Maize miRNAs Involved in Responses to Nitrogen Deficiency
journal, January 2012


Lateral root development in Arabidopsis: fifty shades of auxin
journal, August 2013


Gene Expression Biomarkers Provide Sensitive Indicators of in Planta Nitrogen Status in Maize
journal, October 2011

  • Yang, Xiaofeng S.; Wu, Jingrui; Ziegler, Todd E.
  • Plant Physiology, Vol. 157, Issue 4
  • DOI: 10.1104/pp.111.187898

Nitrogen deprivation promotes Populus root growth through global transcriptome reprogramming and activation of hierarchical genetic networks
journal, June 2013

  • Wei, Hairong; Yordanov, Yordan S.; Georgieva, Tatyana
  • New Phytologist, Vol. 200, Issue 2
  • DOI: 10.1111/nph.12375

Plant Nitrogen Assimilation and Use Efficiency
journal, June 2012


The Arabidopsis AP2/ERF Transcription Factor RAP2.11 Modulates Plant Response to Low-Potassium Conditions
journal, September 2012

  • Kim, Min Jung; Ruzicka, Daniel; Shin, Ryoung
  • Molecular Plant, Vol. 5, Issue 5
  • DOI: 10.1093/mp/sss003

Nitrogen use efficiency of rice reconsidered: What are the key constraints?
journal, October 1993

  • Cassman, K. G.; Kropff, M. J.; Gaunt, J.
  • Plant and Soil, Vol. 155-156, Issue 1
  • DOI: 10.1007/BF00025057

Flavonoids and auxin transport: modulators or regulators?
journal, December 2007


Members of the LATERAL ORGAN BOUNDARIES DOMAIN Transcription Factor Family Are Involved in the Regulation of Secondary Growth in Populus
journal, November 2010

  • Yordanov, Yordan S.; Regan, Sharon; Busov, Victor
  • The Plant Cell, Vol. 22, Issue 11
  • DOI: 10.1105/tpc.110.078634

Signalling mechanisms underlying the morphological responses of the root system to nitrogen in Arabidopsis thaliana
journal, March 2007

  • Zhang, H.; Rong, H.; Pilbeam, D.
  • Journal of Experimental Botany, Vol. 58, Issue 9
  • DOI: 10.1093/jxb/erm114

Estimation of total phenols and flavonoids in extracts of actaea spicata roots and antioxidant activity studies
journal, January 2011

  • Madaan, R.; Kumar, S.; Bansal, G.
  • Indian Journal of Pharmaceutical Sciences, Vol. 73, Issue 6
  • DOI: 10.4103/0250-474X.100242

Plant hormones and nutrient signaling
journal, August 2008

  • Rubio, Vicente; Bustos, Regla; Irigoyen, María Luisa
  • Plant Molecular Biology, Vol. 69, Issue 4
  • DOI: 10.1007/s11103-008-9380-y

Genome-Wide Identification of MicroRNAs in Response to Low Nitrate Availability in Maize Leaves and Roots
journal, November 2011


Systems analysis of transcriptome data provides new hypotheses about Arabidopsis root response to nitrate treatments
journal, January 2014

  • Canales, Javier; Moyano, Tomás C.; Villarroel, Eva
  • Frontiers in Plant Science, Vol. 5
  • DOI: 10.3389/fpls.2014.00022

Genome-wide characterization of new and drought stress responsive microRNAs in Populus euphratica
journal, April 2011

  • Li, Bosheng; Qin, Yurong; Duan, Hui
  • Journal of Experimental Botany, Vol. 62, Issue 11
  • DOI: 10.1093/jxb/err051

Regulation of Flower Development in Arabidopsis by SCF Complexes
journal, March 2004

  • Ni, Weimin; Xie, Daoxin; Hobbie, Lawrence
  • Plant Physiology, Vol. 134, Issue 4
  • DOI: 10.1104/pp.103.031971

Auxin biosynthetic gene TAR2 is involved in low nitrogen-mediated reprogramming of root architecture in Arabidopsis
journal, March 2014

  • Ma, Wenying; Li, Jingjuan; Qu, Baoyuan
  • The Plant Journal, Vol. 78, Issue 1
  • DOI: 10.1111/tpj.12448