Skip to main content
U.S. Department of Energy
Office of Scientific and Technical Information

XYLEM NAC DOMAIN1, an angiosperm NAC transcription factor, inhibits xylem differentiation through conserved motifs that interact with RETINOBLASTOMA‐RELATED

Journal Article · · New Phytologist
DOI:https://doi.org/10.1111/nph.14704· OSTI ID:1778596
 [1];  [2];  [2];  [1];  [1];  [1];  [1];  [3];  [4];  [5];  [1]
  1. Department of Horticulture Virginia Tech Blacksburg VA 24061 USA
  2. Department of Plant Physiology Umeå Plant Science Center Umeå University S‐901 87 Umeå Sweden
  3. Molecular and Developmental Complexity Group Unidad de Genómica Avanzada CINVESTAV Irapuato Guanajuato 36821 México
  4. Plant Developmental Biology Wageningen University &, Research 6708PB Wageningen the Netherlands
  5. Department of Forest Resources and Environmental Conservation Virginia Tech Blacksburg VA 24061 USA
Summary

The Arabidopsis thaliana gene XYLEM NAC DOMAIN1 ( XND1 ) is upregulated in xylem tracheary elements. Yet overexpression of XND1 blocks differentiation of tracheary elements. The molecular mechanism of XND1 action was investigated.

Phylogenetic and motif analyses indicated that XND1 and its homologs are present only in angiosperms and possess a highly conserved C‐terminal region containing linear motifs (CKII‐acidic, LXCXE, E2F TD ‐like and LXCXE‐mimic) predicted to interact with the cell cycle and differentiation regulator RETINOBLASTOMA‐RELATED (RBR). Protein–protein interaction and functional analyses of XND1 deletion mutants were used to test the importance of RBR‐interaction motifs.

Deletion of either the LXCXE or the LXCXE‐mimic motif reduced both the XND1–RBR interaction and XND1 efficacy as a repressor of differentiation, with loss of the LXCXE motif having the strongest negative impacts. The function of the XND1 C‐terminal domain could be partially replaced by RBR fused to the N‐terminal domain of XND1. XND1 also transactivated gene expression in yeast and plants.

The properties of XND1, a transactivator that depends on multiple linear RBR‐interaction motifs to inhibit differentiation, have not previously been described for a plant protein. XND1 harbors an apparently angiosperm‐specific combination of interaction motifs potentially linking the general differentiation regulator RBR with a xylem‐specific pathway for inhibition of differentiation.

Sponsoring Organization:
USDOE
Grant/Contract Number:
FG02-07ER64449
OSTI ID:
1778596
Alternate ID(s):
OSTI ID: 1541609
Journal Information:
New Phytologist, Journal Name: New Phytologist Journal Issue: 1 Vol. 216; ISSN 0028-646X
Publisher:
Wiley-BlackwellCopyright Statement
Country of Publication:
United Kingdom
Language:
English

References (60)

Identification and analysis of a retinoblastoma binding motif in the replication protein of a plant DNA virus: requirement for efficient viral DNA replication. journal August 1995
The human papillomavirus type 16 E7 gene product interacts with and trans-activates the AP1 family of transcription factors. journal April 1996
The Two Nonstructural Proteins from Wheat Dwarf Virus Involved in Viral Gene Expression and Replication Are Retinoblastoma-Binding Proteins journal May 1996
Bean Yellow Dwarf Virus RepA, but Not Rep, Binds to Maize Retinoblastoma Protein, and the Virus Tolerates Mutations in the Consensus Binding Motif journal April 1999
Characterization of NAC domain transcription factors implicated in control of vascular cell differentiation in Arabidopsis and Populus journal May 2010
The human papillomavirus type 16 E7 gene encodes transactivation and transformation functions similar to those of adenovirus E1A journal May 1988
The RETINOBLASTOMA-RELATED Gene Regulates Stem Cell Maintenance in Arabidopsis Roots journal December 2005
A Bistable Circuit Involving SCARECROW-RETINOBLASTOMA Integrates Cues to Inform Asymmetric Stem Cell Division journal August 2012
Programmed Cell Death Controlled by ANAC033/SOMBRERO Determines Root Cap Organ Size in Arabidopsis journal May 2014
Convergent evolution and mimicry of protein linear motifs in host–pathogen interactions journal June 2015
The maize retinoblastoma protein homologue ZmRb-1 is regulated during leaf development and displays conserved interactions with G1/S regulators and plant cyclin D (CycD) proteins journal May 1998
Arabidopsis E2F1 binds a sequence present in the promoter of S-phase-regulated gene AtCDC6 and is a member of a multigene family with differential activities journal January 2001
Structure of the retinoblastoma tumour-suppressor pocket domain bound to a peptide from HPV E7 journal February 1998
Arabidopsis E2FA stimulates proliferation and endocycle separately through RBR-bound and RBR-free complexes : Dual role for E2FA in proliferation and growth journal February 2012
The Norway spruce genome sequence and conifer genome evolution journal May 2013
An Arabidopsis gene regulatory network for secondary cell wall synthesis journal December 2014
Resolution of deep angiosperm phylogeny using conserved nuclear genes and estimates of early divergence times journal September 2014
Phylotranscriptomic analysis of the origin and early diversification of land plants journal October 2014
Adenovirus E1A, simian virus 40 tumor antigen, and human papillomavirus E7 protein share the capacity to disrupt the interaction between transcription factor E2F and the retinoblastoma gene product. journal May 1992
A potent transrepression domain in the retinoblastoma protein induces a cell cycle arrest when bound to E2F sites. journal December 1995
A maize cDNA encoding a member of the retinoblastoma protein family: involvement in endoreduplication. journal August 1996
The E2F Family of Transcription Factors from Arabidopsis thaliana : NOVEL AND CONSERVED COMPONENTS OF THE RETINOBLASTOMA/E2F PATHWAY IN PLANTS journal January 2002
Comprehensive Analysis of NAC Family Genes in Oryza sativa and Arabidopsis thaliana journal January 2003
CYCD3 D-type cyclins regulate cambial cell proliferation and secondary growth in Arabidopsis journal May 2015
MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0 journal October 2013
Global Analysis of Direct Targets of Secondary Wall NAC Master Switches in Arabidopsis journal November 2010
The CtBP binding domain in the adenovirus E1A protein controls CR1- dependent transactivation journal July 1996
Structural basis for the recognition of the E2F transactivation domain by the retinoblastoma tumor suppressor journal December 2002
Transcription switches for protoxylem and metaxylem vessel formation journal August 2005
Structure of the retinoblastoma protein bound to adenovirus E1A reveals the molecular basis for viral oncoprotein inactivation of a tumor suppressor journal November 2007
Structural mechanisms of DREAM complex assembly and regulation journal April 2015
Cell Type-Specific Role of the Retinoblastoma/E2F Pathway during Arabidopsis Leaf Development journal December 2005
Functional Characterization of Poplar Wood-Associated NAC Domain Transcription Factors journal December 2009
Phosphorylation of Retinoblastoma-Related Protein by the Cyclin D/Cyclin-Dependent Kinase Complex Is Activated at the G1/S-Phase Transition in Tobacco journal July 2002
Altered Cell Cycle Distribution, Hyperplasia, and Inhibited Differentiation in Arabidopsis Caused by the D-Type Cyclin CYCD3 journal December 2002
Arabidopsis E2Fc Functions in Cell Division and Is Degraded by the Ubiquitin-SCF AtSKP2 Pathway in Response to Light journal November 2002
The NAC Transcription Factors NST1 and NST2 of Arabidopsis Regulate Secondary Wall Thickenings and Are Required for Anther Dehiscence journal October 2005
The D-Type Cyclin CYCD3;1 Is Limiting for the G1-to-S-Phase Transition in Arabidopsis journal March 2006
VND-INTERACTING2, a NAC Domain Transcription Factor, Negatively Regulates Xylem Vessel Formation in Arabidopsis journal April 2010
SOMBRERO, BEARSKIN1, and BEARSKIN2 Regulate Root Cap Maturation in Arabidopsis journal March 2010
Arabidopsis RETINOBLASTOMA-RELATED Is Required for Stem Cell Maintenance, Cell Differentiation, and Lateral Organ Production journal June 2010
A conserved family of WD-40 proteins binds to the retinoblastoma protein in both plants and animals. journal September 1997
The Medicago CDKC;1-CYCLINT;1 kinase complex phosphorylates the carboxy-terminal domain of RNA polymerase II and promotes transcription: Analysis of the Medicago CDKC;1-CYCLINT;1 complex journal May 2005
Ethylene-induced stomatal closure in Arabidopsis occurs via AtrbohF-mediated hydrogen peroxide synthesis journal September 2006
XND1, a member of the NAC domain family in Arabidopsis thaliana, negatively regulates lignocellulose synthesis and programmed cell death in xylem: XND1 blocks tracheary element differentiation journal October 2007
VASCULAR-RELATED NAC-DOMAIN7 is involved in the differentiation of all types of xylem vessels in Arabidopsis roots and shoots journal August 2008
A NAC domain protein family contributing to the regulation of wood formation in poplar: NAC domain protein family regulates wood formation journal June 2011
The EDLL motif: a potent plant transcriptional activation domain from AP2/ERF transcription factors: Strong plant transcriptional activation domain journal March 2012
Phylogenetic Analyses Unravel the Evolutionary History of nac Proteins in Plants: Evolutionary History of nac Proteins in Plants journal February 2012
The Amborella Genome and the Evolution of Flowering Plants journal December 2013
Contribution of NAC Transcription Factors to Plant Adaptation to Land journal March 2014
The Nanovirus-Encoded Clink Protein Affects Plant Cell Cycle Regulation through Interaction with the Retinoblastoma-Related Protein journal January 2007
Analysis of trans activation by human papillomavirus type 16 E7 and adenovirus 12S E1A suggests a common mechanism. journal January 1991
Three Regions of the pRB Pocket Domain Affect Its Inactivation by Human Papillomavirus E7 Proteins journal June 2002
The J Domain of Simian Virus 40 Large T Antigen Is Required To Functionally Inactivate RB Family Proteins journal March 1998
Decoding the massive genome of loblolly pine using haploid DNA and novel assembly strategies journal January 2014
Retinoblastoma and Its Binding Partner MSI1 Control Imprinting in Arabidopsis journal August 2008
Comparative Genomics of NAC Transcriptional Factors in Angiosperms: Implications for the Adaptation and Diversification of Flowering Plants journal November 2015
NAC-MYB-based transcriptional regulation of secondary cell wall biosynthesis in land plants journal May 2015
Irreversible fate commitment in the Arabidopsis stomatal lineage requires a FAMA and RETINOBLASTOMA-RELATED module journal October 2014

Similar Records

XND1 Regulates Secondary Wall Deposition in Xylem Vessels through the Inhibition of VND Functions
Journal Article · Mon Nov 02 23:00:00 EST 2020 · Plant and Cell Physiology · OSTI ID:1849430

XND1, a member of the NAC domain family in Arabidopsis thaliana, negatively regulates lignocellulose synthesis and programmed cell death in xylem
Journal Article · Tue Oct 23 00:00:00 EDT 2007 · The Protein Journal · OSTI ID:946687

Structures of inactive retinoblastoma protein reveal multiple mechanisms for cell cycle control
Journal Article · Wed Jul 18 00:00:00 EDT 2012 · Genes and Development · OSTI ID:1045688

Related Subjects