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Title: The uncharacterized gene EVE contributes to vessel element dimensions in Populus

Abstract

The radiation of angiosperms led to the emergence of the vast majority of today’s plant species and all our major food crops. Their extraordinary diversification occurred in conjunction with the evolution of a more efficient vascular system for the transport of water, composed of vessel elements. The physical dimensions of these water-conducting specialized cells have played a critical role in angiosperm evolution; they determine resistance to water flow, influence photosynthesis rate, and contribute to plant stature. However, the genetic factors that determine their dimensions are unclear. Here we show that a previously uncharacterized gene, ENLARGED VESSEL ELEMENT ( EVE ) , contributes to the dimensions of vessel elements in Populus , impacting hydraulic conductivity. Our data suggest that EVE is localized in the plasma membrane and is involved in potassium uptake of differentiating xylem cells during vessel development. In plants, EVE first emerged in streptophyte algae, but expanded dramatically among vessel-containing angiosperms. The phylogeny, structure and composition of EVE indicates that it may have been involved in an ancient horizontal gene-transfer event.

Authors:
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Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1598905
Grant/Contract Number:  
SC0003893
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Name: Proceedings of the National Academy of Sciences of the United States of America; Journal ID: ISSN 0027-8424
Publisher:
Proceedings of the National Academy of Sciences
Country of Publication:
United States
Language:
English

Citation Formats

Ribeiro, Cíntia L., Conde, Daniel, Balmant, Kelly M., Dervinis, Christopher, Johnson, Matthew G., McGrath, Aaron P., Szewczyk, Paul, Unda, Faride, Finegan, Christina A., Schmidt, Henry W., Miles, Brianna, Drost, Derek R., Novaes, Evandro, Gonzalez-Benecke, Carlos A., Peter, Gary F., Burleigh, J. Gordon, Martin, Timothy A., Mansfield, Shawn D., Chang, Geoffrey, Wickett, Norman J., and Kirst, Matias. The uncharacterized gene EVE contributes to vessel element dimensions in Populus. United States: N. p., 2020. Web. doi:10.1073/pnas.1912434117.
Ribeiro, Cíntia L., Conde, Daniel, Balmant, Kelly M., Dervinis, Christopher, Johnson, Matthew G., McGrath, Aaron P., Szewczyk, Paul, Unda, Faride, Finegan, Christina A., Schmidt, Henry W., Miles, Brianna, Drost, Derek R., Novaes, Evandro, Gonzalez-Benecke, Carlos A., Peter, Gary F., Burleigh, J. Gordon, Martin, Timothy A., Mansfield, Shawn D., Chang, Geoffrey, Wickett, Norman J., & Kirst, Matias. The uncharacterized gene EVE contributes to vessel element dimensions in Populus. United States. doi:10.1073/pnas.1912434117.
Ribeiro, Cíntia L., Conde, Daniel, Balmant, Kelly M., Dervinis, Christopher, Johnson, Matthew G., McGrath, Aaron P., Szewczyk, Paul, Unda, Faride, Finegan, Christina A., Schmidt, Henry W., Miles, Brianna, Drost, Derek R., Novaes, Evandro, Gonzalez-Benecke, Carlos A., Peter, Gary F., Burleigh, J. Gordon, Martin, Timothy A., Mansfield, Shawn D., Chang, Geoffrey, Wickett, Norman J., and Kirst, Matias. Mon . "The uncharacterized gene EVE contributes to vessel element dimensions in Populus". United States. doi:10.1073/pnas.1912434117.
@article{osti_1598905,
title = {The uncharacterized gene EVE contributes to vessel element dimensions in Populus},
author = {Ribeiro, Cíntia L. and Conde, Daniel and Balmant, Kelly M. and Dervinis, Christopher and Johnson, Matthew G. and McGrath, Aaron P. and Szewczyk, Paul and Unda, Faride and Finegan, Christina A. and Schmidt, Henry W. and Miles, Brianna and Drost, Derek R. and Novaes, Evandro and Gonzalez-Benecke, Carlos A. and Peter, Gary F. and Burleigh, J. Gordon and Martin, Timothy A. and Mansfield, Shawn D. and Chang, Geoffrey and Wickett, Norman J. and Kirst, Matias},
abstractNote = {The radiation of angiosperms led to the emergence of the vast majority of today’s plant species and all our major food crops. Their extraordinary diversification occurred in conjunction with the evolution of a more efficient vascular system for the transport of water, composed of vessel elements. The physical dimensions of these water-conducting specialized cells have played a critical role in angiosperm evolution; they determine resistance to water flow, influence photosynthesis rate, and contribute to plant stature. However, the genetic factors that determine their dimensions are unclear. Here we show that a previously uncharacterized gene, ENLARGED VESSEL ELEMENT ( EVE ) , contributes to the dimensions of vessel elements in Populus , impacting hydraulic conductivity. Our data suggest that EVE is localized in the plasma membrane and is involved in potassium uptake of differentiating xylem cells during vessel development. In plants, EVE first emerged in streptophyte algae, but expanded dramatically among vessel-containing angiosperms. The phylogeny, structure and composition of EVE indicates that it may have been involved in an ancient horizontal gene-transfer event.},
doi = {10.1073/pnas.1912434117},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = ,
volume = ,
place = {United States},
year = {2020},
month = {2}
}

Journal Article:
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DOI: 10.1073/pnas.1912434117

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Works referenced in this record:

A Glimpse of Nucleo-Cytoplasmic Large DNA Virus Biodiversity through the Eukaryotic Genomics Window
journal, January 2017

  • Gallot-Lavallée, Lucie; Blanc, Guillaume
  • Viruses, Vol. 9, Issue 1
  • DOI: 10.3390/v9010017

The Chlorella variabilis NC64A Genome Reveals Adaptation to Photosymbiosis, Coevolution with Viruses, and Cryptic Sex
journal, September 2010

  • Blanc, Guillaume; Duncan, Garry; Agarkova, Irina
  • The Plant Cell, Vol. 22, Issue 9
  • DOI: 10.1105/tpc.110.076406

Optimizing the statistical estimation of the parameters of the Farquhar–von Caemmerer–Berry model of photosynthesis
journal, October 2007


A Golden Gate Modular Cloning Toolbox for Plants
journal, February 2014

  • Engler, Carola; Youles, Mark; Gruetzner, Ramona
  • ACS Synthetic Biology, Vol. 3, Issue 11
  • DOI: 10.1021/sb4001504

Phylotranscriptomic analysis of the origin and early diversification of land plants
journal, October 2014

  • Wickett, Norman J.; Mirarab, Siavash; Nguyen, Nam
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 45
  • DOI: 10.1073/pnas.1323926111

Secondary wall NAC binding element (SNBE), a key cis-acting element required for target gene activation by secondary wall NAC master switches
journal, September 2011

  • McCarthy, Ryan L.; Zhong, Ruiqin; Ye, Zheng-Hua
  • Plant Signaling & Behavior, Vol. 6, Issue 9
  • DOI: 10.4161/psb.6.9.16402

High-throughput CRISPR Vector Construction and Characterization of DNA Modifications by Generation of Tomato Hairy Roots
journal, January 2016

  • Jacobs, Thomas B.; Martin, Gregory B.
  • Journal of Visualized Experiments, Issue 110
  • DOI: 10.3791/53843

Evolutionary genomics of nucleo-cytoplasmic large DNA viruses
journal, April 2006


Hydraulic conductivity traits predict growth rates and adult stature of 40 Asian tropical tree species better than wood density
journal, January 2012


Stem hydraulic supply is linked to leaf photosynthetic capacity: evidence from New Caledonian and Tasmanian rainforests
journal, December 2000


Evolution of plant conducting cells: perspectives from key regulators of vascular cell differentiation
journal, December 2016

  • Ohtani, Misato; Akiyoshi, Nobuhiro; Takenaka, Yuto
  • Journal of Experimental Botany, Vol. 68, Issue 1
  • DOI: 10.1093/jxb/erw473

VASCULAR-RELATED NAC-DOMAIN 7 directly regulates the expression of a broad range of genes for xylem vessel formation: Direct target genes of VND7
journal, March 2011


Phycodnaviridae– large DNA algal viruses
journal, August 2002


Lausannevirus, a giant amoebal virus encoding histone doublets: A giant virus encoding histone doublets
journal, March 2011


A Giant Virus in Amoebae
journal, March 2003


The Plant Vascular System: Evolution, Development and Functions F
journal, April 2013

  • Lucas, William J.; Groover, Andrew; Lichtenberger, Raffael
  • Journal of Integrative Plant Biology, Vol. 55, Issue 4
  • DOI: 10.1111/jipb.12041

Functional Characterization of Poplar Wood-Associated NAC Domain Transcription Factors
journal, December 2009

  • Zhong, Ruiqin; Lee, Chanhui; Ye, Zheng-Hua
  • Plant Physiology, Vol. 152, Issue 2
  • DOI: 10.1104/pp.109.148270

A method for measuring hydraulic conductivity and embolism in xylem
journal, January 1988


Poplar potassium transporters capable of controlling K+ homeostasis and K+-dependent xylogenesis
journal, December 2002


Wood formation of trees in relation to potassium and calcium nutrition
journal, May 2010


Real-time monitoring of PtaHMGB activity in poplar transactivation assays
journal, June 2017

  • Ramos-Sánchez, José M.; Triozzi, Paolo M.; Moreno-Cortés, Alicia
  • Plant Methods, Vol. 13, Issue 1
  • DOI: 10.1186/s13007-017-0199-x

SigHunt: horizontal gene transfer finder optimized for eukaryotic genomes
journal, December 2013


Quantitative genetic analysis of biomass and wood chemistry of Populus under different nitrogen levels
journal, March 2009


Comparative interrogation of the developing xylem transcriptomes of two wood-forming species: Populus trichocarpa and Eucalyptus grandis
journal, February 2015

  • Hefer, Charles A.; Mizrachi, Eshchar; Myburg, Alexander A.
  • New Phytologist, Vol. 206, Issue 4
  • DOI: 10.1111/nph.13277

Exploiting SNPs for biallelic CRISPR mutations in the outcrossing woody perennial Populus reveals 4-coumarate:CoA ligase specificity and redundancy
journal, May 2015

  • Zhou, Xiaohong; Jacobs, Thomas B.; Xue, Liang-Jiao
  • New Phytologist, Vol. 208, Issue 2
  • DOI: 10.1111/nph.13470

Variation of xylem vessel diameters across a climate gradient: insight from a reciprocal transplant experiment with a widespread boreal tree
journal, April 2015

  • Schreiber, Stefan G.; Hacke, Uwe G.; Hamann, Andreas
  • Functional Ecology, Vol. 29, Issue 11
  • DOI: 10.1111/1365-2435.12455

Hydraulic constraints limit height growth in trees at high altitude
journal, September 2010


Hydraulic Consequences of Vessel Evolution in Angiosperms
journal, October 2007

  • Sperry, J. S.; Hacke, U. G.; Feild, T. S.
  • International Journal of Plant Sciences, Vol. 168, Issue 8
  • DOI: 10.1086/520726

Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant.
journal, June 1997


Hydraulic and photosynthetic co-ordination in seasonally dry tropical forest trees
journal, November 2002


RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
journal, January 2014


Genome of Acanthamoeba castellanii highlights extensive lateral gene transfer and early evolution of tyrosine kinase signaling
journal, January 2013


Distant Mimivirus relative with a larger genome highlights the fundamental features of Megaviridae
journal, October 2011

  • Arslan, D.; Legendre, M.; Seltzer, V.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 42
  • DOI: 10.1073/pnas.1110889108

Polar-localised poplar K+ channel capable of controlling electrical properties of wood-forming cells
journal, October 2005


AspWood: High-Spatial-Resolution Transcriptome Profiles Reveal Uncharacterized Modularity of Wood Formation in Populus tremula
journal, June 2017

  • Sundell, David; Street, Nathaniel R.; Kumar, Manoj
  • The Plant Cell, Vol. 29, Issue 7
  • DOI: 10.1105/tpc.17.00153

Xylem cell death: emerging understanding of regulation and function
journal, January 2012

  • Bollhoner, B.; Prestele, J.; Tuominen, H.
  • Journal of Experimental Botany, Vol. 63, Issue 3
  • DOI: 10.1093/jxb/err438

Diversification in the genetic architecture of gene expression and transcriptional networks in organ differentiation of Populus
journal, April 2010

  • Drost, D. R.; Benedict, C. I.; Berg, A.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 18, p. 8492-8497
  • DOI: 10.1073/pnas.0914709107

Geographical and environmental gradients shape phenotypic trait variation and genetic structure in Populus trichocarpa
journal, November 2013

  • McKown, Athena D.; Guy, Robert D.; Klápště, Jaroslav
  • New Phytologist, Vol. 201, Issue 4
  • DOI: 10.1111/nph.12601

The hydraulic architecture of trees and other woody plants
journal, November 1991


Vessel diameter-stem diameter scaling across woody angiosperms and the ecological causes of xylem vessel diameter variation
journal, December 2012

  • Olson, Mark E.; Rosell, Julieta A.
  • New Phytologist, Vol. 197, Issue 4
  • DOI: 10.1111/nph.12097

Universal hydraulics of the flowering plants: vessel diameter scales with stem length across angiosperm lineages, habits and climates
journal, May 2014

  • Olson, Mark E.; Anfodillo, Tommaso; Rosell, Julieta A.
  • Ecology Letters, Vol. 17, Issue 8
  • DOI: 10.1111/ele.12302

Amoebae as Genitors and Reservoirs of Giant Viruses
journal, January 2010

  • Raoult, Didier; Boyer, Mickael
  • Intervirology, Vol. 53, Issue 5
  • DOI: 10.1159/000312917

A simple and efficient method for isolating RNA from pine trees
journal, June 1993

  • Chang, Shujun; Puryear, Jeff; Cairney, John
  • Plant Molecular Biology Reporter, Vol. 11, Issue 2
  • DOI: 10.1007/BF02670468

GoldenBraid: An Iterative Cloning System for Standardized Assembly of Reusable Genetic Modules
journal, July 2011

  • Sarrion-Perdigones, Alejandro; Falconi, Erica Elvira; Zandalinas, Sara I.
  • PLoS ONE, Vol. 6, Issue 7, Article No. e21622
  • DOI: 10.1371/journal.pone.0021622

Evolution of development of vascular cambia and secondary growth: Tansley review
journal, April 2010


Trade-offs between xylem hydraulic properties, wood anatomy and yield in Populus
journal, July 2014


Effects of water stress on vessel size and xylem hydraulic conductivity in Vitis vinifera L
journal, April 1998


Global Analysis of Direct Targets of Secondary Wall NAC Master Switches in Arabidopsis
journal, November 2010

  • Zhong, Ruiqin; Lee, Chanhui; Ye, Zheng-Hua
  • Molecular Plant, Vol. 3, Issue 6
  • DOI: 10.1093/mp/ssq062

Root and stem hydraulic conductivity as determinants of growth potential in grafted trees of apple (Malus pumila Mill.)
journal, April 2003

  • Atkinson, C. J.; Else, M. A.; Taylor, L.
  • Journal of Experimental Botany, Vol. 54, Issue 385
  • DOI: 10.1093/jxb/erg132

Expression of a conifer glutamine synthetase gene in transgenic poplar
journal, November 1999

  • Gallardo, Fernando; Fu, Jianming; Cantón, Francisco R.
  • Planta, Vol. 210, Issue 1, p. 19-26
  • DOI: 10.1007/s004250050649

Pan genome of the phytoplankton Emiliania underpins its global distribution
journal, June 2013

  • Read, Betsy A.; Kegel, Jessica; Klute, Mary J.
  • Nature, Vol. 499, Issue 7457
  • DOI: 10.1038/nature12221

Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation
journal, May 2014

  • Hori, Koichi; Maruyama, Fumito; Fujisawa, Takatomo
  • Nature Communications, Vol. 5, Issue 1
  • DOI: 10.1038/ncomms4978

Overall Alteration of Circadian Clock Gene Expression in the Chestnut Cold Response
journal, October 2008


Poplar stems show opposite epigenetic patterns during winter dormancy and vegetative growth
journal, November 2012


Potassium transporters in plants - Involvement in K + acquisition, redistribution and homeostasis
journal, March 2007


Seasonal Profiles of Sulphur, Phosphorus, and Potassium in Norway Spruce Wood
journal, July 2006