The uncharacterized gene EVE contributes to vessel element dimensions in Populus

Cíntia L. Ribeiro; Daniel Conde; Kelly M. Balmant; Christopher Dervinis; Matthew G. Johnson; Aaron P. McGrath; Paul Szewczyk; Faride Unda; Christina A. Finegan; Henry W. Schmidt; Brianna Miles; Derek R. Drost; Evandro Novaes; Carlos A. Gonzalez-Benecke; Gary F. Peter; J. Gordon Burleigh; Timothy A. Martin; Shawn D. Mansfield; Geoffrey Chang; Norman J. Wickett; Matias Kirst

doi:10.1073/pnas.1912434117

The uncharacterized gene EVE contributes to vessel element dimensions in Populus

Cíntia L. Ribeiro, Daniel Conde, Kelly M. Balmant, Christopher Dervinis, Matthew G. Johnson, Aaron P. McGrath, Paul Szewczyk, Faride Unda, Christina A. Finegan, Henry W. Schmidt, Brianna Miles, Derek R. Drost, Evandro Novaes, Carlos A. Gonzalez-Benecke, Gary F. Peter, J. Gordon Burleigh, Timothy A. Martin, Shawn D. Mansfield, Geoffrey Chang, Norman J. WickettMatias Kirst

Biological Sciences

Research output: Contribution to journal › Article › peer-review

8 Scopus citations

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.

Original language	English
Pages (from-to)	5059-5066
Number of pages	8
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	117
Issue number	9
DOIs	https://doi.org/10.1073/pnas.1912434117
State	Published - Mar 3 2020

Keywords

EVE
Phycodnavirus
Vessel
Vessel dimension
Xylem

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10.1073/pnas.1912434117

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Ribeiro, C. L., Conde, D., Balmant, K. M., Dervinis, C., Johnson, M. G., McGrath, A. P., Szewczyk, P., Unda, F., Finegan, C. A., Schmidt, H. W., Miles, B., Drost, D. R., Novaes, E., Gonzalez-Benecke, C. A., Peter, G. F., Gordon Burleigh, J., Martin, T. A., Mansfield, S. D., Chang, G., ... Kirst, M. (2020). The uncharacterized gene EVE contributes to vessel element dimensions in Populus. Proceedings of the National Academy of Sciences of the United States of America, 117(9), 5059-5066. https://doi.org/10.1073/pnas.1912434117

@article{4160fdf3b1b14523acb4c889acdaa94f,

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.",

keywords = "EVE, Phycodnavirus, Vessel, Vessel dimension, Xylem",

author = "Ribeiro, {C{\'i}ntia L.} and Daniel Conde and Balmant, {Kelly M.} and Christopher Dervinis and Johnson, {Matthew G.} and McGrath, {Aaron P.} and Paul Szewczyk and Faride Unda and Finegan, {Christina A.} and Schmidt, {Henry W.} and Brianna Miles and Drost, {Derek R.} and Evandro Novaes and Gonzalez-Benecke, {Carlos A.} and Peter, {Gary F.} and {Gordon Burleigh}, J. and Martin, {Timothy A.} and Mansfield, {Shawn D.} and Geoffrey Chang and Wickett, {Norman J.} and Matias Kirst",

note = "Funding Information: ACKNOWLEDGMENTS. We thank Pieter Bass, Ron Sederoff, Pamela Soltis, and Douglas Soltis for critical reading of the manuscript; and Thomas Wood for the gift of the LB2003 Escherichia coli. This work was supported by the US Department of Agriculture Plant Feedstock Genomics for Bioenergy Program (Grant 2009-65504-05697) and the Department of Energy Office of Science Biological and Environmental Research (Grant DE-SC0003893). Publisher Copyright: {\textcopyright} 2020 National Academy of Sciences. All rights reserved.",

year = "2020",

month = mar,

day = "3",

doi = "10.1073/pnas.1912434117",

language = "English",

volume = "117",

pages = "5059--5066",

journal = "Proceedings of the National Academy of Sciences of the United States of America",

issn = "0027-8424",

publisher = "Proceedings of the National Academy of Sciences",

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Ribeiro, CL, Conde, D, Balmant, KM, Dervinis, C, Johnson, MG, McGrath, AP, Szewczyk, P, Unda, F, Finegan, CA, Schmidt, HW, Miles, B, Drost, DR, Novaes, E, Gonzalez-Benecke, CA, Peter, GF, Gordon Burleigh, J, Martin, TA, Mansfield, SD, Chang, G, Wickett, NJ & Kirst, M 2020, 'The uncharacterized gene EVE contributes to vessel element dimensions in Populus', Proceedings of the National Academy of Sciences of the United States of America, vol. 117, no. 9, pp. 5059-5066. https://doi.org/10.1073/pnas.1912434117

TY - JOUR

T1 - The uncharacterized gene EVE contributes to vessel element dimensions in Populus

AU - Ribeiro, Cíntia L.

AU - Conde, Daniel

AU - Balmant, Kelly M.

AU - Dervinis, Christopher

AU - Johnson, Matthew G.

AU - McGrath, Aaron P.

AU - Szewczyk, Paul

AU - Unda, Faride

AU - Finegan, Christina A.

AU - Schmidt, Henry W.

AU - Miles, Brianna

AU - Drost, Derek R.

AU - Novaes, Evandro

AU - Gonzalez-Benecke, Carlos A.

AU - Peter, Gary F.

AU - Gordon Burleigh, J.

AU - Martin, Timothy A.

AU - Mansfield, Shawn D.

AU - Chang, Geoffrey

AU - Wickett, Norman J.

AU - Kirst, Matias

N1 - Funding Information: ACKNOWLEDGMENTS. We thank Pieter Bass, Ron Sederoff, Pamela Soltis, and Douglas Soltis for critical reading of the manuscript; and Thomas Wood for the gift of the LB2003 Escherichia coli. This work was supported by the US Department of Agriculture Plant Feedstock Genomics for Bioenergy Program (Grant 2009-65504-05697) and the Department of Energy Office of Science Biological and Environmental Research (Grant DE-SC0003893). Publisher Copyright: © 2020 National Academy of Sciences. All rights reserved.

PY - 2020/3/3

Y1 - 2020/3/3

N2 - 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.

AB - 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.

KW - EVE

KW - Phycodnavirus

KW - Vessel

KW - Vessel dimension

KW - Xylem

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U2 - 10.1073/pnas.1912434117

DO - 10.1073/pnas.1912434117

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AN - SCOPUS:85081065535

SN - 0027-8424

VL - 117

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EP - 5066

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 9

ER -

The uncharacterized gene EVE contributes to vessel element dimensions in Populus

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Keywords

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