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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:
 [1];  [2];  [2];  [2];  [3];  [4];  [4]; ORCiD logo [5];  [6];  [2];  [2];  [6];  [2];  [2];  [7];  [8]; ORCiD logo [2];  [5];  [9]; ORCiD logo [10] more »;  [7] « less
  1. Univ. of Florida, Gainesville, FL (United States). Plant Molecular and Cellular Biology Graduate Program. School of Forest Resources and Conservation
  2. Univ. of Florida, Gainesville, FL (United States). School of Forest Resources and Conservation
  3. Texas Tech Univ., Lubbock, TX (United States). E. L. Reed Herbarium
  4. Univ. of California, San Diego, CA (United States). Skaggs School of Pharmacy and Pharmaceutical Science
  5. Univ. of British Columbia, Vancouver, BC (Canada). Dept. of Wood Science. Faculty of Forestry
  6. Univ. of Florida, Gainesville, FL (United States). Plant Molecular and Cellular Biology Graduate Program
  7. Univ. of Florida, Gainesville, FL (United States). Plant Molecular and Cellular Biology Graduate Program. School of Forest Resources and Conservation. Genetics Inst.
  8. Univ. of Florida, Gainesville, FL (United States). Plant Molecular and Cellular Biology Graduate Program. Dept. of Biology
  9. Univ. of California, San Diego, CA (United States). Skaggs School of Pharmacy and Pharmaceutical Science. Dept. of Pharmacology. School of Medicine
  10. Chicago Botanic Garden, Glencoe, IL (United States). Plant Science and Conservation; Northwestern Univ., Evanston, IL (United States). Plant Biology and Conservation
Publication Date:
Research Org.:
Univ. of Florida, Gainesville, FL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); US Dept. of Agriculture (USDA)
OSTI Identifier:
1598905
Alternate Identifier(s):
OSTI ID: 1625051
Grant/Contract Number:  
SC0003893; 2009-65504-05697
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 117; Journal Issue: 9; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; vessel; xylem; EVE; vessel dimension; phycodnavirus

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. https://doi.org/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. https://doi.org/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 = 9,
volume = 117,
place = {United States},
year = {2020},
month = {2}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1073/pnas.1912434117

Citation Metrics:
Cited by: 8 works
Citation information provided by
Web of Science

Figures / Tables:

Fig. 1 Fig. 1: Vessel number and dimensions are modified in transgenic EVE plants. (A) Xylem cross-section of 2-mo-old, greenhouse-grown P. tremula × alba wildtype and transgenic (CRISPR/Cas9 mutant: eve; overexpression: OX) EVE plants. Cell walls are stained with phloroglucinol and vessels are white. (B) Mean vessel area, (C) vessel count permore » area, and (D) overall vessel area per unit total xylem area in wild-type and transgenic lines of EVE. Data are presented as means ± SE (n = three biological replicates per genotype, with at least three cross-sections measured per replicate). Asterisks indicate significantly lower measures in the mutant eve line, and higher in the transgenic OX line, compared to wild-type, at P < 0.001 (one-way ANOVA followed by Dunnett’s test). Results from three independent OX and eve transgenic lines are presented in SI Appendix, Figs. S4 and S6. (E) Correlation between mean individual vessel area and expression of EVE in a genetically unstructured population of P. trichocarpa. Area of individual vessel elements were measured in partial stem sections of 96 unrelated P. trichocarpa trees grown in common garden for 4 y. Transcript abundance of EVE was quantified in each individual tree by RNAsequencing, and the normalized expression was determined by the number of fragments per kilobase of transcript, per million mapped reads. Linear models fitting vessel phenotypes (number and area) and PotriEVE transcript abundance were generated in Prism 6.01 software. The slope of this model was significant nonzero (P < 0.0001). ***P < 0.001 (one-way ANOVA followed by Dunnett’s test).« less

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Exploiting SNPs for biallelic CRISPR mutations in the outcrossing woody perennial Populus reveals 4-coumarate:CoA ligase specificity and redundancy
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Genome of Acanthamoeba castellanii highlights extensive lateral gene transfer and early evolution of tyrosine kinase signaling
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Real-time monitoring of PtaHMGB activity in poplar transactivation assays
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Overall Alteration of Circadian Clock Gene Expression in the Chestnut Cold Response
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A Glimpse of Nucleo-Cytoplasmic Large DNA Virus Biodiversity through the Eukaryotic Genomics Window
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