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Research ArticleLARGE-SCALE BIOLOGY ARTICLES
Open Access

Desiccation Tolerance Evolved through Gene Duplication and Network Rewiring in Lindernia

Robert VanBuren, Ching Man Wai, Jeremy Pardo, Valentino Giarola, Stefano Ambrosini, Xiaomin Song, Dorothea Bartels
Robert VanBuren
aDepartment of Horticulture, Michigan State University, East Lansing, Michigan 48824
bPlant Resilience Institute, Michigan State University, East Lansing, Michigan 48824
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  • For correspondence: bobvanburen@gmail.com unb137@uni-bonn.de
Ching Man Wai
aDepartment of Horticulture, Michigan State University, East Lansing, Michigan 48824
bPlant Resilience Institute, Michigan State University, East Lansing, Michigan 48824
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Jeremy Pardo
bPlant Resilience Institute, Michigan State University, East Lansing, Michigan 48824
cDepartment of Plant Biology, Michigan State University, East Lansing, Michigan 48824
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Valentino Giarola
dIMBIO, University of Bonn, D-53115 Bonn, Germany
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Stefano Ambrosini
dIMBIO, University of Bonn, D-53115 Bonn, Germany
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Xiaomin Song
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Dorothea Bartels
dIMBIO, University of Bonn, D-53115 Bonn, Germany
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  • For correspondence: bobvanburen@gmail.com unb137@uni-bonn.de

Published December 2018. DOI: https://doi.org/10.1105/tpc.18.00517

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  • © 2018 American Society of Plant Biologists. All rights reserved.

Abstract

Although several resurrection plant genomes have been sequenced, the lack of suitable dehydration-sensitive outgroups has limited genomic insights into the origin of desiccation tolerance. Here, we utilized a comparative system of closely related desiccation-tolerant (Lindernia brevidens) and -sensitive (Lindernia subracemosa) species to identify gene- and pathway-level changes associated with the evolution of desiccation tolerance. The two high-quality Lindernia genomes we assembled are largely collinear, and over 90% of genes are conserved. L. brevidens and L. subracemosa have evidence of an ancient, shared whole-genome duplication event, and retained genes have neofunctionalized, with desiccation-specific expression in L. brevidens. Tandem gene duplicates also are enriched in desiccation-associated functions, including a dramatic expansion of early light-induced proteins from 4 to 26 copies in L. brevidens. A comparative differential gene coexpression analysis between L. brevidens and L. subracemosa supports extensive network rewiring across early dehydration, desiccation, and rehydration time courses. Many LATE EMBRYOGENESIS ABUNDANT genes show significantly higher expression in L. brevidens compared with their orthologs in L. subracemosa. Coexpression modules uniquely upregulated during desiccation in L. brevidens are enriched with seed-specific and abscisic acid-associated cis-regulatory elements. These modules contain a wide array of seed-associated genes that have no expression in the desiccation-sensitive L. subracemosa. Together, these findings suggest that desiccation tolerance evolved through a combination of gene duplications and network-level rewiring of existing seed desiccation pathways.

  • Received July 6, 2018.
  • Revised October 2, 2018.
  • Accepted October 23, 2018.
  • Published October 25, 2018.

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Desiccation Tolerance Evolved through Gene Duplication and Network Rewiring in Lindernia
Robert VanBuren, Ching Man Wai, Jeremy Pardo, Valentino Giarola, Stefano Ambrosini, Xiaomin Song, Dorothea Bartels
The Plant Cell Dec 2018, 30 (12) 2943-2958; DOI: 10.1105/tpc.18.00517

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Desiccation Tolerance Evolved through Gene Duplication and Network Rewiring in Lindernia
Robert VanBuren, Ching Man Wai, Jeremy Pardo, Valentino Giarola, Stefano Ambrosini, Xiaomin Song, Dorothea Bartels
The Plant Cell Dec 2018, 30 (12) 2943-2958; DOI: 10.1105/tpc.18.00517
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  • Peer Review Report
  • In Brief: How Resurrection Plants Survive Being Hung Out to Dry

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The Plant Cell: 30 (12)
The Plant Cell
Vol. 30, Issue 12
Dec 2018
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