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Genome and time-of-day transcriptome of Wolffia australiana link morphological extreme minimization with un-gated plant growth

View ORCID ProfileTodd P. Michael, View ORCID ProfileEvan Ernst, Nolan Hartwick, View ORCID ProfilePhilomena Chu, View ORCID ProfileDouglas Bryant, View ORCID ProfileSarah Gilbert, View ORCID ProfileStefan Ortleb, View ORCID ProfileErin L. Baggs, View ORCID ProfileK. Sowjanya Sree, View ORCID ProfileKlaus J. Appenroth, View ORCID ProfileJoerg Fuchs, View ORCID ProfileFlorian Jupe, View ORCID ProfileJustin P. Sandoval, View ORCID ProfileKsenia V. Krasileva, View ORCID ProfileLjudmylla Borisjuk, View ORCID ProfileTodd C. Mockler, View ORCID ProfileJoseph R. Ecker, View ORCID ProfileRobert A. Martienssen, View ORCID ProfileEric Lam
doi: https://doi.org/10.1101/2020.03.31.018291
Todd P. Michael
1The Salk Institute for Biological Studies, La Jolla, CA, USA
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  • For correspondence: toddpmichael@gmail.com ericl89@hotmail.com
Evan Ernst
2Cold Spring Harbor Laboratory, 1 Bungtown Road, Cold Spring Harbor, NY, USA
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Nolan Hartwick
1The Salk Institute for Biological Studies, La Jolla, CA, USA
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Philomena Chu
3Department of Plant Biology, Rutgers, The State University of New Jersey, New Brunswick, NJ USA
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Douglas Bryant
4Donald Danforth Plant Science Center, St. Louis, MO USA
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Sarah Gilbert
3Department of Plant Biology, Rutgers, The State University of New Jersey, New Brunswick, NJ USA
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Stefan Ortleb
5Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Gatersleben, Germany
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Erin L. Baggs
6Department of Plant and Microbial Biology, University of California, Berkeley, 231 Koshland Hall, Berkeley, CA USA
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K. Sowjanya Sree
7Department of Environmental Science, Central University of Kerala, Periye-671320, India
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Klaus J. Appenroth
8Friedrich Schiller University of Jena, Jena, Germany
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Joerg Fuchs
5Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Gatersleben, Germany
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Florian Jupe
1The Salk Institute for Biological Studies, La Jolla, CA, USA
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Justin P. Sandoval
1The Salk Institute for Biological Studies, La Jolla, CA, USA
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Ksenia V. Krasileva
6Department of Plant and Microbial Biology, University of California, Berkeley, 231 Koshland Hall, Berkeley, CA USA
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Ljudmylla Borisjuk
5Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Gatersleben, Germany
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Todd C. Mockler
4Donald Danforth Plant Science Center, St. Louis, MO USA
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Joseph R. Ecker
1The Salk Institute for Biological Studies, La Jolla, CA, USA
9Howard Hughes Medical Institute, The Salk Institute for Biological Studies, La Jolla, CA, USA
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Robert A. Martienssen
2Cold Spring Harbor Laboratory, 1 Bungtown Road, Cold Spring Harbor, NY, USA
10Howard Hughes Medical Institute, Cold Spring Harbor Laboratory, 1 Bungtown Road, Cold Spring Harbor, NY, USA
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Eric Lam
3Department of Plant Biology, Rutgers, The State University of New Jersey, New Brunswick, NJ USA
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  • For correspondence: toddpmichael@gmail.com ericl89@hotmail.com
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Abstract

Wolffia is the fastest growing plant genus on Earth with a recorded doubling time of less than a day. Wolffia has a dramatically reduced body plan, primarily growing through a continuous, budding-type asexual reproduction with no obvious phase transition. Most plants are bound by the 24-hour light-dark cycle with the majority of processes such as gene expression partitioned or phased to a specific time-of-day (TOD). However, the role that TOD information and the circadian clock plays in facilitating the growth of a fast-growing plant is unknown. Here we generated draft reference genomes for Wolffia australiana (Benth.) Hartog & Plas to monitor gene expression over a two-day time course under light-dark cycles. Wolffia australiana has the smallest genome size in the genus at 357 Mb and has a dramatically reduced gene set at 15,312 with a specific loss of root (WOX5), vascular (CASP), circadian (TOC1), and light-signaling (NPH3) genes. Remarkably, it has also lost all but one of the NLR genes that are known to be involved in innate immunity. In addition, only 13% of its genes cycle, which is far less than in other plants, with an overrepresentation of genes associated with carbon processing and chloroplast-related functions. Despite having a focused set of cycling genes, TOD cis-elements are conserved in W. australiana, consistent with the overall conservation of transcriptional networks. In contrast to the model plants Arabidopsis thaliana and Oryza sativa, the reduction in cycling genes correlates with fewer pathways under TOD control in Wolffia, which could reflect a release of functional gating. Since TOD networks and the circadian clock work to gate activities to specific times of day, this minimization of regulation may enable Wolffia to grow continuously with optimal economy. Wolffia is an ideal model to study the transcriptional control of growth and the findings presented here could serve as a template for plant improvement.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Genome and time-of-day transcriptome of Wolffia australiana link morphological extreme minimization with un-gated plant growth
Todd P. Michael, Evan Ernst, Nolan Hartwick, Philomena Chu, Douglas Bryant, Sarah Gilbert, Stefan Ortleb, Erin L. Baggs, K. Sowjanya Sree, Klaus J. Appenroth, Joerg Fuchs, Florian Jupe, Justin P. Sandoval, Ksenia V. Krasileva, Ljudmylla Borisjuk, Todd C. Mockler, Joseph R. Ecker, Robert A. Martienssen, Eric Lam
bioRxiv 2020.03.31.018291; doi: https://doi.org/10.1101/2020.03.31.018291
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Genome and time-of-day transcriptome of Wolffia australiana link morphological extreme minimization with un-gated plant growth
Todd P. Michael, Evan Ernst, Nolan Hartwick, Philomena Chu, Douglas Bryant, Sarah Gilbert, Stefan Ortleb, Erin L. Baggs, K. Sowjanya Sree, Klaus J. Appenroth, Joerg Fuchs, Florian Jupe, Justin P. Sandoval, Ksenia V. Krasileva, Ljudmylla Borisjuk, Todd C. Mockler, Joseph R. Ecker, Robert A. Martienssen, Eric Lam
bioRxiv 2020.03.31.018291; doi: https://doi.org/10.1101/2020.03.31.018291

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