Genome and time-of-day transcriptome of Wolffia australiana link morphological minimization with gene loss and less growth control - PubMed (original) (raw)

. 2021 Feb;31(2):225-238.

doi: 10.1101/gr.266429.120. Epub 2020 Dec 23.

Evan Ernst # 2 3, Nolan Hartwick # 1, Philomena Chu 4, Douglas Bryant 5, Sarah Gilbert 4, Stefan Ortleb 6, Erin L Baggs 7, K Sowjanya Sree 8, Klaus J Appenroth 9, Joerg Fuchs 6, Florian Jupe 1, Justin P Sandoval 1, Ksenia V Krasileva 7, Ljudmylla Borisjuk 6, Todd C Mockler 5, Joseph R Ecker 1 10, Robert A Martienssen 2 3, Eric Lam 4

Affiliations

Todd P Michael et al. Genome Res. 2021 Feb.

Abstract

Rootless plants in the genus Wolffia are some of the fastest growing known plants on Earth. Wolffia have a reduced body plan, primarily multiplying through a budding type of asexual reproduction. Here, we generated draft reference genomes for Wolffia australiana (Benth.) Hartog & Plas, which has the smallest genome size in the genus at 357 Mb and has a reduced set of predicted protein-coding genes at about 15,000. Comparison between multiple high-quality draft genome sequences from W. australiana clones confirmed loss of several hundred genes that are highly conserved among flowering plants, including genes involved in root developmental and light signaling pathways. Wolffia has also lost most of the conserved nucleotide-binding leucine-rich repeat (NLR) genes that are known to be involved in innate immunity, as well as those involved in terpene biosynthesis, while having a significant overrepresentation of genes in the sphingolipid pathways that may signify an alternative defense system. Diurnal expression analysis revealed that only 13% of Wolffia genes are expressed in a time-of-day (TOD) fashion, which is less than the typical ∼40% found in several model plants under the same condition. In contrast to the model plants Arabidopsis and rice, many of the pathways associated with multicellular and developmental processes are not under TOD control in W. australiana, where genes that cycle the conditions tested predominantly have carbon processing and chloroplast-related functions. The Wolffia genome and TOD expression data set thus provide insight into the interplay between a streamlined plant body plan and optimized growth.

© 2021 Michael et al.; Published by Cold Spring Harbor Laboratory Press.

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Figures

Figure 1.

Figure 1.

Wolffia is a simple plant with a limited number of cells and structures. (A) Brightfield image of wa8730. A video with time tracking of the asexual propagation of wa7733 in culture can be found in the

Supplemental Material

. (B) Phylogenetic relationship between representative species from the five genera of duckweed. Each color represents a distinct genus. Modified from Borisjuk et al. (2015). (C) Cross section (1-µm-thick section) of W. australiana stained with methylene blue: (mf) Mother frond; (df) daughter frond; (gdf) grand-daughter frond; (ep) epidermal cells; (ch) chlorenchyma cells; (pa) parenchyma cells; asterisks indicate some of the stomata; (st) stipe tissue.

Figure 2.

Figure 2.

The Wolffia genome is collinear with Spirodela with bloating and loss of genes owing to transposable elements (TEs). (A) wa8730 scaffold 1 (scf1) is collinear with wa7733 scf8. (B) Conserved core circadian clock genes PRR37 (red ribbon) and LHY (gold ribbon) on sp9509 Chromosome 20 (Chr 20) are collinear in wa8730 scf200 and wa7733 scf432. (C) WOX5 is lost in Wolffia compared to Spirodela owing to TE insertions (yellow boxes). (D) DOT3/NPH3 loci in Spirodela lost in Wolffia owing to LTR-RT insertions. Gray lines represent syntenic connections. Green and blue boxes are forward and reverse representation for genes, respectively. Orange boxes are TEs.

Figure 3.

Figure 3.

Wolffia orthogroups (OGs) analysis reveals significant Gene Ontology (GO) terms relating to growth and defense. (A) An upset plot showing the orthogroups (OGs) present (black circles) or missing (gray circle) across the four duckweed genomes (sp9509, sp7498, wa7733, and wa8730), model species (Arabidopsis thaliana, Oryza sativa ssp. Japonica), and two non-grass monocots (Musa acuminata, Zostera marina). Boxes indicate _Wolffia_-specific, _Wolffia_-missing, and duckweed-specific genes. (B) Significant (FDR < 0.05) GO terms derived from _Wolffia_-specific OGs (A) were plotted in two-dimensional semantic space by multidimensional scaling (MDS) with the color reflecting significance (_P_-value) and circle size reflecting GO frequency. (C) GO terms from Wolffia missing OGs. (D) GO terms from duckweed-specific OGs. All GO terms were summarized using semantic similarity (SimRel), and _P_-values from overrepresentation with REVIGO.

Figure 4.

Figure 4.

Core circadian and light genes cycle in Wolffia with global expression over the day. (A_–_D) Circadian clock and light signaling TOD gene expression in wa8730 is similar to that found in other plants. (A) sMYB (blue) and LHY (red) cycle with dawn specific expression. (B) PRR5 (blue), PRR9 (red), and PRR73 (green) show waves of expression similar to other species. (C) GI (blue), ZTL (red), and ELF3 (green) cycle with evening-specific expression. (D) Light signaling genes CRY (blue), SPA1 (red), and PIL3 (green) cycle over the day. (E) Heatmap of the cycling genes with red indicating high expression and blue indicating low expression. Genes are on the _y_-axis and time is on the _x_-axis.

Figure 5.

Figure 5.

Wolffia has conserved TOD _cis_-elements but lacks others. (A) The Evening Element (EE:AAATATCT) is overrepresented in genes with evening-specific expression. (B) The Telobox (TBX:AAACCCT) is not significantly overrepresented in Wolffia promoters of cycling genes. (C) Sequence logo of the significantly overrepresented Gbox (CACGTG) in Wolffia. (D) Sequence logo of the EE overrepresented _cis_-elements. (E) Sequence logo of the Protein box (PBX: TGGGCCC) overrepresented _cis_-elements.

Figure 6.

Figure 6.

Wolffia cycling genes are focused on energy acquisition. (A) GO term overrepresentation by TOD for Wolffia with GO term summaries for 6-h bins. (B) Venn diagram of cycling orthogroups (OGs) with at least one gene from Wolffia, Arabidopsis, and rice. (C) Venn diagram of cycling GO terms from Wolffia, Arabidopsis, and rice. (D) GO term summary for the 421 Arabidopsis and rice cycling GO terms. (E) GO term summary for the 20 cycling GO terms shared across all three species. (F) GO term summary for the 72 _Wolffia_-specific cycling GO terms. All GO terms were summarized using semantic similarity (SimRel), and _P_-values from overrepresentation with REVIGO.

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