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. 2013 Jul 15;8(7):e68536.
doi: 10.1371/journal.pone.0068536. Print 2013.

Evolution of plant HECT ubiquitin ligases

Ignacio Marín  1
Affiliations

Evolution of plant HECT ubiquitin ligases

Ignacio Marín. PLoS One. .

Abstract

HECT ubiquitin ligases are key components of the ubiquitin-proteasome system, which is present in all eukaryotes. In this study, the patterns of emergence of HECT genes in plants are described. Phylogenetic and structural data indicate that viridiplantae have six main HECT subfamilies, which arose before the split that separated green algae from the rest of plants. It is estimated that the common ancestor of all plants contained seven HECT genes. Contrary to what happened in animals, the number of HECT genes has been kept quite constant in all lineages, both in chlorophyta and streptophyta, although evolutionary recent duplications are found in some species. Several of the genes found in plants may have originated very early in eukaryotic evolution, given that they have clear similarities, both in sequence and structure, to animal genes. Finally, in Arabidopsis thaliana, we found significant correlations in the expression patterns of HECT genes and some ancient, broadly expressed genes that belong to a different ubiquitin ligase family, called RBR. These results are discussed in the context of the evolution of the gene families required for ubiquitination in plants.

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Conflict of interest statement

Competing Interests: The author has declared that no competing interests exist.

Figures

Figure 1
Figure 1. Basic result for the phylogenetic analysis including 413 plant HECT sequences.
The main branches that correspond to the six subfamilies (I – VI) are indicated. Only a few green algal sequences were excluded from those branches. Numbers above those branches correspond to bootstrap support, in percentages. The three numbers correspond to Neighbor-joining (NJ), Maximum Parsimony (MP) and Maximum Likelihood (ML) analyses (order: NJ/MP/ML). The names of the angiosperm genes found in each family (UPL1-UPL8) are also indicated. Subfamily IV is not present in angiosperms (see main text). Numbers in brackets refer to the number of protein sequences which are included in each branch. Only branches with bootstrap support above 50% in all three analyses are indicated. The structures typical of proteins of the different subfamilies are also indicated. In addition to the C-terminal HECT domains (red boxes), other domains can be found, as armadillo repeats (Arm repeats; in Subfamilies I and V), IQ domains (in Subfamilies II and III), UBA domains (Subfamily V) or ubiquitin domains (Ub; Subfamily VI). Proteins are drawn at scale, with the HECT domain corresponding to 350 amino acids.
Figure 2
Figure 2. Subfamily I sequences.
Angiosperm sequences are named accordingto the Arabidopsis genes (UPL3 and UPL4). Bootstrap support and number of sequences are indicated as in Figure 1. The numbers in brackets indicate first the total number of sequences (T) and then the number of sequences in monocots (M), asterid dicots (A), rosid dicots (R), or other dicots not included in those two groups (Other: O).
Figure 3
Figure 3. Sequences corresponding to Subfamilies II and III.
The angiosperm genes UPL7 and UPL6, which respectively belong to Subfamily II and Subfamily III, are indicated. Bootstrap support and number of sequences indicated as in Figure 2.
Figure 4
Figure 4. Subfamily IV sequences.
Notice the low bootstrap values for many internal branches (see text). The question marks indicate two incongruent results, corresponding to two ESTs that most likely did not come from the species to which they were adscribed (see main text).
Figure 5
Figure 5. Subfamily V sequences.
They include the angiosperm genes UPL1/2 (from which derive the A. thaliana recent duplicates UPL1 and UPL2) and UPL8, a new gene, described here for the first time, given that it is absent in A. thaliana (see text). Boostrap values and number of sequences as in Figures 2 and 3.
Figure 6
Figure 6. Subfamily VI sequences.
This subfamily includes the angiosperm UPL5 gene. Bootstrap values and number of sequences indicated as in previous figures, i. e. total (T), monocot (M), dicot rosid (R), dicot asterid (A) and dicot, others (O).
Figure 7
Figure 7. The most parsimonious hypothesis to explain the evolution of HECT genes in plants.
Red rectangles correspond to gene losses and black arrows to gene emergences. Subfamilies are indicated with roman numerals; O means “other”, indicating the presence of an additional gene in green algae (see Figure 1). The numbers in the boxes correspond to the genes deduced to exist in the ancestors of the corresponding lineages. The loss of a Subfamily IV gene in angiosperms is supported by a single fragment of a putative gymnosperm Subfamily IV gene (see text), so it must be considered a provisional result, until additional sequences are available.
Figure 8
Figure 8. Phylogenetic tree comparing plant (green) and animal (red) HECT subfamilies.
Bootstrap values for the most relevant branches are indicated (again as NJ/MP/ML). Asterisk indicate branches for which the three phylogenetic analyses provided values higher than 90%. Only a few sequences cannot be ascribed to the main subfamilies.
Figure 9
Figure 9. Cumulative values of expression for Arabidopsis HECT genes in 79 developmental samples.
Data were obtained from Schmid et al. . The Y-axis is measured in arbitrary expression units. Samples are as follows: 1) root 7 days; 2) root 17 days; 3) root 15 days; 4) root 8 days; 5) root 8 days; 6) root 21 days; 7) root 21 days; 8) stem: hypocotyl; 9) stem: first node; 10) stem: second internode; 11) cotyledons; 12) leaves 1+2; 13) rosette leaf #4, 1 cm long; 14) rosette leaf #4, 1 cm long (gl1-T mutant); 15) rosette leaf # 2; 16) rosette leaf # 4; 17) rosette leaf # 6; 18) rosette leaf # 8; 19) rosette leaf # 10; 20) rosette leaf # 12; 21) rosette leaf # 12 (gl1-T mutant); 22) leaf 7, petiole; 23) leaf 7, petiole; 24) leaf 7, distal half; 25) leaf, 15 days; 26) leaf, senescing; 27) cauline leaves; 28) seedling, green parts, 7 days; 29) seedling, green parts, 8 days; 30) seedling, green parts, 8 days; 31) seedling, green parts, 21 days; 32) seedling, green parts, 21 days; 33) whole plant: developmental drift, entire rosette after transition to flowering, but before bolting, 21 days; 34) whole plant: developmental drift, entire rosette after transition to flowering, but before bolting, 22 days; 35) whole plant: developmental drift, entire rosette after transition to flowering, but before bolting, 23 days; 36) vegetative rosette 7 days; 37) vegetative rosette 14 days; 38) vegetative rosette 21 days; 39) shoot apex, vegetative+young leaves; 40) shoot apex, vegetative; 41) shoot apex, transition (before bolting); 42) shoot apex, inflorescence (after bolting); 43) shoot apex, inflorescence (after bolting) (clv3-7 mutant); 44) shoot apex, inflorescence (after bolting) (lfy-12 mutant); 45) shoot apex, inflorescence (after bolting) (ap1-15 mutant); 46) shoot apex, inflorescence (after bolting) (ap2-6 mutant); 47) shoot apex, inflorescence (after bolting) (ufo-1 mutant); 48) shoot apex, inflorescence (after bolting) (ap3-6 mutant); 49) shoot apex, inflorescence (after bolting) (ag-12 mutant); 50) flowers stage 9; 51) flowers stage 10/11; 52) flowers stage 12; 53) flower stage 12; multi-carpel gynoeceum; enlarged meristem; increased organ number (clv3-7 mutant); 54) flower stage 12; shoot characteristics; most organs leaf-like (lfy-12 mutant); 55) flower stage 12; sepals replaced by leaf-like organs, petals mostly lacking, has secondary flowers (ap1-15 mutant); 56) flower stage 12; no sepals or petals (ap2-6 mutant); 57) flower stage 12; filamentous organs in whorls two and three (ufo-1 mutant); 58) flower stage 12; no petals or stamens (ap3-6 mutant) 59) flower stage 12; no stamens or carpels (ag-12 mutant); 60) flowers stage 15; 61) flowers 28 days; 62) flowers stage 15, pedicels; 63) flowers stage 12, sepals; 64) flowers stage 15, sepals; 65) flowers stage 12, petals; 66) flowers stage 15, petals; 67) flowers stage 12, stamens; 68) flowers stage 15, stamen; 69) mature pollen 70) flowers stage 12, carpels; 71) flowers stage 15, carpels; 72) siliques, w/seeds stage 3; mid globular to early heart embryos; 73) siliques, w/seeds stage 4; early to late heart embryos; 74) siliques, w/seeds stage 5; late heart to mid torpedo embryos; 75) seeds, stage 6, w/o siliques; mid to late torpedo embryos; 76) seeds, stage 7, w/o siliques; late torpedo to early walking-stick embryos; 77) seeds, stage 8, w/o siliques; walking-stick to early curled cotyledons embryos; 78) seeds, stage 9, w/o siliques; curled cotyledons to early green cotyledons embryos; 79) seeds, stage 10, w/o siliques; green cotyledons embryos.
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This study was supported by grant BFU2011-30063 (Spanish government). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.