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. 2002 Mar;128(3):854-64.
doi: 10.1104/pp.010658.

Plant expansins are a complex multigene family with an ancient evolutionary origin

Yi Li  1 , Catherine P Darley, Verónica Ongaro, Andrew Fleming, Ori Schipper, Sandra L Baldauf, Simon J McQueen-Mason
Affiliations

Plant expansins are a complex multigene family with an ancient evolutionary origin

Yi Li et al. Plant Physiol. 2002 Mar.

Abstract

Expansins are a group of extracellular proteins that directly modify the mechanical properties of plant cell walls, leading to turgor-driven cell extension. Within the completely sequenced Arabidopsis genome, we identified 38 expansin sequences that fall into three discrete subfamilies. Based on phylogenetic analysis and shared intron patterns, we propose a new, systematic nomenclature of Arabidopsis expansins. Further phylogenetic analysis, including expansin sequences found here in monocots, pine (Pinus radiata, Pinus taeda), fern (Regnellidium diphyllum, Marsilea quadrifolia), and moss (Physcomitrella patens) indicate that the three plant expansin subfamilies arose and began diversifying very early in, if not before, colonization of land by plants. Closely related "expansin-like" sequences were also identified in the social amoeba, Dictyostelium discoidium, suggesting that these wall-modifying proteins have a very deep evolutionary origin.

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Figures

Figure 1
Figure 1
Alignment of representative α-, β-, and γ-expansins from Arabidopsis. The shaded boxes highlight the conserved areas used in our analyses. α and β insertions within the central core of the expansins and signal sequences are indicated. Intron positions are arrowed, and residues are highlighted at the point of insertion into the predicted exon.
Figure 2
Figure 2
Phylogenetic analysis of the Arabidopsis expansin gene family shows three major groups: α, β, and γ. The composite tree was derived by neighbor-joining distance analysis using ClustalX version 1.8. The main backbone of the tree was calculated with the 90-residue conserved core of amino acid positions alignable among all 38 sequences. The three subtrees were then calculated separately based on additional amino acid positions shared within each group, and were appended to the main backbone tree as indicated by broken horizontal lines. Only bootstrap values over 60% are indicated above the nodes. The major expansin subfamilies α, β, and γ are highlighted by shaded boxes. Hypothetical intron gains and losses are indicated by diamonds followed by intron number. Postulated intron gains are indicated by filled diamonds, and intron losses are indicated by unfilled diamonds. All branches are drawn to scale as indicated by the scale bar (=0.1 substitutions/site).
Figure 3
Figure 3
Deduced chromosomal positions of Arabidopsis expansin (Ath-Exp) genes. Genes are annotated by accession number (protein) and specific name based on the proposed nomenclature system. The positions are given according to the nearest recombinant inbred marker. Genetic distance was calculated using the proportions suggested by the Lister and Dean recombinant map (Lister and Dean, 1993).
Figure 4
Figure 4
Phylogenetic tree for the plant expansin gene family shows an ancient origin of α-, β-, and γ-expansins. Bootstrap values over 60% are indicated above the nodes. The tree was constructed as described in “Materials and Methods.” The major groups are indicated by light-shaded boxes and were strongly supported (>80% bootstrap). Subgroups containing sequences from mixed plant groups in the major branches are further highlighted with dark-shaded boxes. Major plant taxonomic divisions are indicated by accession number color thus: dicot, black; monocot, green; pine, blue; fern, orange; and bryophyte, red. Hypothetical intron gains and losses are indicated as described in Figure 1b. Branches are drawn to scale as indicated by the scale bar (= 0.1 substitutions/1,000 residues). Accession numbers for non-Arabidopsis sequences have a species-specific indentifier as follows: Osa, rice (Oryza sativa); Csa, cucumber (Cucumis sativa); Pta, pine (Pinus taeda); Mqu, Marsilea quadrifolia; Ppa, moss (P. patens); Zma, maize (Zea mays); Pra, Pinus radiata; Lja, Lotus japonicus; Gma, soybean (Glycine max); Gar, Gossypium arborium; Mtr, Medicago truncatula; Cpu, Ceratodon purpureus; Mpo, Marchantia polymorpha; Cja, C. jambhiri; Mcr, common ice plant (Mesembryanthemum crystallinum).
Figure 5
Figure 5
A schematic illustration of the presence of conserved motifs in expansin-like proteins. Positions of conserved motifs and residues are not presented to scale, and are based on information in the comprehensive alignment of protein sequences used in this paper (Fig. S1 in the supplementary material). The table at the top lists the motifs for each class of expansins. Schematics below show the physical arrangements of the motifs within the deduced sequences.
Figure 6
Figure 6
Phylogenetic analysis suggests the “best-guess” root of the expansin family is between the α/β and γ groups. The analysis used five D. discoidium sequences as an outgroup. Only representative sequences from α, β, and all γ were included in this analysis (see Table S1 in the supplementary material). Bootstrap values are indicated against the appropriate branches. The major groups, α, β, and γ, are grouped as highlighted boxes. The lower support for the β subgroup (56% versus 77%) is due to the smaller number of alignable positions used in theses analyses.
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