Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2020 Dec 25;4(12):e00287.
doi: 10.1002/pld3.287. eCollection 2020 Dec.

Origin and evolution of a gibberellin-deactivating enzyme GAMT

Chi Zhang  1 , Minta Chaiprasongsuk  1   2 , Andre S Chanderbali  3   4 , Xinlu Chen  1 , Jianyu Fu  5 , Douglas E Soltis  3   4 , Feng Chen  1
Affiliations

Origin and evolution of a gibberellin-deactivating enzyme GAMT

Chi Zhang et al. Plant Direct. .

Abstract

Gibberellins (GAs) are a major class of plant hormones that regulates diverse developmental programs. Both acquiring abilities to synthesize GAs and evolving divergent GA receptors have been demonstrated to play critical roles in the evolution of land plants. In contrast, little is understood regarding the role of GA-inactivating mechanisms in plant evolution. Here we report on the origin and evolution of GA methyltransferases (GAMTs), enzymes that deactivate GAs by converting bioactive GAs to inactive GA methylesters. Prior to this study, GAMT genes, which belong to the SABATH family, were known only from Arabidopsis. Through systematic searches for SABATH genes in the genomes of 260 sequenced land plants and phylogenetic analyses, we have identified a putative GAMT clade specific to seed plants. We have further demonstrated that both gymnosperm and angiosperm representatives of this clade encode active methyltransferases for GA methylation, indicating that they are functional orthologs of GAMT. In seven selected seed plants, GAMT genes were mainly expressed in flowers and/or seeds, indicating a conserved biological role in reproduction. GAMT genes are represented by a single copy in most species, if present, but multiple copies mainly produced by whole genome duplications have been retained in Brassicaceae. Surprisingly, more than 2/3 of the 248 flowering plants examined here lack GAMT genes, including all species of Poales (e.g., grasses), Fabales (legumes), and the large Superasterid clade of eudicots. With these observations, we discuss the significance of GAMT origination, functional conservation and diversification, and frequent loss during the evolution of flowering plants.

Keywords: gene loss; plant hormone; reproduction; seed plants.

PubMed Disclaimer

Figures

FIGURE 1
FIGURE 1
Phylogenetic analysis of SABATH proteins from 260 sequenced plants (Table S1). In this unrooted phylogenetic tree, the SABATHs were clustered into five groups I to V. Group I was enlarged to illustrate individual plant lineages with bootstrap values (percent out of 1,000 iterations) shown. The shaded clade indicates the putative GAMT clade
FIGURE 2
FIGURE 2
GAMT clade and biochemical activities. (a) Phylogeny of the GAMT clade with major lineages illustrated. (b) The chemical structures of gibberellin A1(GA1), gibberellin A3 (GA3), and gibberellin A4 (GA4). (c) Representative GAMTs and their activity towards to GA1, GA3, and GA4. “+” and “−” indicate “active” and “inactive,” respectively
FIGURE 3
FIGURE 3
Expression patterns of GAMT genes in selected species based on their expression data in public sources. (a) GbGAMT1 and GbGAMT2 from Ginkgo biloba; (b) PaGAMT from Picea abies; (c) PeGAMT from Phalaenopsis equestris; (d) MaGAMT from Musa acuminata; (e) VvGAMT from Vitis vinifera; (f) CisGAMT from Citrus sinensis; (g) CsGAMT1 to CsGAMT7 from Camelina sativa. O, ovules; Mc, male cones; Sl, dtem and leaves; S, stem; L, leaf; R, root; Fs, floral stalk; F, flower; S, sepal; P, petal; La, labellum; G, gynostemium; 40F, 40‐day‐fruit; 60F, 60‐day‐fruit; 80F, 80‐day‐fruit; Yt, young tendril; Yl, young leaf; Sf, senescent leaf; B, bud; Yf, young flower; Rp, ripening pericarp; C, callus; Fr, fruit; Ro, rosette; Cl, cauline leaf; Se, seed. The highest level of expression in each species was arbitrarily set at 1.0. Standard deviations were marked with error bars in (e) and (g), not in other figures due to lack of such information
FIGURE 4
FIGURE 4
Copy number of GAMT and its duplication in Brassicaceae. (a) Distribution of copy numbers of GAMT genes among 69 GAMT‐containing flowering plants. (b) Phylogenetic tree of GAMTs in Brassicales. The two clades (clade I and clade II) in blue and in yellow, respectively, depict two clades that resulted from a whole gene duplication event occurred in the ancestor of Brassicaceae known as At‐α. The three smaller blocks (Brassica 1, Brassica 2, and Brassica 3) for Brassica GAMTs indicate a possible outcome of whole genome triplication event
FIGURE 5
FIGURE 5
Presence/absence of GAMT genes in seed plants. The phylogeny was redrawn from APG IV (2016). The lineages in gray indicated that no species from those lineages was analyzed in this study. The two numbers (red and black) represent the number of species containing the GAMT gene and the total number of species from that specific lineage analyzed in this study. Three taxa with complete loss of GAMTs were shaded
See this image and copyright information in PMC

References

    1. Aravind, L. , Watanabe, H. , Lipman, D. J. , & Koonin, E. V. (2000). Lineage‐specific loss and divergence of functionally linked genes in eukaryotes. Proceedings of the National Academy of Sciences of the United States of America, 97, 11319–11324. 10.1073/pnas.200346997 - DOI - PMC - PubMed
    1. Blazquez, M. A. , Green, R. , Nilsson, O. , Sussman, M. R. , & Weigel, D. (1998). Gibberellins promote flowering of arabidopsis by activating the LEAFY promoter. The Plant Cell, 10, 791–800. - PMC - PubMed
    1. Cannell, N. , Emms, D. M. , Hetherington, A. J. , MacKay, J. , Kelly, S. , Dolan, L. , & Sweetlove, L. J. (2020). Multiple metabolic innovations and losses are associated with major transitions in land plant evolution. Current Biology, 30, 1783–1800. 10.1016/j.cub.2020.02.086 - DOI - PubMed
    1. Cardinal‐McTeague, W. M. , Sytsma, K. J. , & Hall, J. C. (2016). Biogeography and diversification of Brassicales: A 103 million year tale. Molecular Phylogenetics and Evolution, 99, 204–224. 10.1016/j.ympev.2016.02.021 - DOI - PubMed
    1. Chaiprasongsuk, M. , Zhang, C. , Qian, P. , Chen, X. , Li, G. , Trigiano, R. N. , Guo, H. , & Chen, F. (2018). Biochemical characterization in Norway spruce (Picea abies) of SABATH methyltransferases that methylate phytohormones. Phytochemistry, 149, 146–154. 10.1016/j.phytochem.2018.02.010 - DOI - PubMed

LinkOut - more resources