Evidence for ancient origins of bowman-birk inhibitors from Selaginella moellendorffii

Amy M. James, Achala S. Jayasena, Jingjing Zhang, Oliver Berkowitz, David Secco, Gavin J. Knott, James Whelan, Charles S. Bond, Joshua S. Mylne

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Abstract

Bowman-Birk Inhibitors (BBIs) are a well-known family of plant protease inhibitors first described 70 years ago. BBIs are known only in the legume (Fabaceae) and cereal (Poaceae) families, but peptides that mimic their trypsin-inhibitory loops exist in sunflowers (Helianthus annuus) and frogs. The disparate biosynthetic origins and distant phylogenetic distribution implies these loops evolved independently, but their structural similarity suggests a common ancestor. Targeted bioinformatic searches for the BBI inhibitory loop discovered highly divergent BBI-like sequences in the seedless, vascular spikemoss Selaginella moellendorffii. Using de novo transcriptomics, we confirmed expression of five transcripts in S. moellendorffii whose encoded proteins share homology with BBI inhibitory loops. The most highly expressed, BBI3, encodes a protein that inhibits trypsin. We needed to mutate two lysine residues to abolish trypsin inhibition, suggesting BBI3’s mechanism of double-headed inhibition is shared with BBIs from angiosperms. As Selaginella belongs to the lycopod plant lineage, which diverged ~200 to 230 million years before the common ancestor of angiosperms, its BBI-like proteins imply there was a common ancestor for legume and cereal BBIs. Indeed, we discovered BBI sequences in six angiosperm families outside the Fabaceae and Poaceae. These findings provide the evolutionary missing links between the well-known legume and cereal BBI gene families.

Original languageEnglish
Pages (from-to)461-473
Number of pages13
JournalThe Plant Cell
Volume29
Issue number3
DOIs
Publication statusPublished - 1 Mar 2017

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Selaginellaceae
Bowman-Birk inhibitor
Selaginella
Fabaceae
Angiosperms
Trypsin
Helianthus
Poaceae
trypsin
Angiospermae
ancestry
Proteins
legumes
Protease Inhibitors
Computational Biology
Anura
Lysine
Helianthus annuus
Blood Vessels
Peptides

Cite this

James, A. M., Jayasena, A. S., Zhang, J., Berkowitz, O., Secco, D., Knott, G. J., ... Mylne, J. S. (2017). Evidence for ancient origins of bowman-birk inhibitors from Selaginella moellendorffii. The Plant Cell, 29(3), 461-473. https://doi.org/10.1105/tpc.16.00831
James, Amy M. ; Jayasena, Achala S. ; Zhang, Jingjing ; Berkowitz, Oliver ; Secco, David ; Knott, Gavin J. ; Whelan, James ; Bond, Charles S. ; Mylne, Joshua S. / Evidence for ancient origins of bowman-birk inhibitors from Selaginella moellendorffii. In: The Plant Cell. 2017 ; Vol. 29, No. 3. pp. 461-473.
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Evidence for ancient origins of bowman-birk inhibitors from Selaginella moellendorffii. / James, Amy M.; Jayasena, Achala S.; Zhang, Jingjing; Berkowitz, Oliver; Secco, David; Knott, Gavin J.; Whelan, James; Bond, Charles S.; Mylne, Joshua S.

In: The Plant Cell, Vol. 29, No. 3, 01.03.2017, p. 461-473.

Research output: Contribution to journalArticle

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James AM, Jayasena AS, Zhang J, Berkowitz O, Secco D, Knott GJ et al. Evidence for ancient origins of bowman-birk inhibitors from Selaginella moellendorffii. The Plant Cell. 2017 Mar 1;29(3):461-473. https://doi.org/10.1105/tpc.16.00831