An ancient peptide family buried within vicilin precursors

Jingjing Zhang, Colton D Payne, Benjamin Pouvreau, Hanno Schaefer, Mark F Fisher, Nicolas L Taylor, Oliver Berkowitz, James Whelan, K Johan Rosengren, Joshua S Mylne

Research output: Contribution to journalArticle

1 Citation (Scopus)

Abstract

New proteins can evolve by duplication and divergence or de novo, from previously non-coding DNA. A recently observed mechanism is for peptides to evolve within a 'host' protein and emerge by proteolytic processing. The first examples of such interstitial peptides were ones hosted by precursors for seed storage albumin. Interstitial peptides have also been observed in precursors for seed vicilins, but current evidence for vicilin-buried peptides (VBPs) is limited to seeds of the broadleaf plants pumpkin and macadamia. Here, an extensive sequence analysis of vicilin precursors suggested that peptides buried within the N-terminal region of preprovicilins are widespread and truly ancient. Gene sequences indicative of interstitial peptides were found in species from Amborellales to eudicots and include important grass and legume crop species. We show the first protein evidence for a monocot VBP in date palm seeds as well as protein evidence from other crops including the common tomato, sesame and pumpkin relatives, cucumber and the sponge loofah (Luffa aegyptiaca). Their excision was consistent with asparaginyl endopeptidase-mediated maturation and sequences were confirmed by tandem mass spectrometry. Our findings suggest the family is large and ancient and, that based on the NMR solution structures for loofah Luffin P1 and tomato VBP-8, VBPs adopt a helical hairpin fold stapled by two internal disulfide bonds. The first VBPs characterized were a protease inhibitor, anti-microbials, and a ribosome inactivator. The age and evolutionary retention of this peptide family suggests its members play important roles in plant biology.

Original languageEnglish
Pages (from-to)979-993
JournalACS Chemical Biology
Volume14
Issue number5
DOIs
Publication statusPublished - 17 May 2019

Fingerprint

Peptides
Luffa
Seed
Seeds
Cucurbita
asparaginylendopeptidase
Lycopersicon esculentum
Crops
Macadamia
Proteins
plant vicilin protein
Sesamum
Cucumis sativus
Porifera
Tandem Mass Spectrometry
Poaceae
Protease Inhibitors
Ribosomes
Fabaceae
Disulfides

Cite this

Zhang, Jingjing ; Payne, Colton D ; Pouvreau, Benjamin ; Schaefer, Hanno ; Fisher, Mark F ; Taylor, Nicolas L ; Berkowitz, Oliver ; Whelan, James ; Rosengren, K Johan ; Mylne, Joshua S. / An ancient peptide family buried within vicilin precursors. In: ACS Chemical Biology. 2019 ; Vol. 14, No. 5. pp. 979-993.
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Zhang, J, Payne, CD, Pouvreau, B, Schaefer, H, Fisher, MF, Taylor, NL, Berkowitz, O, Whelan, J, Rosengren, KJ & Mylne, JS 2019, 'An ancient peptide family buried within vicilin precursors' ACS Chemical Biology, vol. 14, no. 5, pp. 979-993. https://doi.org/10.1021/acschembio.9b00167

An ancient peptide family buried within vicilin precursors. / Zhang, Jingjing; Payne, Colton D; Pouvreau, Benjamin; Schaefer, Hanno; Fisher, Mark F; Taylor, Nicolas L; Berkowitz, Oliver; Whelan, James; Rosengren, K Johan; Mylne, Joshua S.

In: ACS Chemical Biology, Vol. 14, No. 5, 17.05.2019, p. 979-993.

Research output: Contribution to journalArticle

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AU - Zhang, Jingjing

AU - Payne, Colton D

AU - Pouvreau, Benjamin

AU - Schaefer, Hanno

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AU - Taylor, Nicolas L

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AU - Rosengren, K Johan

AU - Mylne, Joshua S

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AB - New proteins can evolve by duplication and divergence or de novo, from previously non-coding DNA. A recently observed mechanism is for peptides to evolve within a 'host' protein and emerge by proteolytic processing. The first examples of such interstitial peptides were ones hosted by precursors for seed storage albumin. Interstitial peptides have also been observed in precursors for seed vicilins, but current evidence for vicilin-buried peptides (VBPs) is limited to seeds of the broadleaf plants pumpkin and macadamia. Here, an extensive sequence analysis of vicilin precursors suggested that peptides buried within the N-terminal region of preprovicilins are widespread and truly ancient. Gene sequences indicative of interstitial peptides were found in species from Amborellales to eudicots and include important grass and legume crop species. We show the first protein evidence for a monocot VBP in date palm seeds as well as protein evidence from other crops including the common tomato, sesame and pumpkin relatives, cucumber and the sponge loofah (Luffa aegyptiaca). Their excision was consistent with asparaginyl endopeptidase-mediated maturation and sequences were confirmed by tandem mass spectrometry. Our findings suggest the family is large and ancient and, that based on the NMR solution structures for loofah Luffin P1 and tomato VBP-8, VBPs adopt a helical hairpin fold stapled by two internal disulfide bonds. The first VBPs characterized were a protease inhibitor, anti-microbials, and a ribosome inactivator. The age and evolutionary retention of this peptide family suggests its members play important roles in plant biology.

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