Evolutionary origins of a bioactive peptide buried within Preproalbumin

Alysha G. Elliott, Christina Delay, Huanle Liu, Zaiyang Phua, K. Johan Rosengren, Aurelie H. Benfield, Jose L. Panero, Michelle L. Colgrave, Achala Mederian Kotuwe, Kerry M. Dunse, Marilyn A. Anderson, Edward E. Schilling, Daniel Ortiz-Barrientos, Joshua S. Mylne

Research output: Contribution to journalArticle

23 Citations (Scopus)

Abstract

The de novo evolution of proteins is now considered a frequented route for biological innovation, but the genetic and biochemical processes that lead to each newly created protein are often poorly documented. The common sunflower (Helianthus annuus) contains the unusual gene PawS1 (Preproalbumin with SFTI-1) that encodes a precursor for seed storage albumin; however, in a region usually discarded during albumin maturation, its sequence is matured into SFTI-1, a protease-inhibiting cyclic peptide with a motif homologous to unrelated inhibitors from legumes, cereals, and frogs. To understand how PawS1 acquired this additional peptide with novel biochemical functionality, we cloned PawS1 genes and showed that this dual destiny is over 18 million years old. This new family of mostly backbone-cyclic peptides is structurally diverse, but the protease-inhibitory motif was restricted to peptides from sunflower and close relatives from its subtribe. We describe a widely distributed, potential evolutionary intermediate PawS-Like1 (PawL1), which is matured into storage albumin, but makes no stable peptide despite possessing residues essential for processing and cyclization from within PawS1. Using sequences we cloned, we retrodict the likely stepwise creation of PawS1's additional destiny within a simple albumin precursor. We propose that relaxed selection enabled SFTI-1 to evolve its inhibitor function by converging upon a successful sequence and structure. © 2014 American Society of Plant Biologists. All rights reserved.
Original languageEnglish
Pages (from-to)981-995
Number of pages15
JournalThe Plant Cell
Volume26
Issue number3
DOIs
Publication statusPublished - 28 Mar 2014

Cite this

Elliott, A. G., Delay, C., Liu, H., Phua, Z., Rosengren, K. J., Benfield, A. H., ... Mylne, J. S. (2014). Evolutionary origins of a bioactive peptide buried within Preproalbumin. The Plant Cell, 26(3), 981-995. https://doi.org/10.1105/tpc.114.123620
Elliott, Alysha G. ; Delay, Christina ; Liu, Huanle ; Phua, Zaiyang ; Rosengren, K. Johan ; Benfield, Aurelie H. ; Panero, Jose L. ; Colgrave, Michelle L. ; Mederian Kotuwe, Achala ; Dunse, Kerry M. ; Anderson, Marilyn A. ; Schilling, Edward E. ; Ortiz-Barrientos, Daniel ; Mylne, Joshua S. / Evolutionary origins of a bioactive peptide buried within Preproalbumin. In: The Plant Cell. 2014 ; Vol. 26, No. 3. pp. 981-995.
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abstract = "The de novo evolution of proteins is now considered a frequented route for biological innovation, but the genetic and biochemical processes that lead to each newly created protein are often poorly documented. The common sunflower (Helianthus annuus) contains the unusual gene PawS1 (Preproalbumin with SFTI-1) that encodes a precursor for seed storage albumin; however, in a region usually discarded during albumin maturation, its sequence is matured into SFTI-1, a protease-inhibiting cyclic peptide with a motif homologous to unrelated inhibitors from legumes, cereals, and frogs. To understand how PawS1 acquired this additional peptide with novel biochemical functionality, we cloned PawS1 genes and showed that this dual destiny is over 18 million years old. This new family of mostly backbone-cyclic peptides is structurally diverse, but the protease-inhibitory motif was restricted to peptides from sunflower and close relatives from its subtribe. We describe a widely distributed, potential evolutionary intermediate PawS-Like1 (PawL1), which is matured into storage albumin, but makes no stable peptide despite possessing residues essential for processing and cyclization from within PawS1. Using sequences we cloned, we retrodict the likely stepwise creation of PawS1's additional destiny within a simple albumin precursor. We propose that relaxed selection enabled SFTI-1 to evolve its inhibitor function by converging upon a successful sequence and structure. {\circledC} 2014 American Society of Plant Biologists. All rights reserved.",
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Elliott, AG, Delay, C, Liu, H, Phua, Z, Rosengren, KJ, Benfield, AH, Panero, JL, Colgrave, ML, Mederian Kotuwe, A, Dunse, KM, Anderson, MA, Schilling, EE, Ortiz-Barrientos, D & Mylne, JS 2014, 'Evolutionary origins of a bioactive peptide buried within Preproalbumin' The Plant Cell, vol. 26, no. 3, pp. 981-995. https://doi.org/10.1105/tpc.114.123620

Evolutionary origins of a bioactive peptide buried within Preproalbumin. / Elliott, Alysha G.; Delay, Christina; Liu, Huanle; Phua, Zaiyang; Rosengren, K. Johan; Benfield, Aurelie H.; Panero, Jose L.; Colgrave, Michelle L.; Mederian Kotuwe, Achala; Dunse, Kerry M.; Anderson, Marilyn A.; Schilling, Edward E.; Ortiz-Barrientos, Daniel; Mylne, Joshua S.

In: The Plant Cell, Vol. 26, No. 3, 28.03.2014, p. 981-995.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Evolutionary origins of a bioactive peptide buried within Preproalbumin

AU - Elliott, Alysha G.

AU - Delay, Christina

AU - Liu, Huanle

AU - Phua, Zaiyang

AU - Rosengren, K. Johan

AU - Benfield, Aurelie H.

AU - Panero, Jose L.

AU - Colgrave, Michelle L.

AU - Mederian Kotuwe, Achala

AU - Dunse, Kerry M.

AU - Anderson, Marilyn A.

AU - Schilling, Edward E.

AU - Ortiz-Barrientos, Daniel

AU - Mylne, Joshua S.

PY - 2014/3/28

Y1 - 2014/3/28

N2 - The de novo evolution of proteins is now considered a frequented route for biological innovation, but the genetic and biochemical processes that lead to each newly created protein are often poorly documented. The common sunflower (Helianthus annuus) contains the unusual gene PawS1 (Preproalbumin with SFTI-1) that encodes a precursor for seed storage albumin; however, in a region usually discarded during albumin maturation, its sequence is matured into SFTI-1, a protease-inhibiting cyclic peptide with a motif homologous to unrelated inhibitors from legumes, cereals, and frogs. To understand how PawS1 acquired this additional peptide with novel biochemical functionality, we cloned PawS1 genes and showed that this dual destiny is over 18 million years old. This new family of mostly backbone-cyclic peptides is structurally diverse, but the protease-inhibitory motif was restricted to peptides from sunflower and close relatives from its subtribe. We describe a widely distributed, potential evolutionary intermediate PawS-Like1 (PawL1), which is matured into storage albumin, but makes no stable peptide despite possessing residues essential for processing and cyclization from within PawS1. Using sequences we cloned, we retrodict the likely stepwise creation of PawS1's additional destiny within a simple albumin precursor. We propose that relaxed selection enabled SFTI-1 to evolve its inhibitor function by converging upon a successful sequence and structure. © 2014 American Society of Plant Biologists. All rights reserved.

AB - The de novo evolution of proteins is now considered a frequented route for biological innovation, but the genetic and biochemical processes that lead to each newly created protein are often poorly documented. The common sunflower (Helianthus annuus) contains the unusual gene PawS1 (Preproalbumin with SFTI-1) that encodes a precursor for seed storage albumin; however, in a region usually discarded during albumin maturation, its sequence is matured into SFTI-1, a protease-inhibiting cyclic peptide with a motif homologous to unrelated inhibitors from legumes, cereals, and frogs. To understand how PawS1 acquired this additional peptide with novel biochemical functionality, we cloned PawS1 genes and showed that this dual destiny is over 18 million years old. This new family of mostly backbone-cyclic peptides is structurally diverse, but the protease-inhibitory motif was restricted to peptides from sunflower and close relatives from its subtribe. We describe a widely distributed, potential evolutionary intermediate PawS-Like1 (PawL1), which is matured into storage albumin, but makes no stable peptide despite possessing residues essential for processing and cyclization from within PawS1. Using sequences we cloned, we retrodict the likely stepwise creation of PawS1's additional destiny within a simple albumin precursor. We propose that relaxed selection enabled SFTI-1 to evolve its inhibitor function by converging upon a successful sequence and structure. © 2014 American Society of Plant Biologists. All rights reserved.

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KW - VACUOLAR PROCESSING ENZYME

KW - SERINE-PROTEASE INHIBITORS

KW - NMR CHEMICAL-SHIFTS

KW - AMINO-ACID SITES

KW - CONVERGENT EVOLUTION

KW - PROTEINASE-INHIBITORS

KW - ARABIDOPSIS-THALIANA

KW - DOMAIN ARCHITECTURES

KW - POSITIVE SELECTION

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DO - 10.1105/tpc.114.123620

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SP - 981

EP - 995

JO - The Plant Cell

JF - The Plant Cell

SN - 1040-4651

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Elliott AG, Delay C, Liu H, Phua Z, Rosengren KJ, Benfield AH et al. Evolutionary origins of a bioactive peptide buried within Preproalbumin. The Plant Cell. 2014 Mar 28;26(3):981-995. https://doi.org/10.1105/tpc.114.123620