Stepwise Evolution of a Buried Inhibitor Peptide over 45 My.
The de novo evolution of genes and the novel proteins they encode has stimulated much interest in the contribution such innovations make to the diversity of life. Most research on this de novo evolution focuses on transcripts, so studies on the biochemical steps that can enable completely new proteins to evolve and the time required to do so have been lacking. Sunflower Preproalbumin with SFTI-1 (PawS1) is an unusual albumin precursor because in addition to producing albumin it also yields a potent, bicyclic protease-inhibitor called SunFlower Trypsin Inhibitor-1 (SFTI-1). Here, we show how this inhibitor peptide evolved stepwise over tens of millions of years. To trace the origin of the inhibitor peptide SFTI-1, we assembled seed transcriptomes for 110 sunflower relatives whose evolution could be resolved by a chronogram, which allowed dates to be estimated for the various stages of molecular evolution. A genetic insertion event in an albumin precursor gene ∼45 Ma introduced two additional cleavage sites for protein maturation and conferred duality upon PawS1-Like genes such that they also encode a small buried macrocycle. Expansion of this region, including two Cys residues, enlarged the peptide ∼34 Ma and made the buried peptides bicyclic. Functional specialization into a protease inhibitor occurred ∼23 Ma. These findings document the evolution of a novel peptide inside a benign region of a pre-existing protein. We illustrate how a novel peptide can evolve without de novo gene evolution and, critically, without affecting the function of what becomes the protein host.
School of Molecular Sciences & ARC Centre of Excellence in Plant Energy Biology, The University of Western Australia, Perth, Australia.
Achala S
AS
Jayasena
School of Molecular Sciences & ARC Centre of Excellence in Plant Energy Biology, The University of Western Australia, Perth, Australia.
Mark F
MF
Fisher
Department of Integrative Biology, University of Texas, Austin, TX.
Jose L
JL
Panero
School of Molecular Sciences & ARC Centre of Excellence in Plant Energy Biology, The University of Western Australia, Perth, Australia.
David
D
Secco
School of Molecular Sciences & ARC Centre of Excellence in Plant Energy Biology, The University of Western Australia, Perth, Australia.
Kalia
K
Bernath-Levin
Department of Animal, Plant and Soil Sciences, School of Life Sciences & ARC Centre of Excellence in Plant Energy Biology, AgriBio, The Centre for AgriBioscience, La Trobe University, Bundoora, Victoria, Australia.
Oliver
O
Berkowitz
School of Molecular Sciences & ARC Centre of Excellence in Plant Energy Biology, The University of Western Australia, Perth, Australia.
Nicolas L
NL
Taylor
Department of Ecology & Evolutionary Biology, University of Tennessee, Knoxville, TN.
Edward E
EE
Schilling
Department of Animal, Plant and Soil Sciences, School of Life Sciences & ARC Centre of Excellence in Plant Energy Biology, AgriBio, The Centre for AgriBioscience, La Trobe University, Bundoora, Victoria, Australia.
James
J
Whelan
School of Molecular Sciences & ARC Centre of Excellence in Plant Energy Biology, The University of Western Australia, Perth, Australia.
Joshua S
JS
Mylne
D020816:Amino Acid Motifs; D000595:Amino Acid Sequence; D005075:Biological Evolution; D019143:Evolution, Molecular; D006368:Helianthus / Q000235:genetics*; D008958:Models, Molecular; D016254:Mutagenesis, Insertional / Q000235:genetics; D010455:Peptides; D010456:Peptides, Cyclic / Q000235:genetics* / Q000378:metabolism; D010802:Phylogeny; D011228:Prealbumin / Q000235:genetics; D011498:Protein Precursors / Q000235:genetics; D012639:Seeds / Q000235:genetics
D010455:Peptides; D010456:Peptides, Cyclic; D011228:Prealbumin; D011498:Protein Precursors; C448501:SFTI-1 peptide, sunflower; C014771:preproalbumin
Asteraceae; biosynthesis; peptide; protein evolution; sunflower