Abstract Detail


Smith, Chelsea R. [1], Teisher, Jordan [2], Moore, Abigail [3], Straub, Shannon [4], Livshultz, Tatyana [5].

Positive selection on a functional motif predicts two independent origins of homospermidine synthase and pyrrolizidine alkaloids in Apocynaceae.

Premise: Signatures of natural selection can be detected in genes associated with adaptive phenotypes. Since plant defenses are predicted to be under positive selection when they first evolve, evidence of selection on a gene tree can place the origin of novel defenses on a phylogeny. Background: Pyrrolizidine alkaloids (PAs), defensive specialized metabolites, are rare in Apocynaceae, with scattered occurrence. Prior research investigated the evolution of homospermidine synthase (HSS), the only known enzyme of PA biosynthesis, from deoxyhypusine synthase (DHS), to infer the homology of PAs across Apocynaceae. A single duplication in the MRCA of all known PA-producing species gave rise to the functional hss of Parsonsia alboflavescens and hss-like genes of unknown function in related species. Apocynaceae hss-like genes encode three amino acid motifs: VXXXD, correlated with HSS function across angiosperms, IXXXN, putatively nonfunctional, and IXXXD, intermediate. The VXXXD motif was reconstructed as ancestral in all hss-like genes, supporting a single origin of HSS function (and PAs) in Apocynaceae followed by multiple losses, evidenced by loss of the VXXXD motif and/or pseudogenization. Objectives: We revisit ancestral motif reconstruction in hss-like genes and test for selection on branches with transitions among motifs to infer the number of times HSS function evolved. Methods: We increased sequence and species sampling, reconstructed ancestral motifs, identified branches with transitions among motifs, and tested for positive selection on branches that evolved toward the HSS motif (IXXXN to IXXXD; IXXXD to VXXXD) and relaxed selection on branches that evolved away from the HSS motif (VXXXD to IXXXD; IXXXD to IXXXN). Results: A single origin of hss-like genes in Apocynaceae is supported, but with a reconstructed IXXXN motif which evolved into IXXXD in the MRCA of hss-like genes in all known PA-producing species. The VXXXD motif evolved twice from IXXXD, IXXXD evolved once from VXXXD, and IXXXN three times from IXXXD.  Amino acid 269 (I or V) was under positive selection. All other a priori selection hypotheses were rejected. Conclusions: A single duplication gave rise to all hss-like genes in Apocynaceae, but two independent transitions from IXXXD to VXXXD, each accompanied by positive selection on the 269 I to V mutation, support two independent recruitments of hss-like genes to hss function. The inference that there were two independent origins of PAs requires further validation of the VXXXD motif as a predictor of PA biosynthesis and reconciliation of the hss gene tree with the Apocynaceae species tree.

Related Links:
Previous work: Livshultz T, Kaltenegger E, Straub SCK, Weitemier K, Hirsch E, Koval K, Mema L, Liston A. 2018. Evolution of pyrrolizidine alkaloid biosynthesis in Apocynaceae: revisiting the defence de-escalation hypothesis. New Phytol 218:762-773.

1 - Academy of Natural Sciences of Drexel University, Botany, 1900 Benjamin Franklin Parkway, Philadelphia, PA, 19103, United States
2 - The Academy Of Natural Sciences Of Drexel University, Botany, 1900 Benjamin Franklin Parkway, Philadelphia, PA, 19103, United States
3 - University Of Oklahoma, Department Of Microbiology And Plant Biology, 770 Van Vleet Oval, Rm. 208, Norman, OK, 73019, United States
4 - Hobart and William Smith Colleges, Department of Biology, 300 Pulteney Street, Geneva, NY, 14456, USA
5 - Academy Of Natural Sciences Of Drexel University, Department Of Botany, 1900 Benjamin Franklin Parkway, Philadelphia, PA, 19103, United States

pyrrolizidine alkaloids
Gene Duplication
signatures of selection
chemical defense
specialized metabolism
metabolic pathway
enzyme evolution.

Presentation Type: Oral Paper
Number: MACRO1001
Abstract ID:703
Candidate for Awards:None

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