Convergent evolution of a blood-red nectar pigment in vertebrate-pollinated flowers

Rahul Roy, Nickolas Moreno, Stephen A. Brockman, Adam Kostanecki, Amod Zambre, Catherine Holl, Erik M. Solhaug, Anzu Minami, Emilie C. Snell-Rood, Marshall Hampton, Mark A. Bee, Ylenia Chiari, Adrian D. Hegeman, Clay J. Carter

Research output: Contribution to journalArticlepeer-review

2 Scopus citations

Abstract

Nearly 90% of flowering plants depend on animals for reproduction. One of the main rewards plants offer to pollinators for visitation is nectar. Nesocodon mauritianus (Campanulaceae) produces a blood-red nectar that has been proposed to serve as a visual attractant for pollinator visitation. Here, we show that the nectar's red color is derived from a previously undescribed alkaloid termed nesocodin. The first nectar produced is acidic and pale yellow in color, but slowly becomes alkaline before taking on its characteristic red color. Three enzymes secreted into the nectar are either necessary or sufficient for pigment production, including a carbonic anhydrase that increases nectar pH, an aryl-alcohol oxidase that produces a pigment precursor, and a ferritin-like catalase that protects the pigment from degradation by hydrogen peroxide. Our findings demonstrate how these three enzymatic activities allow for the condensation of sinapaldehyde and proline to form a pigment with a stable imine bond. We subsequently verified that synthetic nesocodin is indeed attractive to Phelsuma geckos, the most likely pollinators of Nesocodon. We also identify nesocodin in the red nectar of the distantly related and hummingbird-visited Jaltomata herrerae and provide molecular evidence for convergent evolution of this trait. This work cumulatively identifies a convergently evolved trait in two vertebrate-pollinated species, suggesting that the red pigment is selectively favored and that only a limited number of compounds are likely to underlie this type of adaptation.

Original languageEnglish (US)
Article numbere2114420119
JournalProceedings of the National Academy of Sciences of the United States of America
Volume119
Issue number5
DOIs
StatePublished - Feb 1 2022

Bibliographical note

Funding Information:
ACKNOWLEDGMENTS. The authors recognize the Center for Mass Spectrometry and Proteomics at the University of Minnesota and various supporting agencies, including the NSF for Major Research Instrumentation grants 9871237 and NSF-DBI-0215759 used to purchase the instruments described in this study. We thank the Minnesota NMR Center (with support from the National Institute of General Medical Sciences [1S10OD021536 (G. Veglia)] for access to NMR instrumentation, as well as the University of Minnesota Genomics Center for conducting RNA quality control, RNA-seq library creation, next-generation sequencing, and primary NGS data QC. We also thank Lisa Aston-Philander, Angie Koebler, and Alex Eilts of the CBS Conservatory and Botanical Collection of the University of Minnesota for helpful discussions and access to plant materials. This work was supported by grants from the US NSF to M.H. and C.J.C. (IOS-1339246); E.C.S.-R., M.H., A.D.H., and C.J.C. (IOS-2025297); and A.D.H. (IOS-1238812). R.R. was supported by a postdoctoral fellowship from the United States Department of Agriculture (2018-67012-28038).

Publisher Copyright:
© 2022 National Academy of Sciences. All rights reserved.

Keywords

  • Altomata
  • Gecko
  • Nectar
  • Nectaries
  • Nesocodon
  • Flowers/metabolism
  • Reproduction/physiology
  • Pollination/physiology
  • Magnoliopsida/metabolism
  • Pigmentation/physiology
  • Adaptation, Physiological/physiology
  • Animals
  • Birds/physiology
  • Plant Nectar/metabolism
  • Lizards/physiology
  • Pollen/metabolism

PubMed: MeSH publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.
  • Journal Article
  • Research Support, N.I.H., Extramural

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