Striking developmental convergence in angiosperm endoparasites

Luiza Teixeira-Costa, Charles C. Davis, Gregorio Ceccantini

Research output: Contribution to journalArticlepeer-review

11 Citations (Scopus)

Abstract

Premise: A subset of parasitic plants bear extremely reduced features and grow nearly entirely within their hosts. Until recently, most of these endoparasites were thought to represent a single clade united by their reduced morphology. Current phylogenetic understanding contradicts this assumption and indicates these plants represent distantly related clades, thus offering an opportunity to examine convergence among plants with this life history. Methods: We sampled species from Apodanthaceae, Cytinaceae, Mitrastemonaceae, and Rafflesiaceae spanning a range of developmental stages. To provide a broader comparative framework, Santalaceae mistletoes with a similar lifestyle were also analyzed. Microtomography and microscopy were used to analyze growth patterns and the ontogeny of host–parasite vascular connections. Results: Apodanthaceae, Cytinaceae, Mitrastemonaceae, and Rafflesiaceae species demonstrated a common development characterized by late cell differentiation. These species were also observed to form direct connections to host vessels and to cause severe alterations of host xylem development. Apodanthaceae and Rafflesiaceae species were additionally observed to form sieve elements, which connect with the host phloem. Endophytic Santalaceae species demonstrated a dramatically different developmental pattern, featuring early cell differentiation and tissue organization, and little effect on host anatomy and cambial activity. Conclusions: Our results illuminate two distinct developmental trajectories in endoparasites. One involves the retention of embryonic characteristics and late connection with host vessels, as demonstrated in species of Apodanthaceae, Cytinaceae, Mitrastemonaceae, and Rafflesiaceae. The second involves tissue specialization and early connection with host xylem, as exemplified by Santalaceae species. These differences are hypothesized to be related to the absence/presence of photosynthesis in these plants.

Original languageEnglish
Pages (from-to)756-768
Number of pages13
JournalAmerican Journal of Botany
Volume108
Issue number5
DOIs
Publication statusPublished - May 2021

Bibliographical note

Funding Information:
We thank several people for help provided during sampling efforts in various localities. L.T.C. acknowledges Dr. Rosa Cerros‐Tlatilpa and Luis Gil Galván from the Universidad Autónoma de Morlelos in the collection of . Alexander Vázquez, Daniel Gómez, Fernando Vázquez, Juan Martínez, Juvenal Hernández, and Martín Castillo greatly helped collecting at the Reserva Biológica La Sepultura. C.C.D. and L.T.C. acknowledge staff at the EEB Greenhouse at the University of Connecticut (UConn) and Clinton Morse and Matthew Opel for providing specimens of . G.C. and L.T.C. acknowledge David Shaw from Oregon State University and Robert Mathiasen from Northern Arizona University for help and species identification during the sampling of . We also acknowledge the reviewers and editor for their comments, which helped us improve this paper. L.T.C. was supported by grants from the European Society for Evolutionary Biology and the Harvard University Herbaria. G.C. was supported by the São Paulo Research Foundation (FAPESP‐2013/23322‐3). This research was also supported by National Science Foundation AToL grant to C.C.D. (DEB‐0622764) and DEB‐1120243 grant to C.C.D. and Elena Kramer. Bdallophytum americanum Mitrastemon matudae Viscum minimum Arceuthobium douglasii

Funding Information:
We thank several people for help provided during sampling efforts in various localities. L.T.C. acknowledges Dr. Rosa Cerros-Tlatilpa and Luis Gil Galv?n from the Universidad Aut?noma de Morlelos in the collection of Bdallophytum americanum. Alexander V?zquez, Daniel G?mez, Fernando V?zquez, Juan Mart?nez, Juvenal Hern?ndez, and Mart?n Castillo greatly helped collecting Mitrastemon matudae at the Reserva Biol?gica La Sepultura. C.C.D. and L.T.C. acknowledge staff at the EEB Greenhouse at the University of Connecticut (UConn) and Clinton Morse and Matthew Opel for providing specimens of Viscum minimum. G.C. and L.T.C. acknowledge David Shaw from Oregon State University and Robert Mathiasen from Northern Arizona University for help and species identification during the sampling of Arceuthobium douglasii. We also acknowledge the reviewers and editor for their comments, which helped us improve this paper. L.T.C. was supported by grants from the European Society for Evolutionary Biology and the Harvard University Herbaria. G.C. was supported by the S?o Paulo Research Foundation (FAPESP-2013/23322-3). This research was also supported by National Science Foundation AToL grant to C.C.D. (DEB-0622764) and DEB-1120243 grant to C.C.D. and Elena Kramer.

Publisher Copyright:
© 2021 Botanical Society of America

Copyright:
Copyright 2021 Elsevier B.V., All rights reserved.

Keywords

  • Apodanthaceae
  • Arceuthobium
  • Cytinaceae
  • endoparasite
  • holoparasite
  • mistletoe
  • Mitrastemonaceae
  • parasitic plants
  • plant development
  • Rafflesiaceae

Fingerprint

Dive into the research topics of 'Striking developmental convergence in angiosperm endoparasites'. Together they form a unique fingerprint.

Cite this