Evolution of Portulacineae Marked by Gene Tree Conflict and Gene Family Expansion Associated with Adaptation to Harsh Environments

Ning Wang, Ya Yang, Michael J. Moore, Samuel F. Brockington, Joseph F. Walker, Joseph W. Brown, Bin Liang, Tao Feng, Caroline Edwards, Jessica Mikenas, Julia Olivieri, Vera Hutchison, Alfonso Timoneda, Tommy Stoughton, Raúl Puente, Lucas C. Majure, Urs Eggli, Stephen A. Smith

Research output: Contribution to journalArticlepeer-review

9 Scopus citations

Abstract

Several plant lineages have evolved adaptations that allow survival in extreme and harsh environments including many families within the plant clade Portulacineae (Caryophyllales) such as the Cactaceae, Didiereaceae, and Montiaceae. Here, using newly generated transcriptomic data, we reconstructed the phylogeny of Portulacineae and examined potential correlates between molecular evolution and adaptation to harsh environments. Our phylogenetic results were largely congruent with previous analyses, but we identified several early diverging nodes characterized by extensive gene tree conflict. For particularly contentious nodes, we present detailed information about the phylogenetic signal for alternative relationships. We also analyzed the frequency of gene duplications, confirmed previously identified whole genome duplications (WGD), and proposed a previously unidentified WGD event within the Didiereaceae. We found that the WGD events were typically associated with shifts in climatic niche but did not find a direct association with WGDs and diversification rate shifts. Diversification shifts occurred within the Portulacaceae, Cactaceae, and Anacampserotaceae, and whereas these did not experience WGDs, the Cactaceae experienced extensive gene duplications. We examined gene family expansion and molecular evolutionary patterns with a focus on genes associated with environmental stress responses and found evidence for significant gene family expansion in genes with stress adaptation and clades found in extreme environments. These results provide important directions for further and deeper examination of the potential links between molecular evolutionary patterns and adaptation to harsh environments.

Original languageEnglish (US)
Pages (from-to)112-126
Number of pages15
JournalMolecular biology and evolution
Volume36
Issue number1
DOIs
StatePublished - Jan 1 2019

Bibliographical note

Funding Information:
The authors thank Wynn Anderson, the Bureau of Land Management, the US Forest Service, and the staff of Desert Botanical Garden, Sukkulenten-Sammlung Zürich, Cambridge University Botanic Garden, Missouri Botanical Garden, and the Oberlin College Greenhouse for permission to collect specimens, and thank Hilda Flores, Helga Ochoterena, and Norman Douglas for help with collecting. The authors also thank Jeet Sukumaran for constructive discussion on gene tree discordance. Special thanks to the constructive comments from the editors and three anonymous reviewers. Oscar Vargas provided a thorough review of the first draft of the paper. This work was supported by NSF DEB 1354048 to S.A.S. and NSF DEB 1352907 to M.J.M.

Publisher Copyright:
© The Author 2018.

Keywords

  • Portulacineae
  • gene duplication
  • gene tree conflict
  • molecular evolution
  • paleopolyploidy
  • stress adaptation

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