A molecular basis behind heterophylly in an amphibious plant, Ranunculus trichophyllus

PLoS Genet. 2018 Feb 15;14(2):e1007208. doi: 10.1371/journal.pgen.1007208. eCollection 2018 Feb.

Abstract

Ranunculus trichophyllus is an amphibious plant that produces thin and cylindrical leaves if grown under water but thick and broad leaves if grown on land. We found that such heterophylly is widely controlled by two plant hormones, abscisic acid (ABA) and ethylene, which control terrestrial and aquatic leaf development respectively. Aquatic leaves produced higher levels of ethylene but lower levels of ABA than terrestrial leaves. In aquatic leaves, their distinct traits with narrow shape, lack of stomata, and reduced vessel development were caused by EIN3-mediated overactivation of abaxial genes, RtKANADIs, and accompanying with reductions of STOMAGEN and VASCULAR-RELATED NAC-DOMAIN7 (VDN7). In contrast, in terrestrial leaves, ABI3-mediated activation of the adaxial genes, RtHD-ZIPIIIs, and STOMAGEN and VDN7 established leaf polarity, and stomata and vessel developments. Heterophylly of R.trichophyllus could be also induced by external cues such as cold and hypoxia, which is accompanied with the changes in the expression of leaf polarity genes similar to aquatic response. A closely-related land plant R. sceleratus did not show such heterophyllic responses, suggesting that the changes in the ABA/ethylene signaling and leaf polarity are one of key evolutionary steps for aquatic adaptation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Abscisic Acid / metabolism
  • Acclimatization / drug effects
  • Acclimatization / genetics*
  • Arabidopsis
  • Ecosystem
  • Ethylenes / pharmacology
  • Gene Expression Regulation, Plant / drug effects
  • Plant Growth Regulators / metabolism
  • Plant Leaves / drug effects
  • Plant Leaves / growth & development
  • Plant Leaves / metabolism
  • Plant Stomata / drug effects
  • Plant Stomata / growth & development
  • Plant Stomata / metabolism
  • Plants, Genetically Modified
  • Ranunculus / genetics*
  • Ranunculus / growth & development*
  • Ranunculus / metabolism
  • Seeds / growth & development

Substances

  • Ethylenes
  • Plant Growth Regulators
  • Abscisic Acid
  • ethylene

Grants and funding

This work was supported by Samsung Science and Technology Foundation under Project No. SSTF-BA130103702. MJ was supported by the BK21 Plus Program from the Korean Ministry of Education. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.