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

Juhyun Kim,Jong Yoon Park,Myeongjune Jeon,Ilha Lee,Jinseul Kyung,Youngsung Joo,Ho Gyun Lee,Eunju Lee,Doo Soo Chung,Hao Yu

doi:10.1371/journal.pgen.1007208

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.

Highlights

Since plants are sessile organisms, specific adaptations to their given environments are critical for their survival
Evolutionary adaptation into aquatic environment is widely observed in diverse clades of land plants
To understand the molecular basis behind such adaptation, we analyzed Ranunculus trichophyllus, an amphibious plant producing different leaf shape depending on the growth conditions

Summary

Introduction

Since plants are sessile organisms, specific adaptations to their given environments are critical for their survival. One of the most dramatic plant plasticity is heterophylly, an ability to produce morphologically different types of leaves depending on the growth environments [3]. Amphibious plants produce different shapes of leaves when grown under water compared to terrestrial growth; they usually produce thin and slender leaves in aquatic conditions but produce thick and stout leaves in terrestrial conditions [3]. Plasticity by water adaptation is regulated by plant hormones. Auxin influences hyponastic growth and development of adventitious roots in submerged condition [6, 8]. Ethylene regulates adventitious roots and rapid shoot growth when submerged, especially in deep water rice [7, 9]. Exogenous ABA treatment induces terrestrial leaf development in many aquatic plants whereas exogenous GA induces aquatic leaf development in some aquatic plants [3]

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