Identification and Expression of Nine Oak Aquaporin Genes in the Primary Root Axis of Two Oak Species, Quercus petraea and Quercus robur

Claire Rasheed-Depardieu,Fabienne Tatin-Froux,Nicolas Capelli,Julien Parelle,Claire Parent,Grégoire Le Provost,Michèle Crèvecoeur

doi:10.1371/journal.pone.0051838

Abstract

Aquaporins (AQPs) belong to the Major Intrinsic Protein family that conducts water and other small solutes across biological membranes. This study aimed to identify and characterize AQP genes in the primary root axis of two oak species, Quercus petraea and Quercus robur. Nine putative AQP genes were cloned, and their expression was profiled in different developmental root zones by real-time PCR. A detailed examination of the predicted amino acid sequences and subsequent phylogenetic analysis showed that the isolated AQPs could be divided into two subfamilies, which included six plasma membrane intrinsic proteins (PIPs) and three tonoplast intrinsic proteins (TIPs). We characterized the anatomical features of the roots and defined three developmental root zones: the immature, transition and mature zones. Expression analysis of the AQPs was performed according to these root developmental stages. Our results showed that the expression of PIP2;3 and TIP1 was significantly higher in Quercus petraea compared with Quercus robur in the three root zones. However, PIP2;1 and TIP2;1 were found to be differentially expressed in the mature zone of the two oak species. Of the nine AQP genes identified and analyzed, we highlighted four genes that might facilitate a deeper understanding of how these two closely related tree species adapted to different environments.

Highlights

The maintenance of an optimal water balance is crucial for plant survival
AQPs belong to a large family of highly conserved proteins, called Major Intrinsic Proteins (MIPs), which include plasma membrane intrinsic proteins (PIPs), tonoplast intrinsic proteins (TIPs), NIPs, SIPs and XIPs (X intrinsic proteins) [4]
56 MIPs were identified in Populus trichocarpa and 28 in Vitis vinifera [9,10], but little is known about AQPs in other common tree species, such as walnut, olea, beech and oaks

Summary

Introduction

The maintenance of an optimal water balance is crucial for plant survival. In the soil-plant-atmosphere-continuum, water is transported radially across the root tissues and axially to the aerial part of the plant. In differentiated endodermal and hypodermal tissues, the presence in the root cell walls of a Casparian strip, which is composed of the hydrophobic substance suberin, severely restricts water transport through the apoplastic way [2], and water molecules are forced to transit cellular membranes via water channels called aquaporins (AQPs) [3]. AQPs belong to a large family of highly conserved proteins, called Major Intrinsic Proteins (MIPs), which include PIPs (plasma membrane intrinsic proteins), TIPs (tonoplast intrinsic proteins), NIPs (nodulin 26-like intrinsic proteins), SIPs (small intrinsic proteins) and XIPs (X intrinsic proteins) [4]. These proteins are known to transport water molecules and small solutes through biological membranes. 56 MIPs were identified in Populus trichocarpa and 28 in Vitis vinifera [9,10], but little is known about AQPs in other common tree species, such as walnut, olea, beech and oaks

Objectives

Methods

Results