Plasma Membrane Aquaporins Are Involved in Winter Embolism Recovery in Walnut Tree

Abstract

In perennial plants, freeze-thaw cycles during the winter months can induce the formation of air bubbles in xylem vessels, leading to changes in their hydraulic conductivity. Refilling of embolized xylem vessels requires an osmotic force that is created by the accumulation of soluble sugars in the vessels. Low water potential leads to water movement from the parenchyma cells into the xylem vessels. The water flux gives rise to a positive pressure essential for the recovery of xylem hydraulic conductivity. We investigated the possible role of plasma membrane aquaporins in winter embolism recovery in walnut (Juglans regia). First, we established that xylem parenchyma starch is converted to sucrose in the winter months. Then, from a xylem-derived cDNA library, we isolated two PIP2 aquaporin genes (JrPIP2,1 and JrPIP2,2) that encode nearly identical proteins. The water channel activity of the JrPIP2,1 protein was demonstrated by its expression in Xenopus laevis oocytes. The expression of the two PIP2 isoforms was investigated throughout the autumn-winter period. In the winter period, high levels of PIP2 mRNA and corresponding protein occurred simultaneously with the rise in sucrose. Furthermore, immunolocalization studies in the winter period show that PIP2 aquaporins were mainly localized in vessel-associated cells, which play a major role in controlling solute flux between parenchyma cells and xylem vessels. Taken together, our data suggest that PIP2 aquaporins could play a role in water transport between xylem parenchyma cells and embolized vessels.Winter embolism, the generation of air bubbles in xylem vessels induced by freeze-thaw cycles, often leads to a loss of hydraulic conductivity of the vessels (Cochard and Tyree, 1990; Améglio et al., 2001; Ewers et al., 2001). Vulnerability to winter embolism is related to the anatomy and vessel diameter of woody plants (Cochard and Tyree, 1990) and affects the ability of plants to survive cold climates and the geographic distribution of species (Tyree and Cochard, 1996; Pockman and Sperry, 1997; Lemoine et al., 1999).Detailed physiological studies of the responses of temperate woody plants to winter embolism have been made. Plants minimize the impact of winter embolism by replacing embolized vessels by new functional vessels every year and/or by refilling embolized vessels by generating positive xylem pressures (Holbrook and Zwieniecki, 1999; Tyree et al., 1999; Améglio et al., 2002). Although making new vessels is common to all the plants that exhibit secondary growth, the generation of xylem pressures has only been reported in a few species such as maple (Acer pseudoplatanus; O'Malley and Milburn, 1983; Tyree, 1983; Sperry et al., 1987 Sperry et al., , 1994, grapevine (Vitis vinifera; Sperry et al., 1987), birch (Betula alleghaniensis) (Sperry et al., 1994; Zhu et al., 2000), and walnut (Juglans regia; Améglio et al., 1995Améglio et al., , 2001 Ewers et al., 2001).In walnut trees, depending on the temperature, two types of positive xylem pressures have been ...

Seasonal fluctuation of organic and inorganic components in xylem sap of Populus nigra

“…Though the local exchange of sugars may occur between the vessels and parenchyma cells in stem (Sauter et al 1973), the source of xylem sap glucose was not well identified. The accumulation of free sugars in the xylem sap may promote water movement into xylem vessels to refill embolized xylem by decreasing osmotic potential (Améglio et al 2001, Sakr et al 2003.…”

C depletion and tree dieback in young peach trees: a possible consequence of N shortage?

“…A tree was assumed to be dead when all its vegetative buds had dried deficiency because winter embolism is related to xylem osmolarity, i.e. to the concentrations in soluble C and N compounds Sakr et al 2003;Charrier and Ameglio 2011;Galvez et al 2013). Despite the fact that peach wood porosity is diffuse, positive xylem pressure plays only a minor role in recovery from winter embolism (Ameglio et al 2002).…”

Study of the Consequences of Global Warming in Water Dynamics During Dormancy Phase in Temperate Zone Fruit Crops

“…The discovery of aquaporins in the beginning of 1990's popularized the concept of membrane water channels (Connolly et al, 1998;Engel et al, 2000;Preston & Agre, 1991), and their roles were studied on membrane permeability (Johansson et al, 2000;Maurel, 2007;Sakr et al, 2003;Sarda et al, 1999;Van der Weerd et al, 2002). The most immediate decrease in ADC under dormancy inducing conditions occurred in the axillary buds of poplar followed by the vascular bud trace region (de Fay et al, 2000).…”