Quercitol plays a key role in stress tolerance of Eucalyptus leptophylla (F. Muell) in naturally occurring saline conditions

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Abstract

Understanding trees adaptation to arid, saline conditions is a major challenge for catchment revegetation in Australia. The accumulation of low molecular weight solutes is an established response of trees to the effects of salt and/or drought stress. Recent studies have shown that quercitol – a cyclitol – contributes significantly towards the adjustment of osmotic potential in some species of Eucalyptus. The present study investigated the role of quercitol in leaf tissues of Eucalyptus leptophylla (F. Muell) under fluctuating environmental stresses. Analysis of leaf tissues from trees growing at distances between 0 and 125 m from hyper-saline lakes suggests that quercitol contributes significantly to the adjustment of osmotic potential induced by drought in E. leptophylla. The presence of substantial concentrations of quercitol in xylem sap suggests that quercitol plays additional roles in signalling amelioration of osmotic stress in myrtaceous species. Quercitol concentrations fluctuate in both xylem and leaf tissues on a seasonal basis, suggesting a form of environmental regulation of solutes. The capacity of soil profiles to store rainwater, rather than proximity to hyper-saline groundwater largely determined osmotic stress in studied trees. Understanding such avoidance/tolerance mechanisms will be crucial to advance tree selection and breeding for stress tolerance.

Introduction

Understanding the mechanisms by which native plants cope with naturally saline conditions is a logical starting point for selection and development of salt-tolerant native species for the rehabilitation of land affected by secondary salinity. Studies of native shrubs (Barrett-Lennard, 2003, Short and Colmer, 1999) and grasses (Colmer et al., 1996), have identified traits such as the ability to isolate potentially damaging salts in vacuoles and glands (e.g. Atriplex), and storage of stable osmotica in the cytoplasm (e.g. Halosarcia), as key to salt tolerance. For native tree species, species such as Eucalyptus camaldulensis appear to ‘exclude’ unwanted salts (Akilan et al., 1997, Grieve and Shannon, 1999, Marcar, 1993, Rawat and Banerjee, 1998) while others, e.g. Casuarina obesa (Aswathappa and Bachelard, 1986, Clemens et al., 1983, van der Moezel et al., 1988) can cope with high salt concentrations in leaf tissues. Many screening trials for salt tolerance among native Australian tree species have been conducted (e.g. Niknam and McComb, 2000), and although several candidate species have been identified, we lack mechanistic knowledge of how native trees tolerate saline conditions experienced in the field. For eucalypts, the approach and measurements taken by researchers has varied widely and there is little consensus on the mechanisms responsible for salt tolerance. Lack of repeatability in field experiments, and a lack of consensus in quantifiable traits or characteristics that were useful markers of salt tolerance, were noted by (Niknam and McComb, 2000) as hurdles to the selection and planting of putatively salt-tolerant trees for land rehabilitation purposes.

Modification of osmotic potential and changes to the plasticity of cell walls, are well-described physiological mechanisms by which plants may cope with drought (e.g. Kozlowski and Pallardy, 2002). White et al. (2000) recently identified that some eucalypt species osmotically adjust in tolerating drought while others display an increase in cell-wall plasticity. Osmotic adjustment in response to drought has been demonstrated in an array of eucalypt species, including many elements of the genus, at magnitudes of generally between 0.1 and 0.4 MPa (e.g. Clayton-Greene, 1983, Ngugi et al., 2003, Prior and Eamus, 1999, White et al., 1996, White et al., 2000). Additionally, absolute values of osmotic potential (Merchant et al., 2007b) and solute chemistry (Merchant et al., 2007a) often reflect eucalypt taxonomy and known ecological niche characteristics (e.g. preferred habitat—more xeric or more mesic).

Eucalypt species present an array of physiological mechanisms to tolerate hyper-saline conditions. Both Prat and Fathi-Ettai (1990) and Lemcoff et al. (1994) noted the ability of selected eucalypt species to accumulate a variety of inorganic and organic solutes and adjust osmotic potential, when faced with increasing salinity. Lemcoff et al. (1994) suggests osmotic adjustment could be used as a selective trait in breeding programs for salt and drought tolerance in eucalypts. Numerous authors (Nguyen-Queyrens and Bouchet-Lannat, 2003, Popp et al., 1997, Popp and Smirnoff, 1995) have proposed that cyclitols play a major role as stable osmotica. The cyclitol quercitol (1(4)-deoxy-(+)-inositol) was first isolated from Eucalyptus by (Plouvier, 1963) and consists of a six-carbon ring with five hydroxyl groups. More recently, Adams et al. (2005) found quercitol concentrations up to 27 mg g−1 dry weight of leaf tissue in known salt-tolerant eucalypts (E. spathulata, E. sargentii, E. raveretiana, E. loxophleba) but no quercitol in the non-tolerant species E. globulus. Similarly, Merchant et al., 2006a, Merchant et al., 2007a identified discrete distributions of quercitol among eucalypt subgeneric groups that correlate strongly with environmental and edaphic conditions. The concentrations of quercitol found in these studies suggest that cyclitols can exhibit a large influence over total cellular osmolarity in some eucalypts.

Here we present an initial investigation into the role of quercitol in tissues of Eucalyptus leptophylla—a species that thrives in the proximity of hyper-saline lakes in Australia. We hypothesized that quercitol accumulation would be the major mechanism of osmotic adjustment in E. leptophylla in these environments. To test this hypothesis, we quantified several water relations properties of this species in winter and summer within the Pink Lakes National Park, north-west Victoria.

Section snippets

Site characteristics

The Pink Lakes region in south eastern Australia contains several hyper-saline lakes. Lake Crosbie is situated approximately 140 km west of the township of Ouyen (Lat: −35.068, Long: 142.317) The lake was chosen for its vegetation characteristics, particularly the distribution of eucalypts to the lakeshore. The annual rainfall for this region is approximately 300 mm, the majority of which falls in the winter months (May–October). The landscape consists of a series of lakes separated by dunes

Major patterns in leaf chemistry and site characteristics

ANOVA testing of season and distance effects on leaf and site parameters revealed several patterns (Table 1), notably that all site and leaf water parameters significantly varied with season and distance except for Ψpdwn (distance) and soil water (season). Osmolality of leaf tissues significantly varied with age, distance and season, but not in xylem water. Ca+ varied by tissue age and by season. Quercitol concentration was the only chemical to be significantly influenced by season in both FFE

Discussion

Our data reveal several trends indicating the key role played by quercitol in drought and salt tolerance in E. leptophylla. Our experimental design enabled us to detect gradients of both soil electrical conductivity and water content that varied by distance from the lakeshore. Similarly, a general trend of increasing predawn water potential with increasing distance from the lake was observed, although non-significant within seasons. Ψpdwn and Ψmidday show opposing gradients in the winter,

Acknowledgement

The authors would like to thank the Victorian Department for Conservation and Environment for the permission to study this field site.

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