Quantitative and qualitative changes in carbohydrates associated with spring deacclimation in contrasting Hydrangea species
Research highlights
► Increased temperatures causes a sigmoid deacclimation pattern in Hydrangea. ► In Hydrangea deacclimation kinetics are not correlated with mid-winter hardiness. ► Sugar hydrolysis is an important temperature-driven mechanism of deacclimation. ► 1-Kestose may be involved in freezing tolerance of H. paniculata.
Introduction
In temperate perennials cold hardiness is a seasonal process synchronized with the external seasonal changes in temperature and photoperiod. In autumn plants cold acclimate, whereby they become increasingly tolerant to subzero temperatures. Maximum hardiness is reached midwinter, and in spring plants loose acclimated cold hardiness by deacclimation (Weiser, 1970). Successful over wintering therefore not only requires sufficient maximum freezing tolerance, but also proper timing and rates of acclimation and deacclimation (Suojala and Lindén, 1997). Seasonal timing of acclimation and deacclimation may be an important trait affecting mortality, growth and quality of introduced crops cultivated far from their origin. Studies of the kinetics (timing and rates) of cold acclimation and deacclimation in response to the critical environmental stimuli are additionally much needed, given current predictions of climate change, where growing conditions may favour an altitudinal and poleward shifts in vegetation (Hughes, 2000, Parmesan, 2006).
Parallel to cold acclimation in autumn, temperate-zone woody perennials form terminal buds and develop dormancy (Rohde and Bhalerao, 2007). Despite favourable growth conditions dormancy often inhibits or prevents growth and deacclimation (Kalberer et al., 2006); risk of untimely deacclimation is, therefore, a concern for plants that are no longer dormant. Cold deacclimation is strongly dependent on temperature and can occur much faster than cold acclimation (Leionen et al., 1997; Taulavuori et al., 1997, Kalberer et al., 2007). Previous studies indicate that the rate of deacclimation is not a linear response but may change as deacclimation progresses. In addition, the rate and/or timing of deacclimation may vary between species, cultivars, ecotypes etc., demonstrating genetic variability for deacclimation kinetics and genetic adaptation to the local climate (Leinonen et al., 1997, Suojala and Lindén, 1997, Kalberer et al., 2007).
Regulation of cold acclimation in the autumn and the underlying physiological, biochemical and molecular responses have been extensively studied (Benedict et al., 2006, Welling and Palva, 2006). Less is known about the process of deacclimation (Kalberer et al., 2006). A close association has been established between accumulation of soluble carbohydrates and acquisition of cold tolerance in the autumn (Wanner and Junttila, 1999, Cox and Stushnoff, 2001), whereas the importance of alterations in carbohydrate metabolism in deacclimation is less clear. Some studies have found a correlation between decreasing sugar concentrations and the loss of cold hardiness, and suggested a mechanistic role of carbohydrate catabolism in deacclimation (Svenning et al., 1997, Tinus et al., 2000). In contrast, others have noted a decline in soluble carbohydrates preceding a loss of cold hardiness and, therefore, suggested no unequivocal relationship to spring-deacclimation (Sauter et al., 1996, Lennartsson and Ögren, 2004). To withstand subfreezing temperatures perennials employ two major strategies; supercooling (freeze avoidance) and extracellular freezing (freeze tolerance). Both freezing resistance mechanisms have been associated with accumulation of carbohydrates. In freezing tolerant tissues the protective function of sugars has been ascribed to their ability to stabilize membranes and proteins during freeze-induced dehydration (Crowe et al., 1998, Minorsky, 2003). In deep supercooling cells sugars are believed to aid in depressing the nucleation temperature (Kasuga et al., 2007). In stems of woody plants cortical tissues are strictly non-supercooling, while xylem ray parenchyma cells may exhibit either strategy (Quamme et al., 1972, Karlson et al., 2004). Seasonal changes in soluble carbohydrates in woody perennials have been analyzed in many studies. However, most of these studies have focused on intact stems (Cox and Stushnoff, 2001, Pagter et al., 2008), xylem tissue (Sauter and van Cleve, 1994, Sauter et al., 1996) or more seldom bark tissue (Thomas et al., 2004). Little is known about seasonal changes in soluble carbohydrates in both tissue types, including whether the type and/or concentration of specific sugars differ depending on how the tissues are adapted to freezing (Kasuga et al., 2007).
Hydrangeas are popular flowering shrubs, widely used and commercially important in landscape horticulture. Hydrangea macrophylla is native to Japan (McClintock, 1957) and thrives in maritime regions, but grows and flowers in most temperate regions where it is not damaged by cold temperatures. However, even in the relatively mild climate of Denmark frost-injury/winter-kill of current year shoots is a common problem in its cultivars. In contrast, H. paniculata is much less susceptible to frost (Suojala and Lindén, 1997, Pagter et al., 2008). Insufficient mid-winter hardiness may account for some of the frost injuries encountered in H. macrophylla, but likely late acclimation in fall and/or premature deacclimation in spring also limit successful cultivation of H. macrophylla (Adkins et al., 2003). Seasonal changes in cold hardiness of H. macrophylla and H. paniculata, determined on a rough time-scale, have previously been correlated with variation in a limited number of soluble carbohydrates in intact stems (Pagter et al., 2008). Recently we additionally examined the timing and rate of deacclimation of H. macrophylla and H. paniculata under simulated warm spell conditions (22 °C/17 °C day/night) (Pagter et al., 2011). Constant warm temperatures, however, may not adequately reflect the deacclimation conditions experienced under natural conditions, where continuously varying temperatures exist and where deacclimation presumably is much slower. Hence, the present study was conducted to address the following two main questions: (1) Which characteristics (if any) of deacclimation kinetics are important for Hydrangea to avoid frost injuries in spring? (2) Are soluble carbohydrates involved in controlling the rate and degree of deacclimation in Hydrangea stems and does the accumulation of soluble carbohydrates differ between bark- and xylem tissues? The hypotheses are: Re (1) susceptibility of Hydrangea to frost injuries during spring-deacclimation depends on the timing and rate of deacclimation in response to increasing temperatures. Re (2) genotype-specific differences in cold hardiness during deacclimation are due to variability in alterations in carbohydrate metabolism.
Section snippets
Location, climate and plant material
The experiment was carried out using three-year-old vegetatively propagated and commercially produced Hydrangea macrophylla ssp. macrophylla (Thunb.) Ser. cv. Alma and Hydrangea paniculata Sieb. cv. Vanille Fraise plants grown in 5-L pots containing sphagnum peat. For each species 45 plants were purchased (early January 2009), at which time the plants had been maintained outside (Gunnar Christensen's Nursery, Denmark, latitude 55°26′N) since spring 2008. Hence, the plants had undergone cold
Cold hardiness and deacclimation
Maximum stem cold hardiness was ca. −18 °C and <−30 °C in H. macrophylla and H. paniculata, respectively (Table 1). In H. macrophylla no significant changes in hardiness were observed in January and February, in March a small decrease was observed and from April onwards hardiness decreased at successively later sampling dates. Between mid-January and March 9 stem cold hardiness of H. paniculata was greater than −30 °C but could not be precisely evaluated, as the lowest temperature reached by the
Discussion
Deacclimation in the spring is driven mainly by the rise in temperature, which may influence the process in two ways. Firstly, temperature has a direct, short-term effect on cold hardiness in that, warm temperatures decrease hardiness after a few days, while low temperatures can slow, halt or even reverse deacclimation. Hence, fluctuating temperatures during spring cause fluctuating levels of frost hardiness. Secondly, warm temperatures during spring have a long-term effect on cold hardiness
Acknowledgments
This study was funded by the Danish Research Council for Technology and Production Sciences (grant no. 274-08-0331), the Danish Council for Independent Research through a young researchers award to MPA and The Ib Henriksen Foundation.
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