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First published online July 9, 2004; 10.1104/pp.103.037473 Plant Physiology 135:1654-1665 (2004) © 2004 American Society of Plant Biologists Phylogenetic Analyses in Cornus Substantiate Ancestry of Xylem Supercooling Freezing Behavior and Reveal Lineage of Desiccation Related ProteinsDepartment of Horticulture and Landscape Architecture, Purdue University, West Lafayette, Indiana 47907–1165 (D.T.K., V.E.S., E.N.A.); Department of Botany, North Carolina State University, Raleigh, North Carolina 27695–7612 (Q.-Y.X.); and The Morton Arboretum, Lisle, Illinois 60532–1293 (A.M.S.)
The response of woody plant tissues to freezing temperature has evolved into two distinct behaviors: an avoidance strategy, in which intracellular water supercools, and a freeze-tolerance strategy, where cells tolerate the loss of water to extracellular ice. Although both strategies involve extracellular ice formation, supercooling cells are thought to resist freeze-induced dehydration. Dehydrin proteins, which accumulate during cold acclimation in numerous herbaceous and woody plants, have been speculated to provide, among other things, protection from desiccative extracellular ice formation. Here we use Cornus as a model system to provide the first phylogenetic characterization of xylem freezing behavior and dehydrin-like proteins. Our data suggest that both freezing behavior and the accumulation of dehydrin-like proteins in Cornus are lineage related; supercooling and nonaccumulation of dehydrin-like proteins are ancestral within the genus. The nonsupercooling strategy evolved within the blue- or white-fruited subgroup where representative species exhibit high levels of freeze tolerance. Within the blue- or white-fruited lineage, a single origin of dehydrin-like proteins was documented and displayed a trend for size increase in molecular mass. Phylogenetic analyses revealed that an early divergent group of red-fruited supercooling dogwoods lack a similar protein. Dehydrin-like proteins were limited to neither nonsupercooling species nor to those that possess extreme freeze tolerance.
Due to their sessile nature, plants have been forced to adapt to the dynamic environmental conditions that surround them. Temperature creates a selective pressure on plants growing in temperate climates and has affected their geographical distribution based upon a capacity to survive seasonal thermal fluctuations (Smithberg and Weiser, 1968  ; Sakai and Weiser, 1973; George et al., 1974; Becwar et al., 1981; Gusta et al., 1983). In woody plants, two distinct and fundamentally different strategies for the seasonal survival of subzero temperatures have evolved: freeze tolerance (nonsupercooling) and freeze avoidance (supercooling; Burke et al., 1976; George et al., 1982). Freezing behavior strategies employed by a woody plant vary from tissue to tissue and are species specific. For example, cortical tissues are strictly nonsupercooling; however, buds and xylem ray parenchyma may exhibit either strategy. In nonsupercooling tissues, ice formation is initiated within extracellular spaces and generates a dehydrative vapor pressure gradient between extracellular ice and intracellular water. Nonsupercooling cells readily desiccate in response to extracellular ice formation (George et al., 1982; Fujikawa et al., 1999) and are capable of surviving low temperature extremes (Guy et al., 1986) due to an inherent capacity to tolerate desiccation (Ashworth et al., 1993; Fujikawa et al., 1997). In supercooling tissues, ice may also initiate in extracellular spaces; however, cells are thought to resist intracellular desiccation (Burke et al., 1976; George et al., 1982; Wisniewski and Ashworth, 1985; Fujikawa et al., 1994) and maintain intracellular water in a nonequilibrium condition. The supercooling of intracellular water is limited to the approximate point of homogeneous ice nucleation (–40°C; Rasmussen and MacKenzie, 1972). When the capacity for supercooling is exceeded, spontaneous and lethal intracellular ice formation may occur (Ristic and Ashworth, 1993).
Due to the temperature constraints of supercooling, woody plants which exhibit this freezing behavior are generally limited in geographical and altitude distribution to regions warmer than the –40°C isotherm (Smithberg and Weiser, 1968
In many plants, dehydrin proteins (group 2 late embryogenesis proteins [LEA D-11 family]) are induced by conditions that affect plant water status such as desiccation, salinity stress, and freezing stress (Close et al., 1993
The dogwood genus Cornus consists of approximately 55 species that are mostly woody and mainly distributed in northern temperate regions. The freezing behavior in seven Cornus species has been previously determined and found to consist of both nonsupercooling and supercooling species (George et al., 1974
Characterization of Xylem Freezing Behavior and Protein-Blot Analyses We utilized DTA as a method to distinguish xylem freezing behavior from a wide range of Cornus species and related outgroup species. Twenty-three of the 30 tested Cornus species (excluding the herbaceous Cornus canadensis) exhibited low temperature exotherms (supercooling). The only species found to lack low temperature exotherms were Cornus alba, Cornus amomum, Cornus bretschneideri, Cornus obliqua, Cornus rugosa, and C. sericea. Two interspecific hybrids were also tested, Cornus arnoldiana (C. obliqua x Cornus racemosa) and Cornus horseyi (Cornus macrophylla x C. amomum), and freezing behavior was identical to the maternal parent. C. arnoldiana exhibited the nonsupercooling behavior characteristic of its maternal parent C. obliqua. In contrast, C. horseyi displayed a low temperature exotherm similar to its maternal parent C. macrophylla (Fig. 1).
Freezing behavior data were overlaid upon a Cornus molecular phylogeny as a method to enable us to characterize the evolution of the trait. Outgroup genera, the basal lineage of the blue-fruited clade C. oblonga, the alternate-leaved blue-fruited species, and the red-fruited clade all displayed supercooling freezing behavior. Within the later divergent opposite-leaved blue- or white-fruited dogwoods, xylem freezing behavior varied, where five species were found to exhibit nonsupercooling behavior (Fig. 2B). Data obtained from ITS analysis confirmed that the sixth identified nonsupercooling species, C. bretscheideri, also falls within this same category (Q.-Y. Xiang, D. Thomas, T.K. Seo, J.L. Thorne, W. Zhang, S.R. Manchester, C. Fan, and Z. Murrell, unpublished data).
Protein-blot analyses of winter xylem protein extracts revealed predominant 24-kD-like proteins in 22 Cornus species and 3 outgroup taxa (Davidia involucrata, Nyssa aquatica, and Nyssa ogeche; Table I). A 22-kD protein was detected in D. involucrata and 36- and 34-kD proteins were found within N. aquatica and N. ogeche, respectively. The alternate-leaved species, Cornus alternifolia and Cornus controversa, accumulated a higher molecular mass protein (32.8 and 31.2 kD, respectively). Cross-reacting proteins of similar size to the C. sericea 24-kD protein were exclusively identified within the opposite-leaved blue- or white-fruited dogwood clade. Species in one well-supported clade (Cornus foemina-C. racemosa-Cornus drummondii; Xiang et al., 1998 ) accumulated a protein doublet of similar size to the 24-kD C. sericea dehydrin. Comparisons of total xylem protein extracts from nonacclimated and cold acclimated total xylem protein extracts from 24 selected Cornus species confirmed their winter association (Fig. 3). Two species, C. bretschneideri and Cornus poliophylla, were the only species found to contain significant quantities of 24-kD-like proteins under nonacclimated conditions (Fig. 3). In addition to the most closely related outgroup species (Alangium platinifolium), the early divergent blue-fruited C. oblonga, and the species tested species from the red-fruited group (C. angustata, C. capitata, C. canadensis, C. florida, C. kousa, C. mas, C. officinalis, and C. sessilis), no species accumulated a similar 24-kD-like protein. Usage of a polyclonal antibody specific for dehydrin proteins confirmed the lack of 24-kD-like protein accumulation in winter samples for C. oblonga and all species tested in the red-fruited dogwood clade (data not shown).
Evolution of Xylem Freezing Behavior and Proteins Similar to C. sericea's 24-kD Dehydrin-Like Protein in Cornus Evolutionary analysis of xylem freezing behavior and protein accumulation from a phylogenetic framework determined that the deep supercooling characteristic is ancestral within Cornus (Fig. 2B). Nonsupercooling evolved in five species of the blue- or white-fruited clade. Given that the relationships within this clade are poorly resolved, it is not clear whether nonsupercooling evolved a single time or had evolved independently in different species. The analysis suggested that nonaccumulation of the 24-kD-like protein represents an ancestral state in Cornus (Fig. 2C). With the exception of the unusual C. oblonga, whose lineage separates from the remainder of the blue- or white-fruited species, the accumulation of proteins similar to the 24-kD C. sericea dehydrin-like protein evolved a single time in the ancestor of the clade consisting of all blue- or white-fruited species (Fig. 2C). Within the same blue- or white-fruited group, an ancestral form of a 24- to 24.9-kD protein was documented and was followed by a trend for an increased size to higher molecular masses (Fig. 2D). At least two independent increases were identified: an increase to 31 to 33 kD in the alternate-leaved dogwoods and an increase to 25 to 27 kD in the opposite-leaved group. It is likely that the later increase occurred several times; however, due to the lack of resolution of relationships and incomplete sampling of species within this group, the number cannot be accurately determined.
Since the accumulation of 24-kD-like proteins was not detected within any of the tested species from the red-fruited dogwood clade, we attempted to determine if red-fruited species were capable of accumulating similar proteins when placed under conditions (short day length and water deficit) that are known to induce dehydrins in C. sericea (Karlson, 2001
Prior to the initiation of photoperiod treatments, both supercooling and nonsupercooling species tested exhibited high stem relative water content (SWC) and lacked proteins of similar size to the C. sericea 24-kD protein. Subsequent to 8 weeks of short day exposure, the two representative blue- or white-fruited opposite-leaved dogwoods, C. amomum and C. sericea, reduced SWC and accumulated a 24-kD protein. Neither red-fruited dogwoods, C. florida and C. kousa, exhibited a similar SWC reduction, nor accumulation of a similar sized 24-kD protein. Negative control plants that were grown under 16-h-long day did not reduce SWC nor accumulate a similar sized 24-kD protein in any species (Fig. 4). Subsequent to prolonged water deficit, substantial SWC reduction occurred in all species tested. Vital staining with fluorescein diacetate confirmed sublethality of the water deficit treatment (data not shown). Protein-blot analysis revealed that prolonged water deficit stimulated the accumulation of similar proteins only in C. amomum and C. sericea but not in the two red-fruited species analyzed (Fig. 5). Usage of a polyclonal antibody specific for dehydrin proteins provided a secondary means of confirmation for the lack of 24-kD-like proteins in C. florida and C. kousa under the tested conditions (data not shown). These data strengthen the hypothesis that this difference is likely under genetic constraints.
In woody plants, it is well established that two mechanisms have evolved for the survival of annual seasonal temperature fluctuations. Since the extent of supercooling is limited by the homogenous ice nucleation point (–40°C), this typically dictates the lower temperature limit for species that exhibit this characteristic and thus affects the geographical range (Sakai and Weiser, 1973 ; George et al., 1974) of such species. If the temperature of the homogeneous ice nucleation point is exceeded, the result is presumably lethal intracellular ice formation (Burke et al., 1976; George and Burke, 1977) and subsequent tissue injury (George et al., 1982). Survival of nonsupercooling tissues, however, is dependent upon desiccation tolerance (Ashworth, 1993; Fujikawa et al., 1997), and an absolute physical limitation to low temperature exposure may be nonexistent. As a consequence of dehydration, cellular contents may become highly viscous and nondestructively vitrify. Vitrification may partially explain how C. sericea is capable of surviving the temperature of liquid helium (Guy et al., 1986; Pearce, 2001). From an evolutionary point of view, the acquisition of a nonsupercooling behavior would be advantageous for geographical expansion into harsh low temperature environments. However, little is known about the genetics and the evolution of freezing behaviors in plants. The disparities between supercooling and nonsupercooling freezing behavior creates an interesting scenario to question from both an evolutionary and molecular point of view. By coupling xylem freezing behavior and protein-blot data to a molecular phylogeny, we gained insight into this enigma.
Our analysis provided evidence that freezing behavior is maternally inherited (Fig. 1) and is highly correlated with species phylogeny in Cornus (Fig. 2B). A maternal influence on the inheritance of cold hardiness in various fruit trees (Dorsey and Bushnell, 1925 In Cornus, the supercooling freezing mechanism was employed by most species and was inherited down from the common ancestor of the genus. On the contrary, the nonsupercooling mechanism evolved in only a few species of a single subclade derived from supercooling ancestor(s). Interestingly, five of the six identified nonsupercooling species (exception C. amomum) inhabit the northernmost ranges of the genus (excluding the three rhizomatous herbaceous species). Phylogenies that are based on ITS and matK sequence data (Q.-Y. Xiang, D. Thomas, T.K. Seo, J.L. Thorne, W. Zhang, S.R. Manchester, C. Fan, and Z. Murrell, unpublished data) from a broad range of species indicate that they are scattered in different subclades within the blue- or white-fruited group. As a result, a shift to nonsupercooling freezing behavior may have evolved repeatedly in independent blue- or white-fruited dogwood lineages and may have played a key role in the adaptive radiation of the largest subgroup of Cornus into higher latitudes.
It has been postulated that dehydrin-like proteins play an important role in providing protection from desiccation resultant from the formation of extracellular ice (Close, 1996
Our finding that dehydrin-like protein accumulation occurs widely within supercooling species (Table I; Fig. 3) suggests that the relationship of dehydrins to the nonsupercooling mechanism (extracellular ice formation) requires further investigation. Alternatively, these observations cast doubts on the hypothesis that supercooling is strictly a nondesiccative freeze-avoidance strategy (Burke et al., 1976
In red-fruited dogwoods, the absence of 24-kD-like proteins and the nonresponsiveness of tested species to normally inductive conditions suggest that a genetically determined basis exists for this trait and is attributed to the evolutionary history of their group. In a previous study, we determined that a photoperiod controlled SWC reduction is highly correlated to freeze tolerance and dehydrin-like protein accumulation in C. sericea and likely serves as a cue for the acquisition of freezing tolerance prior to the onset of winter (Karlson et al., 2003 In conclusion, our study has shed light upon a poorly understood area of plant adaptation to low temperature environments. For the first time, to our knowledge, we have demonstrated that there is an evolutionary separation of freezing behavior in a representative woody plant species and documented a maternal influence for this trait. Interestingly, all out-group species and early divergent dogwood species exhibited supercooling behavior, a freezing behavior that has been documented to impose discrete low temperature limitations to woody plants for over-winter survival. Therefore, a conversion to nonsupercooling freezing behavior, which is highly correlated to dessication tolerance and is not physically limited to low temperature extremes, would be an advantageous acquisition and may have facilitated their expansion into northernmost ranges.
Plant Material Current year's growth from stems was randomly harvested from established plantings during winter field conditions for the evaluation of xylem freezing behavior and total protein extractions for 31 Cornus and 4 out-group species. The sources of plant material and sampling dates are respectively listed (Table II). Immediately upon harvest, the cut ends of stem tips were wrapped in parafilm, placed into a plastic bag with a moist paper towel, and packaged on ice. Samples obtained from the Morton Arboretum and the Purdue University campus were immediately brought to the laboratory for freezing behavior determination and total xylem protein extraction as described below. Samples obtained from other sources were similarly packaged and overnight-mailed to Purdue University. Samples were maintained at 4°C in moist paper towels within sealed plastic bag until at least three replicate DTA analyses were completed.
Xylem freezing behavior was determined with DTA as previously described (Malone and Ashworth, 1991
Xylem total protein extractions from winter samples were performed as previously described (Sarnighausen et al., 2002
Total xylem protein extracts were harvested from trees during summer conditions as a negative control to assess the previously observed winter association of dehydrin-like proteins in the majority of sampled species (Table I). Current year's growth from 24 Cornus species was harvested August 5, 1999 from identical specimens and locations that were sampled the previous winter. Protein extraction and blot methods were performed identically as previously described (Sarnighausen et al., 2002
Phylogenetic analyses of Cornus using different molecular data (chloroplastic DNA restriction sites and sequences of matK, rbcL, ITS, and 26S rDNA) have been conducted previously by Xiang and colleagues (Xiang et al., 1996
Previous studies in C. sericea confirmed that 24-kD protein accumulation was highly correlated to water deficit and short day length. We were interested to determine if representative red-fruited dogwood species have the capacity to accumulate similar 24-kD-like proteins under known inductive conditions. Therefore, we reproduced similar controlled experiments as previously described (Karlson et al., 2003
Small 1-year-old seedlings of C. amomum, C. florida, and C. kousa were used as plant material for the study. Replicates of C. sericea were propagated as stem cuttings as previously described (Karlson et al., 2003
Response to water deficit was also tested for these species using replicate seedlings of C. amomum, C. florida, C. kousa, and propagated C. sericea stems. Plants were grown in the temperature controlled glass house (24°C/18°C day/night) and maintained under a controlled long day (16-h) photoperiod regime. Pots were wrapped in plastic bags to minimize evaporative water loss from the soil. Control replicates (n = 6) of each species were watered daily, whereas additional replicates of each species (n = 6) were exposed to a water deficit by withholding water until leaf wilting was observed. After 2 to 3 d of persistent wilting, plants were harvested for SWC determination and subsequent xylem protein extraction. Watered control plants were harvested at the same time for comparative analysis of SWC and total xylem proteins. Total xylem protein extraction and subsequent blotting analyses were performed as previously described (Sarnighausen et al., 2002
The authors thank the following individuals and their corresponding arboretum for the kind donation of material used within the study: Tony Aiello (Morris Arboretum), Mary Hirshfield (Cornell Plantations Arboretum), Tom Ranney (Mountain Horticultural Research Center), Kevin Tunison (National Arboretum), and Tom Ward (Arnold Arboretum). We also thank the Morton Arboretum for allowing us to harvest multiple species from their vast Cornus collection. For our controlled environment studies, we thank Heritage Seedlings for their kind donation of C. kousa seedlings. Likewise, we thank the Indiana Division of Natural Resources for their generous donation of C. amomum and C. florida seedlings. Lastly, we thank Dr. Timothy Close (University of California, Riverside) for graciously donating the antidehydrin specific polyclonal antibody for protein-blot analyses. Received December 9, 2003; returned for revision May 3, 2004; accepted May 4, 2004.
1 Present address: Division of Plant and Soil Science, West Virginia University, Morgantown, WV 26506–6108.  Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.103.037473. * Corresponding author; e-mail dale.karlson{at}mail.wvu.edu; fax 304–293–2960.
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