Abstract
North temperate tree species such as white spruce (Picea glauca [Moench] Voss) have evolved strategies to protect themselves against abiotic and biotic stresses that trees encounter during the inclement winter months. Chitinases not only play well-documented roles in plant defense but also function during physiological and developmental preparations for overwintering, including growth cessation, cold and desiccation acclimation, and dormancy acquisition. Phylogenetic analysis of 31 white spruce and 52 Norway spruce chitinases identified genes falling into each of the five clusters, which sometimes—but not always—separated the different biochemical classes of chitinases. Digital expression profiling of white spruce and Norway spruce chitinases across multiple conditions revealed a range of spatiotemporal expression patterns. Transcript abundance profiling in buds, needles, stems, and roots by quantitative RT-PCR suggested roles for eight white spruce chitinases during the growth-to-dormancy transition. In silico analyses of these eight sequences suggested that two cluster 2/class I chitinases function as chitinolytic enzymes in the tree’s constitutive defense arsenal during the winter months. A cluster 2/class I, cluster 2/class II, and cluster 1/class IV chitinase each exhibit hallmarks of antifreeze proteins. Additionally, two cluster 2/class I chitinases and a cluster 1/class IV chitinase may serve as vegetative storage proteins. One cluster 3/class II chitinase exhibited attributes suggesting that it is a chitinase-like gene functioning in cell wall synthesis. Taken together, our results imply that dormancy-associated chitinases act in concert to (1) confer protection against freezing injury, pests, and pathogens, (2) store nitrogen, and (3) promote cell maturation that precedes growth cessation.
Highlights
North temperate forest trees exhibit a number of adaptations that enable these long-lived species to withstand the inclement conditions of winter
Based on sequence similarity and the presence of one or more characteristic motifs, 32 expressed sequences encoding partial or full-length putative chitinases were identified in the white spruce gene catalog that comprises more than 27,000 unique expressed genes reported by Rigault et al (2011) and Online Resources 1 and 3
After filtering sequences that were too short for alignment, deduced amino acid sequences corresponding to 31 white spruce and 52 Norway spruce sequences were used to construct a phylogenetic tree, together with 58 previously characterized chitinases of Arabidopsis thaliana and other selected plant species (Fig. 1)
Summary
North temperate forest trees exhibit a number of adaptations that enable these long-lived species to withstand the inclement conditions of winter These adaptive traits include dormancy acquisition, bud development and the concomitant cessation of growth, as well as acquisition of cold and desiccation tolerance, seasonal nitrogen remobilization, and, in deciduous species, leaf senescence (Cooke et al 2012). (Holliday et al 2008; Asante et al 2011), including white spruce (Picea glauca [Moench] Voss; El Kayal et al 2011; Galindo-González et al 2012) Several of these studies have highlighted the large number of stress-associated genes that are upregulated during the transition from active growth to dormancy, such as genes coding for dehydrins, thaumatins, 41 Page 2 of 21. These authors observed that protein levels of multiple chitinases became abundant in white spruce prior to dormancy acquisition, suggesting that chitinases play roles in biochemical, cellular, and/or physiological processes that are important for tree survival during autumnal acclimation and the ensuing winter season
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