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Nitrogen storage and seasonal nitrogen cycling in Populus: bridging molecular physiology and ecophysiology

Corresponding Author

Janice E. K. Cooke

Université Laval, Centre de Recherche en Biologie Forestière, Sainte-Foy, Québec G1K 7P4, Canada;

Present address: University of Alberta, Department of Biological Sciences, Edmonton AB T6G 2E9, Canada

Author for correspondence: Janice E. K. Cooke Tel: +1 1780 4920412 Fax: +1 1780 4929234 Email: [email protected]Search for more papers by this author

Martin Weih,

Martin Weih

Swedish University of Agricultural Sciences, Department of Short Rotation Forestry, Vallvägen 10, SE-75007 Uppsala, Sweden;

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Janice E. K. Cooke,

Corresponding Author

Janice E. K. Cooke

Université Laval, Centre de Recherche en Biologie Forestière, Sainte-Foy, Québec G1K 7P4, Canada;

Present address: University of Alberta, Department of Biological Sciences, Edmonton AB T6G 2E9, Canada

Author for correspondence: Janice E. K. Cooke Tel: +1 1780 4920412 Fax: +1 1780 4929234 Email: [email protected]Search for more papers by this author

Martin Weih,

Martin Weih

Swedish University of Agricultural Sciences, Department of Short Rotation Forestry, Vallvägen 10, SE-75007 Uppsala, Sweden;

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First published: 03 May 2005

https://doi.org/10.1111/j.1469-8137.2005.01451.x

Citations: 156

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Summary

While both annual and perennial plants store nitrogen resources during the growing season, seasonal N cycling is a hallmark of the perennial habit. In Populus the vegetative storage proteins BSP, WIN4 and PNI288 all play a role in N storage during active growth, whereas BSP is the major form of reduced N storage during winter dormancy. In this review we explore cellular and molecular events implicated in seasonal N cycling in Populus, as well as environmental cues that modulate both the phenology of seasonal N cycling, and the efficiency and proficiency of autumn N resorption. We highlight recent advances that have been made using Populus genomics resources to address processes germane to seasonal N cycling. Genetic and genecological studies are enabling us to connect our understanding of seasonal N cycling at molecular and cellular levels with that at ecophysiological levels. With the genomics resources and foundational knowledge that are now in place, Populus researchers are poised to build an integrative understanding of seasonal N cycling that spans from genomes to ecosystems.

Introduction

The ability of forest trees to store and internally redistribute nitrogen resources is a fundamental element of the N economy of forest trees and other perennial plants. The internal redistribution, or cycling, of N can be divided into four phases: (1) primary allocation of N from N-assimilating source tissues to sink tissues during the growing season; (2) reallocation of N resources arising from metabolic recycling of N during the growing season; (3) resorption of N from senescing tissues and its transport to perennating tissues during autumn senescence; and (4) remobilization of N from perennating tissues to actively growing tissues during spring flush. The latter two phases constitute seasonal N cycling.

While both annual and perennial plant species have the ability to store, remobilize and recycle N resources during the growing season, seasonal N cycling represents a requisite component of the perennial lifestyle (Staswick, 1994; Stepien et al., 1994). Along with budset, cold acclimation and endodormancy, seasonal N cycling is an important adaptation that perennial plants have acquired to enable overwintering. As a mechanism of N conservation, seasonal N cycling is a determinant of N-use efficiency in perennials (Millard & Proe, 1991). Seasonal N cycling is also a determinant of plant fitness in perennials (May & Killingbeck, 1992), particularly for long-lived perennials such as forest trees that must be able to contend with many years of inter- and intraseasonal variations in N availability before they are able to reproduce sexually.

Nitrogen storage and cycling have traditionally been investigated at the molecular physiology or ecophysiology scales. However, the genomics toolkits that are now available for Populus and other forest trees provide us with an unprecedented opportunity to bridge these traditionally nonintersecting domains. This is particularly true in the case of Populus, where the assembled, annotated genome sequence is the keystone of the toolkit. The tools of the genomics toolkits provide us with the means to begin developing a comprehensive, mechanistic understanding of the processes and regulation of N cycling, spanning from the molecular to the ecosystem scale.

In this review we provide an overview of N storage and cycling from both the molecular physiological and ecophysiological perspectives, incorporating insights that have been gained from recent genomic-scale investigations. We aim to provide a synthesis of research that has already been undertaken, as well as to illuminate the gaps that exist in our knowledge of N storage and cycling. The review focuses on Populus, but we draw on supplemental examples from other tree taxa in cases where our current knowledge of Populus biology is incomplete. Although N storage and cycling is highly integrated with storage and cycling of other nutrient resources – particularly carbon – space constraints preclude treatment of the interrelationships and cross-talk that coordinate storage and cycling of N and with C resources and other nutrients.

Nitrogen storage in Populus: the vegetative storage proteins

Vegetative storage proteins (VSPs) represent the major form of reduced N storage in vegetative tissues of both annual and perennial plants (Staswick, 1994; Stepien et al., 1994). Two schools of thought persist in the classification of proteins as VSPs. In the more stringent view, proteins are considered to be true storage proteins if their synthesis and breakdown are governed by a need to set aside N reserves, rather than an enzymatic function, and if they remain biologically inactive during the period in which they are stored (Staswick, 1994). In the more liberal view, storage proteins are considered to be those proteins that are synthesized with resources that might otherwise be partitioned into growth-promoting processes, and have the potential to be broken down to support future growth (Chapin et al., 1990). In this review our focus is on the process of N storage as an integral component of N cycling, and we adopt the second, broader definition of VSP.

Rubisco as an unconventional vegetative storage protein

While still somewhat controversial, Rubisco is considered by many to serve a dual function as a photosynthetic enzyme and as a form of N storage during periods of active growth (Chapin et al., 1990; Millard, 1993; Stepien et al., 1994; Stitt & Schulze, 1994). Two lines of evidence are often cited to support this theory. First, Rubisco, which may represent half the total leaf protein content (Titus & Kang, 1982), is broken down during leaf senescence, providing considerable resources to support de novo biosynthesis and metabolism important for future growth (Millard, 1993; Masclaux et al., 2001; Hörtensteiner & Feller, 2002). Second, plants appear to synthesize more Rubisco than is needed for C assimilation, particularly under N-replete conditions (Stitt & Schulze, 1994). The most convincing evidence for this latter point comes from experiments with antisense-rbcs tobacco plants, which are summarized by Stitt & Schulze (1994). Thus, although Rubisco does not conform to the more rigorous definition of VSPs as proteins whose synthesis and degradation is regulated strictly according to their role in N storage (Staswick, 1994), Rubisco can be considered an unconventional storage protein by virtue of its contribution to N-reserve formation during the summer months and N recycling during autumn (Chapin et al., 1990; Millard, 1993).

Characterization of the Populus vegetative storage proteins

VSPs that conform to the more rigorous definition of storage protein have been characterized for many species, including forest trees (Stepien et al., 1994), and genes encoding VSPs have been cloned and characterized for a number of these species (Wetzel et al., 1989; Tranbarger et al., 1991; Wetzel & Greenwood, 1991a; DeWald et al., 1992; Berger et al., 1995; Avice et al., 2003). In several cases, functionally characterized VSPs do not exhibit significant sequence similarities to other functionally characterized VSPs at the amino acid level, and may not exhibit robust phylogenetic relationships with other VSP subclasses (J.E.K.C. and F. Bedon, unpublished data) within the VSP superfamily (Coleman, 2004). Different VSPs also have been demonstrated to exhibit different enzymatic activities (Coleman, 2004). Consequently, caution must be exercised in annotating a gene from a given species as a VSP solely on the basis of sequence similarity to a characterized VSP from another species.

The bark-storage protein (BSP) family comprises the major VSPs in Populus. Populus BSPs were first identified by their pattern of accumulation in autumn and disappearance in spring within perennating tissues such as bark, wood and roots (Wetzel et al., 1989; Sauter & van Cleve, 1990; Langheinrich & Tischner, 1991). SDS–PAGE and immunological characterization of BSPs from several Populus species and their hybrids revealed multiple isoelectric point variants with apparent molecular masses between 32 and 38 kDa (Langheinrich & Tischner, 1991). While 32 kDa polypeptides were consistently observed in both Populus and Salix (Sauter et al., 1988; Wetzel et al., 1989; Coleman et al., 1991; Wetzel & Greenwood, 1991b), the 34, 36 and 38 kDa polypeptides were reported only in a subset of tissues and hybrids. Multiple biochemical approaches were used to demonstrate that Populus and Salix BSPs are glycosylated (Langheinrich & Tischner, 1991; Wetzel & Greenwood, 1991b). Antibodies generated against the 32 kDa polypeptides were used to immunolocalize these proteins to membrane-bounded vesicles (protein storage vacuoles) that showed concomitant patterns of seasonal protein accumulation and breakdown (Sauter et al., 1989; Clausen & Apel, 1991). Similar studies have been carried out for Salix (Wetzel & Greenwood, 1991b).

Molecular analyses have demonstrated that the BSP family consists of three subfamilies: BSP, WIN4 and PNI288. cDNAs corresponding to members of the BSP subfamily were first cloned from Populus by screening an expression library with monospecific antibodies generated against the 32 kDa polypeptide identified by SDS–PAGE (Clausen & Apel, 1991; Coleman et al., 1992). WIN4– which encodes a 34 kDa polypeptide – was first identified as a wound-inducible gene (Parsons et al., 1989), but subsequent studies described in the next section provide compelling evidence that WIN4 functions as a VSP (Lawrence et al., 1997). PNI288 is the most recently characterized of the Populus VSPs, and also exhibits gene-expression patterns consistent with a functional role as a VSP (Lawrence et al., 2001). The deduced amino acid sequence derived from the full-length PNI288 cDNA predicts a polypeptide molecular mass of 36 kDa. As described in the following section, the evidence to date suggests that, while each of these subfamilies appears to play a role in N storage, they fulfil different N storage niches.

Inspection of Assembly 1.0 of the Populus trichocarpa genome sequence (http://genome.jgi-psf.org/Poptr1/) suggests that the BSP family in P. trichocarpa consists of seven loci: three members of the BSP subfamily; three members of the WIN4 subfamily; and a single member of the PNI288 subfamily (Fig. 1; Appendix S1, available online as supplementary material). As predicted from the molecular genetic analyses of Davis et al. (1993), the three BSP loci are tightly clustered. The analyses of Davis et al. (1993) further suggested that the clustered BSP and WIN4 loci are linked. At the time of writing, not all scaffolds containing BSP and WIN4 loci have been assembled into linkage groups, thus the physical arrangement of these genes within the genome cannot be determined. However, future versions of the P. trichocarpa genome sequence will undoubtedly allow the physical arrangement of the BSP and WIN4 loci to be ascertained.

Details are in the caption following the image — **Figure 1**
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Phylogenetic relationship of genes identified as members of the *BSP* family in *Populus trichocarpa*. Gene models corresponding to the BSP family were identified by blastn queries of the assembly 1.0 *P. trichocarpa* genome sequence using published sequences of *PdBSP*, *PtdWIN4* and *PtdPNI288* (GenBank accession numbers CAA49660, AAA16342 and AAK01124, respectively). An alignment of the complete predicted amino acid sequences was used to construct a neighbour-joining tree with mega version 2.0 (Kumar *et al*., 2001), using pairwise gap deletion and Poisson distance parameters. Bootstrap values (with percentages based on 1000 replicates) are shown at the tree nodes. Sequences and gene model information are available online as supplementary material in Appendix S1.

Roles of the BSP family in N storage and cycling

Gene-expression analyses that have been carried out to date on BSP, WIN4 and PNI288 in Populus suggest that genes from these three subfamilies play overlapping but nonredundant roles in N storage and cycling. These studies have used standard hybridization techniques such as Northern analyses to quantify transcript abundance, and while these methods can be used to discriminate unambiguously between different BSP subfamilies under the appropriate stringency conditions (Davis et al., 1993; Lawrence et al., 2001), they do not allow discrimination between members of the same subfamily. Therefore discussion is limited to the functional roles of the BSP, WIN4 and PNI288 subfamilies, although conceivably there are differences in regulation between different subfamily members.

BSP, WIN4 and PNI288 all appear to play a role in short-term N storage and cycling. Members of all three subfamilies are upregulated within days at the level of transcription by increased N fertilization, consistent with an N-storage role under ‘surplus’ conditions (Coleman et al., 1994; Lawrence et al., 1997; Lawrence et al., 2001). Zhu & Coleman (2001) have demonstrated induction of the Populus deltoides BSPA promoter activity by increasing in planta N levels, and suggest that glutamine is sufficient to increase promoter activity. VSPs synthesized for short-term N storage can be broken down for recycling of N when the tissue housing the protein encounters a state of N deficiency.

Interestingly, expression of BSP, WIN4 and PNI288 are all also upregulated by mechanical wounding. While wound-inducible BSP transcript accumulation occurs primarily in stems, wound-inducible WIN4 and PNI288 transcript accumulation occurs primarily in leaves (Davis et al., 1993; Lawrence et al., 2001). It remains to be determined whether VSPs that are synthesized during the defence response function strictly in N sequestration, or whether they play a more direct role in defence against herbivory.

Compelling evidence indicates that only the BSP subfamily plays a significant role in storage of N during dormancy. Whereas BSP steady-state mRNA abundance increases markedly in response to dormancy-inducing short-day photoperiods, the abundance of steady-state mRNA corresponding to WIN4 and PNI288 decreases sharply (Coleman et al., 1994; Lawrence et al., 2001). As might be predicted by this response to short-day conditions, expression of PdBSPA is mediated by phytochrome (Zhu & Coleman, 2001). Coleman (2004) presents a conceptual model and tentative evidence for regulation of BSP expression wherein phytochrome-mediated perception of photoperiod invokes a change in source–sink relations which, in turn, generate glutamine and sucrose signals that mediate induction of BSP expression.

The conventional transcription-level studies described above are corroborated by digital-expression profiling of BSP, WIN4 and PNI288 transcript abundance within a large-scale public Populus expressed sequence tag (EST) resource accessible via PopulusDB (Sterky et al., 2004). Digital-expression profiling of ESTs provides a measure of transcript abundance corresponding to a gene relative to the entire transcript pool within a sampled tissue, and thus offers a snapshot of the tissue's transcriptome (Audic & Claverie, 1997; Bhalerao et al., 2003). Digital-expression profiling of clusters corresponding to BSP, WIN4 and PNI288 ESTs across 18 cDNA libraries, representing diverse tissues and conditions (Sterky et al., 2004), indicates that ESTs corresponding to BSP are highly abundant in dormant cambium and dormant bud libraries (Fig. 2). Indeed, ESTs corresponding to BSP represent 20% of all ESTs sequenced from the dormant cambium library (Schrader et al., 2004). In contrast, ESTs corresponding to WIN4 and PNI288 were not sequenced from either dormant cambium or dormant bud libraries, supporting the notion that WIN4 and PNI288 do not play a role in overwintering N storage. BSP, WIN4 and PNI288 ESTs also demonstrate distinct distribution profiles in libraries representing nondormant tissues, suggesting that the subfamilies have distinct patterns of gene expression during the growing season (Fig. 2). In particular, WIN4 and PNI288 ESTs were sequenced more frequently than BSP ESTs from libraries representing actively growing tissues such as floral structures, vegetative shoots and shoot meristems.

The association of BSP family gene expression – particularly that of WIN4 and PNI288– with actively growing (sink) tissues raises the possibility that these VSPs are not just passive reservoirs of reduced N storage in Populus, but rather function as molecular determinants of N sink strength. In other words, synthesis of VSPs by cells within these tissues acts to increase the demand of these tissues for N resources. Given the C content of proteins, BSP, WIN4 and PNI288 also potentially act as molecular determinants of C sink strength. In support of this theory, transgenic antisense-BSP Populus plants exhibit a shift in biomass allocation to leaves from stems, i.e. the major site of BSP synthesis (G.D. Coleman, unpublished).

Physiological and molecular events of seasonal N cycling

Seasonal N cycling is an adaptation of plants to winter-cold seasonal climates in which nutrients (mostly N) are often considered to be the major growth-limiting factor. The necessity of seasonal N cycling arises from an apparent impossibility of individual plants to combine active growth with high frost resistance, and the nature of this trade-off is presumably caused by physiological constraints (Weih, 2003).

Autumn N remobilization

In Populus developing leaves represent a dominant sink for N during the active growing season (Dickson et al., 1985). In the first season of growth, 50% or more of the tree's total N can be found in the leaves of Populus trees (Pregitzer et al., 1990; Dickson, 1991; Cooke et al., 2003), although this percentage is likely to be lower in mature trees that have a relatively greater proportion of biomass in stems and roots. As mentioned in the previous section, much of the leaf N is accumulated in Rubisco protein. Shorter days and cooler temperatures bring about a major internal redistribution of N from leaves to perennating organs such as stems (Thomas & Stoddart, 1980). During autumn leaf senescence, there is a functional shift in leaf metabolism from resource assimilation to resource remobilization and export. N-rich amino acids and other mobile nutrients are transported via the phloem from senescing leaves to perennating tissues, where they are used to synthesize proteins (Sauter et al., 1989; Hörtensteiner & Feller, 2002; Geßler et al., 2004). Rubisco breakdown during autumn leaf senescence in Populus (Brendley & Pell, 1998) accounts for a notable proportion of the N exported from leaves (Titus & Kang, 1982; Millard & Thomson, 1989), and probably contributes significant N resources for BSP synthesis in perennating organs.

The accumulation of protein-filled storage vacuoles in phloem parenchyma cells in bark of P. deltoides during the winter months is shown in Fig. 3. In midwinter up to 95% of bark N constitutes protein in Populus (Höllwarth, 1976). Ray parenchyma cells of the wood also accumulate numerous protein-storage vacuoles (Sauter & Witt, 1997). Based on indirect calculations, it is estimated that BSP represents ≈ 5 µg mg⁻¹ d. wt, or 60–70% of the total protein content of 3-yr-old twig wood (Sauter & Witt, 1997). As mentioned in the previous section, BSP expression is phytochrome-mediated (Zhu & Coleman, 2001) and can also be induced by low temperatures even under long-day conditions (van Cleve & Apel, 1993). During autumn, BSPs accumulate in the bark parenchyma and xylem ray cells of the main stem, branches and roots of the tree. Branches, particularly 1-yr-old branches, accumulate greater protein concentrations than either roots or main stems (Sauter et al., 1989). The supply of photosynthate from source leaves is clearly important for BSP synthesis, as experimental defoliation of trees in June dramatically decreases protein accumulation in stems during autumn (Sauter & Neumann, 1994).

Reduced photoperiod is also sufficient to induce leaf senescence in deciduous perennial plants such as Populus (Andersson et al., 2004). This photoperiodic response, which, like BSP synthesis, is phytochrome-mediated (Olsen et al., 1997), distinguishes autumnal leaf senescence in perennial plants from age-mediated, pathogen-induced or temperature-induced leaf senescence that can occur in both annual and perennial plants (Quirino et al., 2000; Andersson et al., 2004). Although phytochrome is implicated in regulation of both BSP synthesis and autumnal leaf senescence, it has yet to be ascertained whether the two events are triggered by similar or different critical night lengths.

In annual plants the leaf senescence syndrome comprises a relatively well described series of regulated, highly ordered events to recapture resources invested in the leaf. These events include a shift from anabolic to catabolic metabolism, and the breakdown of organelles and macromolecules (reviewed by Thomas & Stoddart, 1980). The transition of chloroplasts to gerontoplasts before degradation is a hallmark of senescence and a major contributor to recaptured N, given that chloroplasts may contain up to 75% of the N housed within mesophyll cells (Hörtensteiner & Feller, 2002). Protein breakdown is the keystone of N remobilization in senescing leaves. There is evidence to suggest that at least some degradation of chloroplast proteins occurs within the chloroplast before the breakdown of these organelles (Hörtensteiner & Feller, 2002). The transport of proteins to the central vacuole via autophagy and their subsequent degradation by vacuolar proteases has been implicated in nutrient remobilization during leaf senescence in annual plants (Masclaux et al., 2001; Doelling et al., 2002; Hanaoka et al., 2002). To date, there does not appear to be evidence indicating a significant role for ubiquitin/26S proteasome proteolysis in wholesale N remobilization, although this pathway does appear to function in regulatory aspects of leaf senescence (Woo et al., 2001).

Enzymes of N metabolism – particularly those implicated in the N-recycling reactions and amino acid interconversions – also play an important role in the remobilization of N during leaf senescence (Masclaux et al., 2001). Studies with various plant species, including woody plants such as Vitis vinifera, demonstrate that glutamate dehydrogenase (GDH) and the cytosolic form of glutamine synthetase (GS1) are upregulated in senescing tissues (Brugière et al., 2000; Paczek et al., 2002), although the functional role of GDH in N metabolism continues to be debated. The localization of these enzymes in phloem companion cells of senescing tissues suggests their participation in N translocation from these senescing tissues (Paczek et al., 2002).

Few papers have addressed the cellular and molecular events of autumnal leaf senescence in deciduous forest trees. However, two recent genomic-scale transcriptome analyses of autumn leaf senescence in Populus offer new insight into changes in gene expression that occur during the senescence process in deciduous perennials, including those germane to seasonal N cycling. Bhalerao et al. (2003) used digital-expression profiling to compare relative EST abundance in senescing and young leaves; while Andersson et al. (2004) used microarray expression profiling to analyse expression profiles across a time course of autumnal leaf senescence. Both studies demonstrated that several cysteine proteases – which are often associated with the central vacuole – were significantly upregulated over the course of leaf senescence, as were selected chloroplastic proteases. BSP was also strongly upregulated in senescing leaves, suggesting that BSP serves as a transient store of amino acids in senescing leaves before their export to perennating tissues. A parallel genomic-scale investigation in Populus that used both EST and microarray analyses to compare gene expression cambial zone tissue collected in July (active cambium) and October (dormant cambium) reveals genes that potentially play a role in autumn N translocation and storage in the stem (Schrader et al., 2004). Not surprisingly, BSP exhibited much greater transcript abundance in dormant vs active cambial zone tissue. Interestingly, two genes putatively involved in N transport were also more highly expressed in dormant cambial zone tissue. All three studies revealed transcription factors and other regulators of gene expression that display significant differential regulation over the course of leaf senescence or dormancy induction, and it will be of great interest to determine if any of these regulators governs expression of genes important for seasonal N cycling. These genomic-level studies represent important first steps towards a more comprehensive understanding of events associated with autumn leaf senescence and cambial dormancy that contribute to the efficiency and proficiency of seasonal N cycling.

Spring N remobilization

During the leafless period in late autumn to early spring, soil temperature and soil mineralization rate are low and uptake of nutrients is minimal, although there is evidence for a capacity of boreal tree species to accumulate N from soil during temporary warmer periods of the winter season (Weih & Karlsson, 1997; Geßler et al., 1998). Limitation of N uptake caused by low soil temperature in early spring thus renders internal nutrient storage critical for new growth.

After moderate winter chilling requirements (Murray et al., 1989) are met, and days lengthen in the spring, N reserves in woody perennial roots and stems are broken down and amino acids are transported to the growing points to supply N for early season development of expanding buds (Bollmark et al., 1999). BSP breakdown appears to be initiated before budburst in Populus (Langheinrich, 1993). Dormancy release in Populus is principally a temperature-dependent phenomenon (Pauley & Perry, 1954), although at least some species of Populus require a certain threshold daylength before accumulated thermal time can initiate budbreak (Heide, 1993). Accordingly, endodormant Populus must first be subjected to dormancy-breaking treatments such as moderate chilling temperatures or hydrogen cyanamide before BSP breakdown can commence under long-day conditions. Furthermore, axillary buds must be present for BSP breakdown to be effected, suggesting that communication from the buds and/or sink demand is requisite for BSP mobilization (Coleman et al., 1993). BSP mobilization is accompanied by a sizeable influx of amino acids within the xylem sap (Sauter & van Cleve, 1992). In Populus, glutamine is the predominant amino acid in this spring influx, indicating that metabolic conversions of BSP-derived amino acids must occur before export (Sauter & van Cleve, 1992). Histochemical studies indicate that nearly complete mobilization of BSP takes place (Sauter & Witt, 1997).

Ecological, genetic and genecological aspects of seasonal N cycling

The physiological and molecular processes involved in seasonal N cycling are governed by complex interactions between individual plants, the environmental conditions that the plants are exposed to, and the communities in which they live. These interactions are conditioned by the genetic makeup (genotype) of the plants. In this section we consider environmental and other factors that influence the timing of N cycling, and the magnitude of N remobilization in autumn, two adaptive traits that influence plant productivity and fitness in boreo-temporal deciduous forest trees such as Populus spp.

Phenology and seasonal N cycling

Seasonal N cycling is intimately tied to phenology, an important adaptive trait in perennials that determines the timing and duration of the growing season (Hänninen, 1990). The duration of the growing season is a major determinant of the annual growth capacity of poplars on the one hand, while an extended growing season increases the risk for spring or autumn frost injury on the other hand. Trade-offs between maximizing growth capacity via a prolonged growing season and spring or autumn frost tolerance strongly affect the performance and survival of trees in northern climates (Howe et al., 2003; Weih, 2004).

Both budburst phenology and budset phenology demonstrate ecotypic and genetic variation in Populus (Howe et al., 2000; Tsarouhas et al., 2001; Pellis et al., 2004). For example, genotypes of Populus from higher latitudes and altitudes complete growth and leaf senescence earlier in the autumn (Pauley & Perry, 1954; Howe et al., 1995). Also, the frost-hardening rate in Salix clones originating from higher latitudes is accelerated (Lennartsson & Ögren, 2002), although it is currently unclear whether the increased hardening rate is correlated with an increased rate of leaf N retranslocation and senescence.

The timing of spring BSP mobilization has been correlated with budburst phenology in Populus (Langheinrich, 1993). Black et al. (2001) have demonstrated both ecotypic and genetic variation in BSP expression associated with autumn N resorption. When grown in a common garden experiment, P. deltoides ecotypes representing a latitudinal cline exhibited dates of maximal bark BSP mRNA accumulation correlated with their latitude of origin. Genetic variation in BSP protein accumulation in bark under both applied short-day conditions and natural midwinter conditions was also detected within several P. trichocarpa × deltoides families. It remains to be determined how much of the observed variation in BSP accumulation between genotypes is accounted for by genetic variation within BSP subfamily loci, and how much of the observed variation resides in regulators controlling BSP gene expression. For example, genetic variation has been detected in the vicinity of the phytochrome loci PHYB1 and PHYB2 (Howe et al., 1998), and given that BSP expression is phytochrome-mediated, it will be germane to determine how much the variation in seasonal BSP accumulation in Populus is explained by genetic variation in these phytochrome loci.

While photoperiod and temperature are the principal environmental cues that govern phenology (Howe et al., 2003), biotic and abiotic factors that affect C–N dynamics have been shown to modulate the phenology of budburst and budset, and these probably also affect seasonal N cycling. For example, the timing of budburst in the spring following a year of heavy defoliation by herbivores can be advanced in some insect–forest tree interactions, but retarded in others (Heichel & Turner, 1976; Tuomi et al., 1989; Quiring & McKinnon, 1999; Carroll & Quiring, 2003). Herbivory-induced shifts in the timing of bud flush have been attributed to reduced accumulation of nutrient reserves in the year of defoliation (delayed budburst), or altered sink–source interactions arising from changes in crown architecture, such as bud type and arrangement, resulting from herbivory (advanced budburst) (Quiring & McKinnon, 1999; Carroll & Quiring, 2003). Comparable studies have not yet been published for Populus. However, given that overwintering protein reserves are decreased following manual defoliation in June (Sauter & Neumann, 1994), it might be predicted that spring N remobilization is altered by defoliation in the previous year.

Higher soil temperatures in autumn – which permit pedospheric N uptake – delay growth cessation and leaf senescence in black cottonwood (Sigurdsson, 2001). Increased N availability is known to delay autumn leaf senescence in Populus and Salix (Silvola & Ahlholm, 1993; Sigurdsson, 2001). Experiments carried out at FACE facilities have demonstrated that elevated CO₂ levels also delay leaf senescence in Populus (Tricker et al., 2004), although other studies have reported no effect or even accelerated leaf senescence (Silvola & Ahlholm, 1993; Sigurdsson, 2001). Elevated CO₂ levels were found to exert little effect on autumn N resorption efficiencies in Populus or Betula (Lindroth et al., 2001). The apparently contradictory reports on the effect of CO₂ on leaf phenology underscore the complexity of interactions between genotype, developmental stage and environment. A more mechanistic understanding of how CO₂ and other environmental factors affect gene expression important for leaf senescence and seasonal N cycling will undoubtedly help in unravelling these complex interactions.

Efficiency and proficiency of leaf N resorption

In apple trees, the percentage of the leaf N pool that is remobilized before leaf abscission in autumn can range from as low as 23% to as high as 70% in young trees subjected to ideal conditions (Titus & Kang, 1982). Reported values for leaf N resorption in Populus species are consistent with this range (Lindroth et al., 2001; García-Plazaola et al., 2003). The resorption of N from leaves is an important process for reducing plant N losses and thereby increasing long-term productivity of perennials, particularly deciduous perennials (Killingbeck, 1996; Eckstein et al., 1999). The efficiency of nutrient resorption is determined by diverse environmental and internal factors. For example, anthocyanin levels – which serve to protect the cellular events necessary for N remobilization from damage by excess light that may otherwise occur during senescence of leaves – are positively correlated with efficiency and proficiency of N resorption (Feild et al., 2001; Hoch et al., 2003). Drought and replete nutrient availability (improved plant N status) are both negatively correlated with leaf resorption efficiency, resulting in higher relative N losses during autumn leaf senescence, although there is an interaction between these factors (Harvey & van den Driessche, 1999; Weih & Nordh, 2002). These studies also found an interaction between drought and N availability on the efficiency of leaf N resorption.

There is evidence to suggest that the efficiency and proficiency of autumn N remobilization from senescing leaves exhibits genetic variation in Populus and other boreo-temporal, deciduous tree species (Aerts, 1996; Killingbeck, 1996; Harvey & van den Driessche, 1999; Weih & Nordh, 2002). Given the importance of N-resorption efficiency to the N economy of the tree, it might be predicted that clones exhibiting greater resorption efficiency also exhibit increased growth rates. There is, however, contradictory evidence about a possible relationship between resorption efficiency and growth rate in different clones of Populus and Salix. Pregitzer et al. (1990) and Weih (2001) found greater autumn N resorption in more productive clones, while Harvey & van den Driessche (1999) and Weih & Nordh (2002) found no relationship between autumn N resorption and productivity in genotype comparisons. The inconsistent pattern with respect to poplars and willows may reflect a similar lack of any general pattern in N-resorption efficiency across different plant taxa and environments (Aerts, 1996). Alternatively, commonly used methods used to express N-resorption efficiency and proficiency may not adequately reflect the targets for selection. More relevant measures of autumn N resorption may help resolve these questions (Eckstein et al., 1999; Weih, 2001).

Genetic variation associated with the efficiency and proficiency of autumn N remobilization could reflect an adaptive mechanism to nutrient availability in the environment of origin (Eckstein et al., 1999). If this is true, it might be predicted that selection for more efficient nutrient resorption would be greater in cold and nutrient-poor environments such as high latitudes and altitudes. Nitrogen recycling from needles of evergreen Pinus has been shown to increase with latitude of genetic origin (Oleksyn et al., 2003). Significant ecotype differentiation in growth and N economy during the growing season has been found in mountain birch originating from different elevations (Weih & Karlsson, 1999), and genetic differences in leaf N concentration during the growing season are likely to influence autumn N retranslocation, because leaf N concentration prior to leaf senescence is a major determinant of autumn N-resorption efficiency (Eckstein et al., 1999). Furthermore, based on results from investigations on N economy in genotypes of Salix and Betula (Weih & Karlsson, 1999; Weih & Nordh, 2002), we might expect significant genotype–environment interactions in autumn N remobilization in Populus.

At the same time that the magnitude of autumn N resorption can be a determinant of individual plant productivity, nutrients that remain in abscised leaves contribute to the nutritional quality of the leaf litter, which has impacts on community dynamics and ecosystem N cycling. Leaf litter from poplars and willows generally has high nutritional quality, facilitating rapid litter decomposition and nutrient release to soils. The phytochemistry of abscised Populus and Salix leaves has been shown to be affected by genotype, with attendant effects on litter decomposition (Lindroth et al., 2002; Weih & Nordh, 2002). There is also a significant influence of the biotic and abiotic environment on litter decomposition rate (Taylor et al., 1989; Slapokas & Granhall, 1991). Whitham et al. (2003) recently introduced the concept of the extended phenotype – genes that have consequences at the community and ecosystem levels. In support of this notion, Schweitzer et al. (2004) demonstrated that genetic variation in condensed tannin content influences Populus litter decomposition and soil net N mineralization, which has diverse impacts on both plant and animal species in the community and on ecosystem-level processes. Given the importance of litter decomposition and soil net N mineralization to communities and ecosystems, the relative N concentrations of abscised plant parts may potentially be a trait linking the processes observed at the individual plant level to those acting at the ecosystem level, and genes that condition leaf N-resorption efficiency and proficiency may also exhibit extended phenotypes.

Towards a comprehensive portrait of seasonal N cycling

Seasonal N cycling represents one of the relatively rare instances in which we have a reasonable grasp of processes involved at the molecular and cellular levels; at the ecophysiological level; and even – to some extent – at the community and ecosystem levels. Seasonal N cycling presents us with an exceptional opportunity to bridge these scales of organization and develop an in-depth understanding of seasonal N cycling. The Populus genomics toolkit represents an important cantilever of this bridge: the genome sequence, EST collections, microarrays, proteomic and metabolomic techniques, and other resources that make up the toolkit will be indispensable in delineating processes important for seasonal N cycling. Contemporary genetic approaches that take advantage of the Populus genomics toolkit, together with current and future Populus genetic resources, represent a second, equally important cantilever. These genetic approaches will allow us to identify genes conditioning adaptive traits germane to seasonal N cycling, and determine the extent of variation in genes within natural and pedigree populations. Perhaps the most important challenge will be the fostering of communication between practitioners of the diverse fields that must come together to develop this comprehensive and integrated understanding of seasonal N cycling from genes to ecosystems.

Acknowledgements

The authors would like to thank Frank Bedon for constructing the BSP phylogenetic tree; Dr John Greenwood for preparing the Populus micrographs; and Dr Gary Coleman for sharing unpublished data. J.E.K.C. would like to acknowledge funding from Genome Canada and Genome Québec, and M.W. from the Swedish Energy Agency.

Supporting Information

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Supplementary material

The following material is available as supplementary material at http://www.blackwellpublishing.com/products/journals/suppmat/NPH/NPH1451/NPH1451sm.htm

Appendix S1

The gene models derived from assembly 1.0 of the Populus trichocarpa genome sequence that were used to construct the phylogenetic tree shown in Fig. 1, provided in FASTA format. For each gene model, the Gene Model Id, one of the predicted gene names corresponding to the locus, and the name corresponding to the phylogenetic tree in Fig. 1 are given.

Citing Literature

Volume167, Issue1

July 2005

Pages 19-30

This article also appears in:

Plant environmental adaptation

Nitrogen storage and seasonal nitrogen cycling in Populus: bridging molecular physiology and ecophysiology

Summary

Introduction

Nitrogen storage in Populus: the vegetative storage proteins

Rubisco as an unconventional vegetative storage protein

Characterization of the Populus vegetative storage proteins

Roles of the BSP family in N storage and cycling

Physiological and molecular events of seasonal N cycling

Autumn N remobilization

Spring N remobilization

Ecological, genetic and genecological aspects of seasonal N cycling

Phenology and seasonal N cycling

Efficiency and proficiency of leaf N resorption

Towards a comprehensive portrait of seasonal N cycling

Acknowledgements

Supporting Information

References

Supplementary material

Appendix S1

Citing Literature

Figures

References

Information

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Nitrogen storage and seasonal nitrogen cycling in Populus: bridging molecular physiology and ecophysiology

Summary

Introduction

Nitrogen storage in Populus: the vegetative storage proteins

Rubisco as an unconventional vegetative storage protein

Characterization of the Populus vegetative storage proteins

Roles of the BSP family in N storage and cycling

Physiological and molecular events of seasonal N cycling

Autumn N remobilization

Spring N remobilization

Ecological, genetic and genecological aspects of seasonal N cycling

Phenology and seasonal N cycling

Efficiency and proficiency of leaf N resorption

Towards a comprehensive portrait of seasonal N cycling

Acknowledgements

Supporting Information

References

Supplementary material

Appendix S1

Citing Literature

Figures

References

Related

Information